From Wood to Vent: First Cocculinid Limpet Associated with Hydrothermal Activity Discovered in the Weddell

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From Wood to Vent: First Cocculinid Limpet Associated with Hydrothermal Activity Discovered in the Weddell See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/340844206 From wood to vent: first cocculinid limpet associated with hydrothermal activity discovered in the Weddell Sea Article in Antarctic Science · April 2020 DOI: 10.1017/S095410202000022X CITATION READS 1 425 2 authors: Chong Chen Katrin Linse Japan Agency for Marine-Earth Science Technology British Antarctic Survey 111 PUBLICATIONS 833 CITATIONS 150 PUBLICATIONS 4,526 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: Deep-sea hydrothermal vents View project State of the Antarctic Ecosystem (AntEco) View project All content following this page was uploaded by Chong Chen on 22 April 2020. The user has requested enhancement of the downloaded file. Antarctic Science page 1 of 13 (2020) © Antarctic Science Ltd 2020 doi:10.1017/S095410202000022X From wood to vent: first cocculinid limpet associated with hydrothermal activity discovered in the Weddell Sea CHONG CHEN 1 and KATRIN LINSE 2 1X-STAR, Japan Agency for Marine-Earth Science and Technology (JAMSTEC),2–15 Natsushima-cho, Yokosuka, Kanagawa Prefecture 237-0061, Japan 2British Antarctic Survey, High Cross, Cambridge CB3 0ET, UK [email protected] This article is registered in ZooBank under: urn:lsid:zoobank.org:pub:296FAB17-E989-4921-9E2D-2F8518B2D05F Cocculina enigmadonta n. sp. is registered in ZooBank under: urn:lsid:zoobank.org:act:0F15867C-6B73-40E3-B0C9-762F8CFE5730 Abstract: Lush 'oases' of life seen in chemosynthetic ecosystems such as hot vents and cold seeps represent rare, localized exceptions to the generally oligotrophic deep ocean floor. Organic falls, best known from sunken wood and whale carcasses, are additional sources of such oases. Kemp Caldera (59°42'S, 28°20'W) in the Weddell Sea exhibits active hydrothermal vents and a natural whale fall in close proximity, where an undescribed cocculinid limpet was found living in both types of chemosynthetic habitats. This represents the first member of the gastropod order Cocculinida discovered from hot vents, and also the first record from the Southern Ocean. Here, we applied an integrative taxonomy framework incorporating traditional dissection, electron microscopy, genetic sequencing and 3D anatomical reconstruction through synchrotron computed tomography in order to characterize this species. Together, our data revealed an unusual member of the genus Cocculina with a highly modified radula for feeding on bacterial film, described herein as Cocculina enigmadonta n. sp. Its phylogenetically derived position within the largely wood-inhabiting Cocculina indicates that it probably evolved from an ancestor adapted to living on sunken wood, providing a compelling case of the 'stepping stone' evolutionary trajectory from organic falls to seeps and vents. Received 8 October 2019, accepted 7 March 2020 Key words: Cocculina, Cocculinidae, Cocculiniformia, mollusc, new species, South Sandwich Arc Introduction Among the limpets, pectinodontids in the genus Pectinodonta typically have gut contents predominantly Deprived of sunlight and photosynthetic primary composed of microscopic pieces of wood, while the gut production, the deep ocean floor is generally oligotrophic contents of cocculinids also include large amounts of with the exception of chemosynthesis-based ecosystems detritus and sediment, meaning that they probably feed driven by the Earth's own geochemistry, such as hot by grazing on the surface bacterial film (Marshall 1985). vents and cold seeps (Van Dover 2000). Microbial As organic falls decay, hydrogen sulphide is produced as chemosynthesis involves deriving energy from reducing a by-product, leading to a chemosynthetic ecosystem not compounds such as hydrogen sulphide, and it allows unlike vents or seeps (Smith & Baco 2003). As such, vents and seeps to host very high levels of animal organic falls have been hypothesized as evolutionary biomass comparable to those of coral reefs, with most 'stepping stones' towards endemism in vents and seeps species becoming specially adapted to these ecosystems (Smith et al. 2015), but with the exception of deep-sea and unable to live anywhere else (Van Dover 2000). bathymodioline mussels (Thubaut et al. 2013), little In addition, organic debris sinking from the sea surface evidence has been presented to show how such also generates localized, ephemeral 'oases' of nutrient transitions might have occurred. enrichment in the deep (Smith & Baco 2003). Primarily Recently,hydrothermal vents (Roterman et al. 2016) and comprising sunken wood and large mammal carcasses a natural whale fall (Amon et al. 2013) were discovered in typified by whales and collectively known as organic close proximity within Kemp Caldera (59°42'S, 28°20'W) falls, these habitats attract and are sources of food for in the Southern Ocean, < 100 km away from deeper numerous animals, including many typical foundation vents on segment E9 of the East Scotia Ridge (Rogers species such as the bone-eating zombie worm Osedax et al. 2012). Located just west of Kemp Seamount on the (Smith et al. 2015), the wood-boring bivalve Xylophaga volcanic South Sandwich Arc (Leat et al. 2016), Kemp and wood-ingesting limpets of the families Caldera is 900–1600 m in depth from sill to base with Pectinodontidae and Cocculinidae (Marshall 1985). white-smoker and diffuse-flow vents mainly concentrated 1 2 CHONG CHEN AND KATRIN LINSE Cocculinidae is a family of hermaphroditic, roughly symmetrical gastropods with limpet-like shells, currently placed in the superfamily Cocculinoidea (subclass Neomphaliones, order Cocculinida) (Bouchet et al. 2017). Previously known only from organic falls, primarily sunken woods (Marshall 1985, McLean & Harasewych 1995, Ardila & Harasewych 2005), 7 genera and over 40 species are currently recognized within the family (Zhang & Zhang 2018). Despite its near-global distribution, no records have been reported from the Southern Ocean. Cocculina, the nominal genus of Cocculinidae with over 20 species, is one of the most abundant invertebrates commonly associated with sunken wood, although two species have been described from cetacean carcasses, including Cocculina craigsmithi McLean 1992 from off California and Cocculina delphinicula Zhang & Zhang, 2018 from the East China Sea (McLean 1992, Zhang & Zhang 2018). Cocculinoidea was originally considered to form a monophyletic clade with Lepetelloidea, another superfamily of morphologically and ecologically similar limpets (Haszprunar 1987, 1988), but these superfamilies are now considered to be two separate, convergent radiations (Aktipis & Giribet 2012). Cocculinoids are more closely affiliated with neomphaloids, which are also restricted to chemosynthetic habitats but mainly radiated in hot vents (Warén & Bouchet 2001), while lepetelloids are placed within the subclass Vetigastropoda (Cunha & Giribet 2019). Fig. 1. Map of a. South Sandwich Arc showing the The Kemp Caldera cocculinid is the first member of the location of Kemp Caldera and b. the distribution of order Cocculinida from hydrothermal vent environments Cocculina enigmadonta n. sp. within Kemp Caldera (black and poses an opportunity to investigate a potential stars, hydrothermal vents; white star, natural whale fall). transition from organic falls to hot vents. It is also the first cocculinid from the Southern Ocean, although its locality around a central resurgent cone (Fig. 1). Although a subset is barely within the limit of the Southern Ocean (60°S), of taxa known from the East Scotia Ridge vents was present which is still debated. Here, we characterize the new at Kemp Caldera vents, some were absent (e.g. Kiwa yeti species morphologically and genetically, provide its formal crabs). In contrast, Kemp Caldera hosts large assemblages description and investigate its evolutionary history and of chemosymbiotic vesicomyid clams that are absent from adaptations to the hydrothermal vent environment. the East Scotia Ridge vents. Perhaps the most astonishing taxon presently known only from Kemp Caldera was an undescribed cocculinid limpet found in great abundance Materials and methods (Fig. 2) that represented a molluscan order that was Research cruises previously unknown from hot vents. The whale fall was also found near the resurgent cone in During expedition JC42 of RRS James Cook in 2010, Kemp Caldera, ∼250 m from the nearest hydrothermally cocculinid limpets were sampled using the suction active area (Amon et al. 2013). Of the species found on sampler or manipulator of the remotely operated vehicle the whale bones, which included typical whale fall taxa (ROV) Isis within Kemp Caldera on the volcanic South such as polychaete worms in the genera Osedax and Sandwich Arc from hydrothermal vents as well as from a Ophryotrocha (Amon et al. 2013), only two species were natural whale fall (Fig. 1) (Amon et al. 2013). In shared with the nearby vents: the vetigastropod limpet diffuse-flow areas of the hot vents, limpets were collected Lepetodrilus concentricus Linse, Roterman & Chen, from substrates including sulphide chimneys, sulphide 2019, known from both East Scotia Ridge and Kemp rubble, vesicomyid clam shells or whale bones (Fig. 2). Caldera vents (Linse et al. 2019), and an undescribed Upon recovery, specimens were preserved in pre-cooled cocculinid limpet (Amon et al. 2013). 96% ethanol. In 2019, expedition PS119 of RV HOT VENT COCCULINID LIMPET 3 Fig. 2. In situ photographs of Cocculina enigmadonta n. sp. in Kemp Caldera living on
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