Trophic Structure of Hydrothermal Vent Communities at Myojin Knoll and Nikko Seamount in the Northwestern Paciﬁc: Implications for Photosynthesis-Derived Food Supply

Plankton Benthos Res 7(2): 35–40, 2012 Plankton & Benthos Research © The Japanese Association of Benthology

Trophic structure of hydrothermal vent communities at Myojin Knoll and Nikko Seamount in the northwestern Paciﬁc: Implications for photosynthesis-derived food supply

1, 2 3 1,2 TAKEFUMI YORISUE *, KOJI INOUE , HIROSHI MIYAKE & SHIGEAKI KOJIMA

1 Graduate School of Frontier Sciences, the University of Tokyo, 5–1–5 Kashiwanoha, Kashiwa, Chiba 277–8561, Japan 2 Atmosphere and Ocean Research Institute, the University of Tokyo, 5–1–5 Kashiwanoha, Kashiwa, Chiba 277–8564, Japan 3 School of Marine Biosciences, Kitasato University, 1–15–1 Kitasato, Minami-ku, Sagamihara, Kanagawa 252–0373, Japan Received 26 September 2011; Accepted 2 February 2012

Abstract: To investigate and compare the trophic structures of hydrothermal vent communities at different depths, the carbon and nitrogen stable isotope ratios of dominant species were analyzed in the communities at Myojin Knoll (1,220–1,360 m) in the Izu-Ogasawara Arc and the Nikko Seamount (380–550 m) in the North Mariana Arc. At the Myojin knoll, a barnacle, Ashinkailepas seepiophila had high δ15N value, which suggested to be derived from photosynthetic products. Similarly, at Nikko Seamount, a polynoid polychaete, Gandulfus yunohana, a xanthid crab, Alvinocaaris sp., and Symphurus thermophilus had high δ15N values. These animals, too, are suggested to consume photosynthetic products. The range of δ13C values at Myojin Knoll was wider than that at Nikko Seamount. The difference between the ranges of these values suggest that different chemical environments between the two vent sites inﬂuence the components and distribution of chemoautotrophic bacteria found at each site, leading to different faunal compositions.

Key words: chemosynthesis-based community, Izu-Ogasawara Arc, North Mariana Arc, stable isotope

communities at shallow vent sites (<200 m; Tarasov et al. Introduction 2005). Isotopic studies have revealed another example of a Hydrothermal vents are found at seafloor spreading cen- significant association between photosynthesis and some ters and submarine volcanoes all over the world (Sibuet & species of deep-sea vent shrimps collected between depth Olu 1998; Van Dover 2000). They provide habitats for of 500 and 3,700 m. The shrimps consume photosynthetic unique biological communities based on chemosynthesis products at early migratory life stages (Gebruk et al. 2000; (Van Dover 2000). Especially in the deep-sea, the main Pond et al. 1997; Stevens et al. 2008; Van Dover 2002). In primary producers in hydrothermal vent communities are addition, it is estimated that 5–10% of organic matter pro- chemosynthetic bacteria, and their faunal composition and duced in the photic layer reaches a depth of 2,000–3,000 m food web structure are significantly different from other in general (Lalli & Parsons 1997), and Karl (1995) noted deep-sea communities. The diversity of vent-obligate that photosynthesic products might play a significant role fauna sharply increases at a depth of 200 m or more, and in deep-sea hydrothermal vent communities. symbiotrophic species dominate below 400–500 m (Tara- In the western Pacific, hydrothermal vent communities sov et al. 2005). However, photosynthetic products also have been discovered in both backarc and forearc basins at contribute to vent communities. For example, the propor- various depths. Therefore, they are ideal targets for verify- tion of primary production by photosynthesis accounts for ing the relationship between photosynthesis and hydrother- more than 50% of primary production within biological mal vent communities at various depths. However, few studies have investigated the food webs of the vent com- * Corresponding author: Takefumi Yorisue; E-mail, [email protected] munities in the western Pacific. This study compares the tokyo.ac.jp trophic structures of the biological communities of two hy- 36 T. Yorisue et al.

(Paralvinella hessleri Desbruyères & Laubier) (Fujikura et al. 2008; Kojima 2002). On the other hand, the Nikko Sea- mount community is dominated by a vestimentiferan tubeworm (Lamellibrachia Satsuma Miura, Tsukahara & Hashimoto), shrimps (Alvinocaris spp.), and a fish (Sym- phurus thermophilus Munroe & Hashimoto), in addition to Neoverruca sp. and G. yunohana. The specimens analyzed in this study are listed in Table 1. All of the specimens were preserved in a freezer (－20°C) until stable isotope analysis. Stable isotope analysis Soft tissues of each specimen were washed with distilled water, freeze-dried, and homogenized. Since fish usually contain a large amount of lipids, a sample of Symphurus thermophilus was subjected to lipid extraction and redried in an oven at 60°C overnight. Then, all of the samples were decalcified using 0.1 M HCl and dried in an oven at 60°C for 48 h. Samples were put into a silver cup and then com- busted in a flash elemental analyzer (Flash-EA 1112; Thermo Electron, Milan, Italy) and transferred to an iso- plus Fig. 1. Hydrothermal vent sites where samples were collected tope ratio mass spectrometer (DELTA XP; Thermo in this study. Finnigan, Bremen, Germany) via a continuous flow device (Conflo-III; Thermo Finnigan). Stable isotope ratios are given in the conventional delta notation (δ13C; δ15N) per drothermal vent sites at different depths in the western Pa- mil (‰) according to the following formula: cific, Myojin Knoll (1,220–1,360 m) and Nikko Seamount 3 (380–550 m), on the basis of carbon and nitrogen stable δX=[(Rsample/Rstandard)－1]×10 isotope ratios, and considers the potential of photosynthetic products as a food source for these communities. where X is 13C or 15N and R is 13C/12C or 15N/14N. Stan- Stable carbon and nitrogen isotopesic compositions are dards for C and N were Pee Dee Belemnite and atmo- good indicators of the origin of consumed food substrates spheric nitrogen, respectively. The significance of the dif- and trophic level, respectively: approximately 1‰ enrich- ferences between δ13C and δ15N values was tested using ment in δ13C and 3‰ enrichment in δ15N can be detected SPSS for Windows ver. 14.0 (SPSS Inc, Chicago, USA). per trophic level increment (Conway et al. 1994; Minagawa & Wada 1984). Stable isotopic analysis is known to be ef- Results fective for examining the trophic relationships of hydrothermal vent communities (e.g. Bergquist et al. 2007). Myojin Knoll The δ13C and δ15N values of specimens collected from Materials and Methods the Myojin Knoll are shown in Fig. 2A. The animals at this site had a wide range of δ13C values, with Paralvinella hes- Specimen collection sleri (9 in Fig. 2A) being the highest (－12.3–－8.1‰) and Specimens were collected by the remotely-operated ve- the gills of Bathymodiolus septemdierum (3 in Fig. 2A) hicle HyperDolphin of the Japan Agency for Marine-Earth being the lowest (－37.4–－35.0‰). Bathymodiolus septem- Science and Technology (JAMSTEC) during the NT09-05 dierum (3 and 4 in Fig. 2A) also had the lowest δ15N value cruise (April 2009) of research vessel Natsushima at the (－1.2–－0.7‰), and a non-vent oplophorid shrimp (21 in Myojin Knoll in the Izu-Ogasawara Arc (32°06′N, Fig. 2A) had the highest δ15N value (11.7‰). Ashinkailepas 139°52′E, depth 1,220–1,360 m) and the Nikko Seamount seepiophila (12 in Fig. 2A) had the highest δ15N values in the North Mariana Arc (23°04′N, 142°20′E, depth 380– among vent species (6.6–10.6‰). The δ13C values of two 550 m). The sampling sites are shown in Fig. 1. The Myojin species of barnacles, Neoverruca sp. (13 in Fig. 2A; Knoll hydrothermal vent site is dominated by a mussel －32.8–－26‰) and A. seepiophila (12 in Fig. 2A; －27.8– (Bathymodiolus septemdierum Hashimoto & Okutani), a －22‰), were significantly different (p<0.01, t-test) as crab (Gandalfus yunohana Takeda, Hashimoto & Ohta), were their δ15N values: Neoverruca sp. (13 in Fig. 2A; 4.8– barnacles (Neoverruca sp. and Ashinkailepas seepiophila 6.4‰) and A. seepiophila (12 in Fig. 2A; 6.6–10.6‰) Yamagushi, Newman & Hashimoto), and the polychaete (p<0.01, t-test). Trophic structure at NW Pacific vents 37

Table 1. Specimens collected at hydrothermal vent sites at Myojin Knoll and Nikko Seamount.

Number of samples analyzed Taxon ID Myojin Knoll Nikko Seamount

Vent fauna Mollusca Gastropoda Phenacolepadidae Shinkailepas sp. 1* 2 1 Turridae Oenopota ogasawarana 1 2 Bivalvia Mytilidae Bathymodiolus septemdierum (gill) 2 3 Bathymodiolus septemdierum (muscle) 2 4 Gigantidas sp. (gill) 2 5 Gigantidas sp. (muscle) 2 6 Polychaeta Siboglinidae Lamellibrachia satsuma (trophosome) 2 7 Lamellibrachia satsuma (muscle) 2 8 Alvinellidae Paralvinella hessleri 2 9 Polynoidae 2 2 10 Amphinomidae 1 11 Arthropoda Pedunculata Eolepadidae Ashinkailepas seepiophila 10* 12 Sessilia Neoverrucidae Neoverruca sp. 10* 12* 13 Decapoda Alvinocaridae Alvinocaris sp. 2 14 Palaemonidae Periclimenes sp. 2 15 Galatheidae Munidopsis sp. 1 16 Bythograeidae Gandalfus yunohana 2 2 17 Xanthidae 2 18 Cnidaria Actiniaria 1 1 19 Osteichthyes Pleuronectiformes Cynoglossidae Symphurus thermophilus 2 20 Non-vent fauna Arthropoda Decapoda Oplophoridae Acanthephyra sp. 1 21

*Five specimens were pooled for each sample. 38 T. Yorisue et al.

in Fig. 2A) among vent species, although barnacles are fil- ter feeders. Non-vent deep-sea fauna usually have higher δ15N values than vent fauna (Van Dover & Fry, 1989; Soto, 2009; Bergquist et al. 2007; Fisher et al. 1994). Indeed, in the present study, the δ15N value of Acanthephyra sp. (21 in Fig. 2A), which is a non-vent species (Fujikura et al. 2008), was higher than those of the vent species. This value is thought to correspond to consumption of photosynthetic products in this area. Therefore, the high δ15N value of A. seepiophila (12 in Fig. 2A) suggests this species partly consumes photosynthetic products that fall from the photic zone. The δ15N values of Bathymodiolus septemdierum (3 and 4 in Fig. 2A) were much lower than those of the other organisms in this area, which may reflect the effect of isotopic fractionation by the enzymes of the endosymbionts in their gill, as suggested for other bathymodiolin mussels (Nelson & Fisher 1995). In chemosynthesis-based ecosystems, bacterial δ13C values reflect the carbon fixation pathway: The rTCA cycle and the CBB cycle using form II RuBisCo result in 2–13‰ and 9–15‰ depletion, respectively; while the CBB cycle using form I RuBisCo results in 27–35‰ depletion (House et al. 2003; Robinson et al. 2003). Form II RuBisCo re-

quires less O2 than form I RuBisCo (Paoli & Tabita 1998). In addition, bacteria with the rTCA cycle, which has high 13 Fig. 2. Carbon and nitrogen stable isotope values. A: Animals δ C values, dominate highly reductive areas close to vent collected from a hydrothermal vent at Myojin Knoll. B: Animals emissions (Nakagawa & Takai 2008). Therefore, Paralvi- collected from a hydrothermal vent at Nikko Seamount. Num- nella hessleri (9 in Fig. 2A) and the polynoid polychaete 13 bers correspond to the identification numbers in Table 1. Crosses (10 in Fig. 2A), which inhabit such areas, had high δ C 13 and a circle indicate vent and non-vent species, respectively. Bars values. In contrast, the δ C value of Neoverruca sp. (13 in indicate range. Fig. 2A) was low, and this species is thought to be mostly dependent on chemoautotrophs with form I RuBisCo. The δ13C value of B. septemdierum was also very low (3 and 4 Nikko Seamount in Fig. 2A). This species has thioautotrophic endosymbionts in the gill, and such low values are common among The δ13C and δ15N values of the specimens collected bathymodiolid mussels with thioautotrophic symbionts from the Nikko Seamount are shown in Fig. 2B. The ani- (Mizota & Yamanaka 2003). Recently, the form I RuBisCo mals at this site also had a wide range of δ13C values, with gene was cloned from the endosymbiotic bacteria of a the trophosome of Lamellibrachia satsuma (7 in Fig. 2B) bathymodiolid mussel (Elsaied et al. 2006). Therefore, the being the highest (－13.9–－13.1‰) and the gills of Giganti- symbionts of B. septemdierum (3 and 4 in Fig. 2A) proba- das sp. (5 in Fig. 2B) being the lowest (－35.4–－33.4‰). bly use form I RuBisCo judging from their low δ13C val- The gills of Gigantidas sp. (5 in Fig. 2B) also had the low- ues. est δ15N value (－5.8–－4.1‰). The δ15N value of Sym- Nikko Seamount phurus thermophilus (20 in Fig. 2B) was the highest (10.9– 12.2‰). The δ13C value of Neoverruca sp. (13 in Fig. 2B; Lamellibrachia satsuma (7 and 8 in Fig. 2B) has thioau- －28.0–－21.8) was significantly higher than that at the totrophic endosymbionts in the trophosome. The δ13C val- Myojin Knoll (p<0.01, t-test) but a significant difference ues of L. satsuma (7 and 8 in Fig. 2B) are the highest was not detected for the δ15N values (5.3–6.7) (p=0.34, t- among the animals at this site. The endosymbiotic bacteria test). of a vestimentiferan tubeworm, Riftia pachyptila, Jones use both the CBB cycle with form II RuBisCo and the rTCA cycle (Markert et al. 2007). Therefore, the endosym- Discussion biotic bacteria of L. satsuma also might use the CBB cycle with form II RuBisCo as well as the rTCA cycle, resulting Myojin Knoll in high δ13C values. Gigantidas sp. (5 and 6 in Fig. 2B) has Ashinkailepas seepiophila had the highest δ15N value (12 the lowest δ13C values among animals at this site, suggest- Trophic structure at NW Pacific vents 39 ing that this species is highly dependent on chemosyn- modiolus septemdierum (3 and 4 in Fig. 2A) is abundant at thetic bacteria using form I RuBisCo. However, the exis- Myojin Knoll, and the δ15N values of higher consumers tence of symbiotic bacteria in this mussel has never been that feed on this species may be affected by its low δ15N examined and further investigation is necessary to clarify value. Further studies are needed to clarify the food web the relationship. structures of these areas on the basis of the stomach con- tents and/or lipid markers of the resident animals. Comparison of Myojin Knoll and Nikko Seamount The δ13C values of CO of the Suiyo Seamount on the 2 Acknowledgments Izu-Ogasawara Arc and of the NW Eifuku Volcano on the northern Mariana Arc are －1.0 and －1.75‰, respectively We thank Dr. T. Miyajima, Mr. Y. Imamura, and Ms. S. (Ishibashi & Urabe 1995; Lupton et al. 2006), so no signifi- Ozeki for their instruction and help with stable isotope 13 cant difference in δ C (CO2) values was expected between analysis. We are also grateful to the scientific team on the the Myojin Knoll and the Nikko Seamount. However, the NT09-05 research cruise, the operating team of the ROV range of δ13C values in animals at the Myojin Knoll was HyperDolphin, and the crew of R/V Natsushima of JAM- found to be wider than that at the Nikko Seamount (Fig. 2), STEC for their help in sample collection. which suggests that the transition of bacterial composition from vent emissions to peripheral zones is more marked at the Myojin Knoll. 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