Abstract
Cabled seafloor platforms can overcome many constraints of stand-alone systems and archived long-term seafloor monitoring, and their advantages include unlimited power, real-time communication, a synchronized clock, and virtually unlimited data storage. Using monthly images from a fixed camera on a cabled deep-sea observatory in the Off Hatsushima seep site in Sagami Bay, Japan, fluctuations in clam density (Phreagena soyoae and P. okutanii) were observed over 5 years, March 1994–July 1999. Eight disturbances were seen, including five phytodetritus deposition events associated with seasonal blooms, two earthquake-associated turbid flows, and one caused by a maintenance visit by a remotely operated vehicle. Overall, these observations indicate that the vesicomyids experienced an ongoing decline throughout the observation series, and strong disturbance events such as earthquakes appeared to be too severe for the clams to survive. As such, vesicomyid clams are unlikely to survive the foreseeable impacts of deep-sea mining. These results show that long-term observations of deep-sea chemosynthetic communities are useful for understanding their resilience and for making an environmental impact assessment.
References
Abbott D, Menke W, Hobart M, Anderson RN, Embley RW (1984) Correlated sediment thickness, temperature gradient and excess pore pressure in a marine fault block basin. Geophys Res Lett 11:485–488
Aguzzi J, Company JB, Costa C, Matabos M, Azzurro E, Lázaro A, Menesatti P, Sarda F, Canals M, Delory E, Cline D, Favali P, Juniper S, Furushima Y, Fujiwara Y, Chiesa JJ, Marotta L, Bahamón N, Priede I (2012) Challenges to the assessment of benthic populations and biodiversity as a result of rhythmic behaviour: video solutions from cabled observatories. Oceanogr Mar Biol 50:235–286
Amyot J-P, Downing J (1997) Seasonal variation in vertical and horizontal movement of the freshwater bivalve Elliptio complanata (Mollusca: Unionidae). Freshw Biol 37:345–354
Ansell AD (1969) Leaping movements in the Bivalvia. J Molluscan Stud 38:387–399
Boss KJ, Turner RD (1980) The giant white clam from the Galapagos Rift, Calyptogena magnifica species novum. Malacologia 20:161–194
Fujikura K, Amaki K, Barry JP, Fujiwara Y, Furushima Y, Iwase R, Yamamoto H, Maruyama T (2007) Long-term in situ monitoring of spawning behavior and fecundity in Calyptogena spp. Mar Ecol Prog Ser 333:185–193
Fujikura K, Okutani T, Maruyama T (2012) Deep-sea life—biological observations using research submersibles, 2nd edn. Tokai University Press, Tokyo
Fujiwara Y, Tsukahara J, Hashimoto J, Fujikura K (1998) In situ spawning of a deep-sea vesicomyid clam: evidence for an environmental cue. Deep Sea Res Part I 45:1881–1889
Hashimoto J, Ohta S, Fujikura K, Fujiwara Y, Sukizaki S (1995) Life habit of vesicomyid clam, Calyptogena soyoae, and hydrogen sulfide concentration in interstitial waters in Sagami Bay, Japan. J Oceanogr 51:341–350
Ikuta T, Igawa K, Tame A, Kuroiwa T, Kuroiwa H, Aoki Y, Takaki Y, Nagai Y, Ozawa G, Yamamoto M, Deguchi R, Fujikura K, Maruyama T, Yoshida T (2016) Surfing the vegetal pole in a small population: extracellular vertical transmission of an ‘intracellular’ deep-sea clam symbiont. R Soc Open Sci 3:160130
Iwase R, Momma H, Kawaguchi K, Fujiwara N, Suzuki S, Mitsuzawa K (1997) Turbidity currents on the deep seafloor triggered by the earthquake swarm in the east off Izu Peninsula in March 1997—observation by the long-term deep seafloor observatory off Hatsushima Island in Sagami Bay. JAMSTEC J Deep Sea Res 13:433–442
Iwase R, Mitsuzawa K, Momma H (1998) Mudflow associated with the swarm earthquakes east off Izu Peninsula in April 1998, observed by the long-term deep sea floor observatory off Hatsushima Island in Sagami Bay. JAMSTEC J Deep Sea Res 14:301–317
Johnson SB, Krylova EM, Audzijonyte A, Sahling H, Vrijenhoek RC (2017) Phylogeny and origins of chemosynthetic vesicomyid clams. Syst Biodivers 15:346–360
Kojima S, Ohta S (1997) Calyptogena okutanii n. sp., a sibling species of Calyptogena soyoae Okutani, 1957 (Bivalvia: Vesicomyidae). Venus 56:189–195
Krylova EM, Sahling H (2010) Vesicomyidae (Bivalvia): current taxonomy and distribution. PLoS One 5:e9957
Levin LA (2005) Ecology of cold seep sediments: interactions of fauna with flow, chemistry and microbes. In: Gibson RN, Atkinson RJA, Gordon JDM (eds) Oceanography and marine biology: an annual review, vol 43. CRC Press, Boca Raton, pp 1–46
Levin LA, Mengerink K, Gjerde KM, Rowden AA, Van Dover CL, Clark MR, Ramirez-Llodra E, Currie B, Smith CR, Sato KN (2016) Defining “serious harm” to the marine environment in the context of deep-seabed mining. Mar Policy 74:245–259
Métivier B, Okutani T, Ohta S (1986) Calyptogena (Ectenagena) phaseoliformis n. sp., an unusual vesicomyid bivalve collected by the submersible Nautile from abyssal depths of the Japan and Kurile Trenches. Venus 45:161–168
Miller KA, Thompson KF, Johnston P, Santillo D (2018) An overview of seabed mining including the current state of development, environmental impacts, and knowledge gaps. Front Mar Sci 4:418
Momma H, Iwase R, Mitsuzawa K, Kaiho Y, Fujiwara Y (1998) Preliminary results of a three-year continuous observation by a deep seafloor observatory in Sagami Bay, central Japan. Phys Earth Planet Inter 108:263–274
Mullineaux LS, Adams DK, Mills SW, Beaulieu SE (2010) Larvae from afar colonize deep-sea hydrothermal vents after a catastrophic eruption. Proc Natl Acad Sci 107:7829–7834
Nakajima R, Komuku T, Yamakita T, Lindsay DJ, Jintsu-Uchifune Y, Watanabe H, Tanaka K, Shirayama Y, Yamamoto H, Fujikura K (2014) A new method for estimating the area of the seafloor from oblique images taken by deep-sea submersible survey platforms. JAMSTEC Rep Res Dev 19:59–66
Nakajima R, Yamamoto H, Kawagucci S, Takaya Y, Nozaki T, Chen C, Fujikura K, Miwa T, Takai K (2015) Post-drilling changes in seabed landscape and megabenthos in a deep-sea hydrothermal system, the Iheya North field, Okinawa Trough. PLoS One 10:e0123095
Okutani T (1957) Two new species of bivalves from the deep water in Sagami Bay collected by the R.V. “Soyo-Maru”. Bull Tokai Reg Fish Res Lab 17:27–30
Okutani T, Egawa K (1985) The first underwater observation on living habit and thanatocoenoses of Calyptogena soyoae in bathyal depth of Sagami Bay. Venus 44:285–289
Okutani T, Fujikura K (1992) A new turrid gastropod associated with metachromatic seabed near the Calyptogena-community in Sagami Bay. Venus 51:1–7
Ozaki H (1958) Stratigraphical and paleontological studies on the Neogene and Pleistocene formations of the Tyosi [= Choshi] district. Bull Natl Sci Mus 4:1–182
Sasaki T, Fujikura K, Okutani T (2007) Molluscs collected in the cruise NT06-04 of R/V Natsushima from methane-seeps off Hatsushima Island, Sagami Bay. Chiribotan 37:197–207
Sasaki T, Warén A, Kano Y, Okutani T, Fujikura K, Kiel S (2010) Gastropods from recent hot vents and cold seeps: systematics, diversity and life strategies. In: Kiel S (ed) The vent and seep biota, topics in geobiology, vol 33. Springer, Berlin, pp 169–254
Shimek RL (1983) The biology of the northeastern Pacific Turridae II. Oenopota. J Molluscan Stud 49:146–163
Shirayama Y, Itoh H, Fukushima T (2017) Recent developments in environmental impact assessment with regard to mining of deep-sea mineral resources. In: Sharma R (ed) Deep-sea mining. Springer, Cham, pp 445–463
Sigwart JD, Chen C, Marsh L (2017) Is mining the seabed bad for molluscs? Nautilus 131:43–49
Sverdrup HU, Johnson MW, Fleming RH (1942) The oceans, their physics, chemistry, and general biology. Prentice-Hall, New York
Thistle D (2003) The deep-sea floor: an overview. In: Tyler PA (ed) Ecosystems of the world. Ecosystems of the deep oceans, vol 28. Elsevier, Amsterdam, pp 5–39
Thurber AR, Sweetman AK, Narayanaswamy BE, Jones DOB, Ingels J, Hansman RL (2014) Ecosystem function and services provided by the deep sea. Biogeosciences 11:3941–3963
Trueman ER (1983) Locomotion in mulluscs. In: Saleuddin ASM, Wilbur KM (eds) The mollusca. Physiology, part 1, vol 4. Academic Press, New York, pp 155–198
Van Dover CL (2011) Tighten regulations on deep-sea mining. Nature 470:31–33
Van Dover CL, German CR, Speer KG, Parson LM, Vrijenhoek RC (2002) Evolution and biogeography of deep-sea vent and seep invertebrates. Science 295:1253–1257
Van Dover CL, Smith CR, Ardron J, Dunn D, Gjerde K, Levin L, Smith S (2012) Designating networks of chemosynthetic ecosystem reserves in the deep sea. Mar Policy 36:378–381
Watanabe H, Seo E, Takahashi Y, Yoshida T, Kojima S, Fujikura K, Miyake H (2013) Spatial distribution of vesicomyid bivalves Calyptogena okutanii and Calyptogena soyoae along an environmental gradient in chemosynthetic biological communities in Japan. J Oceanogr 69:129–134
Wiklund H, Taylor JD, Dahlgren TG, Todt C, Ikebe C, Rabone M, Glover AG (2017) Abyssal fauna of the UK-1 polymetallic nodule exploration area, Clarion-Clipperton Zone, central Pacific Ocean: mollusca. ZooKeys 707:1–46
Yamaoka A, Kitazato H, Iwase R, Momma H (1998) Seasonally appeared dense clouds of suspended particles at benthic boundary layer which were recorded in video images at the real-time deep-sea floor observatory off Hatsushima in Sagami Bay. JAMSTEC J Deep Sea Res 14:319–327
Acknowledgements
The authors thank Hiroshi Morita for his help in image analysis and Takami Nobuhara (Shizuoka University) for helpful discussion. We are greatly indebted to Julia D. Sigwart and Elena M. Krylova for constructive reviews that improved earlier versions of this paper.
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This study was supported by the Environmental Research and Technology Development Fund (S9) of the Ministry of the Environment, Japan.
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Nakajima, R., Chen, C., Iwase, R. et al. Clams after storms: the impact of multiple disturbances on seep vesicomyid clams revealed by long-term monitoring. Mar Biol 166, 35 (2019). https://doi.org/10.1007/s00227-019-3484-6
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DOI: https://doi.org/10.1007/s00227-019-3484-6