The Temporal Dynamics of the Flagellated and Colonial Stages of Phaeocystis Antarctica in the Ross

Deep-Sea Research II 50 (2003) 605–617

The temporal dynamics ofthe ﬂagellated and colonial stages of Phaeocystis antarctica in the Ross Sea

Walker O. Smith Jr.a,*, Mark R. Dennettb, Sylvie Mathota, David A. Caronc a Virginia Institute of Marine Science, College of William and Mary, Gloucester Point, VA, 23062, USA b Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, 02543, USA c Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089-0371, USA

Accepted 27 September 2002

Abstract

Phaeocystis antarctica in the Ross Sea forms colonies, and blooms of colonial P. antarctica often occur over large areas in the southern Ross Sea. Sites where colonies occur often have significant vertical fluxes of carbon in the form of aggregated and flocculent material. P. antarctica also is a key component of the sulfur cycle; therefore, the species is critically important in many ofthe biogeochemical cycles in the Ross Sea. Despite this fundamental role, the lifehistory and temporal dynamics ofthis species are poorly known. This study investigated the contribution ofsolitary, flagellated forms and colonial cells of P. antarctica to phytoplankton abundance and autotrophic carbon, and the factors that might control the relative importance ofthese two morphological forms. Solitary P. antarctica cells numerically dominated the phytoplankton assemblage early in austral spring, although colony formation occurred almost immediately upon the onset ofnet population growth. The percentage ofsolitary cells relative to total cells (colonial+solitary) was high in early austral spring but decreased to a minimum during late spring; specifically, nearly 98% ofthe P. antarctica cells were in colonies in late spring, coinciding with the seasonal chlorophyll maximum. Significant phytoplankton mortality rates were positively correlated with high ratios ofsolitary: total P. antarctica cells. Highest mortality rates were observed during austral spring when solitary cells dominated the P. antarctica population. The abundance ofsolitary P. antarctica cells began to increase again during late summer, but colonial cell numbers were always greater than those ofsolitary cells during this period. This increase in the contribution ofsolitary forms during summer may have been a consequence ofmore severe micronutrient limitation forthe colonies (relative to solitary cells), lifehistory processes of P. antarctica, reduced microzooplankton grazing at that time, or a combination ofthese and other factors. We conclude that the relative abundance ofsolitary and colonial forms ofthis prymnesiophyte alga may be a consequence ofseasonal changes in these factors. The outcome of these interactions affects the contribution of this alga to the vertical flux of carbon and the degree to which P. antarctica participates in the microbial food web of the Ross Sea. r 2003 Elsevier Science Ltd. All rights reserved.

1. Introduction

There has been the recognition during the past few decades that phytoplankton assemblage com- *Corresponding author. Tel.: +1-804-684-7709. position exerts a strong control over pelagic E-mail address: [email protected] (W.O. Smith Jr.). carbon transformations and biogeochemical cycles.

For example, the dominance ofprimary produc- Little is known concerning the environmental tion by small cyanobacteria in oligotrophic systems factors that regulate the dominance of solitary and results in the utilization and remineralization of colonial forms of the alga, although it has been much ofthe production within the euphotic zone suggested that inorganic nutrients and grazing by the microbial food web. In contrast, diatoms may influence the ratio ofthese forms. In the are largely consumed by mesozooplankton, and North Sea when phosphate is reduced to limiting thus contribute significantly to the vertical flux of concentrations, flagellated cells of P. pouchetii organic carbon by virtue oftheir incorporation appeared to be favored (Riegman et al., 1992). into sinking fecal material. Other forms, such as Similarly, solitary cells ofthe same species tend to some prymnesiophytes, overwhelmingly contribute be favored when ammonium is the dominant form to sulfur cycling by releasing large amounts of ofnitrogen available to the alga ( Lancelot et al., dimethylsulfide (DMS) to the water, which then 1998). Riegman and van Boekel (1996) concluded volatilizes and exchanges with the atmosphere. that colonial cells of P. globosa are more effective Coccolithophorids, another type ofprymnesio- competitors for nitrate and are favored at irra- phyte, form calcium carbonate tests, and hence diances above 50 mmol photons m2 s1. A recent exert control over the alkalinity and carbon cycles laboratory study of P. globosa found that colony when present. Thus, not all phytoplankton affect formation and survival were enhanced under elemental and energy flow equally, and present conditions ofenhanced microzooplankton grazing models are beginning to incorporate the critical (Jakobsen and Tang, 2002), confirming the role of roles ofindividual taxa in biogeochemical cycles grazing. However, no clear relationship between (Armstrong, 1999). environmental conditions and life cycle stage for The Southern Ocean has long been considered to P. antarctica can, at present, be determined. be a diatom-dominated system, and indeed many P. antarctica is critical to primary production, locations have substantial numbers ofthese forms elemental transformations and vertical flux in the (e.g., Wilson et al., 1986; Brown and Landry, Ross Sea. For example, massive blooms ofthis 2001). More recently it has been recognized that species occur in the southern Ross Sea, and they Phaeocystis antarctica, a prymnesiophyte with a have been reported to produce some ofthe highest relatively complex life cycle, is extremely important concentrations ofDMS observed in the ocean in some regions. P. antarctica forms large blooms (DiTullio and Smith, 1995; Kettle et al., 1999). in areas ofthe Southern Ocean such as Prydz Bay Furthermore, P. antarctica colonies appear to be (e.g., Davidson and Marchant, 1992) and the relatively ungrazed by microzooplankton in this southern Ross Sea (El-Sayed et al., 1983). Indeed, region (Caron et al., 2000), and thus its role in it is often the dominant species in the latter region carbon export and flux is substantial. Dunbar et al. (DiTullio and Smith, 1996; Arrigo et al., 1999; (1998) compared the vertical fluxes oftwo sites Mathot et al., 2000; Dennett et al., 2001). (one dominated by diatoms and the other domi- P. antarctica is one ofthe fourspecies of nated by P. antarctica) in the southern Ross Sea Phaeocystis that can occur either as solitary, and found that carbon flux rates were approxi- flagellated unicells or as colonies ofhundreds of mately equal (although silica flux rates were an non-flagellated cells (Rousseau et al., 1994; Lan- order ofmagnitude greater at the site dominated celot et al., 1998; Zingone et al., 1999). The by diatoms). The material collected in the traps at colonies are spherical to cylindrical in shape and the P. antarctica-dominated site was largely hollow, and the algal cells are embedded in an aggregates and amorphous organic material, im- organic matrix that is the basis ofthe colony like plying that the material was exported without those of P. globosa (Hamm et al., 1999). It has transformation by the food web. It has also been been reported that P. pouchetii cells are liberated suggested that P. antarctica contributes to sub- from the colonial matrix as the colonies sink in the stantial fluxes during periods ofrapid growth water column, resulting in the generation oflarge during austral spring (DiTullio et al., 2000), but numbers ofsolitary cells ( Wassmann et al., 1990). these flux events have not yet been confirmed by W.O. Smith Jr. et al. / Deep-Sea Research II 50 (2003) 605–617 607 sediment trap collections in the Ross Sea. Collec- B. Palmer. Cruises were completed in early spring tively, this information indicates that detailed (October–November 1996), in late spring (Novem- knowledge ofthis species is essential forunder- ber–December 1997), in summer (January–Febru- standing ecosystem function in this and other ary 1997) and autumn (March–April 1997). Data Antarctic coastal waters. from all of the cruises were merged to produce a This study investigated the contribution of temporal composite (Smith et al., 2000a, b). Much solitary and colonial P. antarctica cells to the ofthe sampling occurred along 76 1300S at a series overall temporal dynamics ofthe phytoplankton ofeight stations, each separated by ca. 60 km assemblages ofthe southern Ross Sea. We (Fig. 1). Ice concentrations were variable during hypothesized that the morphological form of the study with 100% ice cover being observed in the species was important in determining its fate early spring and in autumn and ice-free conditions in the planktonic food web, given that we know occurring during summer (Smith et al., 2000a). that solitary cells were actively grazed by micro- Water samples were collected from the upper zooplankton during spring, while rates ofphyto- 100 m using a trace-metal clean rosette or standard plankton mortality were low (mostly undetectable) Niskin bottles (with Teflon-coated internal when P. antarctica colonies dominated the phyto- springs) mounted on a rosette. Chlorophyll a plankton. Because a variety offactors (nutrients, concentrations were determined fluorometrically irradiance and grazing pressure) may influence the after filtration and extraction for 24 h in 90% proportion oftotal cells in colonies, we sought to acetone (Smith et al., 2000b). Depths sampled for understand these dynamics within the seasonal enumeration ofnano- (2–20 mm) and microplank- phytoplankton bloom in the southern Ross Sea. ton (20–200 mm) varied depending upon water- column characteristics (e.g., depth ofthe chlorophyll maximum or euphotic zone). Up to five 2. Materials and methods depths were routinely sampled from each vertical profile. Samples for the enumeration of photo- This study was part ofAESOPS, the US trophic (i.e. chloroplast-bearing) nanoplankton Southern Ocean Joint Global Ocean Flux Study were preserved with 1% formalin or 0.5% (Smith et al., 2000a). All samples were collected in glutaraldehyde (from 10% stock solutions pre- the southern Ross Sea from the R.V.I.B. Nathaniel pared with filtered seawater) and refrigerated until

Fig. 1. Map showing the location ofsamples collected during the fourcruises. Exact station locations are provided in Dennett et al. (2001). 608 W.O. Smith Jr. et al. / Deep-Sea Research II 50 (2003) 605–617 processed for epifluorescence microscopy (within from measurements of the linear dimensions and 24 h ofcollection). Aliquots were stained with using volume equations ofappropriate geometric DAPI (50 mgml1 final stain concentration), fil- shapes. Volume estimates were converted to tered onto black 0.8 mm polycarbonate filters, carbon biomass using published conversion factors sealed with paraffin onto microscope slides, and (Eppley et al., 1970; Garrison et al., 1998; Mathot stored at 201C(Sherr et al., 1993; Sherr and et al., 2000). Conversion factors of 3.33 and Sherr, 1993). Slides were returned frozen to the 13.6 pg C cell1 were used for flagellated, solitary laboratory for counting. Nanoplankton were cells and non-motile colonial cells of P. antarctica, visualized by DAPI fluorescence, and photo- respectively (Mathot et al., 2000). Carbon esti- trophic nanoflagellates were identified by the mates of P. antarctica colonies include only the autofluorescence ofchlorophyll a using blue light carbon associated with the colonial cells. Depth- excitation. Presumptive solitary P. antarctica cells integrated abundance and biomass values were were distinguished from other phototrophic pro- calculated for the upper 60 m. All data are tists based on cell size and shape, chloroplast available via the internet (http://usjgofs.whoi. arrangement, and the presence offlagella. P. edu/). antarctica colonies generally fall in the range of microplankton or larger. Numbers offlagellated, solitary and colonial (within an organic matrix) 3. Results P. antarctica were counted on all samples. Samples for the enumeration of phototrophic 3.1. Temporal variations in solitary and colonial microplankton (20–200 mm algae, including colo- cell abundance nies of P. antarctica) were preserved in amber glass bottles with acid Lugol’s and/or glutaraldehyde- During early austral spring (i.e., ‘‘pre-bloom’’ Lugol’s solution (35%, v/v) at a final concentra- conditions) phytoplankton biomass was extremely tion of1% or 10% ( Rousseau et al., 1990). All low with surface chlorophyll levels less than samples were stored in the dark (Stoecker et al., 0.1 mgl1 (Smith et al., 2000b) and integrated 1994). Settled volumes varied between 50 and (0–100 m) chlorophyll concentrations less than 400 ml depending upon microplankton abundance. 10 mg m2 (Fig. 2a). Numbers of P. antarctica Samples with low abundance ofmicroplankton cells were also low. The mean abundance of (primarily from the early spring and autumn) were solitary cells during the first portion (prior to allowed to settle in the sample bottle, and then a October 26) ofthe early spring cruise was known volume ofsupernatant was removed before 0.22 Â 106 cells l1 (Fig. 2b), whereas the average transfer of the sample and settling into counting number ofcolonial cells forthe same period was chambers for enumeration using an inverted 0.027 Â 106 cells l1 (Fig. 2c). Hence, most P. microscope (Utermohl,. 1958). A minimum of50– antarctica cells present in the water column prior 100 microplankton were counted within 10–20 to significant biomass increase in spring were fields ofview (160 Â magnification); all cells were solitary forms (Fig. 2d). As phytoplankton bio- grouped by major taxa. Formalin-preserved sam- mass increased during the spring, the numbers of ples ofmicroplankton were filtered onto 0.8- mm flagellated cells relative to the total P. antarctica black, polycarbonate filters, and phototrophic and abundance decreased, although there was consid- heterotrophic forms were distinguished using erable scatter in this ratio as a function of spatial epifluorescence microscopy (Booth, 1993). The heterogeneity along the transect line (Fig. 2d). The coefficient of variation is generally o10% using lowest ratios (i.e. the highest dominance of this procedure (Venrick, 1981). colonial cells) were observed near the time of Biovolume estimates were determined for nano- maximal phytoplankton biomass in late spring (ca. plankton from microscopic measurements of cell December 16). The percentages ofsolitary cells in dimensions and assuming spherical or ellipsoidal several ofthese samples were less than 5%. In shape. Microplankton biovolume was determined addition, the numbers ofdiatoms (both smaller W.O. Smith Jr. et al. / Deep-Sea Research II 50 (2003) 605–617 609

(a) 1.0 (b) 0.8 ) Relative Daily Irradiance -2 ) -1 0.6 L 6 Solitary Cell 0.4 0.2 Chlorophyll a (mg m Abundance (x10 Phaeocystis 0.0 0 100 200 300 400 500 600 0 2 4 6 8 10 12 06-Sep 26-Oct 15-Dec 03-Feb 25-Mar 14-May 07-Sep 27-Oct 16-Dec 04-Feb 26-Mar 15-May Date Date

(c) (d) ) -1 L 6 (%) Colonial Cell tot /P Flag P Abundance (x10 Phaeocystis 024681012 07-Sep 27-Oct 16-Dec 04-Feb 26-Mar 15-May 0255075100 Date 02-Oct 27-Oct 21-Nov 16-Dec 10-Jan 04-Feb 01-Mar Date Fig. 2. (a) Integrated (0–100 m) chlorophyll a concentrations (solid circles) and clear-sky irradiance (heavy line) along 761300Sasa functionoftime ofsampling (fromSmith et al., 2000b). The thin line represents a hand-drawn ‘‘envelope’’ ofmaximum concentrations; (b) abundance (average, depth-weighted from 0–60 m) of solitary, flagellated Phaeocystis antarctica cells in the southern Ross Sea as determined from microscopy. The filled circles and connecting line represent weekly averages; (c) abundance (average, depth-weighted from 0–60 m) of Phaeocystis antarctica colonial cells in the southern Ross Sea as determined from microscopy. The filled squares and connecting line represent weekly averages; (d) Percentage ofsolitary, flagellated cells ( Pflag) relative to the total abundance ofcells ( Ptot; colonies+flagellates) of P. antarctica. and larger than 20 mm), dinoflagellates, and other represented 50% ofthe total P. antarctica cells on autotrophic flagellates also increased (Table 1). that date. The abundance ofcolonial cells also was The appearance ofcolonial P. antarctica was not maximal in summer (on January 10) and equaled correlated with any other taxa (dinoflagellates, 21.7 Â 106 cells l1. Low abundance ofsolitary nano- or microplanktonic diatoms, or photosyn- cells on that date resulted in colonial cells thetic flagellates); however, the abundance of constituting 99.7% ofthe total number of P. diatoms (both size classes) significantly correlated antarctica. with that offlagellated forms of P. antarctica (R2=0.87 and 0.86 for nano- and microplanktonic 3.2. Temporal variations in P. antarctica organic diatoms, corresponding to p=0.01 and po0.001, carbon biomass respectively). During the summer, the numbers ofsolitary The amount oforganic carbon in each mor- cells increased to the maximum observed abun- phological form of P. antarctica followed dance of11.3 Â 106 cells l1 on January 13, which similar trends to the abundance data with a few 610 W.O. Smith Jr. et al. / Deep-Sea Research II 50 (2003) 605–617

exceptions. Integrated carbon in solitary cells and colonies was maximal in summer (Fig. 3a and b), with the greatest values being 2.25 and 17.7 g Cm2, respectively. The contribution ofsolitary cells to total P. antarctica biomass carbon biomass Phaeocystis antarctica ﬂagellated cells was greatest early in spring, while the smallest contributions were observed during the time ofthe maximal chlorophyll concentration in late spring

m, and nanoplankton are cells (Fig. 3c). The ﬂagellate-associated carbon in- m creased during summer and decreased in autumn,

Nanoplanktonic ﬂagellates similar to the trend seen in abundance (Figs. 2b and 3a). The ratios ofthe average abundance of solitary cells relative to colonial cells in early spring, late spring and summer were 58.3%, 23.2% and 33.7%, respectively, whereas these ratios based on carbon during each period were 41.2%,

Nanoplanktonic diatoms 11.6% and 12.6%.

3.3. Spatial patterns of P. antarctica and diatoms

Spatial variations in the contribution ofﬂagel- lated and colonial cells to total P. antarctica

Phaeocystis antarctica colonial cells biomass were examined by pooling data from each station regardless ofthe time ofsampling. Solitary cells were most abundant in the eastern portion of the transect, where solitary cells formed an average ofnearly 53% of P. antarctica abundance at Station Orca (Fig. 4a). In contrast, in the western Microplanktonic ﬂagellates portion ofthe transect only ca. 20% ofthe total number of P. antarctica cells were solitary cells. Organic carbon associated with the cells showed a number ofstations within that sampling period. Microplankton are cells >20

¼ similar pattern. Thirty-five percent ofthe P. n antarctica carbon was contributed by solitary cells at Orca, but less than 10% of P. antarctica carbon Microplanktonic diatoms was derived from flagellates in the western region. Diatom abundance was greatest at the ends ofthe transect and did not show a clear relationship to the ratio ofsolitary and colonial forms of P. antarctica (Fig. 4b). ) ofcells forstations within a certain sampling period 1 Microplanktonic dinoflagellates 4. Discussion n not detected.

¼ Members ofthe genus Phaeocystis occur throughout the world’s oceans, often forming large blooms in a variety ofdiverse locations, m. ND m such as the Ross Sea, North Sea, Greenland Sea, 20 22 Oct1 Nov5 Nov20 Nov 51 Dec 49 Dec 315 138 Jan 820 Jan 49630 4 Jan 231 90907 9 Feb 520 2920 Apr 425 2250 Apr 3240 7The 6140 date represents 2 the median 5 date 2150 ofsampling, and 6 922 2400 2150 205 42,900 655 71 63,100 108,000 153,000 0 1,002,000 161 1 128,000 22 114 162 17,300 31 0 162 26 333 26,900 380,000 181,000 0 666,000 6,826,000 63,400 6 10,860,000 7,718,000 0 4,501,000 2860 2490 ND 1300 1,395,000 138,000 2,404,000 ND ND 130,000 24,600 8770 24,800 190,000 ND 19,300 68,000 16,400 2430 ND ND 84,300 6,172,000 280,000 83,800 ND 2,251,000 110,000 293,000 132,000 ND 1,918,000 69,246 50,304 1,679,000 ND ND 8590 2120 o Date Table 1 Mean abundance (cells l Bering Sea shelfbreak, the Arabian Sea, and the W.O. Smith Jr. et al. / Deep-Sea Research II 50 (2003) 605–617 611

(a) (b) ) ) -2 -2 P. antarctica P. antarctica colonial cells (g C m solitary cells (g C m carbon in Carbon in 0.0 0.5 1.0 1.5 2.0 2.5 0 4 8 121620 07-Sep 27-Oct 16-Dec 04-Feb 26-Mar 15-May 07-Sep 27-Oct 16-Dec 04-Feb 26-Mar 15-May Date Date

(c) (%) tot /C Flag C 0 20 40 60 80 100 07-Sep 27-Oct 16-Dec 04-Feb 26-Mar 15-May Date Fig. 3. Microscopically-derived carbon abundance of(a) solitary, ﬂagellated cells and (b) colonial cells. (c) Percentage ofcarbon contributed by ﬂagellated cells relative to the total P. antarctica cells present. The solid symbols and lines in (a) and (b) represent weekly averages. Note the different axes in (a) and (b).

Barents Sea (see Lancelot et al., 1998). In some carbon tracers; Smith et al., 1999) ofdiatoms and locations (e.g., North Sea) it is believed that Phaeocystis were not significantly different in this Phaeocystis growth occurs after diatoms have environment. Therefore, the causes for the estab- depleted silicic acid, but in other locations the lishment of P. antarctica blooms in the Ross Sea environmental stimulus for its growth is poorly do not appear to be related to mixed-layer depth known. In the Arabian Sea a Phaeocystis bloom or photophysiology. occurred in a water column with a relatively deep The contribution ofsolitary, flagellated forms of mixed layer (Garrison et al., 2000). Arrigo et al. P. antarctica to the total bloom biomass and (1999) also suggested that deep mixed layers in carbon fixation in the Ross Sea is even more some portions ofthe Ross Sea favorthe growth of poorly understood. Arrigo et al. (1999) mapped P. antarctica relative to diatoms, as a result ofthe the distribution of P. antarctica in the southern potentially greater photosynthetic rates of P. Ross Sea and found that diatoms were more antarctica at lower irradiances (Moisan and commonly encountered in the west and in the east Mitchell, 1999). However, mixed layers in the (near the melting ice edge). Smith and Asper Ross Sea were not statistically different between (2001) also found a similar result in a different stations dominated by diatoms or Phaeocystis year. Our results suggest that the spatial variations (Smith and Asper, 2001). Furthermore, the photo- in the contribution offlagellated or colonial synthetic responses (van Hilst and Smith, 2002) forms to the total P. antarctica abundance or and growth rates (determined from silicon and carbon (Fig. 4) also vary spatially, with greater 612 W.O. Smith Jr. et al. / Deep-Sea Research II 50 (2003) 605–617

Fig. 4. The spatial variations of(a) abundance offlagellated P. antarctica cells to total (solitary+colonial) P. antarctica (solid bar) and oforganic carbon offlagellated P. antarctica relative to that ofall P. antarctica cells (open bar), and (b) the relative abundance of flagellated P. antarctica cells (solid bar) and absolute diatom abundance (gray bar). Abundances determined microscopically and organic carbon estimated from abundance data and appropriate equations (see text for details). contributions offlagellated P. antarctica cells in Microzooplankton grazing rates were extremely the east. The carbon contribution is less, largely low in the Ross Sea during this study. Indeed, because of the differences noted in the sizes of the grazing rates as determined by the dilution cells ofeach form. Also, significant temporal technique revealed significant phytoplankton mor- variations in the ratio ofsolitary to colonial cells tality rates at only 13 of51 experiments ( Caron ofthe alga were apparent in our seasonal study et al., 2000). However, for those stations where (Fig. 2d). In addition to the variations in cells of P. significant phytoplankton mortality rates were antarctica, diatoms also varied spatially, and their measured, a positive relationship was observed abundance was positively correlated with that of between mortality rate and the percentage of flagellated P. antarctica (Table 1). The specific solitary cells relative to the total number of P. causes ofthese variations may be numerous, but antarctica cells (Fig. 5). This result appears to our data indicate that at least two features of the indicate that microzooplankton were capable of ecology of Phaeocystis play important roles. grazing solitary cells of P. antarctica but relatively W.O. Smith Jr. et al. / Deep-Sea Research II 50 (2003) 605–617 613

(a) Abundance Carbon (%) tot /C flag or C tot /P flag P 0 102030405060 Minke A E Z O P S Orca Station Name

(b) P. antarctica

) Diatoms -1 cells L 4 (%) or Diatom tot /P flag P Abundance (x10 0 102030405060 Minke A E Z O P S Orca Station Name

Fig. 5. Relationship between phytoplankton mortality rate, as determined from dilution experiments (Caron et al., 2000), and the percentage ofﬂagellated cells relative to the total abundance of P. antarctica.

incapable ofingesting cells in colonies. The results relative to algal growth during much ofthe late ofprevious studies support the finding that spring and summer in the Ross Sea. Reduced solitary, flagellated cells of Phaeocystis spp. are grazing on the colonial form of P. antarctica readily ingested by microzooplankton (e.g., Verity combined with rapid grazing on solitary cells could et al., 1988; Weisse and Scheffel-Moser,. 1990; result in a competitive advantage for colonial cells Weisse et al., 1994; Tang et al., 2001). even ifthe solitary and colonial cells had similar It has been hypothesized that colony formation gross growth rates. Ofcourse, it is also possible is a strategy of Phaeocystis species for avoiding that the life history of P. antarctica in the Ross Sea grazing pressure (Lancelot et al., 1998; Jakobsen has intrinsic controls that favor colony formation and Tang, 2002). Grazing on colonies may take during periods ofgrowth initiation and rapid place at some low level (indeed, this process has growth. This latter behavior would intensify any been noted in some systems; e.g., Weisse et al., selective advantage that colonial cells might have 1994), but this rate appears to be insignificant due to release from grazing pressure. 614 W.O. Smith Jr. et al. / Deep-Sea Research II 50 (2003) 605–617

In addition to differences in susceptibility to because iron is reduced to extremely low concen- microbial grazing, there also may be physiological trations at that time (Sedwick et al., 2000; differences between solitary and colonial cells of Fitzwater et al., 2000). Indeed, during our study P. antarctica that would result in different iron concentrations during late summer at 20 m responses to changes in environmental conditions. were (with only one exception) less than 0.04 nM Mathot et al. (2000) found that solitary cells were (Coale et al., unpublished). Iron has been repeat- significantly smaller (mean spherical diame- edly shown to limit phytoplankton photosynthesis ter¼3.170.60 mm) than those in colonies (mean and growth in the region (Martin et al., 1990; spherical diameter¼5.171.1 mm). Furthermore, Sedwick and DiTullio, 1997; Sedwick et al., 2000; the calculated carbon content ofsolitary vs. Olson et al., 2000). Given that iron limitation in colonial cells was 3.33 and 13.6 pg C cell1,a summer is a common occurrence in the Ross Sea, 4-fold difference (Mathot et al., 2000). It has been we suggest that the increase in flagellated, solitary suggested that macronutrient limitation favors the cells in summer may represent a shift in the smaller, flagellated forms relative to colonies of outcome involving the competition between soli- other species of Phaeocystis (Verity et al., 1988; tary and colonial cells that arises from the Escaravage et al., 1995), and there is no reason to conflicting impacts ofgrazing selectivity (which expect that micronutrient limitation would not appears to favor colonies) and nutrient limitation favor solitary forms as well. Indeed, the diffusive (which appears to favor solitary cells). flux ofiron (calculated fromFick’s Law) into a The exact nature ofthat response, however, is colony with a 4-mm diameter is ca. 106-fold lower unclear. It could simply be a reduced growth of than that into a 4-mm nanoflagellate at the same colonial P. antarctica in concert with constant, ambient iron concentration. Although colonial unchanged losses resulting in a decrease in colonial cells are on the exterior ofthe organic matrix, cell abundance and a negative net growth rate for the size and nature ofthe colony may substantially colonies. We also can speculate that ifthe colonial reduce the iron (and other nutrient) availability to abundance decreased, the mean irradiance avail- colonial P. antarctica cells. able to the remaining cells would increase, and the However, it has recently been suggested that iron demand per cell would decrease due to the iron might complex with the colonial sheath of synergistic effect between irradiance and iron Phaeocystis pouchetii, thus making the absorbed uptake (the Fe requirement is greater under low iron more available to the colonial cells embedded irradiance; Sunda and Huntsman, 1997). Alterna- in the mucilage (Schoemann et al., 2001). Lancelot tively, iron limitation could result in enhanced and Mathot (1985) reported that P. pouchetii colony degradation and liberation offlagellated could utilize the carbon in the mucilage as an cells (Wassmann et al., 1990), thereby directly additional carbon source, and ifthis were true for producing an increase in the net abundance of P. antarctica, then it would provide a mechanism solitary cells. We cannot define the regulatory for enhanced iron uptake by colonial cells, factor(s) at this time, and determination of the providing them a competitive advantage over exact mechanism ofthe differentialproduction of solitary cells. No data exist on the dependence of flagellated P. antarctica remains to be confirmed absorption ofiron and its dependence on ambient by further investigations. dissolved concentrations, particularly in the Ross The co-occurrence offlagellated P. antarctica Sea, so the importance of this effect cannot be cells with colonies ofthe same species is not critically evaluated. However, such a mechanism unexpected, as the same situation has been might explain how colonial cells increase their reported in other systems (Lancelot et al., 1998) relative contribution to biomass when iron is not and ofcourse colonial forms can give rise to limiting (e.g., during austral spring), particularly in flagellated forms of the species. However, based on concert with reduced losses due to grazing. the magnitude ofthe blooms attained by this This effect presumably would be especially species and the very different trophic pathways important during austral summer in the Ross Sea taken by solitary and colonial cells, the form of W.O. Smith Jr. et al. / Deep-Sea Research II 50 (2003) 605–617 615

P. antarctica in the Ross Sea has a disproportio- tic Polar front region at 1701W during austral spring 1997. nately large and varied effect on carbon transfor- Journal ofGeophysical Research 106, 13917–13930. mations and biogeochemical cycles. Flagellated Caron, D.A., Dennett, M.R., Lonsdale, D.J., Moran, D.M., Shalapyonok, L., 2000. Microplankton herbivory in cells seem to actively participate in the microbial the Ross Sea, Antarctica. Deep-Sea Research II 47, food web, whereas colonial cells are less effectively 3249–3272. controlled by microbial predators. Therefore, Davidson, A.T., Marchant, H.J., 1992. Protist abundance and understanding the mechanisms by which the two carbon concentration during a Phaeocystis-dominated morphological forms of this species are generated bloom at an Antarctic coastal site. Polar Biology 12, is critical to understanding the controls on the 387–395. Dennett, M.R., Mathot, S., Caron, D.A., Smith Jr., W.O., microbial food web in the Ross Sea. Similarly, an Lonsdale, D., 2001. Abundance and distribution ofphoto- appreciation ofthe response ofthe forms of P. trophic and heterotrophic nano- and microplankton in the antarctica to varying environmental conditions southern Ross Sea. Deep Sea Research II 48, 4019–4038. (especially micronutrient concentrations and irra- DiTullio, G.R., Smith Jr., W.O., 1995. Relationship between diance) should provide insights into the regulation dimethylsulfide and phytoplankton pigment concentrations in the Ross Sea, Antarctica. Deep-Sea Research I 42, ofbiogeochemical cycles ofthe area. While an 873–892. understanding ofthe temporal and spatial dy- DiTullio, G.R., Smith Jr., W.O., 1996. Spatial patterns in namics of Phaeocystis antarctica is important, it is phytoplankton biomass and pigment distributions in just as important to understand the controlling the Ross Sea. Journal ofGeophysical Research 101, factors for the two phases of this species. Without 18467–18478. DiTullio, G.R., et al., 2000. Rapid and early export of such information our understanding of the role of Phaeocystis antarctica blooms in the Ross Sea Antarctica. this keystone species in present and past environ- Nature 404, 595–598. ments will remain incomplete. Dunbar, R.B., Leventer, A.R., Mucciarone, D.A., 1998. Water column sediment fluxes in the Ross Sea, Antarctica: atmospheric and sea ice forcing. Journal of Geophysical Research 103, 10741–10760. Acknowledgements El-Sayed, S.Z., Biggs, D.C., Holm-Hansen, O., 1983. Phyto- plankton standing crop, primary productivity, and near- We thank David Kirchman, David Hutchins surface nitrogenous nutrient fields in the Ross Sea, and Jill Peloquin for stimulating discussions on Antarctica. Deep-Sea Research 30, 871–886. Eppley, R.W., Reid, F.M.H., Strickland, J.D.H., 1970. The this topic, and K.J. Brown, D.M. Moran, and L. ecology of the plankton off La Jolla, California, in the Shalapyonok for technical assistance. This work period April through September 1967. Part III. Estimates of was supported by NSF grants OPP-9531990 phytoplankton crop size, growth rate and primary produc- (WOS) and OCE-9634241 (DAC). tion. Bulletin ofthe Scripps Institution ofOceanography 17, 33–42. Escaravage, V., Peperzak, L., Prins, T.C., Peters, J.C., Joordens, J.C., 1995. The development ofa Phaeocystis References bloom in a mesocosm experiment in relation to nutrients, irradiance and coexisting algae. Ophelia 42, 55–74. Arrigo, K.R., Robinson, D.H., Worthen, D.L., Dunbar, R.B., Fitzwater, S.E., Johnson, K.S., Gordon, R.M., Coale, K.H., DiTullio, G.R., Van Woert, M., Lizotte, M.P., 1999. Phyto- Smith Jr., W.O., 2000. Trace metal concentrations in the plankton community structure and the drawdown ofnutrients Ross Sea and their relationship with nutrients and growth.

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