Cathaica

Notes on wentletrap snail Alexania inazawai (Kuroda, 1943) from Xiamen, China, and its obligatory ectoparasitic behaviour on Orange-Striped Anemone Diadumene lineata (Verrill, 1869)

福建厦门潮间带的稻泽亚梯螺及其专性寄生纵条矶海葵的记述

1 24 Fengdanbailu, 185 Xiufeng Road, Jin’an District, Fuzhou 350012, China;

[枫丹白鹭 秀峰路185号 晋安区 福州 350012 福建省 中国]

 https://orcid.org/0000-0001-9467-6893; Email: linliwen0911@foxmail.com

2 1 Yongjiandingshang, 185 Fanghu South Road, Huli District, Xiamen 361009, China.

[永建顶尚 枋湖南路185号 湖里区 厦门 361009 福建省 中国]

Published on 23 November 2024        DOI: https://doi.org/10.5281/zenodo.13834464

ZooBank Code: https://zoobank.org/References/4A1DD804-96C9-40BA-B1F3-9039B89A3854

Download 下载: PDF

Abstract: Alexania inazawai (Kuroda, 1943) is an ectoparasitic epitoniid obligatorily feeding on the sea anemone Diadumene lineata (Verrill, 1869). Alexania inazawai is originally described from Japan and had several records in China in recent years. In this work, Alexania inazawai populations discovered from three different sites in Xiamen are reported, and their habit and the evolutionary feature of this species is discussed.

摘  要：稻泽亚梯螺 Alexania inazawai (Kuroda, 1943) 是一种专一以纵条矶海葵 Diadumene lineata (Verrill, 1869) 为食的寄生性海生腹足纲动物。这个物种最初描述于日本，近些年在中国有过多次记录。本文中作者报道了来自厦门三个不同采样点的种群，并对这个物种的习性和演化特征进行探讨。

Key words. China, Xiamen, malacofauna, obligatory parasite

关键词：中国，福建，软体动物相，专性寄生

Introduction

Epitoniidae Berry, 1910, commonly known as wentletraps, is a large family within Caenogastropoda. Most wentletraps have white, conical shells and are predatory or ectoparasitic benthic gastropods that feed on anthozoans (Cnidaria), including sea anemones (Actiniaria), flower corals (Zoantharia), and stony corals (Scleractinia). Uniquely, a specialized group of planktonic wentletraps, including Janthina Röding, 1798, and Recluzia Petit de la Saussaye, 1853, feeds on colonial cnidarians such as Physalia Lamarck, 1801, Velella Lamarck, 1801, and Porpita Lamarck, 1801 (Gittenberger et al., 2006; Churchill et al., 2011; Gittenberger & Hoeksema, 2013; Beu, 2017).

The epitoniid genus Alexania Strand, 1928, comprises several benthic species with globose shells. This genus was originally named Alexandria Tomlin, 1926, with its type species, Alexandria natalensis Tomlin, 1926, described from South Africa (Tomlin, 1926). However, Alexandria was later recognized as a junior homonym of Alexandria Pfeffer, 1881, prompting Strand (1928) to propose the replacement name Alexania. Subsequently, Strand (1932) proposed Tomlinula Strand, 1932 as another replacement name for Alexandria Tomlin, 1926, though it became a junior objective synonym of Alexania.

The monotypic species Habea inazawai Kuroda, 1943 was originally described from Kamakura, Japan, and assigned to the family Epitoniidae based on its anatomical and ecological characteristics (Kuroda, 1943). Another species, Habea callizona Habe, 1961, was described from Kashiwaima, Japan (Habe, 1961). This species has a shell shape similar to the former but features a distinct banded pattern (Habe, 1961; Tsuchida & Hasegawa, 2017).

Robertson and Habe (1965) later recognized, based on similarities in the radular structures and shell characteristics, that Habea Kuroda, 1943 is a synonym of Alexania Strand, 1928. They also proposed that Alexania exhibits obligatory ectoparasitic behaviour, specifically on Diadumene species. Tsuchida and Hasegawa (2017) provided illustrations of Alexania inazawai and Alexania callizona and noted that Alexania inazawai is often found attached to Diadumene lineata on rocks in intertidal zones.

Alexania inazawai from China was firstly reported in a result on intertidal fauna in southeastern China, but the detailed distribution was not mentioned (Liu et al., 2023). In this paper, we report on three intertidal sites in Xiamen where Alexania inazawai were observed, represent the first record of this species in China. Its habitat and habits are also discussed.

Materials and methods

Living individuals of Alexania inazawai were observed from the intertidal zones in Xiajinwan [厦金湾], Huangcuo [黄厝] and Zengshan [曾山], respectively in the east, southeast and south of Xiamen Island from May, 2022 to February, 2023. Shell materials attached on Diadumene lineata on the reefs in Zengshan at extremely low tide were collected for study. Identification of Alexania inazawai and its sympatric species based on Tsuchida and Hasegawa (2017) and Zhang (2008). Photos of the shell specimens were taken using Nikon D80 camera with Laowa 60mm F2.8 Macro 2:1 lens and were modified in Adobe Photoshop CS6 2012.

Systematics

Family Epitoniidae S. S. Berry, 1910 (1812)

Genus Alexania Strand, 1928

Alexandria Tomlin, 1926: 287 (non Alexandria Pfeffer, 1881 [Echinodermata]).

Alexania Strand, 1928: 63 (replacement name of Alexandria Tomlin, 1926).

Tomlinula Strand, 1932: 193 (replacement name of Alexandria Tomlin, 1926).

Habea Kuroda, 1943: 12. [Type species: Habea inazawai Kuroda, 1943, type by monotypy]

Stenacme Pilsbry, 1945: 113. [Type species: Stenacme floridana Pilsbry, 1945, type by original designation]

Type species. Alexandria natalensis Tomlin, 1926, type by typification of replaced name.

Alexania inazawai (Kuroda, 1943)

稻泽亚梯螺

(Fig. 2A–H, Fig. 3A–B)

Habea inazawai Kuroda, 1943: 12; Habe, 1961: 417, 423.

Alexania inazawai – Tsuchida & Hasegawa, 2017: 901, pl. 190, fig. 5.

Alexania inazawai – Liu et al., 2023: 521, figs in text.

Material examined. Living individuals were observed in Xiajinwan [厦金湾], Huangcuo [黄厝] and Zengshan [曾山], all from Xiamen, Fujian Province, China. A female and a male shell specimens collected from Zengshan are in Li-Wen Lin's private collection.

Description. Shell fragile, pale reddish-brown. Spire small; body whorl increases rapidly, forming inflated shape. Aperture round, outer lip thin. Columellar lip white and relatively thick, covering umbilicus. Female shell larger and generally more globose than male. In Xiamen individuals, female shells 7–11 mm; male shells rarely over 5 mm. Operculum thin, horny.

Soft part light grey to light yellow with dark grey patterns; characterized by epipodium-like flaps extending from both sides of foot, completely covering shell (Fig. 4H).

Distribution. CHINA: Fujian (Xiamen); JAPAN (Sagami Bay, Seto Inland Sea and western Japan Sea).

Habitat. Alexania inazawai is found on reefs in intertidal zones where the orange-striped anemone D. lineata grows in high densities. In Zengshan, the reefs inhabited by A. inazawai are fully exposed at low tide and are about three-quarters submerged at high tide. Alexania inazawai is well adapted to temporary exposure to air as the tides ebb and flow.

In the same environment in Xiamen, many other common intertidal mollusks were observed coexisting with A. inazawai, including Mitrella bella (Reeve, 1859), Patelloida pygmaea (Dunker, 1860), Littoraria sinensis (Philippi, 1847), Planostrea pestigris (Hanley, 1846), Barbatia grayana Dunker, 1867, Neotrapezium sublaevigatum (Lamarck, 1819), Acanthochitona rubrolineata (Lischke, 1873), and Acanthopleura loochooana (Broderip & G. B. Sowerby I, 1829). 

Habit. The behaviour of A. inazawai aligns closely with that of typical epitoniid species
(excluding Janthina and Recluzia), maintaining an obligatory or general parasitic relationship with coelenterates such as sea anemones and corals (Gittenberger & Hoeksema, 2013; Kokshoorn et al., 2007).

Although we lack complete knowledge of the life history of A. inazawai due to the difficulty of observing its planktonic veliger stage, the diet and reproductive habits of adult snails are easily observed at low tide in intertidal zones. Alexania inazawai feeds exclusively on D. lineata, a common sea anemone species widely distributed in the Northern Hemisphere. The adult snails live on or near D. lineata and rarely move more than 5 cm away from their hosts. Most of the snails observed by the authors were attached to the sea anemones, feeding through their elongated proboscises. Other sea anemone species observed in the same habitat did not have any A. inazawai on them.

Usually, one female A. inazawai is accompanied by one to three males, all residing on the same anemone. Females lay eggs directly on the surface of the sea anemones or nearby. Around 20 to 30 egg capsules are clustered together on sea anemones or reefs, with both females and males remaining near the egg capsules.

 Discussion

The population of Alexania inazawai appears seasonally and somewhat randomly at various sites in Xiamen. Since 2021, the authors and others have conducted extensive field observations during different months, revealing that A. inazawai spawns in spring and summer, with few individuals observed on the reefs after September. In Zengshan, the population was concentrated in a relatively small reef area (Fig. 3). In 2022, approximately one-fiftieth of the observed D. lineata were consumed by A. inazawai, and this population completely disappeared by 2023 and 2024. The population density in Xiajinwan was low, with no more than five individuals recorded by the authors. In contrast, the population at Huangcuo in 2022 was thriving, with snails found attached to nearly every sea anemone observed, although this population also vanished by 2023. The density of D. lineata remains relatively constant at the same site during the same season each year, suggesting that the significant fluctuations in the population of A. inazawai may be attributed to variable local ocean currents, which affect the appearance of veligers. Reports on A. inazawai outside Japan are scarce (Liu et al., 2023); however, extensive fieldwork indicates that this species also has a wide distribution in China. Alexania inazawai was first recorded from Fujian and Taiwan in Southeast China (Liu et al., 2023; Liu Y., pers. comm.). Subsequent results have emerged from Qingdao and Yantai in Shandong Province, North China. Molecular analyses have confirmed that specimens from Shandong are conspecific with those from Japan (Han X., pers. comm.).

The adult habits of A. inazawai resemble those of traditionally known wentletrap snails, such as Epitonium spp. and Amaea spp., which are commonly found in intertidal zones and shallow continental shelves in Chinese waters (Zhang, 2008). However, Alexania inazawai exhibits distinct shell morphology, differing from the conical, tall-spired shells with developed ribs typical of common wentletrap snails. Instead, its shell morphology is more similar to that of Recluzia and Janthina, characterized by thin, globose shells, although it possesses a horny operculum, a feature typical of traditional wentletrap snails (Beu, 2017; Tsuchida & Hasegawa, 2017). Anatomical studies have shown that Recluzia and Janthina belong to the family Epitoniidae, supported by molecular analysis indicating they represent a specialized group of planktonic wentletrap snails that have late differentiated within the phylogenetic tree of Epitoniidae (Beu, 2017; Takano & Kano, 2014). As anticipated, Alexania inazawai is closely related to the clade of Recluzia and Janthina, which may explain its habits resembling those of traditional wentletrap snails and its shell morphology similar to Recluzia (Churchill et al., 2011; Beu, 2017). Other epitoniid genera, such as Globiscala (de Boury, 1909), Alora (H. Adams, 1861), and Iphitus (Jeffreys, 1883), also feature thin, globose shells (Tsuchida & Hasegawa, 2017). Thus, further research is necessary to clarify the relationships among these genera, the Recluzia-Janthina group, Alexania inazawai, and traditional wentletrap snails. 

Acknowledgements

Thanks go to Yi Liu [刘毅] and Xiao Han [韩骁] for sharing the information of Alexania inazawai.

References

Berry, S. S. (1910) [Review of] Report on a collection of shells from Peru, with a summary of littoral marine Mollusca of the Peruvian zoological province. By William Healey Dall, 1909, Proc. USNM, 37, pp. 147–294, pls. 20–28. The Nautilus, 23(10): 130–132.

Beu, A. G. (2017) Evolution of Janthina and Recluzia (Mollusca: Gastropoda: Epitoniidae). Records of the Australian Museum, 69(3): 119–222.

Churchill, C. K. C., Foighil, D. Ó, Strong, E. E. & Gittenberger, A. (2011) Females floated first in bubblerafting snails. Current Biology, 21(19): R802–R803.

Gittenberger, A. & Hoeksema, B. W. (2013) Habitat preferences of coral-associated wentletrap snails (Gastropoda: Epitoniidae). Contributions to Zoology, 82(1): 1–25.

Gittenberger, A., Kokshoorn, B. & Gittenberger, E. (2006) A molecular phylogeny of Epitoniidae (Mollusca: Gastropoda), focusing on the species associated with corals. In: Gittenberger, A. The evolutionary history of parasitic gastropods and their coral hosts. PhD Thesis, Leiden University, 2006, Chapter 8, pp. 207–213.

Habe, T. (1961) Descriptions of fifteen new species of Japanese shells. Venus, 21(4): 416–431. [波部忠重 (1961) 日本産貝類15新種. Venus, 21(4): 416–431.]

Kokshoorn, B., Goud, J., Gittenberger, E. & Gittenberger, A. (2007) Epitoniid parasites (Gastropoda, Caenogastropoda, Epitoniidae) and their host sea anemones (Cnidaria, Actiniaria, Ceriantharia) in the Spermonde archipelago, Sulawesi, Indonesia. Basteria, 71: 33–56.

Kuroda, T. (1943) On a new gastropod genus Habea. Venus, 13(1–4): 11–14. [黑田德米 (1943) 新属新種卷貝イナザハハベガヒに就いて. Venus, 13(1–4): 11–14.]

Tsuchida, E. & Hasegawa, K. (2017) Family Epitoniidae. In: Okutani, T. (ed.) Marine Mollusks in Japan, The Second Edition. Tokai University Press, Tokyo, pp. 889–901, pls 179–190. [土田英治, 長谷川和範 (2017) イトカケガイ科. In: 奥谷喬司 (ed.) (2017) 日本近海産貝類図鑑 (第2版). 東海大学出版部, 東京, pp. 889–901, pls 179–190.]

Liu, Y, Zhong, D.-D. & Guo, X. (2023) Intertidal fauna in southeastern of China, vol 1 & vol 2. Strait Publishing House, Fuzhou, 787 pp. [刘毅, 钟丹丹, 郭翔 (2023) 东南潮间带生物图鉴. 海峡书局, 福州, 787 pp]

Pfeffer, G. J. (1881) Die Clypeastriden des Hamburger Museums. Verhandlungen des Naturwissenschaftlichen Vereins in Hamburg, Neue Folge 5: 56–70.

Pilsbry, H. A. (1945) Stenacme floridana, an American member of the Amphibolacea. The Nautilus, 58(4): 112–116, pl. 5.

Robertson, R. & Habe, T. (1965) Alexania replaces Habea (Epitoniidae). The Nautilus, 78(4): 140–141.

Strand, E. (1928) Miscellanea nomenclatoria zoologica et palaeontologica. I–II. Archiv für Naturge-schichte, 92A(8): 30–75.

Strand, E. (1932) Miscellanea nomenclatorica zoologica et palaeontologica. III, IV. Folia Zoologica et Hydrobiologica. 4(1): 133–147; 4(2): 193–196.

Takano, T. & Kano, Y. (2014) Molecular phylogenetic investigations of the relationships of the echinoderm–parasite family Eulimidae within Hypsogastropoda (Mollusca). Molecular Phylogenetics and Evolution, 79: 258–269.

Tomlin, J. R. le B. (1926) On South African marine Mollusca, with descriptions of new species. Annals of the Natal Museum, 5(3): 283–301.

Zhang, S.-P. (2008) Seashells of China. The Ocean Publishing Company, Beijing, 383 pp. [张素萍 (2008) 中国海洋贝类图鉴. 海洋出版社, 北京, 383 pp.]