Abstract
The control mechanisms within the pelagic microbial food web of the oligotrophic Gulf of Aqaba and the northern Red Sea were investigated in the spring of 1999. Nutrient conditions and potential grazer impact were manipulated in a series of dilution experiments. Ambient nutrient concentrations and autotrophic biomass were very low (0.23–1.21 µmol NO3 l−1, 0.06–0.98 µmol NH4 l−1, 1.08–1.17 µmol Si l−1, 0.08–0.12 µmol P l−1, 0.15–0.36 µg chlorophyll a l−1). The planktonic community was characterized by low abundances [3.0–5.5×105 heterotrophic bacteria ml−1, 0.58–7.2×103 ultraphytoplankton <8 µm ml−1 (small eukaryotic photoautotrophs and Prochlorococcus sp., excluding Synechococcus sp.), 0.45–4.4×104 Synechococcus sp. ml−1, 0.32–1.2×103 heterotrophic nanoflagellates ml−1, 1.3–3.8×103 phytoplankton >8 µm l−1, 0.93–5.4×102 microzooplankton l−1] and dominated by small forms (0.2–8 µm). Dinoflagellates and oligotrichous ciliates were the most common groups in initial samples among the phytoplankton >8 µm and microzooplankton, respectively. Results show that bottom-up and top-down control mechanisms operated simultaneously. Small organisms were vulnerable to grazing, with maximum grazing rates of 1.1 day−1 on heterotrophic bacteria and 1.3 day−1 on ultraphytoplankton. In contrast, algae >8 µm showed stronger signs of nutrient limitation, especially when the final assemblages were dominated by diatoms. Synechococcus sp. were not grazed and only showed moderate to no response to nutrient additions. The high spatial and temporal variation of our results indicates that the composition of the planktonic community determines the prevailing control mechanisms. It further implies that, at this transitional time of the year (onset of summer stratification), the populations fluctuate about an equilibrium between growth and grazing.






References
Adrian R, Wickham SA, Butler NM (2001) Trophic interactions between zooplankton and the microbial community in contrasting food webs: the epilimnion and deep chlorophyll maximum of a mesotrophic lake. Aquat Microb Ecol 24:83–97
Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263
Bell T, Kalff J (2001) The contribution of picophytoplankton in marine and freshwater systems of different trophic status. Limnol Oceanogr 46:1243–1248
Berninger U-G, Finlay BJ, Kuuppo-Leinikki P (1991) Protozoan control of bacterial abundances in freshwater. Limnol Oceanogr 36:139–147
Boenigk J, Arndt H (2000) Comparative studies on the feeding behavior of two heterotrophic nanoflagellates: the filter-feeding choanoflagellate Monosiga ovata and the raptorial-feeding kinetoplastid Rhynchomonas nasuta. Aquat Microb Ecol 22:243–249
Buck K (1994) Diatom aggregates from the open ocean. J Plankton Res 16:1449–1457
Burkill PH, Leakey RJG, Owens NJP, Mantoura RFC (1993) Synechococcus and its importance to the microbial foodweb of the northwestern Indian Ocean. Deep-Sea Res II 40:773–782
Campbell L, Carpenter EJ (1986) Estimating the grazing pressure of heterotrophic nanoplankton on Synechococcus spp. using the sea water dilution and selective inhibitor techniques. Mar Ecol Prog Ser 33:121–129
Carlson CA, Ducklow HW (1996) Growth of bacterioplankton and consumption of dissolved organic carbon in the Sargasso Sea. Aquat Microb Ecol 10:69–85
Caron DA, Lim EL, Miceli G, Waterbury JB, Valois FW (1991) Grazing and utilization of chroococcoid cyanobacteria and heterotrophic bacteria by protozoa in laboratory cultures and a coastal plankton community. Mar Ecol Prog Ser 76:205–212
Caron DA, Cam HG, Kremer P, 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 42:943–972
Caron DA, Peele ER, Lim EL, Dennett MR (1999) Picoplankton and nanoplankton and their trophic coupling in surface waters of the Sargasso Sea south of Bermuda. Limnol Oceanogr 44:259–272
Caron DA, Lim EL, Sanders RW, Dennett MR, Berninger U-G (2000) Response of bacterioplankton and phytoplankton to organic carbon and inorganic nutrient additions in contrasting oceanic ecosystems. Aquat Microb Ecol 22:175–184
Christaki U, Giannakourou A, Wambeke F van, Gregori G (2001) Nanoflagellate predation on auto- and heterotrophic picoplankton in the oligotrophic Mediterranean Sea. J Plankton Res 23:1297–1310
Crosbie ND, Furnas MJ (2001) 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 24:209–224
Dolan J, Gallegos CL, Moigis A (2000) Dilution effects on microzooplankton in dilution grazing experiments. Mar Ecol Prog Ser 200:127–139
Dolan JR, Simek K (1997) Processing of ingested matter in Strombidium sulcatum, a marine ciliate (Oligotrichida). Limnol Oceanogr 42:393–397
Ducklow HW (1999) The bacterial component of the oceanic euphotic zone. FEMS Microbiol Ecol 30:1–10
Elser JJ, Frees DL (1995) Microconsumer grazing and sources of limiting nutrients for phytoplankton growth: application and complications of a nutrient-deletion/dilution-gradient technique. Limnol Oceanogr 40:1–16
Elser JJ, Stabler LB, Hassett RP (1995) Nutrient limitation of bacterial growth and rates of bacterivory in lakes and oceans: a comparative study. Aquat Microb Ecol 9:105–110
Fogg GE (1995) Some components of picoplankton and its importance in the pelagic ecosystem. Aquat Microb Ecol 9:33–39
Gallegos CL (1989) Microzooplankton grazing on phytoplankton in the Rhode River, Maryland: non linear feeding kinetics. Mar Ecol Prog Ser 57:23–33
Gasol JM (1994) A framework for the assessment of top-down vs bottom-up control of heterotrophic nanoflagellate abundance. Mar Ecol Prog Ser 113:291–300
Genin A, Lazar B, Brenner S (1995) Vertical mixing and coral death in the Red Sea following the eruption of Mount Pinatubo. Nature 112:507–510
Guillou L, Jacquet S, Chrétiennot-Dinet M-J, Vaulot D (2001) Grazing impact of two small heterotrophic flagellates on Prochlorococcus and Synechococcus. Aquat Microb Ecol 26:201–207
Kimor B, Golandsky B (1977) Microplankton of the Gulf of Elat: aspects of seasonal and bathymetric distribution. Mar Biol 42:55–67
Kivi K, Setälä O (1995) Simultaneous measurement of food particle selection and clearance rates of planktonic oligotrich ciliates (Ciliophora: Oligotrichina). Mar Ecol Prog Ser 119:125–137
Klinker J, Reiss Z, Kropach C, Levanon I, Harpaz H, Shapiro Y (1978) Nutrients and biomass distribution in the Gulf of Aqaba (Elat), Red Sea. Mar Biol 45:53–64
Landry MR, Hassett RP (1982) Estimating the grazing impact of marine micro-zooplankton. Mar Biol 67:283–288
Landry MR, Kirshtein J, Constantinou J (1995) A refined dilution technique for measuring the community grazing impact of microzooplankton, with experimental tests in the central equatorial Pacific. Mar Ecol Prog Ser 120:53–63
Latasa M, Landry MR, Schlüter L, Bidigare RR (1997) Pigment-specific growth and grazing rates of phytoplankton in the central equatorial Pacific. lo 42:289–298
Lindell D, Post AF (1995) Ultraphytoplankton succession is triggered by deep winter mixing in the Gulf of Aqaba (Eilat), Red Sea. Limnol Oceanogr 40:1130–1141
Lynn DH, Corliss JO (1991) Ciliophora. In: Harrison FW, Ruppert EE (eds) Microscopic anatomy of invertebrates. Wiley-Liss, New York, pp 333–467
Moigis AG (1999) Photosynthetic rates in the surface waters of the Red Sea: the radiocarbon versus the non-isotopic dilution method. J Plankton Res 22:713–727
Murrell MC, Hollibaugh JT (1998) Microzooplankton grazing in northern San Francisco Bay measured by the dilution method. Aquat Microb Ecol 15:53–63
Nejstgaard JC, Naustvoll L-J, Sazhin A (2001) Correcting for underestimation of microzooplankton grazing in bottle incubation experiments with mesozooplankton. Mar Ecol Prog Ser 221:59–75
Pätzold J, Halbach PE, Hempel G, Weikert H (2000) Östliches Mittelmeer—Nördliches Rotes Meer 1999. Cruise no. 44, 22 January–16 May 1999. Meteor-Berichte 00-3. Leitstelle Meteor, Institut für Meereskunde der Universität Hamburg, Hamburg
Pedros-Alio C, Calderon-Paz J-I, Guixa-Boixereu N, Estrada M, Gasol JM (1999) Bacterioplankton and phytoplankton biomass and production during summer stratification in the northwestern Mediterranean Sea. Deep-Sea Res I 46:985–1019
Pernthaler J, Simek K, Sattler B, Schwarzenbacher A, Bobkova A, Psenner R (1996) Short-term changes of protozoan control on autotrophic picoplankton in an oligo-mesotrophic lake. J Plankton Res 18:443–462
Plaehn O, Baschek B, Badewien TH, Walter M, Rhein M (2002) Importance of the Gulf of Aqaba for the formation of bottom water in the Red Sea. J Geophys Res 107:1–17
Porter KG (1973) Selective grazing and differential digestion of algae by zooplankton. Nature 244:179–180
Post AF, Dedej Z, Gottlieb R, Li H, Thomas DN, El-Absawi M, El-Naggar A, El-Gharabawi M, Sommer U (2002) Spatial and temporal distribution of Trichodesmium spp. in the stratified Gulf of Aqaba, Red Sea. Mar Ecol Prog Ser 239:241–250
Reckermann M, Veldhuis MJW (1997) Trophic interactions between picophytoplankton and micro- and nanozooplankton in the western Arabian Sea during the NE monsoon 1993. Aquat Microb Ecol 12:263–273
Reiss Z, Hottinger L (1984) The Gulf of Aqaba: ecological micropaleontology. (Ecological studies, vol 50) Springer, Berlin Heidelberg New York
Sanders RW, Caron DA, Berninger U-G (1992) Relationship between bacteria and heterotrophic nanoplankton in marine and fresh waters: an inter-ecosystem comparison. Mar Ecol Prog Ser 86:1–14
Sherr EB, Rassoulzadegan F, Sherr BF (1989) Bacterivory by pelagic choreotrichous ciliates in coastal waters of the NW Mediterranean Sea. Mar Ecol Prog Ser 55:235–240
Simek K, Bobkova J, Macek M, Nedoma J (1995) Ciliate grazing on picoplankton in a eutrophic reservoir during the summer phytoplankton maximum: a study at the species and community level. Limnol Oceanogr 40:1077–1090
Simek K, Hartman P, Nedoma J, Pernthaler J, Springmann D, Vrba J, Psenner R (1997) Community structure, picoplankton grazing and zooplankton control of heterotrophic nanoflagellates in a eutrophic reservoir during the summer phytoplankton maximum. Aquat Microb Ecol 12:49–63
Smetacek V (1999) Diatoms and the ocean carbon cycle. Protist 150:25–32
Sommer U (1994) Are marine diatoms favoured by high Si:N ratios? Mar Ecol Prog Ser 115:309–315
Sommer U (2000) Scarcity of medium-sized phytoplankton in the northern Red Sea explained by strong bottom-up and weak top-down control. Mar Ecol Prog Ser 197:19–25
Sommer U, Berninger UG, Boettger-Schnack R, Cornils A, Hagen W, Hansen T, Al-Najjar T, Post AF, Schnack-Schiel SB, Stibor H, Stuebing D, Wickham S (2002) Grazing during early spring in the Gulf of Aqaba and the northern Red Sea. Mar Ecol Prog Ser 239:251–261
Weisse T (1989) The microbial loop in the Red Sea: dynamics of pelagic bacteria and heterotrophic nanoflagellates. Mar Ecol Prog Ser 55:241–250
Yahel G, Post AF, Fabricus K, Marie D, Vaulot D, Genin A (1998) Phytoplankton distribution and grazing near coral reefs. Limnol Oceanogr 43:551–563
Acknowledgements
We would like to acknowledge the captain and crew of F.S. “Meteor” for their help and support during the cruise M 44/2 and Prof. G. Hempel for his excellent job as cruise leader. We thank S. Ballmeier and C. Stielau for counting the microzoo- and phytoplankton and for general assistance in the laboratory, and T. Hansen for the measurements of chlorophyll and nutrient concentrations. We are grateful to O. Plaehn, M. Walters, and T. Badewien for making CTD data available to us. This study obtained financial support from the Deutsche Forschungsgemeinschaft through grant BE 2279/1-1 and the German BMBF (“Red Sea Project of Marine Sciences”). The experiments performed comply with the current laws of Germany.
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Communicated by O. Kinne, Oldendorf/Luhe
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Berninger, UG., Wickham, S.A. Response of the microbial food web to manipulation of nutrients and grazers in the oligotrophic Gulf of Aqaba and northern Red Sea. Marine Biology 147, 1017–1032 (2005). https://doi.org/10.1007/s00227-005-1565-1
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DOI: https://doi.org/10.1007/s00227-005-1565-1