Is It Sex in Chains? Potential Mating Stacks in Deep-Sea Hydrothermal Vent Snails

Plankton Benthos Res 13(1): 25–27, 2018 Plankton & Benthos Research © The Japanese Association of Benthology Note Is it sex in chains? Potential mating stacks in deep-sea hydrothermal vent snails 1, 2 2 CHONG CHEN *, LEIGH MARSH & JONATHAN T. COPLEY 1 Department of Subsurface Geobiological Analysis and Research, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2–15 Natsushima-cho, Yokosuka, Kanagawa 237–0061, Japan 2 Ocean and Earth Science, University of Southampton, National Oceanography Centre Southampton, European Way, Southampton SO14 3ZH, United Kingdom Received 31 October 2017; Accepted 18 November 2017 Responsible Editor: Shigeaki Kojima Abstract: “Mating stacks” have been widely documented in calyptraeid slipper limpets, which are protandric and exhibit sequential hermaphroditism. Gigantopelta is a genus of peltospirid snails endemic to deep-sea hydrothermal vents containing two species, one distributed on the East Scotia Ridge in the Southern Ocean and another on the Southwest Indian Ridge in the Indian Ocean. Here, we report the observation that both species form extensive (often >15 individuals) “snail chains”. These chains are potentially analogous to ‘mating stacks’ of calyptraeids, or alternatively, maybe a behaviour to facilitate spermatophore transfer. Both Gigantopelta species apparently have separate sexes and are sexually mature at a small size. However, it remains unclear whether they undergo sex change during their life. Key words: Chemosynthetic ecosystems, Gastropoda, Hermaphroditism, Mollusca, Neomphalina Deep-sea hydrothermal vents are challenging environments 37°47.03′S 49°38.97′E) by the ROV Kiel 6000 during RRS for animals because of various environmental stresses, such James Cook voyage JC67 (Copley et al. 2016). About a dozen as increased temperature, heavy metal concentrations, and de- chains were observed for each species in their natural environ- creased oxygen concentration, when compared with the sur- ment. No samples of the chain series were obtained. rounding deep-sea floor (Van Dover 2000). The life history These chains are reminiscent of stacking “snail chains” of vent-endemic animals has been studied extensively in the widely documented in the protandric slipper limpets belong- past few decades, but much remains to be learned about the ing to Calyptraeidae, such as Crepidula fornicata (Linnaeus, reproductive ecology of newly discovered species. The recently 1758) and Bostrycapulus odites Collin, 2005 (Cledón et al. described genus Gigantopelta (Mollusca: Gastropoda: Neom- 2015). In those species, mature female limpets are at the bot- phalina) is currently composed of two species endemic to abys- tom of the stack, with copulatory young males above them sal hydrothermal vents: Gigantopelta chessoia Chen et al., 2015 that transform to females in their later life stages; the chain from the Southern Ocean and Gigantopelta aegis Chen et al., grows with the settlement of successive young males. Al- 2015 from the Indian Ocean (Fig. 1; Chen et al., 2015a). These though Gigantopelta spp. apparently have separate sexes and are very large peltospirid snails that rely on sulfur-oxidizing are already sexually mature at a small size of ca. 3 mm shell endosymbionts for nutrition (Heywood et al. 2017), with the length (Reid et al. 2016, Chen et al. 2017), no further details shell length of adults averaging around 35 mm. are available as to whether they undergo any sex change dur- Here, we report that both species were observed to form ing their lives. In addition, no differences in size were ob- peculiar long chains, hanging upside-down from hydrother- served across the chain. Matabos & Thiebaut (2010) studied mal outcrops (Fig. 2). The chains were variable in length, and the reproductive biology of three peltospirids belonging to ranged from as few as four individuals to more than 15 indi- genera Nodopelta and Peltospira, but they could not deter- viduals. This observation was made for G. chessoia at Segment mine the minimum maturity size because of the lack of small E2, East Scotia Ridge (depth 2395 m; 60°03.00′S 29°57.66′W) animals among their specimens. They noted, however, that using the remotely operated vehicle (ROV) Isis on-board RRS females of Nodopelta spp. began reproducing at around half James Cook voyage JC42 (Rogers et al. 2012) and for G. ae- the maximum size for the species. gis at Longqi Field, Southwest Indian Ridge (depth 2770 m; The scaly-foot gastropod Chrysomallon squamiferum Chen et al., 2015 is the only other peltospirid that certainly relies on * Corresponding author: Chong Chen; E-mail, [email protected] endosymbiont for nutrition (Nakagawa et al. 2014) and its size 26 C. CHEN et al. Fig. 1. Gigantopelta spp. Left: Gigantopelta chessoia (shell length 45.9 mm) from E2 segment, East Scotia Ridge, ROV Isis Dive 189, 2012/xii/12. Right: Gigantopelta aegis (shell length 40.2 mm) from Longqi Vent Field, Southwest Indian Ridge, ROV Kiel 6000 Dive 142, 2011/xi/29. Fig. 2. Gigantopelta “snail chains”. The left image shows Gigantopelta chessoia chains at the “Ivory Tower” chimney, Segment E2, East Scotia Ridge, Southern Ocean (depth 2395 m; 60°03.00′S 29°57.66′W) (Rogers et al. 2012), the right image shows Gigantopelta aegis at the “Tiamat” chimney, Longqi Vent Field, Southwest Indian Ridge (depth 2770 m; 37°47.03′S 49°38.97′E) (Copley et al. 2016). The arrow heads indicate snail chains hanging from the outcrop. Is it sex in chains? 27 is similar to that of Gigantopelta; however, it is a simultaneous References hermaphrodite (Chen et al. 2015b). Although C. squamiferum Chen C, Linse K, Roterman CN, Copley JT, Rogers AD (2015a) A new co-occurred with G. aegis at the same site (Longqi Vent Field) genus of large hydrothermal vent-endemic gastropod (Neomphalina: on the Southwest Indian Ridge, it was not observed to form Peltospiridae). Zool J Linn Soc 175: 319–335. “snail chains”. Except for C. squamiferum, all known pelto- Chen C, Copley JT, Linse K, Rogers AD, Sigwart J (2015b) The heart of a dragon: 3D anatomical reconstruction of the ‘scaly-foot gastropod’ spirids are gonochoristic (Fretter 1989, Warén et al. 2003, Chen (Mollusca: Gastropoda: Neomphalina) reveals its extraordinary circu- et al. 2015b). All members of Peltospiridae lack a penis, but it latory system. Front Zool 12: 13. doi: 10.1186/ s12983-015-0105-1 has been suggested that they exhibit internal fertilisation from Chen C, Uematsu K, Linse K, Sigwart JD (2017) By more ways than their anatomy (Fretter 1989). This was confirmed on the ba- one: Rapid convergence in adaptations to hydrothermal vents shown sis of the sperm ultrastructure of Rhynchopelta concentrica by 3D anatomical reconstruction of Gigantopelta (Mollusca: Neom- phalina). BMC Evol Biol 17: 62. doi: 10.1186/s12862-017-0917-z McLean, 1989, as its spermatozoa were found to be filiform Cledón M, Nuñez JD, Ocampo EH, Sigwart JD (2015) Sexual traits plas- introsperm (Hodgson et al. 2009). Fertilization in this fam- ticity of the potentially invasive limpet Bostrycapulus odites (Gastrop- ily is known to occur by transfer of spermatophore packets, oda: Calyptraeidae) within its natural distribution in South America. which has been confirmed in Pachydermia laevis Warén & Mar Ecol. 37: 433–441. doi: 10.1111/maec.12329 Bouchet, 1989 (Warén et al. 2003) and C. squamiferum (Chen Copley JT, Marsh L, Glover AG, Huhnerbach V, Nye VE, Reid WDK, Sweeting CJ, Wigham BD, Wiklund H (2016) Ecology and biogeogra- et al. 2015b). It is possible that forming snail chains facilitates phy of megafauna and macrofauna at the first known deep-sea hydro- transfer of spermatophores in aphallic Gigantopelta gastro- thermal vents on the ultraslow-spreading Southwest Indian Ridge. Sci pods, even if they do not undergo sex change. Rep 6: 38158. doi: 10.1038/srep39158 The greater majority of Gigantopelta spp. snails were not Fretter V (1989) The anatomy of some new archaeogastropod limpets forming ‘snail chains’ but instead formed clusters around dif- (Superfamily Peltospiracea) from hydrothermal vents. J Zool 218: 123–169. doi:10.1111/j.1469-7998.1989.tb02530.x fuse flow venting (Fig. 2; Marsh et al. 2012). A clear benefit Heywood JL, Chen C, Pearce DA, Linse K (2017) Bacterial communi- for this behaviour is that the holobiont snails need to access ties associated with the Southern Ocean vent gastropod, Gigantopelta the hydrothermal fluid containing hydrogen sulfide required chessoia: indication of intergenerational, horizontal symbiont transfer. by their thioautotrophic endosymbionts to carry out chemo- Polar Biol. 40: 2335–2342. doi: 10.1007/s00300-017-2148-6 synthesis (Chen et al. 2017). However, this behaviour may Hodgson AN, Eckelbarger KJ, Young CM (2009) Sperm ultrastructure and spermatogenesis in the hydrothermal vent gastropod Rhynchopel- also have a reproductive aspect to it. The Antarctic limpet ta concentrica (Peltospiridae). J Moll Stud 75: 159–165. doi: 10.1093/ Nacella concinna (Strebel, 1908), for example, is known to mollus/eyp014 form temporary “mating stacks” prior to spawning to increase Marsh L, Copley JT, Huvenne VAI, Linse K, Reid WDK, Rogers AD, fertilisation success (Picken & Allan 1983). Although Gigan- Sweeting CJ, Tyler PA (2012) Microdistribution of faunal assemblages topelta spp. are internal fertilisers, clustering may facilitate at deep-sea hydrothermal vents in the Southern Ocean. PLOS ONE 7: e48348. doi: 10.1371/journal.pone.0048348 copulation or spermatophore transfer, and formation of chains Matabos M, Thiebaut E (2010) Reproductive biology of

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