Spatial Differences in East Scotia Ridge Hydrothermal Vent Food Webs: Influences of Chemistry, Microbiology and Predation on Trophodynamics

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Reid, William D K ^a   Sweeting, Christopher J ^a   Wigham, Ben D ^a   Zwirglmaier, Katrin ^b,e   Hawkes, Jeffrey A ^c   McGill, Rona A R ^d   Linse, Katrin ^b   Polunin, Nicholas V C ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b BRITISH ANTARCTIC SURVEY   (United Kingdom)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^d SCOTTISH UNIVERSITIES ENVIRONMENTAL RESEARCH CENTRE   (United Kingdom)

^e TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON 13; NITROGEN 15; SULFUR; TRICARBOXYLIC ACID;

ANEMONE; ANIMAL TISSUE; ARTICLE; CARBON FIXATION; CONTROLLED STUDY; CRAB; ENVIRONMENTAL PARAMETERS; EPIBIONT; FEMALE; FOOD CHAIN; FOOD WEB; GAMMAPROTEOBACTERIA; GASTROPOD; GEOGRAPHIC DISTRIBUTION; HYDROTHERMAL VENT; MALE; MICROBIOLOGY; NONHUMAN; PHOTOSYNTHESIS; POPULATION DYNAMICS; PREDATION; SPECIES DIFFERENTIATION; TROPHODYNAMICS;

ANALYSIS OF VARIANCE; ANIMALS; ANTARCTIC REGIONS; CARBON ISOTOPES; FOOD CHAIN; GEOGRAPHY; HYDROTHERMAL VENTS; INORGANIC CHEMICALS; ISOTOPE LABELING; PREDATORY BEHAVIOR; SPATIAL ANALYSIS;

ACTINIARIA; DECAPODA (CRUSTACEA); GAMMAPROTEOBACTERIA; GASTROPODA; PELTOSPIROIDEA; THORACICA;

EID: 84878776105     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065553     Document Type: Article

References (59)

1. Kelley DS, Karson JA, Blackman DK, Fruh-Green GL, Butterfield DA, et al. (2001) An off-axis hydrothermal vent field near the Mid-Atlantic Ridge at 30°N Nature. 412: 145-149.
2. Staudigel H, Hart SR, Pile A, Bailey SE, Baker ET, et al. (2006) Vailulu'u seamount, Samoa: Life and death on an active submarine volcano. Proc Natl Acad Sci USA. 103: 6448-6453.
3. Tunnicliffe V, Juniper SK, Sibuet M (2003) Reducing environments of the deep-sea floor. In: Tyler PA, editor. Ecosystems of the Deep Ocean. Amsterdam: Elsevier Science. 81-110.
4. Cavanaugh CM, Gardiner SL, Jones ML, Jannasch HW, Waterbury JB, (1981) Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones- possible chemoautotrophic symbionts. Science 213: 340-342.
5. German CR, Ramirez-Llodra E, Baker MC, Tyler PA, (2011) Deep-water chemosynthetic ecosystem research during the Census of Marine Life decade and beyond: A proposed deep-ocean road map. PLoS ONE 6: 16.
6. German CR, Von Damm KL (2003) Hydrothermal Processes. In: Elderfield H, editor. The ocean and marine geochemistry. Oxford: Elsevier. 181-222.
7. Karl DM (1995) Ecology of free-living, hydrothermal vent microbial communities. In: Karl DM, editor. The microbiology of deep-sea hydrothermal vents. Boca Raton: CRC Press Inc. 35-124.
8. McCollom TM, Shock EL, (1997) Geochemical constraints on chemolithoautotrophic metabolism by microorganisms in seafloor hydrothermal systems. Geochim Cosmochim Acta 61: 4375-4391.
9. Campbell BJ, Cary SC, (2004) Abundance of reverse tricarboxylic acid cycle genes in free-living microorganisms at deep-sea hydrothermal vents. Appl Environ Microbiol 70: 6282-6289.
10. Desbruyeres D, Alaysedanet AM, Ohta S, Antoine E, Barbier G, et al. (1994) Deep-sea hydrothermal communities in the southwestern Pacific back-arc basins (the North Fiji and Lau Basins)- composition, microdistribution and food web. Mar Geol 116: 227-242.
11. Hugler M, Sievert SM (2011) Beyond the Calvin Cycle: Autotrophic carbon fixation in the ocean. Ann Rev Mar Sci. Palo Alto: Annual Reviews. 261-289.
12. De Busserolles F, Sarrazin J, Gauthier O, Gelinas Y, Fabri MC, et al. (2009) Are spatial variations in the diets of hydrothermal fauna linked to local environmental conditions? Deep Sea Res Part II Top Stud Oceanogr 56: 1649-1664.
13. Riou V, Colaco A, Bouillon S, Khripounoff A, Dando PR, et al. (2010) Mixotrophy in the deep sea: a dual endosymbiotic hydrothermal mytilid assimilates dissolved and particulate organic matter Mar Ecol Prog Ser. 405: 187-201.
14. Colaco A, Dehairs F, Desbruyeres D, (2002) Nutritional relations of deep-sea hydrothermal fields at the Mid-Atlantic Ridge: a stable isotope approach. Deep Sea Res Part I Oceanogr Res Pap 49: 395-412.
15. Rau GH, Hedges JI, (1979) Carbon-13 depletion in a hydrothermal vent mussel- suggestion of a chemosynthetic food source. Science 203: 648-649.
16. Van Dover CL, Fry B, (1994) Microorganisms as food resources at deep-sea hydrothermal vents. Limnol Oceanogr 39: 51-57.
17. Levin LA, Mendoza GF, Konotchick T, Lee R, (2009) Macrobenthos community structure and trophic relationships within active and inactive Pacific hydrothermal sediments. Deep Sea Res Part II Top Stud Oceanogr 56: 1632-1648.
18. Limen H, Juniper SK, (2006) Habitat controls on vent food webs at Eifuku Volcano, Mariana Arc. Cah Biol Mar 47: 449-455.
19. Van Dover CL, (2002) Trophic relationships among invertebrates at the Kairei hydrothermal vent field (Central Indian Ridge). Mar Biol 141: 761-772.
20. German CR, Livermore RA, Baker ET, Bruguier NI, Connelly DP, et al. (2000) Hydrothermal plumes above the East Scotia Ridge: an isolated high-latitude back-arc spreading centre. Earth Planet Sci Lett 184: 241-250.
21. Rogers AD, Tyler PA, Connelly DP, Copley JT, James R, et al. (2012) The discovery of new deep-sea hydrothermal vent communities in the Southern Ocean and implications for biogeography. PLoS Biol 10: e1001234.
22. Marsh L, Copley JT, Huvenne VAI, Linse K, Reid WDK, et al. (2012) Microdistribution of faunal assemblages at deep-sea hydrothermal vents in the Southern Ocean. PLoS ONE 7: e48348.
23. Bergquist DC, Eckner JT, Urcuyo IA, Cordes EE, Hourdez S, et al. (2007) Using stable isotopes and quantitative community characteristics to determine a local hydrothermal vent food web. Mar Ecol Prog Ser 330: 49-65.
24. Van Dover CL, Fry B, (1989) Stable isotopic compositions of hydrothermal vent organisms. Mar Biol 102: 257-263.
25. Fisher CR, Childress JJ, Macko SA, Brooks JM, (1994) Nutritional interactions in Galapagos Rift hydrothermal vent communities- inferences from stable carbon and nitrogen isotope analyses. Mar Ecol Prog Ser 103: 45-55.
26. Guy RD, Fogel ML, Berry JA, (1993) Photosynthetic fractionation of the stable isotopes of oxygen and carbon. Plant Physiology 101: 37-47.
27. Robinson JJ, Scott KM, Swanson ST, O'Leary MH, Horken K, et al. (2003) Kinetic isotope effect and characterization of form II RuBisCO from the chemoautotrophic endosymbionts of the hydrothermal vent tubeworm Riftia pachyptila. Limnol Oceanogr 48: 48-54.
28. Roeske CA, O'Leary MH, (1984) Carbon isotope effects on the enzyme-catalyzed carboxylation of ribulose bisphosphate. Biochemistry 23: 6275-6284.
29. House CH, Schopf JW, Stetter KO, (2003) Carbon isotopic fractionation by Archaeans and other thermophilic prokaryotes. Org Geochem 34: 345-356.
30. Suzuki Y, Sasaki T, Suzuki M, Nogi Y, Miwa T, et al. (2005) Novel chemoautotrophic endosymbiosis between a member of the Epsilonproteobacteria and the hydrothermal-vent gastropod Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean. Appl Environ Microbiol 71: 5440-5450.
31. Wirsen CO, Sievert SM, Cavanaugh CM, Molyneaux SJ, Ahmad A, et al. (2002) Characterization of an autotrophic sulfide-oxidizing marine Arcobacter sp that produces filamentous sulfur. Appl Environ Microbiol 68: 316-325.
32. Michener RH, Kaufman L (2007) Stable isotope ratios as tracers in marine food webs: an update. In: Michener RH, Lajtha K, editors. Stable isotopes in ecology and environmental science. 2nd ed. Singapore: Blackwell Publishing. 238-282.
33. Herzig PM, Hannington MD, Arribas A Jr, (1998) Sulfur isotopic composition of hydrothermal precipitates from the Lau back-arc: implications for magmatic contributions to seafloor hydrothermal systems. Mineralium Deposita 33: 226-237.
34. Erickson KL, Macko SA, Van Dover CL, (2009) Evidence for a chemoautotrophically based food web at inactive hydrothermal vents (Manus Basin). Deep Sea Res Part II Top Stud Oceanogr 56: 1577-1585.
35. Reid WDK, Wigham BD, McGill RAR, Polunin NVC, (2012) Elucidating trophic pathways in benthic deep-sea assemblages of the Mid-Atlantic Ridge north and south of the Charlie-Gibbs Fracture Zone. Mar Ecol Prog Ser 463: 89-103.
36. Layman CA, Arrington DA, Montana CG, Post DM, (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88: 42-48.
37. Quinn GP, Keough MJ (2002) Experimental Design and Data Analysis for Biologists. Cambridge: Cambridge University Press. 537 p.
38. R Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/.
39. Brooks JM, Kennicutt MC, Fisher CR, Macko SA, Cole K, et al. (1987) Deep-sea hydrocarbon seep communities- evidence for energy and nutritional carbon sources. Science 238: 1138-1142.
40. Childress JJ, Fisher CR, (1992) The biology of hydrothermal vent animals- physiology, biochemistry and autotrophic symbioses. Oceanogr Mar Biol 30: 337-441.
41. Campbell BJ, Engel AS, Porter ML, Takai K, (2006) The versatile epsilon-Proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4: 458-468.
42. Campbell BJ, Stein JL, Cary SC, (2003) Evidence of chemolithoautotrophy in the bacterial community associated with Alvinella pompejana, a hydrothermal vent polychaete. Appl Environ Microbiol 69: 5070-5078.
43. Levesque C, Juniper SK, Marcus J, (2003) Food resource partitioning and competition among alvinellid polychaetes of Juan de Fuca Ridge hydrothermal vents. Mar Ecol Prog Ser 246: 173-182.
44. Suzuki Y, Kojima S, Sasaki T, Suzuki M, Utsumi T, et al. (2006) Host-symbiont relationships in hydrothermal vent gastropods of the genus Alviniconcha from the Southwest Pacific. Appl Environ Microbiol 72: 1388-1393.
45. Thurber AR, Jones WJ, Schnabel K, (2011) Dancing for food in the deep sea: bacterial farming by a new species of yeti crab. PLoS ONE 6: e26243.
46. Flores GE, Campbell JH, Kirshtein JD, Meneghin J, Podar M, et al. (2011) Microbial community structure of hydrothermal deposits from geochemically different vent fields along the Mid-Atlantic Ridge. Environ Microbiol 13: 2158-2171.
47. Takai K, Nunoura T, Horikoshi K, Shibuya T, Nakamura K, et al. (2009) Variability in microbial communities in black smoker chimneys at the NW Caldera vent field, Brothers Volcano, Kermadec Arc. Geomicrobiol J 26: 552-569.
48. Nakagawa S, Takai K, (2008) Deep-sea vent chemoautotrophs: diversity, biochemistry and ecological significance. FEMS Microbiol Ecol 65: 1-14.
49. Vetter RD, Fry B, (1998) Sulfur contents and sulfur-isotope compositions of thiotrophic symbioses in bivalve molluscs and vestimentiferan worms. Mar Biol 132: 453-460.
50. Luther GW, Rozan TF, Taillefert M, Nuzzio DB, Di Meo C, et al. (2001) Chemical speciation drives hydrothermal vent ecology. Nature 410: 813-816.
51. Chikaraishi Y, Ogawa NO, Kashiyama Y, Takano Y, Suga H, et al. (2009) Determination of aquatic food-web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnol Oceanogr Methods 7: 740-750.
52. McClelland JW, Montoya JP, (2002) Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 83: 2173-2180.
53. Markert S, Arndt C, Felbeck H, Becher D, Sievert SM, et al. (2007) Physiological proteomics of the uncultured endosymbiont of Riftia pachyptila. Science 315: 247-250.
54. Suzuki Y, Sasaki T, Suzuki M, Tsuchida S, Nealson KH, et al. (2005) Molecular phylogenetic and isotopic evidence of two lineages of chemoautotrophic endosymbionts distinct at the subdivision level harbored in one host-animal type: The genus Alviniconcha (Gastropoda: Provannidae). FEMS Microbiol Lett 249: 105-112.
55. Trask JL, Van Dover CL, (1999) Site-specific and ontogenetic variations in nutrition of mussels (Bathymodiolus sp.) from the Lucky Strike hydrothermal vent field, Mid-Atlantic Ridge. Limnol Oceanogr 44: 334-343.
56. Levesque C, Juniper SK, Limen H, (2006) Spatial organization of food webs along habitat gradients at deep-sea hydrothermal vents on Axial Volcano, Northeast Pacific. Deep Sea Res Part I Oceanogr Res Pap 53: 726-739.
57. Levesque C, Limen H, Juniper SK, (2005) Origin, composition and nutritional quality of particulate matter at deep-sea hydrothermal vents on Axial Volcano, NE Pacific. Mar Ecol Prog Ser 289: 43-52.
58. Shank TM, Fornari DJ, Von Damm KL, Lilley MD, Haymon RM, et al. (1998) Temporal and spatial patterns of biological community development at nascent deep-sea hydrothermal vents (9 degrees 50′ N, East Pacific Rise). Deep Sea Res Part II Top Stud Oceanogr 45: 465-515.
59. Cuvelier D, Sarrazin J, Colaco A, Copley JT, Glover AG, et al. (2011) Community dynamics over 14 years at the Eiffel Tower hydrothermal edifice on the Mid-Atlantic Ridge. Limnol Oceanogr 56: 1624-1640.