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Taxonomic Variability of Phosphorus Stress in Sargasso Sea Phytoplankton

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Taxonomic Variability of Phosphorus Stress in Sargasso Sea Phytoplankton Notes 2303 P. R. PUGH, AND M. H. THURSTON. 1984. The diel migrations 2002. Midnight sinking behaviour in Calanus ®nmarchicus:A and distributions within a mesopelagic community in the north response to satiation or krill predation? Mar. Ecol. Prog. Ser. east Atlantic. 1. Introduction and sampling procedures. Prog. 240: 183±194. Oceanogr. 13: 245±268. THUESEN,E.V.,AND J. J. CHILDRESS. 1993. Enzymatic activities ROSS,T.,AND R. LUECK. 2003. Sound scattering from oceanic tur- and metabolic rates of pelagic chaetognaths: Lack of depth- bulence. Geophys. Res. Lett. 30: 10.1029/2002GL016733. related declines. Limnol. Oceanogr. 38: 935±948. SAMEOTO, D., N. COCHRANE, AND A. HERMAN. 1993. Convergence VOLK,T.,AND M. I. HOFFERT. 1985. Ocean carbon pumps: Analysis of acoustic, optical and net-catch estimates of Euphausiid of relative strengths and ef®ciencies in ocean-driven atmo- abundance: Use of arti®cial light to reduce net avoidance. Can. spheric pCO2 changes, p. 99±110. In E. T. Sundquist and W. J. Fish. Aquat. Sci. 50: 334±346. S. Broecker [eds.], The carbon cycle and atmospheric CO2, SCHNETZER, A., AND D. K. STEINBERG. 2002. Active transport of natural variations Archean to Present. American Geophysical particulate organic carbon and nitrogen by vertically migrating Union monograph 32. zooplankton in the Sargasso Sea. Mar. Ecol. Prog. Ser. 234: WIEBE, P. H. 1988. Functional regression equations for zooplankton 71±84. displacement volumes, wet weight, dry weight and carbon: A STEINBERG, D. K., C. A. CARLSON,N.R.BATES,S.A.GOLD- correction. Fish. Bull. 86: 833±835. THWAIT,L.P.MADIN, AND A. F. MICHAELS. 2000. Zooplankton ,T.K.STANTON,M.BENFIELD,D.MOUNTAIN,C.GREENE. vertical migration and the active transport of dissolved organic 1997. High frequency acoustic volume backscattering in the and inorganic carbon in Sargasso Sea. Deep-Sea Res. I 47: Georges Bank coastal region and its interpretation using scat- 137±158. tering models. IEEE J. Ocean. Eng. 22: 445±464. STEMMANN, L., M. PICHERAL, AND G. GORSKY. 2000. Diel variation in the vertical distribution of particulate matter (.0.15 mm) in the NW Mediterranean Sea investigated with the underwater Received: 1 December 2003 video pro®ler. Deep-Sea Res. I 47: 505±531. Amended: 14 June 2004 TARLING, G. A., T. JARVIS,S.M.EMSLEY, AND J. B. L. MATTHEWS. Accepted: 17 June 2004 Limnol. Oceanogr., 49(6), 2004, 2303±2310 q 2004, by the American Society of Limnology and Oceanography, Inc. Taxonomic variability of phosphorus stress in Sargasso Sea phytoplankton AbstractÐLow inorganic phosphorus (SRP) concentrations ring 1967) and export production (Eppley and Peterson and high inorganic nitrogen to phosphorus ratios suggest that 1979) paradigms were developed based upon a nitrogen-lim- phytoplankton production in the northwestern Sargasso Sea ited ocean, a view that found support in prominent publi- may be controlled to some extent by the availability of phos- cations (e.g., Hecky and Kilham 1988). In the past two de- phorus. Phosphorus stress in marine phytoplankton was qual- itatively assessed by using a single-cell enzyme-linked ¯uo- cades this view has changed and it is now widely accepted rescent (ELF) assay for the enzyme alkaline phosphatase, that marine primary production can be limited by inorganic which is induced at low SRP concentrations. During the highly phosphorus (SRP), iron, and silica, as well as nitrogen (e.g., strati®ed summer period, ;30% of the observed autotrophic Martin and Fitzwater 1988; Boyd et al. 1999). Part of this eukaryotes in the surface waters were ELF-labeled, whereas change in thought is due to a greater appreciation of nitro- in the well-mixed fall period, nearly 70% of the observed au- gen-®xing organisms that by de®nition cannot be nitrogen- totrophic eukaryotes in the surface waters were ELF-labeled. limited. During the summer, autotrophic ¯agellates displayed signi®- A number of studies in the Sargasso Sea have presented cantly higher ELF-labeling than did both diatoms and dino¯a- gellates, and this labeling did not vary with depth, whereas in evidence supporting the hypothesis that this region may cur- the fall, autotrophic ¯agellates and diatoms displayed statisti- rently be SRP-limited. Early geochemical studies (Fanning cally similar and decreasing percentages of ELF-labeled cells 1992; Michaels et al. 1996) noted dissolved inorganic N : P as a function of depth. This assay allowed for rapid assessment ratios that were substantially greater than the canonical Red- of the in situ physiological condition of individual autotrophic ®eld (1958) ratio, and that have recently been con®rmed by phytoplankton in the Sargasso Sea. By using this assay, we high-sensitivity nutrient analytical methods (Wu et al. 2000; were able to identify taxonomic and potential seasonal vari- Cavender-Bares et al. 2001). The biological interpretation of ability of phosphorus stress within the autotrophic phytoplank- nutrient limitation associated with these high N : P ratios is ton community. not straightforward, because there is little physiological in- formation on the N : P ratio at which phytoplankton transi- tion from nitrogen to phosphorus limitation. Examination of For decades, biologists and geochemists have debated available data suggests that this ratio may range from ;20 which nutrient, nitrogen or phosphorus, limits marine pri- to 50 (reviewed by Geider and LaRoche 2002). mary production (e.g., Codispoti 1989). In the 1960s and The enzyme alkaline phosphatase (AP), which is induced 1970s, the open-ocean new production (Dugdale and Goe- by SRP limitation in many phytoplankton species (Cembella 2304 Notes et al. 1984), has been used as a physiological indicator of Table 1. During BATS cruises, samples were collected from phosphorus stress in marine phytoplankton. This enzyme hy- two separate casts taken on consecutive days so that the total drolyzes phosphate groups from molecules within the dis- number of separate summer casts was four (two at the BATS solved organic phosphorus (DOP) pool, which is often site and two at Hydrostation S) and the total number of sep- many-fold greater than the SRP pool (e.g., Ammerman et al. arate fall casts was ®ve (four at the BATS site and one at 2003). At the Bermuda Atlantic Time-series Study (BATS) Hydrostation S). Bulk water samples were collected at 1-, site, chlorophyll-normalized bulk AP activity peaked during 60-, 100-, and 160-m (BATS site) or 1-, 50-, 100-, and 150- the late spring±early summer ;1 month after the seasonal m (Hydrostation S) depths on each cast in 12-liter Te¯on- phytoplankton biomass maximum (Ammerman et al. 2003). coated Ocean Test Equipment bottles with Te¯on-coated These elevated AP ratios suggested increased phosphorus stainless steel rings mounted on a 24-position SeaBird SBE- stress in the phytoplankton community, but the AP mea- 32 rosette. From each collection depth, duplicate sample ®l- surements included heterotrophic AP activity (to an unquan- ters (see below) were made and these duplicates were av- ti®ed extent), resulting in an overestimate of the autotrophic eraged to represent a single value for each depth on a component when normalized to chlorophyll. A similarly el- speci®c cast. Statistical analyses (analysis of variance and evated chlorophyll-normalized bulk AP activity was found Student's t-test, StatView Statistical Software) were con- at the northern extreme of the Sargasso Sea during summer ducted on these averaged data (n 5 4orn 5 5), and, there- (Guildford and Hecky 2000). The results from these bulk fore, the error estimates presented re¯ect both environmental AP assays have found support from a study employing an and methodological variability. Collection of nutrient and enzyme-linked ¯uorescent (ELF) single-cell AP assay in this hydrographic data followed standard BATS protocols. ocean region (Dyhrman et al. 2002). A signi®cant observa- To assess phosphorus-stress, the standard ELF staining tion from the latter study was that not all phytoplankton procedure (e.g., Gonzales-Gil et al. 1998) was used but with groups in the same water mass had the same AP activity, an the following slight modi®cations. Samples (several millili- observation previously made for freshwater systems (e.g., ters for cultures and ;0.25 to 1 liter for ®eld samples) were Rengefors et al. 2003). We collected samples of phytoplank- gently ®ltered (50 mm Hg) onto Irgalan Black±stained 0.4- ton populations at several depths during summer and fall, mm polycarbonate ®lters and placed in a clean petri dish for and, by using the single-cell ELF-97 assay, tested the hy- cell membrane permeablization with 70% ethanol. Small cy- pothesis that phosphorus stress in Sargasso Sea phytoplank- anobacteria, likely Synechococcus (based upon cell size), ton differed both among phytoplankton groups and between present in the ®eld samples were not found to be ELF-la- seasons. beled, and it was not clear if 70% ethanol adequately per- meablized cyanobacterial cell membranes. A 10% dimeth- MethodsÐAlthough previously tested with cyanobacteria ylsulfoxide (DMSO) solution in ethanol was tested to and dino¯agellate and cryptophyte species (Gonzales-Gil et increase cell membrane permeability, but cyanobacteria re- al. 1998; Dyhrman and Palenik 1999; Dyhrman et al. 2002; mained unlabeled. More importantly, the use of the 10% Nedoma et al. 2003), this assay was tested with several ad- DMSO in ethanol solution resulted in clearer images of ELF- ditional eukaryotic phytoplankton species isolated from the labeled eukaryotic phytoplankton cells both in culture and Sargasso Sea. Cultures of Chaetoceros sp. (Bacillariophy- in the ®eld and therefore was used for the data reported ceae, Culture Collection of Marine Phytoplankton [CCMP] herein. 199), Helicotheca thamesis (Bacillariophyceae, CCMP 826), After permeabilization with 10% DMSO in ethanol for 30 Akashiwo sanguinea (Dinophyceae, CCMP 1837), and Te- min, ®lters were carefully transferred back to the ®lter tower, traselmis sp. (Chlorophyceae) were grown in f/2 medium vacuum rinsed with 0.2-mm-®ltered Sargasso Sea water and (Chaetoceros sp., H.
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