Trophic structure of the macrofauna associated to deep-vents of the southern Gulf of California: Pescadero Basin and Pescadero Transform Fault


Autoři: Diana L. Salcedo aff001;  Luis A. Soto aff002;  Jennifer B. Paduan aff003
Působiště autorů: Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Mexico City, Mexico aff001;  Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Mexico City, Mexico aff002;  Monterey Bay Aquarium Research Institute, Moss Landing, California, United States of America aff003
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224698

Souhrn

Newly discovered hydrothermal systems in the Pescadero Basin (PB) and the neighboring Pescadero Transform Fault (PTF) at the mouth of the Gulf of California disclosed a diverse macrofauna assemblage. The trophic structure of both ecosystems was assessed using carbon (δ13C), nitrogen (δ15N), and sulfur (δ34S) stable isotopes. The δ13C ranged from -40.8 to -12.1‰, revealing diverse carbon sources and its assimilation via Calvin-Benson-Bassham and the reductive tricarboxylic acid cycles. The δ15N values were between -12.5 and 18.3‰, corresponding to primary and secondary consumers. The δ34S values fluctuated from -36.2 to 15.1‰, indicating the sulfide assimilation of biogenic, magmatic, and photosynthetic sources. In PB high-temperature vents, primary consumers including symbiont-bearing, bacterivores and filter-feeders predominated. The secondary consumers within the scavengers/detritivores and predator guilds were scarce. The siboglinid Oasisia aff alvinae dominated the macrofauna assemblage at PB, but rather than playing a trophic role, it provides a substrate to vent dwellers. In PTF low-temperature vents, only symbiont-bearing primary consumers were analyzed, displaying the lowest δ34S values. This assemblage was dominated by the coexisting siboglinids Lamellibrachia barhami and Escarpia spicata. δ34S values allowed to distinguish between PB and PTF vent communities, to exclude the presence of methanotrophic organisms, and the detection of photosynthetic organic matter input.

Klíčová slova:

Consortia – Fractionation – Hydrothermal vents – Stable isotopes – Sulfates – Sulfides – Sulfur – Sea anemones


Zdroje

1. Corliss JB, Dymond J, Gordon LI, Edmond JM, von Harzen RP, Ballard RD, et al. Submarine thermal springs on the Galapagos Rift. Science. 1979; 203:1073–1083. doi: 10.1126/science.203.4385.1073 17776033

2. Beaulieu SE, Szafranski K. InterRidge Global database of active submarine hydrothermal vent fields: Prepared for InterRidge, Version 3.4. http://vents-date.interridge.org

3. Clague DA, Caress DW, Dreyer BM, Lunsted L, Paduan JB, Portner RA, et al. Geology of the Alarcón Rise Southern Gulf of California. Geochem Geophys. 2018; 19(3):807–837.

4. Paduan JB, Zierenberg RA, Clague DA, Spelz RM, Caress DW, Troni G, et al. Discovery of Hydrothermal Vent Fields on Alarcón Rise and in Southern Pescadero Basin, Gulf of California. Geochem Geophys. 2018; 19:1–32. doi: 10.1029/2018GC007771

5. Goffredi AK, Johnson S, Tunnicliffe V, Caress D, Clague D, Escobar E, et al. Hydrothermal vent fields discovered in the southern Gulf of California clarify the role of habitat in augmenting regional diversity. Proc R Soc Lon B Biol. 2017; 284(1859):1–10. doi: 10.1098/rspb.2017.0817 28724734

6. Adams JA, van Oevelen D, Bezemer TM, De Deyn GB, Hol WHG, van Donk E, et al. Soil and Freshwater and Marine Sediment Food Webs: Their Structure and Function. Bioscience. 2013; 63:35–42. doi: 10.1525/bio.2013.63.1.8

7. Tunnicliffe V. The biology of hydrothermal vents: ecology and evolution. Oceanogr Mar Biol Ann Rev. 1991; 29(2):319–407.

8. Govenar B. Energy transfer through food webs at hydrothermal vents: Linking the lithosphere to the biosphere. Oceanography. 2012; 25(1):246–255. doi: 10.5670/oceanog.2012.23

9. Middelburg JJ. Stable isotopes dissect aquatic food webs from the top to the bottom. Biogeosciences. 2014; 11(8):2357–2371. doi: 10.5194/bg-11-2357-2014

10. Peterson BJ, Fry B. Stable isotopes in ecosystem studies. Ann Rev Ecol Syst. 1987; 18:293–320. doi: 10.1146/annurev.es.18.110187.001453

11. Post DM. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology. 2002; 83(3):703–718. doi: 10.2307/3071875

12. Bouillon S, Gilikin DP, Conolly RM. Use of stable isotopes to understand food webs and ecosystem functioning in estuaries. In: Wolanski E, Mclusky DS, editors. Treatise on Estuarine and Coastal Science. Waltham: Academic Press; 2012. pp. 143–173.

13. Hügler M, Sievert SM. 2011 Beyond the Calvin Cycle: Autotrophic Carbon Fixation in the Ocean. Annu Rev Mar Sci. 2011; 3:261–289. doi: 10.1146/annurev-marine-120709-142712 21329206

14. Reid WD, Sweeting CJ, Wigham BD, Zwirglmaier K, Hawkes JA, McGill RA, et al. Spatial Differences in East Scotia Ridge Hydrothermal Vent Food Webs: Influences of Chemistry, Microbiology and predation on Trophodynamics. PlosONE. 2013; 8(6):1–11. doi: 10.1371/journal.pone.0065553 23762393

15. Minagawa M, Wada E. Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta. 1984; 48(5):1135–1140. doi: 10.1016/0016-7037(84)90204-7

16. Deniro MJ, Epstein S. Influence of Diet on the Distribution of Nitrogen Isotopes in Animals. Geochim Cosmochim Acta. 1981; 45:341–351. doi: 10.1016/0016-7037(81)90244-1

17. Van Audenhaege L, Fariñas-Bermejo A, Schultz T, Van Dover CL. An environmental baseline for food-webs at deep-sea hydrothermal vents in Manus Basin (Papua New Guinea). Deep Sea Res Part I. 2019. doi: 10.1016/j.dsr.2019.04.018

18. Kessler WS. The circulation of the eastern tropical Pacific: A review. Prog Oceanogr. 2006; 69:181–217. doi: 10.1016/j.pocean.2006.03.009

19. Lavín MF, Beier E, Badan A. Estructura hidrográfica y circulación del Golfo de California: escalas estacional e interanual. In: Lavín MF, editor. Contribuciones a la oceanografía física en México. Unión Geofísica Mexicana, Monografía No. 3; 1997. pp. 141–171.

20. Campbell BJ, Engel AS, Porter ML, Takai K. The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat Microbiol Rev. 2006; 4: 458–468. doi: 10.1038/nrmicro1414 16652138

21. Van Dover CL, Fry B. Microorganisms as food sources at deep-sea hydrothermal vents. Limnol Oceanogr. 1994; 39:51–57. doi: 10.4319/lo.1994.39.1.0051

22. Fisher CR, Childress JJ, Macko SA, Brooks JM. Nutritional interactions in Galapagos Rift vent communities: inferences from stable carbon and nitrogen isotope analyses. Mar Ecol Prog Ser. 1994; 103(1–2):45–55. doi: 10.3354/meps103045

23. Soto LA. Stable carbon and nitrogen isotopic signatures of fauna associated with the Deep-sea hydrothermal vent system of Guaymas Basin, Gulf of California. Deep Sea Res Part II. 2009; 56(19):1675–1682. doi: 10.1016/j.dsr2.2009.05.013

24. Welhan JA, Lupton JE. Light hydrocarbons in Guaymas Basin hydrothermal fluids: Thermogenic versus abiogenic origin. Amer Assoc Petr Geol Bull. 1987; 71:215–223. doi: 10.1306/94886D76-1704-11D7-8645000102C1865D

25. Kessler JD, Reeburgh WS, Valentine DL, Kinnaman FS, Peltzer ET, Brewer PG, et al. A survey of methane isotope abundance (14C, 13C, 2H) from five nearshore marine basins that reveals unusual radiocarbon levels in subsurface waters. J Geophys Res. 2008; 113(12):C12021. doi: 10.1029/2008JC004822

26. Mizota C, Yamanaka T. Strategic adaptation of a deep-sea, chemosynthesis-based animal community: an evaluation based on soft body part carbon, nitrogen, and sulfur isotopic signatures. Jap Jour Benth. 2003; 58:56–69. doi: 10.5179/benthos.58.56

27. Schuett C, Doepke H, Grathoff A, Gedde M. Bacterial aggregates in the tentacles of the sea anemone Metridium senile. Helgol Mar Res. 2007; 61:211–216. doi: 10.1007/s10152-007-0069-4

28. Muller EM, Fine M, Ritchie KB. The stable microbiome of inter and sub-tidal anemone species under increasing pCO2. Sci Rep. 2016; 6:1–11.

29. Markert S, Arndt C, Felbeck H, Becher D, Sievert SM, Hügler M, et al. Physiological proteomics of the uncultured endosymbiont of Riftia pachyptila. Science. 2007; 315:247–250. doi: 10.1126/science.1132913 17218528

30. Lelièvre Y, Sarrazin J, Marticorena J, Schaal G, Day T, Legendre P, et al. Biodiversity and trophic ecology of hydrothermal vent fauna associated with tubeworm assemblages on the Juan de Fuca Ridge. Biogeosciences. 2018; 15:2629–2647. doi: 10.5194/bg-15-2629-2018

31. MacAvoy SE, Fisher CR, Carney RS, Macko SA. Nutritional associations among fauna at hydrocarbon seep communities in the Gulf of Mexico. Mar Ecol Prog Ser. 2005; 292:51–60. doi: 10.3354/meps292051

32. Windoffer R, Giere O. Symbiosis of the hydrothermal vent gastropod Ifremeria nautilei (Provannidae) with endobacteria—structural analyses and ecological considerations. Biol Bull. 1997; 193:381–392. doi: 10.2307/1542940 28574764

33. Michener RH, Kaufman L. Stable isotope ratios as tracers in marine food wens: an update. In: Michener RH, Lathja K, editors. Stable isotopes in ecology and environmental science. Singapore: Blackwell Publishing; 2007. pp. 238–282.

34. Portail M, Olu K, Dubois SF, Escobar-Briones E, Gelinas Y, Menot L, et al. Food-Web Complecity in Guaymas Basin Hydrothermal Vents and Cold Seeps. PlosONE. 2016; 11(9):1–33. doi: 10.1371/journal.pone.0162263 27683216

35. Nelson DC, Fisher CR. Chemoautotrophic and methanotrophic endosymbiotic bacteria at vents and seeps. In: Karls DM, editor. Microbiology of Deep-Sea Hydrothermal Vents. CRC Press; 1995. pp 125–167.

36. Yorisue T, Inoue K, Moyake H, Kojima S. 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. 2012; 7(2):35–40. doi: 10.3800/pbr.7.35

37. Lee RW, Childress JJ. Inorganic N assimilation and ammonium pools in a Deep-sea mussel containing methanotrophic endosymbionts. Biol Bull. 1996; 190(3):373–384. doi: 10.2307/1543030 29227702

38. Rau GH. Low 15N/14N in hydrothermal vent animals: Ecological implications. Nature. 1981; 289:484–485. doi: 10.1038/289484a0

39. Bourbonnais A, Lehmann MF, Butterfield DA, Juniper SK. Subseafloor nitrogen transformations in diffuse hydrothermal vent fluids of the Juan de Fuca Ridge, evidenced by the isotopic composition of nitrate and ammonium. Geochem Geophys. 2012; 13(2):1–23. doi: 10.1029/2011GC003863

40. Fabri MC, Bargain A, Briand P, Gebruk A, Fouquet Y, Morineaux M, et al. The hydrothermal vent community of a new deep-sea field, Ashadze-1, 12°58´N on the Mid-Atlantic Ridge. J Mar Biol Assoc UK. 2011; 91(1):1–13. doi: 10.1017/S0025315410000731

41. Van Dover CL, Fry B. Stable isotopic compositions of hydrothermal vent organisms. Mar Biol. 1989; 102(2):257–263. doi: 10.1007/BF00428287

42. Copley JTP, Tyler PA, Van Dover CL, Schultz A, Dickson P, Singh S, et al. Subannual Temporal Variation in Faunal Distributions at the TAG Hydrothermal Mound (26°N, Mid-Atlantic Ridge). Mar Ecol. 1999; 20(3):291–306. doi: 10.1046/j.1439-0485.1999.2034076.x

43. Kim ES, Sakai H, Hashimoto J, Yanagisawa F, Ohta S. Sulfur isotopic ratios of hydrothermal vent-animals at Ogasawara Arc and Mid-Okinawa Trough–Evidence for microbial of hydrogen sulfide at low-temperature submarine hydrothermal areas. Geochem J. 1989; 23(4):195–208. doi: 10.2343/geochemj.23.195

44. Mekhtiyeva VL, Pankiva RG, Gavrilov EY. Distribution and isotopic composition of forms of sulfur in water animals and plants. Geochem Int. 1976; 13(5):82–87.

45. Sakai H, Dickson FW. Experimental determination of the rate and equilibrium fractionation factors of sulfur isotope exchange between sulfate and sulfide in slightly acid solutions at 300°C and 1000 bars. Earth Planet Sci Lett. 1978; 39:151–161. doi: 10.1016/0012-821X(78)90151-6

46. Erickson KL, Macko SA, Van Dover CL. Evidence for a chemoautotrophically based food web at inactive hydrothermal vents (Manus Basin). Deep Sea Res Part II. 2009; 56(19):1577–1585. (doi: 10.1016/j.dsr2.2009.05.002)

47. Fry B, Gest H, Hayes JM. Sulfur isotopic composition of deep-sea hydrothermal vent animals. Nature. 1983; 306(5938): 51–52. doi: 10.1038/306051a0

48. Yamanaka T, Shimamura S, Nagashio H, Yamagami S, Onishi Y, Hyodo A, et al. A compilation of the stable isotopic compositions of carbon, nitrogen, and sulfur in soft body parts of animals collected from deep-sea hydrothermal vent and methane seep fields: variations in energy source and importance of subsurface microbial processes in the sediment-hosted systems. In: Ishibashi JI, Okino K, Sunamura M, editors. Subseafloor Biosphere Linked to Hydrothermal Systems: TAIGA concept. Japan, Tokyo: Springer; 2015. pp 105–129.

49. Freytag JK, Girguis PR, Bergquist DC, Andras JP, Childress JJ, Fisher CR. A paradox resolved: sulfide acquisition by roots of seep tubeworms sustains net chemoautotrophy. Proc Natl Acad Sci. 2001; 98(23):13408–13413. doi: 10.1073/pnas.231589498 11687647

50. Lalli C, Parsons TR. Biogeochemical Oceanography: An Introduction. Pergamon Press; 1997.


Článek vyšel v časopise

PLOS One


2019 Číslo 11