Advertisement

Coral Reefs

, 30:555 | Cite as

Uptake of picophytoplankton, bacterioplankton and virioplankton by a fringing coral reef community (Ningaloo Reef, Australia)

  • N. L. Patten
  • A. S. J. Wyatt
  • R. J. Lowe
  • A. M. Waite
Report

Abstract

We examined the importance of picoplankton and virioplankton to reef trophodynamics at Ningaloo Reef, (north-western Australia), in May and November 2008. Picophytoplankton (Prochlorococcus, Synechococcus and picoeukaryotes), bacterioplankton (inclusive of bacteria and Archaea), virioplankton and chlorophyll a (Chl a) were measured at five stations following the consistent wave-driven unidirectional mean flow path of seawater across the reef and into the lagoon. Prochlorococcus, Synechococcus, picoeukaryotes and bacterioplankton were depleted to similar levels (~40% on average) over the fore reef, reef crest and reef flat (=‘active reef’), with negligible uptake occurring over the sandy bottom lagoon. Depletion of virioplankton also occurred but to more variable levels. Highest uptake rates, m, of picoplankton occurred over the reef crest, while uptake coefficients, S (independent of cell concentration), were similarly scaled over the reef zones, indicating no preferential uptake of any one group. Collectively, picophytoplankton, bacterioplankton and virioplankton accounted for the uptake of 29 mmol C m−2 day−1, with Synechococcus contributing the highest proportion of the removed C. Picoplankton and virioplankton accounted for 1–5 mmol N m−2 day−1 of the removed N, with bacterioplankton estimated to be a highly rich source of N. Results indicate the importance of ocean–reef interactions and the dependence of certain reef organisms on picoplanktonic supply for reef-level biogeochemistry processes.

Keywords

Coral reef Picoplankton Virus Uptake Ningaloo Reef Indian Ocean 

Notes

Acknowledgments

We thank D. Krikke, F. McGregor, S. Hinrichs, A. Chalmers and K. Meyers for assistance in the field. Funding was provided by grants from the University of Western Australia (UWA), The Faculty of Engineering, Computing and Mathematical Sciences and the Western Australian Marine Science Institution (Node 3) to A.M.W.; an Australian Research Council (ARC) Discovery Grant #DP0663670 to A.M.W. et al., an ARC Discovery Grant #DP0770094 to R.J.L. and postdoctoral research funding from UWA and The Australian Institute of Marine Science to N.L.P. The authors acknowledge the facilities, scientific and technical assistance of the Australian Microscopy & Microanalysis Research Facility at the Centre for Microscopy, Characterisation and Analysis, UWA, a facility funded by The University, State and Commonwealth Governments. We finally thank two anonymous reviewers who provided valuable comments that improved this manuscript.

Supplementary material

338_2011_777_MOESM1_ESM.doc (28 kb)
ESM, Table 1 Conversion factors from literature values for estimates of carbon (C) and nitrogen (N) biomass for picophytoplankton, bacterioplankton and virioplankton. (DOC 30 kb)
338_2011_777_MOESM2_ESM.doc (54 kb)
ESM, Table 2 Changes (given as cell numbers and as a %) in Prochlorococcus (Pro), Synechococcus (Syn), picoeukaryotes (Peuk), bacterioplankton (Bac) and virioplankton (Vir) between adjacent stations on individual sampling days in May and November 2008. Note that positive values indicate depletion (= uptake) of cells between adjacent stations. nd = not determined because samples from one or both stations were missing. (DOC 43 kb)
338_2011_777_MOESM3_ESM.eps (443 kb)
ESM, Fig. 1 Uptake rates m (× 109 cell m−2 d−1) versus cell concentrations (× 103 cells ml−1) over the reef crest and reef flat for (a) Prochlorococcus, (b) Synechococcus, (c) picoeukaryotes, (d) bacterioplankton and (e) virioplankton. Black closed circles denote values in May and open circles denote values in November 2008. Significant relationships occurred for (a) Prochlorococcus; r2 = 0.75, F1,16 = 48.76, p < 0.001, (b) Synechococcus: r2 = 0.60, F1,16 = 24.13, p < 0.001, (c) picoeukaryotes; r2 = 0.61, F1,16 = 24.89, p < 0.001 (lines represent the best least squares fit). The relationship was not significant for bacterioplankton; r2 = 0.13, F1,16 = 2.40, p = 0.14 and virioplankton; r2 = 0.07, F1,16 = 1.20, p = 0.288 (hence no regression lines are included). Note that the scaling of cell concentrations (x axis) and uptake rates m (y axis) differs for each group of cells. (EPS 443 kb)
338_2011_777_MOESM4_ESM.eps (3.4 mb)
ESM, Fig. 2 Positive uptake coefficients S (m d−1) versus current velocity U (m s−1) over thereef crest and reef flat for (a) Prochlorococcus, (b) Synechococcus, (c) picoeukaryotes, (d)heterotrophic microbes and (e) viruses. Black closed circles denote values in May and opencircles represent values in November 2008. Significant relationship between water velocity Uand reef crest and flat uptake coefficients S during May and Nov 2008 for (a)Prochlorococcus; r2 = 0.19; F1,8 = 4.01, p = 0.05, (b) Synechococcus; r2 = 0.63, F1,13 = 53.1, p< 0.001, (c) picoeukaryotes r2 = 0.41, F1,13 = 21.13, p < 0.001, (d) bacterioplankton; r2=0.27,F1,14 = 12.12, p < 0.01, and (e) virioplankton; r2 = 0.09, F1,8 = 2.56, p = 0.12. (EPS 3,497 kb)

References

  1. Agostini S, Suzuki Y, Casareto BE, Nakano Y, Hidaka M, Badrun N (2009) Coral symbiotic complex: Hypothesis through vitamin B12 for a new evaluation. Galaxea 11:1–11CrossRefGoogle Scholar
  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  3. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth, UKGoogle Scholar
  4. Ayukai T (1995) Retention of phytoplankton and planktonic microbes on coral reefs within the Great Barrier Reef, Australia. Coral Reefs 14:141–147CrossRefGoogle Scholar
  5. Bertilsson S, Berglund O, Karl D, Chisholm SW (2003) Elemental composition of marine Prochlorococcus and Synechococcus: Implications for the ecological stoichiometry of the sea. Limnol Oceanogr 48:1721–1731CrossRefGoogle Scholar
  6. Brussaard CPD (2004) Optimization of procedures for counting viruses by flow cytometry. Appl Environ Microbiol 70:1506–1513CrossRefPubMedPubMedCentralGoogle Scholar
  7. Caron DA, Dam HG, Lessard EJ, Madin LP, Malone TC, Napp JM, Peele ER, Roman MR, Youngbluth MJ (1995) The contribution of microorganisms to particulate carbon and nitrogen in surface waters of the Sargasso Sea near Bermuda. Deep-Sea Res 42:943–972CrossRefGoogle Scholar
  8. Charpy L, Blanchot J (1999) Picophytoplankton biomass, community structure and productivity in the Great Astrolabe Lagoon, Fiji. Coral Reefs 18:255–262CrossRefGoogle Scholar
  9. Crosbie ND, Furnas M (2001a) Net growth rates of picocyanobacteria and nano-/microphytoplankton inhabiting shelf waters of the central (17°S) and southern (20°S) Great Barrier Reef. Aquat Microb Ecol 24:209–224CrossRefGoogle Scholar
  10. Crosbie ND, Furnas MJ (2001b) Abundance, distribution and flow-cytometric characterization of picophytoprokaryote populations in central (17°S) and southern (20°S) shelf waters of the Great Barrier Reef. J Plankton Res 23:809–828CrossRefGoogle Scholar
  11. Dinsdale EA, Pantos O, Smigra S, Edwards R, Angly F, Wegley L, Hatay M, Hall D, Brown E, Haynes M, Krause L, Sala E, Sandin SA, Vega Thurber R, Willis BL, Azam F, Knowlton N, Rohwer F (2008) Microbial ecology of four coral atolls in the Northern Line Islands. PLoS ONE 3(2):e1584. doi: 10.1371/journalpone0001584 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Fabricius KE, Dommisse M (2000) Depletion of suspended particulate matter over coastal reef communities dominated by zooxanthellate soft corals. Mar Ecol Prog Ser 196:157–167CrossRefGoogle Scholar
  13. Fagerbakke KM, Heldal M, Norland S (1996) Content of carbon, nitrogen, oxygen, sulfur and phosphorous in native and cultured bacteria. Aquat Microb Ecol 10:15–27CrossRefGoogle Scholar
  14. Falter JL, Atkinson MJ, Schar DW, Lowe RJ, Monismith SG (2011) Short-term coherency between gross primary production and community respiration in an algal-dominated reef flat. Coral Reefs 30:53–58CrossRefGoogle Scholar
  15. Feng M, Wild-Allen K (2009) The Leeuwin Current. In: Liu KK, Atkinson L (eds) Carbon and nutrient fluxes in continental margins: a global synthesis. Springer, New YorkGoogle Scholar
  16. Feng M, Meyers G, Pearce A, Wijffels S (2003) Annual and interannual variations of the Leeuwin Current at 32°S. J Geophys Res Oceans 108:3355. doi: 10.1029/2002JC001763 CrossRefGoogle Scholar
  17. Ferrier D (1991) Net uptake of dissolved free amino acids by four scleractinian corals. Coral Reefs 10:183–187CrossRefGoogle Scholar
  18. Ferrier-Pagés C, Furla P (2001) Pico- and nanoplankton biomass and production in the two largest atoll lagoons of French Polynesia. Mar Ecol Prog Ser 211:63–76CrossRefGoogle Scholar
  19. Ferrier-Pagés C, Gattuso JP (1998) Biomass, production and grazing rates of pico- and nanoplankton in coral reef waters (Miyako Island, Japan). Microb Ecol 35:46–57CrossRefPubMedGoogle Scholar
  20. Ferrier-Pagés C, Allemand D, Gattuso JP, Jaubert J, Rassoulzadegan F (1998) Microheterotrophy in the zooxanthellate coral Stylophora pistillata: effects of light and ciliate density. Limnol Oceanogr 43:1639–1648CrossRefGoogle Scholar
  21. Fu F-X, Warner ME, Zhang Y, Feng Y, Hutchins DA (2007) Effects of increased temperature and CO2 on photosynthesis, growth and elemental ratios of marine Synechococcus and Prochlorococcus (cyanobacteria). J Phycol 43:485–496CrossRefGoogle Scholar
  22. Fukuda R, Ogawa H, Nagata T, Koike I (1998) Direct determination of carbon and nitrogen contents of natural bacterial assemblages in marine environments. Appl Environ Microbiol 64:3352–3358PubMedPubMedCentralGoogle Scholar
  23. Genin A, Monismith SG, Reidenbach MA, Yahel G, Koseff JR (2009) Intense benthic grazing of phytoplankton in a coral reef. Limnol Oceanogr 54:938–951CrossRefGoogle Scholar
  24. Ginsburg RN (1983) Geological and biological roles of cavities in coral reefs. In: Barnes DJ (ed) Perspectives on coral reefs. Australian Institute of Marine Science, pp 148–153Google Scholar
  25. Glynn PW (1973) Ecology of a Caribbean coral reef: Porites reef-flat biotop. 2. Plankton community with evidence for depletion. Mar Biol 22:1–21CrossRefGoogle Scholar
  26. Gobler CJ, Hutchins DA, Fisher NS, Cosper EM, Wilhemy-Sanudo SA (1997) Release and bioavailability of C, N, P, Se and Fe following viral release of a marine chrysophyte. Limnol Oceanogr 42:1492–1504CrossRefGoogle Scholar
  27. Goldberg WM (2002) Gastrodermal structure and feeding responses in the scleractinian Mycetophyllia reesi, a coral with novel digestive filaments. Tissue Cell 34:246–261CrossRefPubMedGoogle Scholar
  28. Grossart H-P, Allgaier M, Passow U, Riebesell U (2006) Testing the effect of CO2 concentration on the dynamics of marine heterotrophic bacterioplankton. Limnol Oceanogr 51:1–11CrossRefGoogle Scholar
  29. Grottoli AG, Rodriguez LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189CrossRefPubMedGoogle Scholar
  30. Grover R, Maguer JF, Allemand D, Ferrier-Pages C (2003) Nitrate uptake in the Scleractinian coral Stylophora pistillata. Limnol Oceanogr 48:2266–2274CrossRefGoogle Scholar
  31. Grover R, Maguer JF, Allemand D, Ferrier-Pages C (2006) Urea uptake by the scleractinian coral Stylophora pistillata. J Exp Mar Biol Ecol 332:216–225CrossRefGoogle Scholar
  32. Gundersen K, Heldal M, Norland S, Purdie DA, Knap AH (2002) Elemental C, N and P cell content of individual bacteria collected at the Bermuda Atlantic time-series study (BATS) site. Limnol Oceanogr 47:1525–1530CrossRefGoogle Scholar
  33. Hadas E, Marie D, Shpigel M, Ilan M (2006) Virus predation by sponges is a new nutrient-flow pathway in coral reef food webs. Limnol Oceanogr 51:1548–1550CrossRefGoogle Scholar
  34. Hanson CA, Pattiaratchi C, Waite AM (2005) Sporadic upwelling on a downwelling coast: Phytoplankton responses to spatially variable nutrient dynamics off the Gascoyne region of Western Australia. Cont Shelf Res 25:1561–1582CrossRefGoogle Scholar
  35. Heldal M, Scanlan DJ, Norland S, Thingstad F, Mann NH (2003) Elemental composition of single cells of various strains of marine Prochlorococcus and Synechococcus using x-ray microanalysis. Limnol Oceanogr 48:1723–1743CrossRefGoogle Scholar
  36. Hewson I, Vargo GA, Fuhrman JA (2003) Bacterial diversity in shallow oligotrophic marine benthos and overlying waters: Effects of virus infection, containment, and nutrient enrichment. Microb Ecol 46:322–336CrossRefPubMedGoogle Scholar
  37. Houlbrèque F, Tambuttè E, Ferrier-Pagés C (2003) Effects of zooplankton availability on the rates of photosynthesis, and tissue and skeletal growth in the scleractinian coral Stylophora pistillata. J Exp Mar Biol Ecol 296:145–166CrossRefGoogle Scholar
  38. Houlbrèque F, Tambuttè E, Richard C, Ferrier-Pagés C (2004a) Importance of a micro-diet for scleractinian corals. Mar Ecol Prog Ser 282:151–160CrossRefGoogle Scholar
  39. Houlbrèque F, Tambuttè E, Allemand D, Ferrier-Pagés C (2004b) Interactions between zooplankton feeding, photosynthesis and skeletal growth in the Scleractinian coral Stylophora pistillata. J Exp Biol 207:1461–1469CrossRefPubMedGoogle Scholar
  40. Houlbrèque F, Delesalle B, Blanchot J, Montel Y, Ferrier-Pagès C (2006) Picoplankton removal by the coral reef community of La Prévoyante, Mayotte Island. Aquat Microb Ecol 44:59–70CrossRefGoogle Scholar
  41. IPCC (2007) Climate change 2007: The physical science basis. In: Solomon S, Qin D, Manning M, Chen Z, Marquis MC, Averyt K, Tignor M, Miller HL (eds) Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Intergovernmental panel on Climate Change. Cambridge University Press, Cambridge, UK and New York, USAGoogle Scholar
  42. Kappner I, Al-Moghrabi SM, Richter C (2000) Mucus-net feeding by the vermetid gastropod Dendropoma maxima in coral reefs. Mar Ecol Prog Ser 204:309–313CrossRefGoogle Scholar
  43. Marie D, Partensky F, Vaulot D, Brussard C (1999) Enumeration of phytoplankton, bacteria, and viruses in marine samples. In: Robinson JPEA (ed) Current protocols in cytometry, suppl 10. John Wiley & Sons, Inc, New York, pp 11.11.11–11.11.15Google Scholar
  44. Middelboe M, Jorgensen NOG (2006) Viral lysis of bacteria: an important source of dissolved amino acids and cell wall compounds. J Mar Biol Assoc UK 86:605–612CrossRefGoogle Scholar
  45. Miyajima T, Suzumura M, Umezawa Y, Koike I (2001) Microbiological nitrogen transformation in carbonate sediments of a coral-reef lagoon and associated seagrass beds. Mar Ecol Prog Ser 217:273–286CrossRefGoogle Scholar
  46. Naumann MS, Richard C, el-Zibdah M, Wild C (2009) Coral mucus as an efficient trap for picoplanktonic cyanobacteria: implications for pelagic–benthic coupling in the reef ecosystem. Mar Ecol Prog Ser 385:65–76CrossRefGoogle Scholar
  47. Parsons TR, Maita Y, Lalli CM (1984) A manual for chemical and biological methods for seawater analysis. Pergamon Press, New YorkGoogle Scholar
  48. Partensky F, Blanchot J, Vaulot D (1999) Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: a review. In: Charpy L, Larkum AWD (eds) Marine cyanobacteria. Bulletin de l’Institut Océanographique, Monaco, pp 457–475Google Scholar
  49. Patten NL, Mitchell JG, Middelboe M, Seuront L, Harrison PL, Glud RN (2008) Bacterial and viral dynamics during a mass coral spawning period on the Great Barrier Reef. Aquat Microb Ecol 50:201–220CrossRefGoogle Scholar
  50. Pearce AF (1991) Eastern Boundary Currents of the southern hemisphere. J R Soc West Aust 74:35–45Google Scholar
  51. Pinnegar JK, Polunin NVC (2006) Planktivorous damselfish support significant nitrogen and phosphorous fluxes to Mediterranean reefs. Mar Biol 148:1089–1099CrossRefGoogle Scholar
  52. Ribes M, Atkinson MJ (2007) Effects of water velocity on picoplankton uptake by coral reef communities. Coral Reefs 26:413–421CrossRefGoogle Scholar
  53. Ribes M, Coma R, Atkinson MJ, Kinzie RA III (2003) Particle removal by coral reef communities: picoplankton is a major source of nitrogen. Mar Ecol Prog Ser 257:13–23CrossRefGoogle Scholar
  54. Richter C, Wunsch M (1999) Cavity-dwelling suspension feeders in coral reefs a new link in reef trophodynamics. Mar Ecol Prog Ser 188:105–116CrossRefGoogle Scholar
  55. Richter C, Wunsch M, Rasheed M, Kötter I, Badran MI (2001) Endoscopic exploration of Red Sea coral reefs reveals dense populations of cavity-dwelling sponges. Nature 413:726–730CrossRefPubMedGoogle Scholar
  56. Scheffers SR, Nieuwland G, Bak RPM, van Duyl FC (2004) Removal of bacteria and nutrient dynamics within the coral reef framework of Curacao (Netherlands Antilles). Coral Reefs 23:413–422CrossRefGoogle Scholar
  57. Sebens KP, Vandersall KS, Savina LA, Graham KR (1996) Zooplankton capture by two scleractinian corals, Madracis mirabilis and Monastrea cavernosa, in a field enclosure. Mar Biol 127:303–318CrossRefGoogle Scholar
  58. Seymour JR, Patten NL, Bourne DG, Mitchell JG (2005) Spatial dynamics of virus-like particles and heterotrophic bacteria within a shallow coral reef system. Mar Ecol Prog Ser 288:1–8CrossRefGoogle Scholar
  59. Smith RL, Huyer A, Godfrey JS, Church JA (1991) The Leeuwin Current off Western Australia, 1986–1987. J Phys Oceanogr 21:323–345CrossRefGoogle Scholar
  60. Sorokin YI (1973) On the feeding of some Scleractinian corals with bacteria and dissolved organic matter. Limnol Oceanogr 18:380–385CrossRefGoogle Scholar
  61. Stockner JG (1988) Phototrophic picoplankton: an overview from marine and freshwater ecosystems. Limnol Oceanogr 33:765–775Google Scholar
  62. Suttle CA (2007) Marine viruses major players in the global ecosystem. Nat Rev Microbiol 5:801–811CrossRefPubMedGoogle Scholar
  63. Tortell PD, Maldonado MT, Granger J, Price NM (1999) Marine bacteria and biogeochemical cycling of iron in the oceans. FEMS Microbiol Ecol 29:1–11CrossRefGoogle Scholar
  64. Verity PG, Robertson CY, Tronzo CR, Andrews MG, Nelson JR, Sieracki ME (1992) Relationship between cell volume and the carbon and nitrogen content of marine photosynthetic nanoplankton. Limnol Oceanogr 37:1434–1446CrossRefGoogle Scholar
  65. Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127–181CrossRefPubMedGoogle Scholar
  66. Wild C, Rasheed M, Werner U, Franke U, Johnstone R, Huettel M (2004) Degradation and mineralization of coral mucus in reef environments. Mar Ecol Prog Ser 267:159–171CrossRefGoogle Scholar
  67. Wilhelm SW, Suttle CA (1999) Viruses and nutrient cycles in the sea. Bioscience 49:781–788CrossRefGoogle Scholar
  68. Woo M, Pattiaratchi C, Schroeder W (2006) Summer surface circulation along the Gascoyne continental shelf, Western Australia. Cont Shelf Res 26:132–152CrossRefGoogle Scholar
  69. Wyatt ASJ, Lowe RJ, Humphries S, Waite AM (2010) Particulate nutrient fluxes over a fringing coral reef: relevant scales of phytoplankton production and mechanisms of supply. Mar Ecol Prog Ser 405:113–130CrossRefGoogle Scholar
  70. Yahel G, Post AF, Fabricius K, Marie D, Vaulot D, Genin A (1998) Phytoplankton distribution and grazing near coral reefs. Limnol Oceanogr 43:551–563CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • N. L. Patten
    • 1
    • 3
    • 4
  • A. S. J. Wyatt
    • 1
    • 3
    • 5
  • R. J. Lowe
    • 2
    • 3
  • A. M. Waite
    • 1
    • 3
  1. 1.School of Environmental Systems Engineering, M015The University of Western AustraliaCrawleyAustralia
  2. 2.School of Earth and Environment, M004The University of Western AustraliaCrawleyAustralia
  3. 3.The Oceans Institute, M470The University of Western AustraliaCrawleyAustralia
  4. 4.Australian Institute of Marine Science, The Oceans Institute, M470The University of Western AustraliaCrawleyAustralia
  5. 5.Scripps Institution of OceanographyUniversity of CaliforniaSan DiegoUSA

Personalised recommendations