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Estuarine Microbial Food Web Patterns in a Lake Erie Coastal Wetland

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Abstract

Composition and distribution of planktonic protists were examined relative to microbial food web dynamics (growth, grazing, and nitrogen cycling rates) at the Old Woman Creek (OWC) National Estuarine Research Reserve during an episodic storm event in July 2003. More than 150 protistan taxa were identified based on morphology. Species richness and microbial biomass measured via microscopy and flow cytometry increased along a stream–lake (Lake Erie) transect and peaked at the confluence. Water column ammonium (NH +4 ) uptake (0.06 to 1.82 μM N h–1) and regeneration (0.04 to 0.55 μM N h–1) rates, measured using 15NH +4 isotope dilution, followed the same pattern. Large light/dark NH +4 uptake differences were observed in the hypereutrophic OWC interior, but not at the phosphorus-limited Lake Erie site, reflecting the microbial community structural shift from net autotrophic to net heterotrophic. Despite this shift, microbial grazers (mostly choreotrich ciliates, taxon-specific growth rates up to 2.9 d–1) controlled nanophytoplankton and bacteria at all sites by consuming 76 to 110% and 56 to 97% of their daily production, respectively, in dilution experiments. Overall, distribution patterns and dynamics of microbial communities in OWC resemble those in marine estuaries, where plankton productivity increases along the river–sea gradient and reaches its maximum at the confluence.

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References

  1. H Arndt (1993) ArticleTitleRotifers as predators on components of the microbial food web (bacteria, heterotrophic flagellates, ciliates): a review. Hydrobiologia 255 231–246

    Google Scholar 

  2. TH Blackburn (1979) ArticleTitleMethod for measuring rates of NH +4 turnover in anoxic marine sediments using a 15NH +4 dilution technique. Appl Environ Microbiol 37 760–765 Occurrence Handle1:CAS:528:DyaE1MXks1agt7o%3D

    CAS  Google Scholar 

  3. A Bode Q Dortch (1996) ArticleTitleUptake and regeneration of inorganic nitrogen in coastal waters influenced by the Mississippi River: spatial and seasonal variations. J Plankton Res 18 2251–2268 Occurrence Handle1:CAS:528:DyaK2sXosl2kuw%3D%3D

    CAS  Google Scholar 

  4. KR Boissonneault-Cellineri M Mehta DJ Lonsdale DA Caron (2001) ArticleTitleMicrobial food web interactions in two Long Island embayments. Aquat Microb Ecol 26 139–155

    Google Scholar 

  5. J Caperon D Schell J Hirota E Laws (1979) ArticleTitleAmmonium excretion rates in Kaneohe Bay, Hawaii, measured by a 15 N isotope dilution technique. Mar Biol 54 33–40 Occurrence Handle1:CAS:528:DyaL3cXpvFaitQ%3D%3D

    CAS  Google Scholar 

  6. Caron, DA (2001) “Protistan herbivory and bacterivory.” In: Paul, JH (Ed.) Marine Microbiology. Methods Microbiol 30:289–315

    Article  Google Scholar 

  7. DA Caron RW Sanders EL Lim C Marrase LA Amaral S Whitney RB Aoki KG Porter (1993) ArticleTitleLight-dependent phagotrophy in the freshwater mixotrophic chrysophyte. Dynobrion cylindricum 25 93–111

    Google Scholar 

  8. HJ Carrick GL Fahnenstiel (1990) ArticleTitlePlanktonic protozoa in Lakes Huron and Michigan: Seasonal abundance and composition of ciliates and dinoflagellates. J Great Lakes Res 16 319–329

    Google Scholar 

  9. HJ Carrick GL Fahnenstiel EF Stoermer RG Wetzel (1991) ArticleTitleThe importance of zooplankton–protozoan trophic couplings in Lake Michigan. Limnol Oceanogr 36 1335–1345

    Google Scholar 

  10. HJ Carrick GL Fahnenstiel WD Taylor (1992) ArticleTitleGrowth and production of planktonic protozoa in Lake Michigan: In situ versus in vitro comparisons and importance to food web dynamics. Limnol Oceanogr 37 1221–1255

    Google Scholar 

  11. JB Cotner BA Biddanda (2002) ArticleTitleSmall players, large role: microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosystems 5 105–121 Occurrence Handle10.1007/s10021-001-0059-3 Occurrence Handle1:CAS:528:DC%2BD38XjtlCnur4%3D

    Article  CAS  Google Scholar 

  12. VV Dham AM Heredia S Wafar M Wafar (2002) ArticleTitleSeasonal variation in uptake and in situ regeneration of nitrogen in mangrove waters. Limnol Oceanogr 47 241–254 Occurrence Handle1:CAS:528:DC%2BD38XhtlSqsbw%3D

    CAS  Google Scholar 

  13. JR Dolan CL Gallegos (2001) ArticleTitleEstuarine diversity of tintinnids (planktonic ciliates). J Plankton Res 23 1009–1027 Occurrence Handle10.1093/plankt/23.9.1009

    Article  Google Scholar 

  14. GL Fahnenstiel AE Krause MJ McCormick HJ Carrick CL Schelske (1998) ArticleTitleStructure of the planktonic food web in the St. Lawrence Great Lakes. J Great Lakes Res 23 531–554

    Google Scholar 

  15. GL Fahnenstiel MJ McCormick GA Lang DG Redalje SE Lohrenz M Markowitz B Wagoner HJ Carrick (1995) ArticleTitleTaxon-specific growth and loss rates for dominant phytoplankton populations from the northern Gulf of Mexico. Mar Ecol Progr Ser 117 229–39

    Google Scholar 

  16. RL Ferguson EN Buckley AV Palumbo (1984) ArticleTitleResponse of marine bacterioplankton to differential filtration and confinement. Appl Environ Microbiol 47 49–55 Occurrence Handle1:STN:280:BiuC38nnsVc%3D Occurrence Handle6696422

    CAS  PubMed  Google Scholar 

  17. Foissner, W, Berger, H, Schaumburg, J (1999) Identification and ecology of limnetic plankton ciliates. Landesamtes für Wasserwirtschaft, Heft 3/99, Munich, pp 1–739

  18. PW Froneman (2002) ArticleTitleTrophic cascading in an oligotrophic temperate estuary, South Africa. J Plankton Res 24 807–816 Occurrence Handle10.1093/plankt/24.8.807

    Article  Google Scholar 

  19. CL Gallegos WN Vant KA Safi (1996) ArticleTitleMicrozooplankton grazing of phytoplankton in Manukau Harbor, New Zealand. N Z J Mar Fresh Res 30 423–434

    Google Scholar 

  20. WS Gardner HA Bootsma C Evans PA St. John (1995) ArticleTitleImproved chromatographic analysis of 15 N:14 N ratios in ammonium or nitrate for isotope addition experiments. Mar Chem 48 271–282 Occurrence Handle10.1016/0304-4203(94)00060-Q Occurrence Handle1:CAS:528:DyaK2MXjs1Ggt7s%3D

    Article  CAS  Google Scholar 

  21. Gardner, WS, Lavrentyev, PJ, Cavaletto, JF, McCarthy, MJ, Eadie, BJ, Johengen, TH, Cotner, JB (2004) Distribution and dynamics of nitrogen and microbial plankton in southern Lake Michigan during spring transition 1999-2000. J Geophys Res-Oceans 109 (C3): art. no. C03007

  22. PM Glibert (1988) Primary productivity and pelagic nitrogen cycling. TH Blackburn J Sørensen (Eds) Nitrogen Cycling in Coastal Marine Environments Wiley Chichester, UK 3–31

    Google Scholar 

  23. PM Glibert JC Goldman EJ Carpenter (1982) ArticleTitleSeasonal variations in the utilization of ammonium and nitrate by phytoplankton in Vineyard Sound, Massachusetts, USA. Mar Biol 70 237–249

    Google Scholar 

  24. N Godhantaraman S Uye (2003) ArticleTitleGeographical and seasonal variations in taxonomic composition, abundance and biomass of microzooplankton across a brackish-water lagoonal system of Japan. J Plankton Res 25 465–482 Occurrence Handle10.1093/plankt/25.5.465 Occurrence Handle1:CAS:528:DC%2BD3sXktVCgur8%3D

    Article  CAS  Google Scholar 

  25. I Hernandez SJ Hwang RT Heath (1996) ArticleTitleMeasurement of phosphomonoesterase activity with a radiolabelled glucose-6-phosphate. Role in the phosphorus requirement of phytoplankton and bacterioplankton in a temperate mesotrophic lake. Arch Hydrobiolog 137 265–280

    Google Scholar 

  26. SJ Hwang RT Heath (1997) ArticleTitleBacterial productivity and protistan bacterivory in coastal and offshore communities of Lake Erie. Can J Fish Aquat Sci 54 788–799 Occurrence Handle10.1139/cjfas-54-4-788

    Article  Google Scholar 

  27. A Iriarte I Madariaga M Revilla A Sarobe (2003) ArticleTitleShort-term variability in microbial food web dynamics in a shallow tidal estuary. Aquat Microb Ecol 31 145–161

    Google Scholar 

  28. FJ Jochem (2001) ArticleTitleMorphology and DNA content of bacterioplankton in the northern Gulf of Mexico: analysis by epifluorescence microscopy and flow cytometry. Aquat Microb Ecol 25 179–194

    Google Scholar 

  29. I Joint P Henriksen GA Fonnes D Bourne TF Thingstad B Riemann (2002) ArticleTitleCompetition for inorganic nutrients between phytoplankton and bacterioplankton in nutrient manipulated mesocosms. Aquat Microb Ecol 29 145–159

    Google Scholar 

  30. RL Kepner JR Pratt (1996) ArticleTitleCharacterization of surface-associated protozoan communities in a Lake Erie coastal wetlands (Old Woman Creek, Ohio). J Great Lakes Res 22 63–76

    Google Scholar 

  31. DM Klarer DF Millie (1992) ArticleTitleAquatic macrophytes and algae at Old Woman Creek estuary and other Great Lakes coastal wetlands. J Great Lakes Res 18 622–633

    Google Scholar 

  32. DM Klarer DF Millie (1994) ArticleTitleRegulation of phytoplankton dynamics in a Laurentian Great Lakes estuary. Hydrobiologia 286 97–108

    Google Scholar 

  33. AI Kopylov EV Moiseev (1983) ArticleTitleReproduction rate and production of zooflagellates in the northeastern part of the Black Sea. Okeanologya 23 640–643

    Google Scholar 

  34. CJ Krebs (1989) Ecological Methodology Harper-Collins New York

    Google Scholar 

  35. CM Lalli TR Parsons (1997) Biological Oceanography: An Introduction Butterworth-Heinemann Oxford

    Google Scholar 

  36. FL Landacre (1908) ArticleTitleThe protozoa of Sandusky Bay and vicinity. Proc Ohio Acad Sci 4 1–68

    Google Scholar 

  37. MR Landry (1994) ArticleTitleMethods and controls for measuring the grazing impact of planktonic protists. Mar Microb Food Webs 8 37–57

    Google Scholar 

  38. MR Landry RP Hassett (1982) ArticleTitleEstimating the grazing impact of marine micro-zooplankton. Mar Biol 67 283–288

    Google Scholar 

  39. PJ Lavrentyev HA Bootsma TH Johengen JF Cavaletto WS Gardner (1998) ArticleTitleMicrobial plankton response to recourse limitation: insights from the community structure and seston stoichiometry in Florida Bay, USA. Mar Ecol Prog Ser 165 45–57 Occurrence Handle1:CAS:528:DyaK1cXjtlGqtL8%3D

    CAS  Google Scholar 

  40. PJ Lavrentyev WS Gardner JF Cavaletto JR Beaver (1995) ArticleTitleEffects of the zebra mussel (Dreissena polymorpha Pallas) on protozoa and phytoplankton in Saginaw Bay, Lake Huron. J Great Lakes Res 21 545–557

    Google Scholar 

  41. PJ Lavrentyev WS Gardner JR Johnson (1997) ArticleTitleCascading trophic effects on aquatic nitrification: experimental evidence and potential implications. Aquat Microb Ecol 13 161–175

    Google Scholar 

  42. BSC Leadbeater (1993) Preparation of pelagic protists for electron microscopy. PF Kemp BF Sherr EB Sherr JJ Cole (Eds) Handbook of Methods in Aquatic Microbial Ecology Boca Raton Lewis 241–252

    Google Scholar 

  43. JS LeBlanc WD Taylor OE Johannsson (1997) ArticleTitleThe feeding ecology of the cyclopoid copepod Diacyclops thomasi in Lake Ontario. J Great Lakes Res 23 369–381

    Google Scholar 

  44. JC Lehrter JR Pennock GB McManus (1999) ArticleTitleMicrozooplankton grazing and nitrogen excretion across a surface estuarine–coastal interface. Estuaries 22 113–125 Occurrence Handle1:CAS:528:DyaK1MXjtFynsrY%3D

    CAS  Google Scholar 

  45. AJ Lewitus ET Koepfler JT Morris (1998) ArticleTitleSeasonal variation in the regulation of phytoplankton by nitrogen and grazing in a salt-marsh estuary. Limnol Oceanogr 43 636–646 Occurrence Handle1:CAS:528:DyaK1cXlsFWqsbs%3D

    CAS  Google Scholar 

  46. M Loferer-Krößbacher J Klima R Psenner (1998) ArticleTitleDetermination of bacterial cell dry mass by transmission electron microscopy and densitometric image analysis. Appl Environ Microbiol 64 688–694 Occurrence Handle9464409

    PubMed  Google Scholar 

  47. S Menden-Deuer EJ Lessard (2000) ArticleTitleCarbon to volume relationships for, dinoflagellates, diatoms, and other protist plankton. Limnol Oceangor 54 569–579

    Google Scholar 

  48. DJS Montagnes JA Berges PJ Harrison JFR Taylor (1994) ArticleTitleEstimating carbon, protein, and chlorophyll a from volume in marine phytoplankton. Limnol Oceanogr 39 1044–1060 Occurrence Handle1:CAS:528:DyaK2MXitVWjs7Y%3D

    CAS  Google Scholar 

  49. H Müller W Geller (1993) ArticleTitleMaximum growth rates of ciliated protozoa: the dependence on body size and temperature reconsidered. Arch Hydrobiol 126 315–327

    Google Scholar 

  50. MC Murrel JT Hollibaugh (1998) ArticleTitleMicrozooplankton grazing in northern San Francisco Bay measured by the dilution method. Aquat Microb Ecol 15 53–63

    Google Scholar 

  51. TG Nielsen T Kiørbe (1991) ArticleTitleEffects of a storm event on the structure of the pelagic food web with special emphasis on planktonic ciliates. J Plankton Res 13 35–51

    Google Scholar 

  52. GS Park HG Marshall (2000) ArticleTitleThe trophic contributions of rotifers in tidal freshwater and estuarine habitats. Estuar Coast Shelf Sci 51 729–742 Occurrence Handle10.1006/ecss.2000.0723

    Article  Google Scholar 

  53. GL Pernie D Scavia ML Pace HJ Carrick (1990) ArticleTitleMicrograzer impact and substrate limitation of bacterioplankton in Lake Michigan. Can J Fish Aquat Sci 47 1836–1841

    Google Scholar 

  54. M Putt DK Stoecker (1989) ArticleTitleAn experimentally determined carbon: volume ratio for marine oligotrichous ciliates from estuarine and coastal waters. Limnol Oceanogr 34 177–183

    Google Scholar 

  55. MR Roman DV Holliday LP Sanford (2001) ArticleTitleTemporal and spatial patterns of zooplankton in the Chesapeake Bay turbidity maximum. Mar Ecol Prog Ser 213 215–227

    Google Scholar 

  56. KO Rothhaupt (1997) ArticleTitleNutrient turnover by freshwater bacterivorous flagellates: differences between a heterotrophic and a mixotrophic chrysophyte. Aquat Microb Ecol 12 65–70

    Google Scholar 

  57. RW Sanders DA Caron JM Davidson MR Dennett DM Moran (2001) ArticleTitleNutrient acquisition and population growth of a mixotrophic alga in axenic and bacterized cultures. Microb Ecol 42 513–523 Occurrence Handle10.1007/s00248-001-1024-6 Occurrence Handle1:CAS:528:DC%2BD38XntFWrtQ%3D%3D Occurrence Handle12024234

    Article  CAS  PubMed  Google Scholar 

  58. CL Schelske HJ Carrick FJ Aldridge (1995) ArticleTitleCan wind-induced resuspension of meroplankton affect phytoplankton dynamics? J N Am Benthol Soc 14 616–630

    Google Scholar 

  59. RW Sheldon P Nival F Rassoulzadegan (1986) ArticleTitleAn experimental investigation of fiagellate-ciliate-copepod food chain with some observations relevant to the linear biomass hypothesis. Limnol Oceanogr 31 184–188

    Google Scholar 

  60. EB Sherr DA Caron BF Sherr (1993) Staining of heterotrophic protists for visualization via epifluorescence microscopy. PF Kemp BF Sherr EB Sherr JJ Cole (Eds) Handbook of Methods in Aquatic Microbial Ecology Lewis Boca Raton, FL 213–228

    Google Scholar 

  61. EB Sherr F Rassoulzadegan BF Sherr (1989) ArticleTitleBacterivory by pelagic choreotrichous ciliates in coastal waters of the Mediterranean Sea. Mar Ecol Progr Ser 55 235–240

    Google Scholar 

  62. EB Sherr BF Sherr (2000) Marine microbes: An overview. DL Kirchman (Eds) Microbial Ecology of the Oceans Wiley New York 13–46

    Google Scholar 

  63. CK Sieracki ME Sieracki CS Yentch (1998) ArticleTitleAn imaging-in-flow system for automated analysis of marine microplankton. Mar Ecol Prog Ser 168 285–296

    Google Scholar 

  64. O Skibbe (1994) ArticleTitleAn improved quantitative protargol stain for ciliates and other planktonic protists. Arch Hydrobiol 130 339–347

    Google Scholar 

  65. S Strom (2000) Bacterivory: Interactions between bacteria and their grazers. DL Kirchman (Eds) Microbial Ecology of the Oceans Wiley New York 351–386

    Google Scholar 

  66. WD Taylor ML Heynen (1987) ArticleTitleSeasonal and vertical distribution of Ciliophora in Lake Ontario. Can J Fish Aquat Sci 44 2185–2191

    Google Scholar 

  67. L Tupas I Koike (1991) ArticleTitleSimultaneous uptake and regeneration of ammonium by mixed assemblages of heterotrophic marine bacteria. Mar Ecol Prog Ser 70 273–282

    Google Scholar 

  68. JT Turner JC Roff (1993) ArticleTitleTrophic levels and trophospecies in marine plankton: lessons from the microbial food web. Mar Microb Food Web 7 225–248

    Google Scholar 

  69. T Weisse (1991) ArticleTitleThe annual cycle of heterotrophic freshwater nanoflagellates: role of bottom-up versus top-down control. J Plankton Res 13 167–185

    Google Scholar 

  70. NA Welschmeyer (1994) ArticleTitleFluorometric analysis of chlorophyll-a in the presence of chlorophyll-b and pheopigments. Limnol Oceanogr 39 1985–1992 Occurrence Handle1:CAS:528:DyaK2MXks1Sru70%3D

    CAS  Google Scholar 

  71. RG Wetzel (1992) ArticleTitleWetlands as metabolic gates. J Great Lakes Res 18 529–532

    Google Scholar 

  72. KD Yin RH Goldblatt PJ Harrison MA St John PJ Clifford RJ Beamish (1997) ArticleTitleImportance of wind and river discharge in influencing nutrient dynamics and phytoplankton production in summer in the central Strait of Georgia. Mar Ecol Prog Ser 161 173–183

    Google Scholar 

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Acknowledgments

The National Science Foundation Microbial Observatories program (grant no. 0239997) supported this study. We thank UA students Ken Moats and Kathy Dunmire for laboratory and field assistance and Dr. Francisco Moore and the OWC NERR staff for logistical support.

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Authors and Affiliations

  1. Department of Biology, The University of Akron, Akron, OH, 44325, USA

    P.J. Lavrentyev

  2. Marine Science Institute, The University of Texas, Port Aransas, TX, 78373, USA

    M.J. McCarthy & W.S. Gardner

  3. The Old Woman Creek National Estuarine Research Reserve, Huron, OH, 44839, USA

    D.M. Klarer

  4. Marine Biology Program, Florida International University, Miami, FL, 33181, USA

    F. Jochem

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  1. P.J. Lavrentyev
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Correspondence to P.J. Lavrentyev.

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Lavrentyev, P., McCarthy, M., Klarer, D. et al. Estuarine Microbial Food Web Patterns in a Lake Erie Coastal Wetland. Microb Ecol 48, 567–577 (2004). https://doi.org/10.1007/s00248-004-0250-0

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