ZooKeys 327: 35–42, doi: 10.3897/zookeys.327.5732
Intraspecific variation in the turtle barnacle, Cylindrolepas sinica Ren, 1980 (Cirripedia, Thoracica, Coronuloidea), with brief notes on habitat selectivity
Ryota Hayashi 1,2
1 International Coastal Research Center, Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5, Kashiwanoha, Kashiwa, Chiba, 277-8564, Japan
2 Current address: Seikai National Fisheries Research Institute, Fisheries Research Agency 1551–8, Tairamachi, Nagasaki, 851–2213, Japan

Corresponding author: Ryota Hayashi (bubobubo32@gmail.com)

Academic editor: Niel Bruce

received 3 June 2013 | accepted 20 August 2013 | Published 28 August 2013


(C) 2013 Ryota Hayashi. This is an open access article distributed under the terms of the Creative Commons Attribution License 3.0 (CC-BY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


For reference, use of the paginated PDF or printed version of this article is recommended.

Citation: Hayashi R (2013) Intraspecific variation in the turtle barnacle, Cylindrolepas sinica Ren, 1980 (Cirripedia, Thoracica, Coronuloidea), with brief notes on habitat selectivity. ZooKeys 327: 35–42. doi: 10.3897/zookeys.327.5732

Abstract

Specimens of the turtle barnacle Cylindrolepas sinica Ren, 1980 were collected from sea turtles in Japanese waters. The specimens were hexagonal in shape and were found burrowing into the sea turtle plastron. Specimens were dissected and the hard and soft parts were compared with the original description.

Keywords

Turtle barnacle, Cylindrolepas, epibiont, variation, redescription, mitochondrial genes 12S and 16S

Introduction

Ren (1980) described a new species of barnacle, Cylindrolepas sinica, collected from green sea turtles, Chelonia mydas (Linnaeus, 1758). Hayashi (2009) subsequently recorded Cylindrolepas sinica from three species of sea turtle: the green sea turtle, Chelonia mydas, loggerhead, Caretta caretta (Linnaeus, 1758), and hawksbill, Eretmochelys imbricata (Linnaeus, 1766). Subsequently, 13 species of the superfamily Coronuloidea, including Cylindrolepas sinica, were recorded during a 10-year (2002–2011) survey of epibionts attached to marine vertebrates from Japanese waters (Hayashi 2012). As shown in previous studies (Hayashi 2009, 2012), Cylindrolepas sinica is a common species on Japanese sea turtles.

This species was described as a cylindrical and rounded barnacle in previous studies (as shown in Fig. 1A and 1B). This study describes the intraspecific variation occurring in Cylindrolepas sinica and emphasises the morphological differences between Cylindrolepas sinica and related species. Brief comments on host selectivity are also presented.

Figure 1.

Cylindrolepas sinica Ren, 1980. A–B original variant occurring on the soft skin of sea turtles (RUMF-ZC-02030) C–H hexagonal variant occurring on the plastron of sea turtles (RUMF-ZC-02045) A and C, upper, basal, upper oblique and lateral views B and D parietal plates (surface and back view) E sutural elaboration of the parietal wall F upper view of radii G inner view of basal margin H basal margin with parietal ribs I hexagonal shell wall of Xenobalanus globicipitis.

Materials and methods

Epibiotic barnacles were sampled from sea turtles on breeding beaches, in bycatch, and from strandings in Japanese waters (see Hayashi 2012). Specimens of Cylindrolepas sinica were collected from the turtle (skin and plastron) and preserved in 99% ethanol. The specimens were dissected and their soft parts mounted on slides with a drop of glycerine. The specimens examined have been deposited in Fujukan, the Museum of the University of Ryukyus, under accession numbers RUMF-ZC.

Systematics
Class Maxillopoda Dahl, 1956 Subclass Cirripedia Burmeister, 1834 Superorder Thoracica Darwin, 1854 Order Sessilia Lamarck, 1818 Suborder Balanomorpha Pilsbry, 1916 Superfamily Coronuloidea Newman & Ross, 1976 Family Platylepadidae Newman & Ross, 1976 Genus Cylindrolepas Pilsbry 1916
Cylindrolepas sinica Ren, 1980

http://species-id.net/wiki/Cylindrolepas_sinica

Figs 1, 2
Cylindrolepas sinica Ren, 1980: 194, fig. 6; pl. 2 figs 12–20. Hayashi 2009: 1, fig. 1A, B. Hayashi 2012: 118, figs 10, 15g, pl. 3d.
Platylepas decorata Zardus & Balazs, 2007: 1303, figs 7–9. Frick and Zardus 2010: 294.
Material examined.

From the plastron of a green sea turtle stranded on Ishigaki Island, Okinawa, Japan, November 25, 2001, Ryota Hayashi coll. (RUMF-ZC-02047); from the plastron of a living green sea turtle, April 17, 2004, Hahajima Island, Ogasawara, Tokyo, Japan, Ryota Hayashi coll. (RUMF-ZC-02045); from a plastic tag on a stranded loggerhead sea turtle, September 26, 2010 at Yomitan, Okinawa, Japan, Ryota Hayashi coll. (RUMF-ZC-02048).

Additional description of intraspecific variation in the parietal wall.

Wall outline stellate, parietes concave (Fig. 1C); translucent between external ornamentation, external longitudinal ridges low, broad, poorly defined, growth ridges numerous, fine, closely spaced; (Fig. 1D); sutural elaborations opaque, erect, irregular ridges slightly directed toward apex, not cupped (Fig. 1E); radii very narrow, externally teeth partly concealed by sutural elaborations (Fig. 1F); internal midrib broad, short, flaring terminally or club-shaped, directed more downward than medially (Fig. 1G); internal lateral ribs well developed, moderately broad, short, extending below the basal margin, approximately same size and number of ribs on each side of midrib on all plates (Fig. 1G–H); sheath about two-thirds height of wall, basally terminating abruptly, not depending (Fig. 1D). Opercular valves and soft parts as described in Ren (1980) and Hayashi (2012).

Remarks.

The original description of Cylindrolepas sinica described the rounded, cylindrical form and is accurate for individuals occurring on the soft skin of sea turtles. The general morphology of this species is as described by Ren (1980) and Hayashi (2012) and illustrated in the present work in Figs 1A, 1B, and 2A. Frick and Zardus (2010) and Frick (2013) regarded Cylindrolepas sinica as a junior synonym of Platylepas decorata Darwin, 1854. However, morphological differences between Cylindrolepas sinica and Platylepas decorata are clearly detailed by Monroe and Limpus (1979), Ren (1980), Young (1991), and Hayashi (2012). Cylindrolepas sinica can be distinguished fromother species easily by the morphological characteristics listed in Table 1. In addition, the mitochondrial sequence variation of this and related species has been confirmed (the 12S rRNA, tRNA-Val and 16S rRNA regions, Table 2, see Appendix). Therefore, Cylindrolepas sinica is a valid species. In the phylogenetic analysis of Hayashi et al. (2013), Cylindrolepas sinica clustered with the whale barnacles (Xenobalanus, Coronula, and Cryptolepas). The pseudo-stalked barnacle Xenobalanus globicipitis also has hexagonal and cylindrical shell walls (Fig. 1A–I). Comparing these findings, Cylindrolepas sinica is likely ancestral to the whale barnacles (Hayashiet al. 2013).

Table 1.

Comparative features of Cylindrolepas spp. and Platylepas spp.

Labrum Basal margin of sheath Ornamentation of suture Longitudinal ridges on parietes Radii Midrib folds Secondary ribs Inner surface of parietes
Cylindrolepas sinica with a few teeth on each crest continuous with inner laminae present absent not visible not visible present smooth
Cylindrolepas darwiniana multidentate continuous with inner laminae rudimentary rudimentary not visible not visible present smooth
Platylepas decorata multidentate depending present present not visible conspicuous present smooth
Platylepas hexastylos with a few teeth on each crest depending absent absent visible, narrow conspicuous absent with longitudinal ridges
Table 2.

List of the materials examined. The GenBank accession numbers are from Hayashi et al. (2013).

Host animal Collected Locality Materials deposited number GenBank accession numbers
Cylindrolepas sinica (hexagonal form) Chelonia mydas Hahajima I., Ogasawara, Tokyo RUMF-ZC-02045 AB723955
Cylindrolepas sinica (hexagonal form) Chelonia mydas Hahajima I., Ogasawara, Tokyo RUMF-ZC-02047 AB723954
Cylindrolepas sinica (rounded form) Chelonia mydas Kanna, Ginoza, Okinawa RUMF-ZC-02030 AB723953
Cylindrolepas darwiniana Caretta caretta Toya, Yomitan, Okinawa RUMF-ZC-02029 AB723959
Cylindrolepas darwiniana Caretta caretta Toya, Yomitan, Okinawa RUMF-ZC-02028 AB723960
Platylepas decorata Chelonia mydas Kanna, Ginoza, Okinawa RUMF-ZC-02042 AB723950
Platylepas decorata Chelonia mydas Kanna, Ginoza, Okinawa RUMF-ZC-02046 AB723951
Platylepas decorata Chelonia mydas Kanna, Ginoza, Okinawa RUMF-ZC-02027 AB723952
Platylepas hexastylos Caretta caretta Otsuchi, Iwate RUMF-ZC-02025 AB723956
Discussion

The rounded form (Fig. 1A and 1B) of this species (described by Ren 1980; Hayashi 2012) is found in the soft skin of sea turtles and forms colonies in proximity to other individuals, as well as in aggregations (Fig. 2A). The hexagonal variant of this species burrows into the hard parts of the turtle body (plastron) and is often found as isolated individuals (Fig. 2B). Therefore, the shell morphology of Cylindrolepas sinica exhibits phenotypic plasticity through habitat selection.

Figure 2.

Habitat of Cylindrolepas sinica Ren, 1980. A the original rounded form aggregated on the tail of a green sea turtle B the hexagonal variant burrowing into a green sea turtle plastron C an unusual specimen attached to a plastic tag on a loggerhead sea turtle D close-up view of the individual attached to the plastic tag.

In a rare case, one individual was collected from a plastic tag attached to a loggerhead sea turtle (Fig. 2C, D). The tagged turtle was captured on June 24, 2010 in a set net at Yomitan, Okinawa, Japan, and recaptured in the same net on August 26, and finally found as a floating stranding nearby on September 26. These records indicate that this turtle was a resident in this coastal area, as reported in Hayashi (2009), and the presence of Cylindrolepas sinica is consistent with the previous report. In addition, this is the first record of the occurrence of Cylindrolepas sinica on an artificial object. This case indicates that Cylindrolepas sinica can attach to hard substrates, as well as living soft tissue, and the host selectivity of Cylindrolepas sinica is not the substrate material. Nogata and Matsumura (2006) reported the larval development and settlement of the whale barnacle, Coronula diadema (Linnaeus, 1767), which settled in a polystyrene Petri dish containing a small, isolated piece of skin tissue from the host whale. They suggested the involvement of a chemical cue from the host whale tissue in inducing larval settlement. In light of these findings, our finding of Cylindrolepas sinica settling on a plastic tag, and not directly on the body of the turtle, suggests that this settlement was triggered by a similar chemical cue. More information is necessary to clarify the settlement mechanism of epibiotic barnacles.

Acknowledgements

This study was supported by the Shikata Memorial Trust for Nature Conservation. The author thanks Prof. William A. Newman for making many constructive comments on the early manuscript, Dr. Diana Jones and an anonymous biologist as reviewers, and Dr. Niel Bruce as an editor who provided helpful comments and criticism of the manuscript, and the many people who generously helped during the course of this study in various ways, with both fieldwork and observations.

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Appendix
Phylogenetic analysis

The consensus trees in the neighbour-joining and maximum-parsimony analyses were inferred from 1000 bootstrap replicates and both analyses were conducted using MEGA ver. 5.0 (Tamura et al. 2011). The sequences were aligned using MUSCLE included in MEGA ver. 5.0. At each node, the numbers separated by the slash indicate the percentage NJ and MP bootstrap support, respectively (1000 replicates).