Nutrient limitation of picophytoplankton photosynthesis and growth in the tropical North Atlantic

Identification of the proximal nutrient limiting primary production is a necessary first step toward evaluating the physiological state of phytoplankton communities and the biogeochemical constraints on the current oceanic carbon cycle. We conducted 48-h nutrient addition bioassay experiments to evaluate nitrogen, phosphorus, and iron limitation of primary productivity, net chlorophyll synthesis, and net increase in cell numbers of the dominant picophytoplankton from the tropical North Atlantic. Our results indicate that N was the proximal limiting factor for primary production during the autumn of 2002, followed by P and then Fe. Net chlorophyll synthesis was significantly stimulated by addition of N alone and further stimulated by addition of P. Analysis of picophytoplankton populations by analytical flow cytometry revealed a more complex response. Cellular red fluorescence, an index of cell chlorophyll content, increased in Prochlorococcus, Synechococcus, and picoeukaryotes in response to addition of NH4NO3 but was not affected by single or combined additions of P and Fe. In contrast, cell abundance in these picophytoplankton populations increased only after combined N and P (63% of comparisons) or N and Fe (21% of comparisons) additions. Thus, our experiments revealed that chlorophyll synthesis and primary production were limited by the availability of nitrogen alone, while net increase in cell abundance was colimited by N and P or N and Fe in the majority of these picophytoplankton populations. Nitrogen and phosphorus have long been considered the nutrients that limit primary productivity in the oligotrophic tropical and subtropical North Atlantic, with nitrogen assigned the role of the proximate limiting factor and phosphorus the ultimate limiting nutrient (Tyrrell 1999). This assertion has been challenged recently (Ammerman et al. 2003; Vidal et al. 2003) based on low soluble reactive phosphorus (Wu et al. 2000) and high inorganic N : P ratios in subtropical North Atlantic surface waters (CavenderBares et al. 2001). With the N : P of the dissolved inorganic, dissolved organic and particulate pools exceeding the Redfield ratio of 16 mol N : 1 mol P (Ammerman et al. 2003; Vidal et al. 2003), it has been suggested that phosphate deficiency in the North Atlantic is an emerging paradigm (Ammerman et al. 2003). High aeolian inputs of dust to the North Atlantic have been hypothesized to relieve nitrogen fixation from limitation by Fe in this basin (Falkowski 1997), thus accentuating phosphate depletion in the subtropical North Atlantic relative to the subtropical 1 Current address: Department of Geophysics, Stanford University, Stanford, California 94305. 2 Current address: Université Pierre et Marie Curie, LOCEANIPSL, 4 place Jussieu, 75252 Paris, France. 3 Corresponding author ( [email protected]). Acknowledgments We thank the captain and crew of the F/S Meteor and the scientists aboard the Meteor 55 SOLAS cruise, especially D. Wallace, K. Lochte, H. Bange, P. Croot, M. Voss, P. Fritsche, F. Malien, and R. Langlois. D. Wallace provided insightful comments on the manuscript. W. Balzer of the University of Bremen loaned the clean container used during M55. We thank P. Fritsche and F. Malien for the nutrient analyses and Dr. P. Croot for providing calculations of the mixed-layer depth for the geographical positions of the bioassay experiments. This work was supported by a Deutsche Forschungsgemeinschaft grant to J.L.R., a Natural Environment Research Council grant to R.J.G., Plymouth Marine Laboratory, Core Strategic Research Programme, and a Marie Curie Postdoctoral fellowship to C.R. We thank two anonymous reviewers and Dr. John Cullen for useful comments and suggestions. Limnol. Oceanogr., 53(5), 2008, 1722–1733 E 2008, by the American Society of Limnology and Oceanography, Inc.