Cirripedia: Thoracica: Tetraclitoidea) in the Pacific Waters of Taiwan and Okinawa

Species Diversity 20: 183–189 25 November 2015 DOI: 10.12782/sd.20.2.183

New Records of the Tetraclitid Barnacle Tesseropora alba (Cirripedia: Thoracica: Tetraclitoidea) in the Pacific Waters of Taiwan and Okinawa

Ryota Hayashi1,3 and Benny K. K. Chan2 1 Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba 277-8564, Japan E-mail: [email protected] 2 Biodiversity Research Center, Academia Sinica, Taipei 115, Taiwan 3 Corresponding author (Received 8 December 2014; Accepted 6 August 2015)

The four-plated barnacle Tesseropora alba Ren and Liu, 1979 is recorded for the first time away from its type locality in the Xisha Islands, South China Sea. The new localities are northwestern Taiwan and Okinawa. The species is redescribed in detail, with a discussion of its likely geographical range in the Pacific. Key Words: Tetraclitidae, distribution, redescription, western Pacific.

In Southeast Asia, a small-sized white barnacle, Tessero- Introduction pora alba Ren and Liu, 1979 was described in Xisha Islands, South China Sea, Hainan Province of China. There have Tesseropora is a genus of barnacle of the superfam- been no subsequent records of this species, but we have re- ily Tetraclitoidea, and its species are among the most ple- cently collected T. alba from the Pacific coast of Taiwan and siomorphic members of the superfamily. The first species also from a buoy stranded in Okinawa, Japan, after a rough of Tesseropora was described by Krauss (1848), as Tetraclita weather (Fig. 1). These represent new records of this spe- rosea Kraus, 1848. Tesseropora was later proposed as a sub- cies in the Pacific Ocean. The morphological features of the genus of Tetraclita, distinguished by having four plates and species including hard and soft parts, are redescribed herein single row of pores in the parietal walls (Pilsbry 1916). Ross and compared with the description of the type specimen in (1969) raised Tesseropora from subgenus to genus level. In Ren and Liu (1979). Specimens were preserved in 99% etha- Tesseropora, 11 species (including five fossil species) and nol and deposited in the collections of the Coastal Ecology one subspecies have been described from all over the world Laboratory, Academia Sinica, Taiwan (CEL) and the Mu- (Table 1). The oldest known fossils of Tesseropora were col- seum of the University of Ryukyus, Fujukan (RUMF-ZC), lected from Oligocene deposits (de Alessandri 1895; Table Okinawa. 2).

Table 1. Distributional records of extent species of genus Tesseropora.

Species Localities References Tesseropora rosea (Krauss, 1848) Australia, the Kermadec Islands, South Africa Krauss (1848); Zullo (1968); Newman and Ross (1977); Otway and Anderson (1985); Costa and Jones (2000) Tesseropora pacifica (Pilsbry, 1928) Wake Island, Marshall Islands, Fiji, Guam Pilsbry (1927); Zullo (1968); Foster (1974); Pauley and Ross (2003) Tesseropora atlantica Newman and Bermuda, Azores, Saint Paul’s Rock (equatorial Newman and Ross (1977); Edwards and Lubbock Ross, 1977 Atlantic) (1983a, b); Southward (1998); Costa and Jones (2000) Tesseropora wireni (Nilsson-Cantell, Sumatra and Palau Islands Nilsson-Cantell (1921); Hiro (1935); Zullo (1968) 1921) Tesseropora wireni africana (Nilsson- Dar-es-Salaam, Diego-Garcia Nilsson-Cantell (1932); Newman and Ross (1976) Cantell, 1932) Tesseropora arnoldi Young, 1998* Azores. Young (1998) Tesseropora alba Ren and Liu, 1979 Xisha Islands, Taiwan, Okinawa Ren and Liu (1979); present study * Costa and Jones (2000) suggested the necessity for taxonomic work to confirm the status of T. atlantica and T. arnoldi.

Table 2. Records of fossil species of Tesseropora and the closely related Tesseroplax.

Species Age Locality Reference Tesseropora isseli Oligocene Italy de Alessandri (1894) Tesseropora dumortieri Miocene Western Tethys; eastern Atlantic Fischer (1866); Carriol (2008) coast Tesseropora sp.* Middle Miocene France (Atlantic coast) Carriol (2005) Tesseropora chilensis Pliocene Chile Carriol and Schneider (2013) Tesseropora sulcata Plio-Pleistocene France (Channel coast) Carriol (1993) Tesseropora canariana Lower Pliocene Canary Islands Hornung (2014) Tesseroplax unisemita** Middle-Upper Pliocene Guardra Is., Gulf of California Zullo (1968) * Tesseropora sp. is a T. dumortieri according to Carriol (2008); ** Zullo (1968) described the new fossil species as Tesseropora unisemita, but Ross (1969) divided this species from Tesseropora and proposed the new genus Tesseroplax for it.

Fig. 1. Type locality and sampling localities reported herein for Tesseropora alba.

Order Sessilia Lamarck, 1818 Tesseropora alba Ren and Liu, 1979: 344.—Liu and Ren Suborder Balanomorpha Pilsbry, 1916 2007: 345, fig. 155. Superfamily Tetraclitoidea Gruvel, 1903 Tesseropora sp.: Shuto and Hayashi 2013: fig. 3b. Family Tetraclitidae Gruvel, 1903 Subfamily Tetraclitinae Gruvel, 1903 Materials examined. CEL-Te-sp-001, Suao, Taiwan, Genus Tesseropora Pilsbry, 1916 September, 2010, one specimen attached to shell of barna- Tesseropora alba Ren and Liu, 1979 cle Megabalanus tintinnabulum (Linnaeus, 1758). RUMF- ZC-02049, Kanna River Estuary, Ginoza village, Okinawa

Fig. 2. Tesseropora alba Ren and Liu, 1979. A, an individual from Suao, Taiwan, attached to Megabalanus tintinnabulum ; B, shell wall of an individual from Kanna River Estuary, Ginoza, Okinawa, upper, basal, upper oblique, and lateral views; C, lateral compartment (external, internal and basal views); D, details of opercular plates (outer and inner), surfaces of tergum (upper) and scutum (lower); E, nauplius larva collected from within mantle cavity, with poorly developed swimming limbs and body with rich lipid reserves. Tesseropora alba from Okinawa and Taiwan 185 186 R. Hayashi and B. K. K. Chan

Fig. 3. Trophi and cirri of Tesseropora alba Ren and Liu, 1979 (Kanna River Estuary, Ginoza, Okinawa). A, palp; B, labrum; C, mandible; D, maxilla I; E, maxilla II; F, cirrus I; G, cirrus II; H, cirrus III; I, cirrus IV; J, cirrus V; K, cirrus VI.

December, 2006, several specimens collected from a strand- occludent margin with fine teeth, dorsal surface with promi- ed buoy. nent horizontal growth ridges; on ventral surface, adductor Diagnosis. Shell white, small, conical, external surface ridge prominent, rounded, extending about halfway up total smooth but with longitudinal ridges on basal region of wall height of scutum; articular ridge inconspicuous. Tergum plates. Radii narrow, summit oblique. Scutum white, basal narrow, apex pointed; spur apex blunt. margin convex, slightly longer than occludent margin. Ter- Mandibular palp rectangular, with serrulate setae on su- gum narrow, without medial furrow on dorsal surface, spur perior margin. Labrum bilobed with shallow notch, bearing long, apex of spur blunt. a few small teeth on each lobe. Mandibles with 5 sharp teeth Description. Shell small, conical, white; shell wall com- excluding inferior angle; second and third teeth bidentate, posed of 4 plates and singly tubiferous; tubes filled with liv- fourth tooth with serrate cutting edge, fifth tooth smallest, ing tissue; external surface of wall plates smooth, except for located close to lower margin; lower margin with 13 pecti- longitudinal ridges close to their basal region; radii narrow, nations, inferior angle ending in 2 large pectinations. Maxil- non-tubiferous; basis calcareous. Scutum triangular, basal lule notched, with 2 large setae above notch, 3 small setae margin rounded and slightly longer than occludent margin, at notch, and 10 setae below notch, cutting margin straight.

Fig. 4. Details of trophi of Tesseropora alba Ren and Liu, 1979 (Suao, Taiwan). A, mandibulatory palp; B, serrulate setae on superior margin of mandibulatory palp; C, labrum; D, notch of labrum; E, mandibles; F, maxillule G, maxilla; H, serrulate setae at margins of maxilla. Scale bars in µm. Tesseropora alba from Okinawa and Taiwan 187 188 R. Hayashi and B. K. K. Chan

Table 3. Number of segments in each cirrus (anterior ramus, posterior ramus) of Tesseropora alba.

Cirrus I Cirrus II Cirrus III Cirrus IV Cirrus V Cirrus VI 6, 10 7, 8 11, 13 14, 16 16, 17 17, 18

Maxilla oval, with serrulate setae at the superior margin and cause the specimens were dry and poorly preserved. Howev- distally. Cirri I–III as maxillipeds, and cirri IV–VI as cteno- er, our re-examination of the shell walls and opercular plates pods. Segment number of each cirrus listed in Table 3. of these specimens allows us to confirm that these barnacles Remarks. The morphology of our specimens fits the de- were indeed T. alba. This represents a further record of this scription of T. alba in Ren and Liu (1979). In Taiwan, this species in Japan. species was collected low on an exposed rocky shore, on the surface of the barnacle Megabalanus tintinnabulum. In Oki- nawa, T. alba was collected on the surface of Megabalanus Acknowledgments sp. found attached to a stranded buoy on the beach near the Kanna Estuary, Ginoza village, after a rough weather. The We are much indebted to Prof. William A. Newman for type specimens of T. alba were collected from the surface providing his knowledge and references concerning bar- of the barnacle Megabalanus xishaensis (Ren and Liu 1978) nacles, and RH’s friend, Tomoaki Nakamura (Okinawa Zoo found low on the shore on basalt rocks in the Xisha Islands and Museum), for finding the encrusted buoy while beach (Ren and Liu 1979). combing. We also thank R.-P. Carriol (Muséum national d’Histoire naturelle, Paris, France), Mark J. Grygier (Lake Biwa Museum) and another, anonymous referee who im- Discussion proved the previous version of this manuscript.

Larval ecology of Tesseropora alba. Some of the specimens collected in Okinawa contained eggs and nauplius lar- References vae in the mantle cavity (Fig. 2E). The swimming limbs of the nauplius larvae were poorly developed (Fig. 2E), which Anderson, D. T. 1986. The circumtropical barnacle Tetraclitella divisa suggests that T. alba broods the nauplii within mantle cav- (Nilsson-Cantell) (Balanomorpha, Tetraclitidae): cirral activity ity until the larvae have metamorphosed to cyprids, which and larval development. Proceedings of the Linnean Society of New South Wales 109: 107–116. are then released to the external environment. Such an ab- Carriol, R. P. 1993. Tesseropora (Cirripedia, Thoracica) du Néogène de breviated mode of larval development has been reported in France. Geobios 26: 709–713. Tetraclitella divisa (Nilsson-Cantell 1921) in Australia (An- Carriol, R. P. 2005. Re-examination and new species of Cirripedes derson 1986) and Taiwan (Chan et al. 2014): that T. divisa (Thoracica, Tetraclitidae, and Balanidae) from the Middle Mio- has only 4 naupliar stages and the nauplii are brooded inside cene of the faluns of Touraine (France). Annales de Paléontologie the mantle cavity until the cypris stage. Cirripedes with ab- 91: 117–126. breviated larval development often have specific habitat re- Carriol, R. P. 2008. New genus and new species of Cirripedia (Chtha- quirements, or the required habitat is rare. Tesseropora alba malidae, Tetraclitidae, Archaeobalanidae and Balanidae) from the has only been reported on shells of Megabalanus and does Middle Miocene of the faluns of Touraine (France). Zootaxa 1675: 31–48. not occur in high abundance. The habitat requirements and Carriol, R. P. and Schneider, S. 2013. New species of fossil sessile barna- population genetics of T. alba should receive further atten- cles (Verrucidae, Tetraclitidae) from the Pliocene of central Chile. tion. Neues Jahrbuch für Geologie und Paläontologie—Abhandlungen, Some uncertain records of Tesseropora. There are 270 (3): 233–244. some earlier records of Tesseropora barnacles in the western Chan, B. K. K., Høeg, J. T. and Kado, R. 2014. Thoracica. Pp. 116–122. Pacific. Newman (1960) recorded Tesseropora sp. from this In: Martin, J. W., Olesen, J., and Hoeg, J. T. (Eds) Atlas of Crusta- region, but his written description was not accompanied by cean Larvae. John Hopkins University Press, Maryland, USA. diagrams to illustrate the morphology of the species. Pauley Costa, A. C. and Jones, M. B. 2000. The genus Tesseropora and Ross (2003) recorded an unidentified barnacle as ‘Tes- (Cirripedia:Tetraclitidae) from São Miguel, Azores. Arquipélago. seropora sp. 1’ from Guam, which they described as: “in- Life and Marine Sciences. Supplement 2 (Part A): 71–78. de Alessandri, G. 1894. Contribuzione allo studio dei Cirripedi fossili tertidal, wall ribbed, dia. to about 7 mm”. The ribbed shell d’Italia. Bolletino de la Società Geologica Italiana 13: 234–314. might indicate that this was T. alba, but the description by Edwards, A. and Lubbock, R. 1983a. The ecology of Saint Pauls Rocks Paulay and Ross (2003) was not very detailed and there was (Equatorial Atlantic). Journal of Zoology 200: 51–69. no information on specimen deposition. Without further Edwards, A. and Lubbock, R. 1983b. Marine zoogeography of Saint sampling in the areas concerned, we cannot confirm wheth- Pauls Rocks. Journal of Biogeography 10: 65–72. er the specimens mentioned by Newman (1960) and Pauley Fischer, P. 1866. Description de nouvelles espèces d’invertébrés fossiles and Ross (2003) were T. alba, or not. dans le bassin du Rhône (formation tertiaire moyen). Pp. 434– Shuto and Hayashi (2013) reported an unidentified Tes- 440. In: Falsan, A. and Locard, A. (Eds) Monographie Géologique seropora sp. collected from the Fish Aggregating Devices in du Mont d’Or Lyonnais et de ses Dépendances. Paris. Foster, B. A. 1974. The barnacles of Fiji, with observations on the ecol- Okinawa. They could not provide a detailed description be- Tesseropora alba from Okinawa and Taiwan 189

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