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Geochemistry Drives the Allometric Growth of the Hydrothermal Vent Tubeworm Riftia Pachyptila (Annelida: Siboglinidae)

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Geochemistry Drives the Allometric Growth of the Hydrothermal Vent Tubeworm Riftia Pachyptila (Annelida: Siboglinidae) applyparastyle “fig//caption/p[1]” parastyle “FigCapt” Zoological Journal of the Linnean Society, 2021, 193, 281–294. With 3 figures. Geochemistry drives the allometric growth of the hydrothermal vent tubeworm Riftia pachyptila (Annelida: Siboglinidae) NADEZHDA RIMSKAYA-KORSAKOVA1,*, , DIEGO FONTANETO2, SERGEY GALKIN3, Downloaded from https://academic.oup.com/zoolinnean/article/193/1/281/6048373 by guest on 27 September 2021 VLADIMIR MALAKHOV1 and ALEJANDRO MARTÍNEZ2, 1Department of Invertebrate Zoology, Faculty of Biology, Lomonosov Moscow State University, 119234 Moscow, Russia 2Molecular Ecology Group (MEG), Water Research Institute (IRSA), National Research Council of Italy (CNR), 28922 Verbania Pallanza, Italy 3Laboratory of Ocean Benthic Fauna, Shirshov Institute of Oceanology of the Russian Academy of Science, 117218 Moscow, Russia Received 23 May 2020; revised 15 September 2020; accepted for publication 15 October 2020 The tubeworm Riftia pachyptila is a key primarily producer in hydrothermal vent communities due to the symbiosis with sulphur-oxidizing bacteria, which provide nourishment to the worm from sulphides, oxygen and carbon dioxide. These substances diffuse from the vent water into the bloodstream of the worm through their tentacular crowns, and then to the bacteria, hosted in a specialized organ of the worm, called a trophosome. The uptake rates of these substances depend on the surface/volume relationship of the tentacles. We here describe two morphotypes, ‘fat’ and ‘slim’, respectively, from the basalt sulphide-rich vents at 9 °N and 21 °N at the East Pacific Rise, and the highly sedimented, sulphide-poor vents at 27 °N in the Guaymas Basin. The ‘fat’ morphotype has a thicker body and tube, longer trunk and smaller tentacular crowns, whereas the ‘slim’ morphotype has shorter trunk, thinner body and tube, and presents longer tentacular crowns and has a higher number of tentacular lamellae. Given the dependence on sulphides for the growth of R. pachyptila, as well as high genetic connectivity of the worm’s populations along the studied localities, we suggest that such morphological differences are adaptive and selected to keep the sulphide uptake near to the optimum values for the symbionts. ‘Fat’ and ‘slim’ morphotypes are also found in the vestimentiferan Ridgeia piscesae in similar sulphide-rich and poor environments in the northern Pacific. ADDITIONAL KEYWORDS: East Pacific Rise – Guaymas Basin – lamellae – morphometrics – obturaculum – sulphides – tubes – tentacles – Vestimentifera. INTRODUCTION as the vestimentiferan annelid Riftia pachyptila Jones, 1981 (family Siboglinidae), are today amongst The discovery of the unique fauna of hydrothermal the best-known and most characteristic species of zones of the oceans was one of the most important hydrothermal vent communities (Rouse, 2001). Riftia events in marine biodiversity of recent decades pachyptila is gutless and it obtains nourishment (Corliss et al., 1979; Bright & Lallier, 2010; Hilário solely through a highly efficient symbiosis with et al., 2011). The submersible DSV Alvin found chemoautotrophic bacteria, allowing the worm to reach large, red, tube-dwelling worms rising up to several up to 3 m in length at growth rates of 160 cm per year meters above the seafloor around the vent smokers (Thiébaut et al., 2002). Populations of R. pachyptila (Corliss & Ballard, 1977; Ballard & Grassle, 1979; are key ecosystem engineers of hydrothermal vent Corliss et al., 1979). These worms, formally described communities, especially in the Pacific Ocean rifts (Scott & Fisher, 1995; Shank et al., 1998), where they reach *Corresponding author: E-mail: nadezdarkorsakova@gmail. a large biomass responsible for most of the primary com production in the ecosystem (Lutz et al., 1994; Thiébaut © 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, 193, 281–294 281 282 N. RIMSKAYA-KORSAKOVA ET AL. et al., 2002; Bright et al., 2010). For all these reasons, 1981, 1985; Karaseva et al., 2016; Goffredi et al., 2017). R. pachyptila has attracted extensive interdisciplinary Basalt-hosted vents exhibit higher hydrogen sulphide attention from ecologists, biochemists, microbiologists concentration (so called, high sulphide-flux), lower and physiologists (Malakhov & Galkin, 1998; Van concentrations of oxidized sulphur compounds and Dover, 2000; Gebruk, 2002; Bright et al., 2010). lower concentrations of dissolved organic carbon and Riftia pachyptila, together with other ammonium than sedimented hydrothermal sites (von vestimentiferans, has also been in the spotlight of Damm et al., 1985a, b; Childress & Beehler, 1988a; zoologists and systematists, provoking a heated debate Johnson et al., 1988a, b; Luther et al., 2001; Bogdanov, around its phylogenetic affinities, largely instigated by 2002; Le Bris et al., 2006). In contrast, sedimented its bizarre lifestyle and morphology. Unlike any other hydrothermal vents are restricted to some localities in Downloaded from https://academic.oup.com/zoolinnean/article/193/1/281/6048373 by guest on 27 September 2021 annelids, the body of vestimentiferans comprises of the Guaymas Basin with a high sedimentation rate. In four parts. The anterior obturaculum, often bearing fact, the Guaymas Basin is considered one of the few a conspicuous crowns of tentacles, followed by the key sites to study carbon release in a rift basin exposed vestimentum, the trunk (hosting the symbionts to high sedimentation rates (von Damm, 1985b; and the gonads) and the opisthosoma. Like other Campbell et al., 1988; Dean, 2006; Geilert et al. 2018). hydrothermal vestimentiferans of the subfamily Hydrothermal fluids in these areas are characterized Tevniinae, Riftia pachyptila uptakes reduced sulphur, by slow rates of diffuse flow of sulphides (so called, oxygen and carbon dioxide from the water column low sulphide-flux), a consequence of the injection using the crown of tentacles on the obturaculum of the fluid from the vent through the thick layer of (Hilário et al., 2011). These substances are then organic-rich sediment. The sediments partially cover transported by the vascular system inside the body the colonies of R. pachyptila growing in these vents, trunk, where the chemoautotrophic symbiotic bacteria which appear to contain lower amounts of elemental oxidize the sulphur and fix the carbon dioxide, directly sulphur in their trophosomes than those recovered feeding the host (Cavanaugh et al., 1981; Felbeck, from basalt-hosted vents (von Damm et al., 1985a, b; 1981). In contrast, vestimentiferans from hydrocarbon Campbell et al., 1988; Gamo, 1995; von Damm, 2000; seeps and shipwrecks, Lamellibrachiinae and Bogdanov, 2002; Shock & Canovas, 2010; Robidart Escarpiinae, uptake sulphides through the epidermis et al., 2011). Such ecological differences between of the entire body, even if the process is more efficient vents, mostly reflected by the different availability through the so-called ‘roots’, which are structures in of sulphides, might favour a differential development the posterior end of the body buried into the substrate of the body parts related to sulphide uptake, thereby (Scott & Fisher, 1995; Julian et al., 1999; Hilário optimizing the feeding of the symbionts. It has been et al., 2011). The two different strategies of sulphide shown that, regardless of the physiological plasticity absorption are reflected in the proportions of body of its bacterial symbionts (Robidart et al., 2011; parts: the obturaculum is proportionally shorter in Zimmermann et al., 2014), Riftia pachyptila buffers Lamellibrachiinae and Escarpiinae than in Tevniinae, the environmental changes in sulphide concentrations where it is used to absorb sulphides (Malakhov & to keep bacteria growing at an optimal rate (Childress Galkin, 1998; Andersen et al., 2002; Karaseva et al., et al., 1984; Goffredi et al., 1997; Zal et al., 1997; Gru 2016, 2019). Such differences might have been selected et al., 1998; Van Dover, 2000; Girguis & Childress, to optimize the diffusion of chemicals into the body 2006). Thus, different availability of sulphides in the of the worms, since long and thin structures have a environment could lead to different morphological higher surface/volume ratio, which makes the diffusion adaptations to maintain a homogeneous and stable rate higher. However, testing this idea across different environment for the symbionts. Interestingly, species of siboglinids is confounded by the effects of notwithstanding the potential ecological differences phylogeny and the different habitat preferences by and the large geographic distances between types of different members of the family. Nevertheless, most of vents, high genetic connectivity has been found across these factors can be controlled when individuals of the all known populations of Riftia pachyptila (Black et al., same species are available for comparison, especially 1994; Hurtado et al., 2004). if they occur in replicated habitats differing only in The goal of our study is to describe how the growth few ecological parameters, such as the availability of patterns of the various body parts in Riftia pachyptila sulphides. change with age and between sedimented and basalt- Riftia pachyptila is found in the Pacific Ocean, in hosted hydrothermal vents. Our first hypothesis is either basalt-hosted hydrothermal vents, widespread that all body parts increase with body length but at along the East Pacific Rise (EPR) and the Galapagos different rates. We expected a positive correlation Rift, or in sediment-rich
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