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

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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 vents, geographically restricted between each body part and the total length of the to the Guaymas Basin in the California Gulf (Jones, animals, with different slopes of the relationship

© 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, 193, 281–294 GROWTH OF THE TUBEWORM RIFTIA PACHYPTILA 283 depending on each body part. Due to the ephemeral similar protocols, thereby reducing possible bias due to nature of hydrothermal vents, a life history that different rates of post-mortem contraction. involves fast growth to reproductive size has obvious Direct measurements were taken from each advantages to fauna strictly dependent on the vent individual (Fig. 2). Body width was measured as the effluent as energy sources for their symbionts (Fustec diameter of the animal at the mid-vestimentum, et al., 1987; Tunnicliffe et al., 1990; Lutz et al., 1994; because this body part hardly changes due to Fisher, 1996; Tunnicliffe et al., 1997; Thiébaut et al., muscular contractions. The length of the obturaculum 2002). These differences might be higher in the worms was measured as the distance between the anterior from the basalt hosted vents and they are expressed end of the animal and the anterior margin of the particularly higher in the animal's trunk, which ventral ciliary field; the length of the vestimentum Downloaded from https://academic.oup.com/zoolinnean/article/193/1/281/6048373 by guest on 27 September 2021 contains the gonads and the trophosome. In contrast, was measured from this point to the posterior margin we did not expect differences in the opisthosoma, whose of the ventral ciliary field (Fig. 2A). Relative lengths function is limited to attachment of the worms into the were calculated as the ratio of each body part to the tube. Then, assuming that the worms tend to keep the total body length. Adults were defined by the presence uptake of nutrients at nearly optimal value for their of developed sexual structures: males were identified symbionts, our second hypothesis is that the body parts by the presence of genital grooves, which are absent in directly related to the nutrient input into the body, will females (Fig. 2B). be better developed in those worms collected from the sulphide-rich vents (Urcuyo et al., 2003; Tunnicliffe et al., 2014). The number of tentacle lamellae could Statistical analyses be affected by the diffuse flow rate (Andersen et al., Our goal is to describe the growth pattern of Riftia 2002; Gantsevich et al., 2019; Karaseva et al., 2019), pachyptila tubeworms, and how this pattern changes while the diameter of the tube opening and the across hydrothermal vent areas with different diameter of the midpart of the vestimentum could be environmental conditions. We first investigated the bigger when there is higher supply of energy sources effect of body size and environmental differences on for the symbionts, allowing for a faster growth of the the size and proportions of the different body parts, body part hosting symbiotic bacteria (Lutz et al., 1994; and afterwards on selected continuous trophic traits Robidart et al., 2011). Our overall hypothesis is that, related to sulphide uptake. The three sampling sites despite the genetic connectivity between areas, the have different availability of energy sources, with growth of R. pachyptila is strongly influenced by the 9 °N EPR and 21 °N EPR considered rich in hydrogen nutrient availability between basalt- and sediment- sulphide in comparison to 27 °N EPR, which is poor hosted hydrothermal vents highlighting the adaptive in this energy source (Robidart et al., 2011). Thus, we plasticity of this species to different ecological would expect the first two sites to be more similar conditions. between each other than to the latter in the body parts related to intake of nutrients. We acknowledge that with only three sampling sites, the power of MATERIAL AND METHODS the inference from the analyses is low, but we aim to provide a baseline for hypotheses to be tested on more Sample collection and measurements populations, currently unavailable for these worms Vestimentiferan tubeworms Riftia pachyptila were due to the difficulty in obtaining them. collected during the dives of DSRV “Pisces” and All measurements of body length, the length and “Mir” from three hydrothermal areas in the East width of different body parts and trophic traits, and Pacific Rift (EPR): 9 °N EPR, 21 °N EPR and the the count data were transformed into logarithms, in Guaymas Basin in the Gulf of California (27 °N EPR) order to account for the biological effect of size and (Fig. 1). A total of 241 individuals of R. pachyptila counts (Packard, 2014). Correlations between pairs were measured, including 210 complete and 31 partial of variables were calculated using the Pearson’s specimens (Table 1). Only complete specimens were correlation coefficient. All analyses were performed in included in the analyses. Our dataset includes the whole R 3.6.3. (R Core Team, 2020). The assumptions of the collection of the P. P. Shirshov Institute of Oceanology statistical tests were controlled using the R package of Russian Academy of Science and of the Department performance v.0.4.6 (Lüdecke et al., 2020). of Invertebrate Zoology of Lomonosov Moscow State University. These two institutions together hold one of the largest collections of R. pachyptila material in Allometric growth the world, gathered from oceanographic expeditions We started with a general analysis on total body between 1986 and 2003. All investigated animals length as a function of differences between the were fixed using 4% formaldehyde solution following three sampling stations, accounting for obvious

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Figure 1. A, map showing the position of the vents investigated in this study. For details on each sampling stations see Table 1. B, C, the hydrothermal landscapes in the sediment-hosted hydrothermal vents on the Guaymas Basin (27 °N EPR). D–F, basalt-hosted hydrothermal vents in the 21 °N EPR and 9 °N EPR fields. Photo taken using DSRV “Mir” camera. differences between juveniles and adults, as well to host the maturing oocytes or a longer crown of as potential differences between adult males and tentacles in order to catch the spermatophores in females (i.e. females might have a larger trunk the current of the diffuse flow). We did so by using

Table 1. Sampling locations and number of studied individuals of Riftia pachyptila from three hydrothermal vent fields located along the East Pacific Rise (EPR) during cruises of Akademik Mstislav Keldysh (AMK). A dash means that the coordinates were not identified at the time of collection. Coordinates are in WGS84 reference system. The number of complete individuals is written in parentheses

Vent field Cruise/station/ deep-sea Date Latitude, Longitude Depth (m) Individuals submersible vessel

27 °N EPR 12/АМК-1519/Pisces VII 16/10/1986 N 27 °02.45’ 1990 41(37) W 111 °22.80’ 12/АМК-1575/Pisces VII 26/10/1986 N 27 °00.70’ 1999 13(12) Downloaded from https://academic.oup.com/zoolinnean/article/193/1/281/6048373 by guest on 27 September 2021 W 111 °24.00’ 49/АМК-4697/Mir 1 16/10/2003 - - 16(15) - 49/АМК-4701/Mir 2 17/10/2003 - - 14(11) - 49/АМК-4710/Mir 2 19/10/2003 - - 16(10) 49/ АМК-4714/ Mir 2 20/10/2003 N 27 °00.47’ 2001 55(45) W 111 °24.57’ 21 °N EPR 22/ АМК-2368/ Mir 1 17–18/10/1990 N 20 °50.40’ 2640 8(7) W 109 °05.73’ 49/ АМК-4679/ Mir 1 09–10/10/2003 N 20 °19.86’ 2997 57(54) W 109 °06.20’ 9 °N EPR 49/ АМК-4623/ Mir 1 05/09/2003 N 09 °50.52’ 2524 17(15) W 104 °17.52’ 49/ АМК-4655/ Mir 2 21/09/2003 - - 4(4)

an ANalysis Of VAriance (ANOVA) test with body gonads and the trophosome with symbiotic bacteria, length as a response-dependent variable, and we expect that the trunk should be the body part with sampling site (three levels), age (two levels: juvenile the steepest slope of the relation. or adult) and gender (two levels for adults: male or We tested these hypotheses in two steps. First, we female), as explanatory independent variables. We used a Multivarite ANalysis Of VAriance (MANOVA) used this first analysis to decide which confounding test to check whether all body parts for adults are factors would affect the following analyses. Given positively influenced by total body length, while that no differences were found in body length controlling for potential differences between the between genders (see Results), we did not consider three sampling sites as an additional explanatory this variable in the following analyses; differences variable. After this overall assessment, we analysed between juveniles and adults were significant the relationship between each body part and the total (see results) and we considered only adults in the length separately, using linear regression models following analyses. Sampling site (three levels) (LM). The output of the results is presented as type-II was included in all analyses, because we want to analysis-of-variance tables for model objects obtained explicitly test its effect on body length. with the R package car v.3.0.7 (Fox & Weisberg, 2018). We assessed the relationships between the length For the cases of significant effects of differences of the four body parts and the total length of the between sites, we performed a post-hoc Tukey body. A differential growth of the body parts in Riftia Honestly Significant Difference (HSD) test to identify pachyptila has been suggested (Andersen et al., 2002; significant differences between pairs of sites, using the Thiébaut et al., 2002), but their rate of increase, and if R package multcomp v.1.4.13 (Hothorn et al., 2008). some parts may even diminish in their relative length, After assessing the relationship between the are unknown. Our hypothesis is that all four body absolute lengths of each body part with total body parts, namely opisthosoma, trunk, vestimentum and length, we explored the relationship between their obturaculum (Fig. 2A–F), would grow but each of them relative proportions. Even if all body parts grow, their with different rates, depending on the environment. In relative growth may be different, and thus their ratio addition, given that the trunk is the body part with the with total length could increase or even diminish at

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Figure 2. Morphology of the vestimentiferan tubeworms Riftia pachyptila. A, drawings of a female in different positions. Body parts measured in this study: obturaculum (ob) comprising the obturacular lobes (obl) and tentacular lamellae (tl), vestimentum (vm), trunk (tr), and opisthosoma (op). B, male individual distinguished by genital grooves (gg). C, the unique finding of Riftia individuals from the Guaymas Basin with split lobes of the ventral posterior vestimental fold (pvm). D–F, individuals with different body proportions: D, juvenile female; E, F, adult females. different rates. We used the same set of analyses also Development of the trophic traits for relative proportions: MANOVA for the overall We used MANOVA to check the overall effect of relationship and then linear models for each body differences between sampling sites on trophic traits part, including sampling site as a covariate, followed (number of tentacle lamellae, diameter of tube opening by Tukey HSD when needed. and diameter of the midpart of the vestimentum)

© 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, 193, 281–294 GROWTH OF THE TUBEWORM RIFTIA PACHYPTILA 287 and then separated a linear model for each trait, with split lobes of the ventral posterior vestimental fold always including sampling site and body length as (Fig. 2C). explanatory variables, followed by Tukey HSD, when No differences are found in body length among needed. sampling sites (ANOVA: F = 1.3, P = 0.261) and between sexes (F = 2.8, P = 0.097). Due to significant differences in body size between adults and juveniles (ANOVA: RESULTS F = 217.5; P < 0.001), only adults are considered in the In total, 210 complete worms were measured, with body following analyses. length spanning from 0.4 to 100.7 cm. The average body The lengths of the four body parts in adults are length for juveniles was 2.4 cm (range: 0.4–4.2 cm) and significantly related to the total length of the animal Downloaded from https://academic.oup.com/zoolinnean/article/193/1/281/6048373 by guest on 27 September 2021 for adults was 25.7 cm (range: 1.32–100.70 cm). Among (MANOVA: Pillai’s trace = 0.99, F = 8548.4, P < 0.0001) the large number of studied specimens, we found four and differ significantly among sites (Pillai’s trace = 0.22, Riftia Jones, 1981 tubeworms from the Guaymas Basin F = 5.1, P < 0.0001). Total body length is a significant

Table 2. Results of the linear model on the effect of sampling locality and body length on body parts and on their relative proportions. Results are reported as type-II analysis-of-variance tables. Significant effects are marked with bold P-values

Sum of Squares Degrees of freedom F-value P-value

Obturaculum Body length 105.824 1 1582.4 < 0.0001 Locality 1.584 2 1582.4 < 0.0001 Residuals 11.302 169 Vestimentum Body 94.606 1 1674.5 < 0.0001 Locality 0.228 2 2.02 0.1358 Residuals 9.605 170 Trunk Body 150.941 1 2831.5 < 0.0001 Locality 1.014 2 9.5 < 0.0001 Residuals 9.062 170 Opisthosoma Body 35.463 1 705.0 < 0.0001 Locality 0.197 2 2.0 0.1446 Residuals 8.552 170 Obturaculum / Body Body length 0.03908 1 6.2 0.01389 Locality 0.17938 2 14.2 < 0.0001 Residuals 1.06855 169 Vestimentum/Body Body 0.024829 1 30.9 < 0.0001 Locality 0.00273 2 1.7 0.1855 Residuals 0.136393 170 Trunk/Body Body length 0.43553 1 51.2 < 0.0001 Locality 0.18698 2 11.0 < 0.0001 Residuals 1.44744 170 Opisthosoma / Body Body length 0.099637 1 426.8 < 0.0001 Locality 0.001233 2 2.6 0.0742 Residuals 0.039689 170

© 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, 193, 281–294 288 N. RIMSKAYA-KORSAKOVA ET AL. and positive predictor for the length of all body parts The overall effect of body length (Pillai’s trace = 0.95, (Table 2). The length of the trunk exhibits the highest F = 431.3, P < 0.0001) and sampling site (MANOVA: slope and the only one above 1. Sampling site affects the Pillai’s trace = 0.36, F = 5.2, P < 0.0001) is significant obturaculum (in 9 °N EPR and 21 °N EPR shorter than for the number of tentacular lamellae, diameter of in 27 °N EPR), the vestimentum (in 21 °N EPR longer the tube opening and diameter of the midpoint of than in 27 °N EPR) and the trunk (in 21 °N EPR longer the vestimentum. All these traits significantly differ than in 27 °N EPR), but not the opisthosoma (Tables 2, across sites (Table 4). The number of tentacle lamellae 3). The lengths of all body parts were highly correlated is significantly smaller in 27 °N EPR than in 9 °N among each other (Pearson’s r correlation = 0.90–0.94). EPR and in 21 °N EPR, while the diameters of the The relative length of the body parts was related to vestimentum and of the tube opening are larger in 9 °N Downloaded from https://academic.oup.com/zoolinnean/article/193/1/281/6048373 by guest on 27 September 2021 body length (MANOVA: Pillai’s trace = 0.79, F = 185.5, EPR and 21 °N EPR than in 27 °N EPR, regardless of P < 0.0001) and sampling site (Pillai’s trace = 0.14, differences in body length of the animal (Table 5). The F = 3.8, P < 0.0001). In detail, the relative length is selected trophic traits are highly correlated among unrelated to the body length for the obturaculum, each other (Pearson’s r correlation = 0.86–0.98). marginally negatively related for the vestimentum, significantly positively related for the trunk and significantly negatively related for the opisthosoma DISCUSSION (Table 2). The effect of sampling site is significant for the relative proportion of the obturaculum (in 21 °N Our analyses on 210 complete individuals of Riftia EPR shorter than in 27 °N EPR), vestimentum (in pachyptila collected in three vent areas along the 21 °N EPR longer than in 27 °N EPR) and trunk (in East Pacific support our hypothesis that the growth of 9 °N EPR and in 21 °N EPR longer than in 27 °N EPR), R. pachyptila is strongly influenced by the differences but not for the relative proportion of the opisthosoma in availability of energy sources for symbionts between (Table 2, 3). Contrary to the high correlation between basalt- and sediment-hosted hydrothermal vents. absolute measurements of the four body parts, the First, we found that all body parts increase with body correlations between their proportions are lower length, but that these rates are higher for the trunk and (Pearson’s r correlation = 0.02–0.81). minimal at the opisthosoma (Fig. 3A). Furthermore, the differences in growth rate are influenced by the habitat conditions: comparing animals of the same Table 3. Results of the Tukey Honest Significant size, they are thicker and have a longer trunk from Difference test across sites. 9 °N EPR and 21 °N ERP the basalt-hosted hydrothermal vents than from the correspond to the sulphide-rich localities; 27 °N EPR sediment-hosted vents, where they have a longer represents the sediment-hosted sites at Guaymas Basin. obturaculum carrying more tentacle lamellae (Fig. 3B). Significant differences are marked with bold P-values

T-value P-value Allometric growth As expected, the four body parts of R. pachyptila, namely Obturaculum obturaculum, vestimentum, trunk and opisthosoma, 9 °N EPR–27 °N EPR –2.5 0.0337 are allometrically related to the total body length 21 °N EPR–27 °N EPR –4.6 < 0.0001 (Fig. 3A). However, our analyses show that their rate 21 °N EPR–9 °N EPR –0.5 0.8468 of growth varies: the trunk grows proportionally more than the other parts, while the proportional length of Trunk the opisthosoma remains constant or even decreases 9 °N EPR–27 °N EPR 1.9 0.15 as R. pachyptila grows. Therefore, the decrease in the 21 °N EPR–27 °N EPR 4.3 < 0.0001 growth rate of other body parts is a consequence of the 21 °N EPR–9 °N EPR 0.9 0.631 predominant growth of the trunk. These changes are Obturaculum / Body related to the ontogeny of the worm. The trunk hosts 9 °N EPR–27 °N EPR –2.7 0.0193 the trophosome and the reproductive system, so it 21 °N EPR–27 °N EPR –5.1 < 0.0001 grows more in mature animals (Felbeck & Childress, 1988; Julian et al., 1999; Urcuyo et al., 2003; Tunnicliffe 21 °N EPR–9 °N EPR –0.6 0.7984 et al., 2014). In contrast, while the opisthosoma is Trunk / Body important for the settlement and anchoring of the 9 °N EPR–27 °N EPR 2.3 0.0594 young worm, it only secures the animal in the tube in 21 °N EPR–27 °N EPR 4.5 < 0.0001 adults. An increase in the relative size of the trunk has 21 °N EPR–9 °N EPR 0.7 0.7823 been shown in the small non-dominant vestimentiferan Oasisia alvinae Jones, 1985 (Gantsevich et al., 2019;

Table 4. Results of the linear model on the effect of sampling locality and body length on trophic related traits. Results are reported as type-II analysis-of-variance tables. Significant effects are marked with bold P-values

Sum of Squares Degrees of freedom F-value P-value

Number of tentacular lamellae Body length 63.588 1 939.4 < 0.0001 Locality 0.602 2 4.4 0.01296 Residuals 13.2 195

Diameter of the vestimentum Downloaded from https://academic.oup.com/zoolinnean/article/193/1/281/6048373 by guest on 27 September 2021 Body length 196.56 1 2293.9 < 0.0001 Locality 6.683 2 39.0 < 0.0001 Residuals 17.309 202 Diameter of the tube opening Body length 132.34 1 1778.2 < 0.0001 Locality 2.995 2 20.1 < 0.0001 Residuals 8.187 110

Table 5. Results of the Tukey Honest Significant Pacific Rise (Fig. 3B). The ‘fat’ morphotype has a Difference test on the difference of trophic related traits thicker body (vestimentum was measured) and wider between sites (from the test reported in Table 4). 9 °N EPR tube opening, longer trunk and shorter tentacular and 21 °N ERP correspond to the sulphide-rich localities; crowns and smaller number of lamellae, whereas 27 °N EPR represents the sediment-hosted sites at the ‘slim’ morphotype has shorter trunk, thinner Guaymas Basin. Significant differences are marked with body (vestimentum was measured) and narrow tube bold P-values opening, and presents longer tentacular crowns and a higher number of tentacular lamellae. Since these T-value P-value populations belong to the same species and maintain significant gene flow between populations (Black

Tentacular lamellae et al., 1994; Shank et al., 1998), we can speculate that 9 °N EPR–27 °N EPR –0.1 0.999 the morphological differences between the two areas 21 °N EPR–27 °N EPR –2.9 0.010 are related to different availability of sulphides, the 21 °N EPR–9 °N EPR –1.6 0.225 main energy source for symbionts of R. pachyptila. Diameter of vestimentum Animals from the sulphide-rich vents at the East 9 °N EPR–27 °N EPR 4.7 < 0.0001 Pacific Rise (9 °N EPR and 21 °N EPR) have indeed 21 °N EPR–27 °N EPR 8.3 < 0.0001 a longer vestimentum, longer trunk and shorter 21 °N EPR–9 °N EPR 0.4 0.901 obturaculum than worms from the sedimented sulphide-poor Guaymas Basin (27 °N EPR). Notably, Diameter of tube opening the ‘slim’ animals from the Guaymas Basin not only 9 °N EPR–27 °N EPR 5.1 < 0.0001 have a longer obturaculum, but also a higher number 21 °N EPR–27 °N EPR 4.2 0.0001 of the tentacular lamellae than the ‘fat’ animals from 21 °N EPR–9 °N EPR –1.1 0.486 the basalt-hosted vents region at the East Pacific Rise, structures used to absorb sulphide from the water column (Andersen et al., 2002; Hilario et al., 2011). The environment in the basalt-hosted hydrothermal Karaseva et al., 2019), but this is the first time that fields in the East Pacific Rise, namely 21 °N EPR this pattern is shown in a large vestimentiferan. and 9 °N EPR, have a high sulphide flux, which is also ephemeral and unstable due to volcanic activity, leading to a high individual mortality rate and Effect of habitat turnover in the populations of R. pachyptila (von Our analyses revealed differences in body proportions Damm et al., 1985a; Johnson et al., 1986; Lutz et al., between individuals of Riftia pachyptila collected 1994; Thiébaut et al., 2002; Le Bris et al., 2006). These from the sediment-hosted (in Guaymas Basin) and conditions favour the selection of those individuals that the basalt-hosted hydrothermal vents along the East grow quickly and produce a large number of gametes

© 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, 193, 281–294 290 N. RIMSKAYA-KORSAKOVA ET AL. Downloaded from https://academic.oup.com/zoolinnean/article/193/1/281/6048373 by guest on 27 September 2021

Figure 3. Summary of our findings on the allometric growth of Riftia pachyptila. A, all body parts, namely obturaculum (ob), vestimentum (vm), trunk (tr), and opisthosoma (op), are shorter in juveniles than in adults; the growth rate is higher for the trunk, and minimal for the opisthosoma (Hypothesis 1). The lines connect the body parts to make these differences even more evident. B, the different conditions between the basalt-hosted, sulphide-rich vents at 9 °EPR and 21 °N EPR, and the highly sedimented, sulphide-poor vents at 27 °N EPR in the Guaymas Basin affect the growth of each body part (Hypothesis 2). The ‘fat’ morphotype from basalt locations is characterized by the presence of thicker vestimentum (Ø vm), wider tube opening (Ø tb), longer trunk (L tr), and comparatively shorter obturaculum (L ob) and smaller number of tentacular lamellae (N lam). The ‘slim’ morphotype from the sedimented vents has thinner and shorter trunk, but longer tentacular crowns and higher number of lamellae. This variability might be adaptive and selected to keep the sulphide uptake near to the optimum values for the symbionts. to ensure successful dispersal and settlement in areas Damm et al., 1985b; Campbell et al., 1988; Dean, 2006; with suitable conditions (Lutz et al., 1994; Thiébaut Geilert et al., 2018). The hydrothermal fluid, before et al., 2002). In response, individuals in these areas emerging onto the seafloor, has to cross this thick sediment have not only longer, but also thicker trunks, as this layer, cooling down (Bogdanov, 2002) and favouring the is the body region that hosts the bacterial symbionts precipitation of metal ions Fe, Mn, Cu and Zn, which and the reproductive system (Rimskaya-Korsakova react forming sulphides at low temperatures (Gieskes, et al., 2017). Indeed, the diameter of the tube opening 1983; von Damm et al., 1985b; Gieskes et al., 1988). As and the vestimentum were larger in animals from the a consequence, sulphides accumulate in the sediment 21 °N EPR and 9 °N EPR vents than in those from (von Damm et al., 1985a, b), but become undetectable in 27 °N EPR in the Guaymas Basin. the seawater around the R. pachyptila plumes (Robidart In contrast, conditions in the hydrothermal vent field et al., 2011). This transition also favours an increased in the Guaymas Basin, 27 °N EPR, are more stable concentration of carbon dioxide and the NH4+ ion, than in any other hydrothermal vent of the East Pacific raising the pH, which has been measured at 5.9–7.12 in Rise (von Damm et al., 1985a, b; Campbell et al., 1988; Guaymas compared to measurements of 2.6–5.98 in the Gamo, 1995; von Damm, 2000; Bogdanov, 2002; Shock & 9 °N EPR, and at 3.3–4.0 in 21 °N EPR (von Damm et al., Canovas, 2010). The sediments carried by the Colorado 1985a; Campbell et al., 1988; Gamo, 1995; von Damm, River accumulated in layers of at least 500 m of thickness 2000; Robidart et al., 2011). The increased pH and on the Guaymas Basin seafloor rift (Calvert, 1966; von sulphur depletion plays a major role in the metabolism

© 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, 193, 281–294 GROWTH OF THE TUBEWORM RIFTIA PACHYPTILA 291 of R. pachyptila, because the uptake of the carbon ACKNOWLEDGEMENTS dioxide from the environment into the alkaline blood We thank the crews of RV Akademik Mstislav Keldysh of the worm depends on the presence of a pH gradient and manned submersibles PISCES, MIR-1 and MIR-2 (Childress et al., 1993; Goffredi et al., 1997; Van Dover especially Anatoliy Sagalevich for the submersible & Lutz, 2004). Therefore, as the pH of the environment collections of tubeworms. We thank Lev Moskalev and becomes less acidic and the gradient decreases, less CO 2 Alexander Semenov for fruitful discussions facilitating diffuses (Goffredi et al., 1997), making the growth rate the work. Graphic symbols designed by macrovector slower and favouring a thinner morphotype. Likewise, and ibrandify/Freepik. The work was financially the lower concentration of sulphides in the fluid, due supported by the Russian Science Foundation (grant to precipitation at low temperature (von Damm et al., no. 18-14-00141). Alejandro Martínez was supported Downloaded from https://academic.oup.com/zoolinnean/article/193/1/281/6048373 by guest on 27 September 2021 1985a, b; von Damm, 2000; Robidart et al., 2011), may by the Marie Skłodowska-Curie Individual Fellowship select for a more elongated obturaculum with more (grant number 745530—ANCAVE – ‘Anchialine caves tentacular lamellae, significantly increasing the surface to understand evolutionary processes’). Sergey Galkin available for sulphide uptake. in part was supported by the Minobrnauki of Russian ‘Short-fat’ and ‘long-slim’ phenotypes have been Federation State assignment No 0149-2019-0009 and described in the hydrothermal vent worm Ridgeia, Agreement No 075-15-2020-796. in the high- and low-sulphide fluids (Southward et al., 1995; Galkin, 1998; Sarrazin & Juniper, 1999; Tunnicliffe et al., 2014). However, worms in low- sulphide vents do not develop longer tentacular CONFLICT OF INTERESTS crowns, but instead they present so-called ‘roots’ in the The authors declare that there is no conflict of interests. posterior end of the body, which function as an organ that absorbs sulphides directly from the sediment (Urcuyo et al., 2003, 2007). In the same manner, the seep vestimentiferans acquire sulphides by ‘roots’ DATA AVAILABILITY STATEMENT extending deeply into the sediment (Scott & Fisher, Original pictures of the vents sites taken using 1995; Julian et al., 1999). Riftia does not present DSRV “Mir” camera” are kept by Anatoliy Sagalevich ‘roots’ penetrating the sediment or basalt cracks to (Institute of Oceanology, Moscow) and available reach the sulphide fluid, but instead elevates the body by personal request. The rest of the data (original at a certain distance from the bottom to extend the photographs of worms, graphs, schemes) are kept by tentacular plume into the fluid (Gaill et al., 1997) in NRK and available by personal request. order to obtain more energy sources for its symbionts.

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