JPR Advance Access originally published online on April 7, 2009
Journal of Plankton Research 2009 31(7):701-712; doi:10.1093/plankt/fbp022
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Size-fractionated photosynthesis/irradiance relationships during Phaeocystis antarctica-dominated blooms in the Ross Sea, Antarctica
,*Virginia Institute of Marine Science, College of William and Mary, Gloucester Pt, VA 23062, USA
* CORRESPONDING AUTHOR: shields.amy{at}epa.gov
Received on September 25, 2008; accepted on March 13, 2009
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODRESULTSDISCUSSIONFUNDINGREFERENCES |
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In the Ross Sea, there are two major phytoplankton functional groups: diatoms and prymnesiophytes (dominated by Phaeocystis antarctica). Phaeocystis antarctica often occurs in colonial form, but also as solitary cells, and the two forms have distinct ecological roles. A comparison of the growth characteristics of solitary and colonial forms of Phaeocystis sp. is essential to understanding the differential impact each has on biogeochemical and ecological processes, and to allow parameterization of each form in numerical models. We measured the biomass and photosynthetic responses of two size fractions (>20 and <20 µm), representing colonies and solitary cells, at locations dominated by P. antarctica to assess the relative photosynthetic potential of the two forms. While the relative contribution of each form to total P. antarctica biomass differed among years, there were no significant differences between maximum photosynthetic rates of colonial and solitary forms within years. Substantial interannual variations in biomass and maximum photosynthetic rates normalized to chlorophyll a (P
) and initial light-limited rates of photosynthesis (
) were observed among years for the colonial fractions; however, interannual variations in maximum rates of photosynthesis or of solitary cells were not observed. A laboratory experiment with P. antarctica, together with field data, showed that growth stage of colonies strongly affected the maximum photosynthetic rates. Under nutrient-replete conditions and exponential growth, colonial cells had higher maximum photosynthetic rates than solitary cells, but as growth rate declined and senescence began, the solitary cells' rates became greater. This may be a reason for the high abundance of colonies that is often found in the Ross Sea during austral spring. Our results suggest that photosynthetic rates may influence the composition of the morphotypes of Phaeocystis, but do not appear to be the sole factor in regulating this critical biological variable. |
INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODRESULTSDISCUSSIONFUNDINGREFERENCES |
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Waters of the Southern Ocean have a disproportionate effect on the global carbon and sulfur cycles (Sarmiento et al., 2000
), and because the composition of phytoplankton regulates energy flow within food webs and material flow in biogeochemical cycles (Boyd and Newton, 1999), knowledge of the impact of assemblage structure is especially critical there. The Ross Sea has a relatively predictable phytoplankton bloom due to the physical properties of annual sea ice retreat, polynya formation and water column stratification (Arrigo et al., 1999; Smith et al., 2006). The waters have a narrow range of environmental variables and are known to have a relatively restricted diversity of functional groups (Arrigo et al., 1999). Specifically, there are two major functional phytoplankton groups: diatoms and prymnesiophytes, with the latter being dominated by Phaeocystis antarctica (Arrigo et al., 1999; Smith and Asper, 2001). Phaeocystis antarctica has two morphotypes (Rousseau et al., 1994): a colonial form and a solitary, single-celled form. Colonies are distinguished by being large (up to 2 mm), relatively unavailable to grazers (Caron et al., 2000), and are major components of blooms in the Ross Sea (Arrigo et al., 1999); conversely, solitary cells are small (ca. 5 µm), and a component of the microbial food web (Smith et al., 2003), and can represent more than 50% of the total P. antarctica numbers during summer (Mathot et al., 2000). Understanding the differences between the two forms is essential to understanding their spatial and temporal distributions in the Southern Ocean.
Three species of Phaeocystis, including P. antarctica, exist as single, flagellated cells or as non-flagellated cells in colonies (Rousseau et al., 1994; Schoemann et al., 2005). There are several life stages in which a motile cell with a flagellum can develop into a hollow, spherical colony with a diameter >2 mm and with active division of the cells within the matrix (Mathot et al., 2000). In all assemblages of Phaeocystis in nature, both solitary and colonial forms co-exist, and in some cases one dominates over the other. For example, Mathot et al. (Mathot et al. 2000) found that spatial and temporal trends in relative abundance occurred between solitary and colonial cells in the southern Ross Sea. Most P. antarctica cells were associated with colonies during the austral spring through the time of maximum biomass (mid-December), and thereafter the number of solitary cells increased. Wassmann et al. (Wassmann et al., 2005) found that single cells dominated at most times in Norwegian fjords, as well as in the White and Barents Seas. Indeed, they found numerous blooms in which colonies were nearly absent. Smith et al. (Smith et al., 2003) investigated the percentage of cells associated with colonies in 1996–97, and found that <10% were colonial in late October, but more than 98% of the cells were in colonies at the time of the maximum chlorophyll concentration (mid-December), although this percentage subsequently declined to 
50% in colonies by February. Integrated over the entire growing season, solitary cells contributed 33% of the total P. antarctica abundance. Smith et al. (Smith et al., 2003) suggested that the abundance of solitary cells might be controlled by grazing microzooplankton and heterotrophic flagellates, whereas the growth and abundance of colonial cells may be controlled by iron. Although evidence is contradictory about the environmental factors that control colony formation and subsequent release of solitary cells from colonies of P. antarctica, inorganic nutrient concentrations, micronutrients, grazing and irradiance all have been suggested to influence the form of Phaeocystis sp. (Verity et al., 1988; Smith et al., 2003; Tang et al., 2008).
Mathot et al. (Mathot et al., 2000) also found that cell size and carbon content differed between the solitary and colonial P. antarctica cells, with solitary cells being smaller and having only 25% of the cellular carbon of colonial cells. Veldhuis et al. (Veldhuis et al., 2005) found that colonial cells had much higher growth rates than did solitary cells of P. globosa and P. pouchetii (up to 3.8-times greater), but Perperzak et al. (Peperzak et al., 2000) found only a 10% difference. No data exist on the relative growth rates of P. antarctica colonial and solitary cells; similarly, no data are available on the morphotypes' relative rates of photosynthesis and nutrient uptake. Specific metabolic rates and phytoplankton cell size have a strong relationship (Banse, 1976), so these observations of larger colonies growing more rapidly are unexpected. Lancelot and Mathot (Lancelot and Mathot, 1985) found that the mucous envelope formed could act as a reserve for the cells and was reabsorbed during darkness by colonial cells of P. pouchetii, providing a potential means of enhanced growth and survival of colonies and colonial cells.
It has been suggested that this relatively restricted phytoplankton assemblage in the Ross Sea results from a differential photosynthetic response of the two groups, with P. antarctica being able to more effectively photosynthesize (and presumably grow) at lower irradiances than diatoms (Arrigo et al., 1999). Arrigo et al. (Arrigo et al., 1999) and Smith and Asper (Smith and Asper, 2001) found that P. antarctica abundance was greater in deeper mixed layers (and hence experienced lower irradiances). However, van Hilst and Smith (van Hilst and Smith, 2002) found no statistically significant differences in the measured photosynthetic parameters between the two groups, and concluded that other factors were also important in generating the spatial differentiation. They suggested that iron might play an important role, as it is reduced to extremely low concentrations by biological removal during the austral spring and summer. Iron has been shown to limit phytoplankton growth in summer within the Ross Sea (Sedwick and DiTullio, 1997; Sedwick et al., 2000; Olson et al., 2000), and it has been speculated that variations in input of iron might give rise to spatial variations in assemblage composition (Sedwick et al., 2000). Colonial P. antarctica has been shown to have a greater iron requirement than diatoms (Sedwick et al., 2007), and it has been suggested that small cells have an advantage over large cells and colonies by virtue of their increased cell surface:volume ratios (Sunda and Huntsman, 1997; Raven, 1998).
The goals of this study were to assess the relative photosynthetic potential of solitary and colonial P. antarctica cells from both in situ phytoplankton assemblages as well as cultures. Although there have been studies on how P. antarctica and other phytoplankton groups compare with respect to photosynthesis, it is not known how single and colonial cells differ. It has been suggested that P. globosa and P. pouchetii colonial cells have much greater rates of growth than do solitary cells, but these results were confounded by variations of chlorophyll within cells (Veldhuis et al., 2005). Chlorophyll-specific photosynthetic measurements of solitary and colonial forms should help characterize the physiological acclimation and shifts in size-specific phytoplankton carbon fixation rates. Since light-limited rates of photosynthesis are affected by physiological differences, a comparison between solitary and colonial forms will provide information on which form would perform better under lower irradiances. Similarly, light-saturated rates of photosynthesis are affected by temperature and nutrients, so differences among forms might clarify strategies used in stratified or high irradiance environments. Such a comparison will elucidate the potential physiological differences between forms that ultimately may be a factor in controlling the relative abundance of colonies and solitary cells in the environment.
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METHOD |
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TOPABSTRACTINTRODUCTIONMETHODRESULTSDISCUSSIONFUNDINGREFERENCES |
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Study site and field measurements
Water samples were collected from the southern Ross Sea as part of the Interannual Variations in the Ross Sea (IVARS) program conducted from 2001 to 2006 (Fig. 1; Smith et al., 2006). Photosynthesis/irradiance (P/E) measurements were completed in November–December during the period of maximum biomass. Additional data were collected during cruise NBP06-08 to the southern Ross Sea in November–December 2006. The euphotic zone was sampled using a SeaBird 911 + CTD/rosette system from which samples for nutrients, biomass and rate determinations were collected. The depth of the euphotic zone was determined from a BioSpherical Instruments PAR sensor mounted on the rosette, and at least seven depths were sampled within the euphotic zone. Chlorophyll a was determined by fluorescence after filtering the samples through Whatman GF/F filters and extracting in 90% acetone for 24 h at –20°C (Smith et al., 2006). Chlorophyll extracts were read on a Turner Designs Model 10AU fluorometer that had been calibrated with a known concentration of commercially purified chlorophyll a (Sigma Chemical). Samples for HPLC pigments, particulate organic carbon/nitrogen concentrations, biogenic silica concentrations, and samples for phytoplankton abundance were also collected (Smith et al., 2006). Phytoplankton samples were preserved in parformaldehyde solution (1–2% final concentration) and were stored in amber glass bottles at 4°C until cells could be stained with acridine orange (1% final concentration). A subset of the samples (1–20 mL) was filtered onto a black 0.8 µm polycarbonate filter which was then mounted onto a slide for epifluoresence microscopy. Thirty fields of view and 100–200 cells were counted per slide (J. Peloquin, Switzerland, personal communication).
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Separate samples of natural phytoplankton assemblages were size-fractionated by filtering from 50–250 mL through 20 µm polycarbonate filters (Poretics). The material retained on the filter was assumed to represent colonial cells for P. antarctica dominated assemblages, as the size of colonies is substantially >20 µm (from 50 to 2000 µm; Mathot et al., 2000
). An independent study found that only 0.3% of the total Phaeocystis sp. colonial fraction passed through 11 µm mesh (Jakobsen and Tang, 2002). The fraction that passed through the 20 µm filters was assumed to represent solitary cells, although it would also contain a few small colonies. The 20 µm polycarbonate filters were extracted directly in acetone and kept at –20°C for 24 h before fluorometric analyses. Hereafter, the >20 µm fraction is referred to as colonial Phaeocystis, whereas the <20 µm fraction is considered to be solitary P. antarctica. Phaeocystis antarctica-dominated stations were identified based on cell abundances for solitary and colonial cells (Table I; J. Peloquin, Switzerland, personal communication).
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Photosynthesis/irradiance measurements
P/E relationships were determined at 12 stations where P. antarctica overwhelmingly dominated. P/E relationships of solitary and colonial forms were determined by using a large-volume irradiance gradient incubator (Platt and Jassby, 1976). Water for P/E experiments was collected from the 50% light depth, after which 23 samples (265 mL each) were placed in Qorpak bottles, to which ca. 150 µCi NaH14CO3 were added to each. The samples were added to the P/E incubator (fitted with a high intensity xenon-arc light; Fig. 2) and incubations lasted 2 h (Fig. 2). Surface seawater surrounded the samples and circulated through the incubator to maintain samples at ambient temperatures (flow ca. 10 L min–1). The light also passed through a heat sink, which consisted of two plates of tempered glass that held flowing surface seawater (5 cm thick) between the incubator and light source, to insure that no heating of the samples occurred. Because the light was mounted on one end of the incubator, an irradiance gradient naturally occurred as distance from the light increased. A bottle wrapped in aluminum foil was used as a dark control. All external surfaces were blackened to minimize external light from entering. Irradiance was measured within each bottle with a BioSpherical Sensor quantum meter. After incubation, each sample was size-fractionated by filtering an aliquot of known volume through a 20 µm Poretics filter, and a separate volume through a 25 mm GF/F filter (0.7 µm). Colonial carbon fixation was assumed to be retained on the 20 µm filter, and the difference between GFF and 20 µm filters was the carbon fixation of solitary forms. Only particulate organic carbon production was measured, as DOC release in 2 h is generally much less than 10% (unpublished data). Each filter was placed in a 7 mL scintillation vial, and 0.25 mL of 10% HCl solution was added to degas any inorganic carbon on the filter. After ventilation for at least 24 h, 5 mL Ecolume® (ICN) was added, and after another 24 h in the dark, all samples counted on a liquid scintillation counter. Total inorganic 14C-bicarbonate available during incubation was assessed by counting a 0.1 mL aliquot (to which 0.05 mL β-phenethylamine, a CO2 trap, was added) directly in Ecolume.
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Laboratory culture experiments
Phaeocystis antarctica (CCMP 1374) cultures were grown in environmental rooms at Crary Laboratory, McMurdo Station, Antarctica for 16 d in 2005–06. An acid-cleaned, 50-L polycarbonate carboy with filtered (<0.2 µm) McMurdo Sound seawater was inoculated with P. antarctica culture (initial chlorophyll 2 µg L–1). The culture was grown in acid-cleaned polycarbonate carboys at ca. –2°C under 50 µmol photons m–2 s–1 irradiance (constant irradiance) to simulate natural conditions. Every fourth day, P/E experiments were performed in the same manner as the field samples (total volume removed 6 L each sampling period), with the incubation being completed in a –2°C environmental room to keep samples at a constant temperature. Additional volumes for nutrients, numerical abundance and chlorophyll determinations were collected. The photosynthetron used in the laboratory experiments utilized high output fluorescent lights rather than a xenon-arc light to minimize heat output, and although the two types of lights were not directly compared, their irradiance outputs were similar in both quality and quantity. All samples processed as described above, and the data were fitted to a photosynthesis–irradiance model.
Since photoinhibition was not significantly different from zero in our study, photosynthetic rates were fitted to the Webb et al. (Webb et al., 1974) empirical model:
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is the initial, light-limited, photosynthetic rate [mg C (mg chl a)–1 h–1 (µmol photons m–2 s–1)] and E the irradiance (µmol photons m–2 s–1). The data were fitted to this equation using SigmaPlot (Version 10). After the data were fitted to the Webb et al. (Webb et al., 1974) model, plots of the photosynthetic responses for each experiment were generated, and the regression estimates for PmB and computed; those values are reported only when P < 0.05. A parameter from these variables, Ek (light saturation index), is derived by:
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The parameter values resulting from the non-linear regressions were compared using the non-parametric Kruskal–Wallis analysis of variance (ANOVA) and a posteriori Mann–Whitney tests, as the data did not meet the normality and variance assumptions of the ANOVA. A critical P-value of 0.05 was selected a priori to evaluate the effects of temporal variations in the parameters and significant differences between size fractions. Systat (Version 12) was used to perform the statistical analyses. For the laboratory data, a comparison of the 95% confidence interval was used to compare parameter values between size fractions.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODRESULTSDISCUSSIONFUNDINGREFERENCES |
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Species composition during field studies
Microscopic abundance data show that P. antarctica was most abundant during austral spring of 2001, 2003 and 2006 (Table I). However, the size structure of the P. antarctica assemblages differed markedly between years. Mean chlorophyll concentrations in the colonial size fraction for the 3 years were 2.26, 3.39 and 0.68 µg L–1, which represented 56, 76 and 21% of the total phytoplankton chlorophyll, respectively (Table I). These variations in the absolute amounts of chlorophyll were associated with the date of collection and the development of the spring Phaeocystis bloom. The rest of the assemblage was composed largely of diatoms, including Chaetoceros sp., Fragilariopsis sp. and Pseudonitzschia sp. (unpublished data).
Photosynthetic relationships of colonial and solitary P. antarctica
Colonial and solitary maximum photosynthetic rates also reflect the development of the spring bloom (Fig. 3A). During 2001, the PmB for colonies averaged 1.8 ± 0.7 mg C (mg chl a)–1 h–1 and ranged from 1.1–2.8 mg C (mg chl a)–1 h–1, whereas that of solitary cells averaged 2.2 ± 0.1 mg C (mg chl a)–1 h–1 and ranged from 2.1–2.2 mg C (mg chl a)–1 h–1. During 2003, colonial PmB averaged 0.5 ± 0.2 mg C (mg chl a)–1 h–1; solitary cells averaged 2.3 ± 1.6 mg C (mg chl a)–1 h–1. During November 2006, colonial and solitary cell PmB averaged 2.5 ± 0.7 and 1.3 ± 0.9 mg C (mg chl a)–1 h–1, respectively. PmB for 2001 and 2006 were significantly higher than 2003 for colonies (Fig. 3A; Kruskal–Wallis and a posteriori Mann–Whitney tests, P = 0.019), but no significant difference was found for solitary cells (Kruskal–Wallis, P = 0.764).
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The initial light-limited rate of photosynthesis (
) for colonies was also significantly lower in 2003 than during the other 2 years (Fig. 3B, Kruskal–Wallis and a posteriori Mann–Whitney tests, P = 0.008). There was no significant difference in the solitary cell between 2003 and 2006 (Kruskal–Wallis, P = 0.079). During 2003, solitary was significantly higher than colonial (Fig. 3B, Mann–Whitney, P = 0.034). Ek (the index of photoadaptation) for colonies was significantly lower in 2006 than in 2001 and 2003 (Fig. 3C, Kruskal–Wallis and a posteriori Mann–Whitney tests, P = 0.023). The Ek of the solitary cell-size fraction during November 2006 was significantly less than 2003 (Kruskal–Wallis and a posteriori Mann–Whitney tests, P = 0.034). Lastly, linear regressions were performed to assess the relationship between PmB and . The colonial fraction exhibited a significant relationship between PmB versus (Fig. 4; r2 = 0.63; P = 0.002), while solitary cells showed no significant relationship between the two (r2=0.05, P = 0.63).
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When the percentage of colonial cells within an assemblage was compared with the colonial PmB with a least squares linear regression, a significant, negative relationship was found (Fig. 5A; r2 = 0.40; P = 0.03). Similarly, when the colonial P. antarctica maximum photosynthetic rate was compared with the percentage of chlorophyll in the >20 µm fraction, a clear negative relationship was observed (Fig. 5B; r2 = 0.49, P = 0.011). These data suggest that colonial photosynthetic capacity (e.g. PmB rates) decrease when chlorophyll and colonial contributions becomes maximal, and presumably reflect decreased growth rates at the onset of growth limitation by either irradiance or nutrients.
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P/E relationships from cultured Phaeocystis
The biomass and activity of colonial and solitary cells was monitored in a monoculture of P. antarctica to assess whether there was a difference in photosynthetic parameters and growth rates between the two morphotypes (Fig. 6). Both forms showed maximum growth between days 4 and 8 (Table II), but colonial growth rates were 2.8 times as great (0.38 versus 0.13 day–1); after 8 days colonial growth ceased, while growth of solitary cells continued. Maximum photosynthetic rates for colonies were initially 1.47 mg C (mg chl a)–1 h–1, but declined by nearly an order of magnitude during the rest of the experiment. PmB of cultured P. antarctica was observed to be 1.02 ± 0.56 and 1.86 ± 0.76 in other studies (van Hilst and Smith, 2002). PmB of solitary cells were initially 0.60 mg C (mg chl a)–1 h–1, and the rates declined slightly with time, but not to the extent that they did for colonial forms. Although the maximum photosynthetic rates of solitary cells were lower than the colonial cells at the beginning of the experiment, they fall within the lower ranges of previous studies (van Hilst and Smith, 2002). During the first 8 days, the PmB was significantly higher for colonies, but on the 16th day solitary cells' PmB was greater than that of colonies (Fig. 6, 95% CI).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODRESULTSDISCUSSIONFUNDINGREFERENCES |
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Distribution of Phaeocystis antarctica
Although the Ross Sea is one of the locations where large accumulations of P. antarctica have been repeatedly observed (Arrigo et al., 1999; Smith and Asper, 2001), there are few data from the Southern Ocean on the temporal and spatial distributions of colonies (non-flagellated) and solitary forms (Mathot et al., 2000), and none on variations in growth rates and photosynthetic parameters. A conceptual diagram that illustrates the seasonal relationships among environmental factors (irradiance, iron concentrations), biomass of colonial and solitary forms, and growth rates of the two morphotypes are presented (Fig. 7). The overall pattern is one characterized by initial, rapid growth of colonies (and accumulation of biomass) under high iron concentrations, followed by a rapid decrease in growth rates of colonial cells, which results in the eventual relative dominance by solitary cells during high light, reduced iron concentration conditions. Smith et al. (Smith et al., 2006) found that in both 2001 and 2003 prymnesiophytes represented ca. 80% of the phytoplankton chlorophyll (ca. 6 µg L–1) in December, and that the contributions of P. antarctica to phytoplankton chlorophyll decreased markedly, to <1 µg L–1 by February. Microscopic abundance during November–December of 2001, 2003 and 2006 further suggest that P. antarctica dominated the Ross Sea polynya during those time periods (Table I). In some years, large diatom blooms occurred after the decline of the P. antarctica blooms, with a diatom bloom in equal magnitude to the spring bloom in February 2004 (Smith et al., 2006; Peloquin and Smith, 2007). These large diatom blooms, possibly due to iron-enriched modified circumpolar deep water intrusions, appear to occur in summer approximately every 2–4 years (Peloquin and Smith, 2007). Even if diatoms do not reach high concentrations, during January and February they generally dominate the phytoplankton assemblage.
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Variations between colonial and solitary cells
Our results are the first to suggest that colonial P. antarctica dominance (relative to solitary P. antarctica) in the Ross Sea may be due to higher growth and maximum photosynthetic rates of colonial cells during the onset of the bloom, rather than solely due to a grazing defense mechanism. Both the field and laboratory results support this contention (Fig. 3A–C, Fig. 6; Table II). The culture experiments further illustrate the capabilities of colonies, which exhibited significantly higher PmB values and a faster growth rate during the first 8 days of the study (Fig. 6). Other studies have suggested that Phaeocystis sp. colonies are capable of higher growth rates than solitary flagellates (e.g. Veldhuis et al., 2005), but investigations of P. antarctica growth rates are limited. While this contrasts with theoretical models that suggest that solute exchange increases with decreased cell radius (Raven, 1998), other physiological mechanisms such as nutrient storage or increasing scalable components may give colonial P. antarctica cells an advantage. Large phytoplankton cells are often capable of higher growth rates or maximum carbon specific photosynthesis (under nutrient-replete conditions and high irradiance) than small-sized phytoplankton, but previous studies are not consistent (Furnas, 1991; Frenette et al., 1996; Crosbie and Furnas, 2001; Cermeño et al., 2005). Colonial cells of P. globosa have been found to divide at the same rate as motile cells (Veldhuis et al., 2005); however, it has also been shown for P. pouchetii that colonies have lower specific growth rates. The variations in growth rates are important to consider in models of primary production in P. antarctica-dominated ecosystems, as well as their impacts on local ecology and biogeochemical cycles (Lancelot and Rousseau, 1994; Peperzak et al., 2000).
It is plausible to ask why solitary cells do not more consistently dominate the assemblage, particularly under high-light, low iron conditions. Colonial biomass accumulation could be enhanced due to extensive grazing of solitary forms by heterotrophic microzooplankton (Caron et al., 2000; Smith et al., 2003). Such forms of phytoplankton grazers are common in the Ross Sea and display a clear seasonal increase (Dennett et al., 2001). We suggest that the early growth of solitary cells can be near maximal, but that ultimately their abundance is limited by micro-heterotrophic ingestion. Interestingly, in the culture experiment, solitary cells did reach a higher biomass than did colonial cells under conditions where microzooplankton were substantially reduced in biomass. Colonial biomass did not reach concentrations found in situ, which may reflect a limitation by irradiance (either shading or the reduced photon flux density in the culturing environment). The environmental controls of the two forms appear to be different, with colony growth and abundance limited by bottom-up factors (iron limitation, enhanced aggregate formation and increased sinking), whereas solitary cell abundance is limited by loss rates (transformation into new colonies) and grazing. Laboratory studies, however, suggest that some microzooplankton may be capable of grazing individual colonial cells, and further research on grazing and morphotype development is needed in the Ross Sea to fully understand P. antarctica dynamics (Shields and Smith, 2008).
Interannual variability of colonial Phaeocystis antarctica photosynthesis
Colonial Phaeocystis antarctica PmB rates were significantly lower in 2003 than during other years; however, there was no significant interannual variability among solitary P. antarctica PmB rates. While the lower colonial PmB in 2001 and 2003 could be due to differences in growth stage when compared with 2006, the lower colonial PmB during those time periods could also have resulted from iron limitation during the strongly stratified summer (Olson et al., 2000; Smith and Asper, 2001). If such declines were indeed initiated by the onset of iron limitation, it is logical that colonies would reflect that limitation first, as single cells (by virtue of their greater surface area: volume ratio due to smaller size, as well as the absence of a mucoid sheath) (Mathot et al., 2000) would likely be less stressed under low nutrient conditions than larger colonies (Smith et al., 2003). Colonial PmB rates in 2003 tended to be lower (although not significantly lower; Kruskal–Wallis, P = 0.083) than those of solitary cells and may reflect iron stress, as has been shown in diatoms (Lindley et al., 1995). While no measurements of iron concentrations were made, Peloquin and Smith (Peloquin and Smith, 2007) reported low maximum quantum yields (Fv/Fm) of 0.3–0.4 during 2003 and suggested the assemblages were under severe micronutrient stress. While we observed a decrease in PmB from austral spring to summer, van Hilst and Smith (van Hilst and Smith, 2002) observed an increase in PmB over time, and suggested that acclimation to in situ irradiance occurred from November to December, a period of rapidly increasing irradiance and declining ice concentrations. It is possible that iron limitation occurred earlier in our study, especially in 2003 (Peloquin and Smith, 2007), and this impacted photosynthetic parameters. The percentage of colonial P. antarctica in the phytoplankton assemblage also affects field measurements of PmB in the Ross Sea; that is, a lower PmB occurred when the percentage of colonial P. antarctica was highest (Table I; Fig. 5A and B). As colonial growth proceeds, it is likely that the degree of iron limitation also increases through time (Fig. 7). It is clear that models looking at phytoplankton dynamics in the Ross Sea must consider not only the morphotypes of P. antarctica separately, but the interannual differences in the environmental controls of photosynthetic parameters.
An alternative hypothesis implies that colonial P. antarctica may not exhibit iron stress before solitary cells. It has been shown that manganese, phosphate and possibly iron (Davidson and Marchant, 1987; Lubbers et al., 1990; Veldhuis et al., 1991) can be sequestered in the colonial matrix and subsequently reused during later growth, thereby giving colonies a competitive advantage over single cells during periods of micronutrient limitation. It may be possible that other negative effects associated with colonies (e.g. self-shading), rather than micronutrient limitation, were occurring in 2003. Robinson et al. (Robinson et al., 2003) argued that colonial bloom development could cease due to excessive colonial carbon requirements restricting colony size. These reductions in both forms would be consistent with the onset of iron limitation earlier in 2003 than in 2001 (Smith et al., 2006).
Adaptation to low irradiance by Phaeocystis antarctica
Tagliabue and Arrigo (Tagliabue and Arrigo, 2003) suggested that large colonial P. antarctica blooms during austral spring results from its shade acclimation capabilities. This shade acclimation and rapid growth at the low irradiances found in spring in the Ross Sea allows P. antarctica to become uncoupled with zooplankton grazing, resulting in blooms. Shade acclimation, denoted by low PmB and Ek values and a higher , has been observed in a variety of other studies as well (e.g. Holm-Hansen and Mitchell, 1991; Boyd et al., 1995). For example, Boyd et al. (Boyd et al., 1995) measured PmB rates (0.70 mg C (mg chl a)–1 h–1), Ek (20 µmol photons m–2 s–1) and elevated values (0.04 mg C (mg ch1 a)–1 h–1 (µmol photons m–2 s–1)–1) during an early spring bloom in the Bellingshausen Sea, Antarctica, and both P. antarctica and diatoms have been found to be well adapted to low-irradiance levels in the austral spring in the Ross Sea, indicated by higher photosynthetic efficiency () and a low Ek (van Hilst and Smith, 2002). During our study, the November 2006 P. antarctica solitary cells appear to have these shade acclimation characteristics, with low PmB rates (1.3 mg C (mg chl a)–1 h–1), low Ek (14.9 µmol photons m–2 s–1) and high values (0.09 mg C (mg ch1 a)–1 h–1 (µmol photons m–2 s–1)–1). Our values fall within the range of those observed by van Hilst and Smith (van Hilst and Smith, 2002), with the solitary P. antarctica cells having a higher during 2001 than previous observations. While it is clear that shade acclimation does occur in spring, our results also suggest that there is a significant temporal pattern in both the solitary and colonial fraction photosynthetic response (Fig. 7). While a lower Ek during the early spring could suggest low-irradiance acclimation, increased values during austral summer demonstrated that P. antarctica can also adapt to the higher irradiance levels encountered at that time. This is important to consider in primary production models that assume that P. antarctica is low-light adapted and less likely to compete with diatoms in high irradiance, stratified environments (Tagliabue and Arrigo, 2003). van Hilst and Smith (van Hilst and Smith, 2002) observed the lowest Ek values in cultured phytoplankton grown at the lowest irradiance, further suggesting their ability to adapt to the irradiance regime of high-latitude environments.
The variations in values we observed could be due to the colonial cells changing concentrations of photosynthetically active accessory pigments, variable photosystem I: photosystem II ratios, or nonphotochemical quenching (Behrenfeld et al., 2004). Behrenfeld et al. (Behrenfeld et al., 2004) suggest that covariation in PmB and can exist temporally in assemblages dominated by one species. Harding et al. (Harding et al., 1987) described seasonal changes in P/E parameters for Prorocentrum mariaelebouriae and found a significant relationship between PmB and , as we did between colonial PmB and . Antarctic studies also demonstrate the covariation of PmB and (Claustre et al., 1997; Moline et al., 1998). The covariance between and PmB may suggest that nutrient limitation caused a shift in net carbon partitioning due to changes in the fraction of photosynthetically produced reductants. This observation is essential to a description of the temporal changes in colonial P. antarctica photosynthetic parameters and how these morphotypes may be affected more strongly by nutrient limitation than solitary cells of P. antarctica. Covariation of PmB and may also represent the ability of phytoplankton to keep Ek relatively constant in an unchanging light environment. Assuming light is not changing substantially but nutrients are decreasing, phytoplankton will reduce both PmB and to accommodate the lower nutrient supply (keeping Ek relatively unchanged), and thus the two will covary. Experiments will be needed to examine the biophysical mechanisms by which colonial P. antarctica varies.
The forms of P. antarctica exist in a dynamic equilibrium in nature, and a distinct temporal trend occurs in these forms. Different controls of each morphotype likely exist, and hence the relative importance of these controls (bottom-up controls on colonies versus top-down controls on small flagellates), as well as the differential rates of photosynthesis and growth between them, will ultimately regulate their biomass within a bloom. Our data are relatively limited, but represent the first field data showing differences in the photosynthetic parameters and growth rates between the morphotypes of P. antarctica. Further study will clarify the importance of these differences, as well as the environmental and ecological regulation of the exchanges between the two forms. Understanding these differences will allow greater insights into the influence of phytoplankton composition on biogeochemical cycles in the Ross Sea.
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This research was supported by NSF grants OPP-0087401 and 0440478 to W.O.S.
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J. Peloquin and J. Dreyer assisted with laboratory analysis and we thank K. Tang, E. Canuel, D. Caron and D. Steinberg for comments on an earlier version of this manuscript. We thank S. Tozzi for his preparation of Fig. 1, and J. Morgan for her statistics help. The US Coast Guard, RVIB Nathaniel B. Palmer, and McMurdo Station support was invaluable to this study. The research herein was developed by the author, an employee of the US Environmental Protection Agency (EPA), prior to her employment with EPA. It was conducted independent of EPA employment and has not been subjected to the Agency's peer and administrative review. Therefore, the conclusions and opinions drawn are solely those of the author and are not necessarily the views of the Agency. VIMS Contribution Number 3011.
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Present Address: United States Environmental Protection Agency, Region 7, Water, Wetlands and Pesticide Division, 901N, 5th Street, Kansas City, Kansas 66101. 
Corresponding editor: William Li
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODRESULTSDISCUSSIONFUNDINGREFERENCES |
|---|
Arrigo K. R., Robinson D. H., Worthen D. L., et al. Phytoplankton community structure and the drawdown of nutrients and CO2 in the Southern Ocean. Science (1999) 283:365–367.
Banse K. Rates of growth, respiration and photosynthesis of unicellular algae as related to cell size- a review. J. Phycol. (1976) 12:135–140.[Web of Science]
Behrenfeld M. J., Prasil O., Babin M., et al. In search of a physiological basis for covariations in light-limited and light saturated photosynthesis. J. Phycol. (2004) 40:4–25.[Web of Science]
Boyd P., Newton P. Does planktonic community structure determine downward particulate organic carbon flux in different oceanic provinces? Deep-Sea Res. I (1999) 46:63–91.[CrossRef]
Boyd P. W., Robinson C., Savidge G. J., et al. Water column and sea ice production during austral spring in the Bellingshausen Sea. Deep-Sea Res. II (1995) 42:1177–1200.[CrossRef]
Caron D. A., Dennett M. R., Lonsdale D. J., et al. Microzooplankton herbivory in the Ross Sea, Antarctica. Deep-Sea Res. II (2000) 47:3249–3272.[CrossRef]
Cermeño P., Maranon E., Rodriguez J., et al. Large-sized phytoplankton sustain higher carbon-specific photosynthesis than smaller cells in a coastal eutrophic ecosystem. Mar. Ecol. Prog. Ser. (2005) 297:51–60.[CrossRef]
Claustre H., Moline M., Prézelin B. B. Sources of variability in the column photosynthetic cross section for Antarctic coastal waters. J. Geophys. Res. (1997) 102:25047–25060.[CrossRef]
Crosbie N. D., Furnas M. J. 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. (2001) 24:209–224.[CrossRef]
Davidson A. T., Marchant H. J. Binding of manganese by the mucilage of Antarctic Phaeocystis pouchetii and the role of bacteria in its release. Mar. Biol. (1987) 95:481–487.[CrossRef]
Dennett M. R., Mathot S., Caron D. A., et al. Abundance and distribution of phototrophic and heterotrophic nano- and microplankton in the southern Ross Sea. Deep-Sea Res. II (2001) 48:4019–4037.[CrossRef]
Frenette J. J., Vincent W. F., Legendre L. L., et al. Size dependent changes in phytoplankton C and N uptake in the dynamic mixed layer of Lake Biwa. Fresh Biol. (1996) 36:101–116.
Furnas M. J. Net in-situ growth rates of phytoplankton in an oligotrophic, tropical shelf ecosystem. Limnol. Oceanogr. (1991) 36:13–29.
Harding L. W. Jr, Fisher T. R., Tyler M. A. Adaptive responses of photosynthesis in phytoplankton: specificity to time-scale of change in light. Biol. Oceanogr. (1987) 4:403–437.
Holm-Hansen O., Mitchell B. G. Spatial and temporal distribution of phytoplankton and primary production in the western Bransfield Strait region. Deep-Sea Res. (1991) 38:961–980.[Web of Science]
Jakobsen H. H., Tang K. W. Effects of protozoan grazing on colony formation in Phaeocystis globosa (Prymnesiophyceae) and the potential costs and benefits. Aquat. Microb. Ecol. (2002) 27:261–273.[CrossRef]
Lancelot C., Mathot S. Biochemical fractionation of primary production by phytoplankton in Belgian coastal waters during short- and long-term incubations with 14C -bicarbonate. II. Phaeocystis pouchetii colonial population. Mar. Biol. (1985) 86:227–232.[CrossRef]
Lancelot C., Rousseau V. Ecology of Phaeocystis: the key role of colony forms. In: The Haptophyte Algae—Green J. C., Leadbeater B. S. C., eds. (1994) New York: Clarendon Press. 229–245.
Lindley S. T., Bidigare R. R., Barber R. T. Phytoplankton photosynthesis parameters along 140°W in the equatorial Pacific. Deep-Sea Res. II (1995) 42:441–464.[CrossRef]
Lubbers G. W., Gieskes W. W. C., del Castilho P., et al. Manganese accumulation in the high pH environment of Phaeocystis sp. (Haptophyceae) colonies from the North Sea. Mar. Ecol. Prog. Ser. (1990) 59:285–293.[CrossRef]
Mathot S., Smith W. O. Jr, Carlson C. A., et al. Estimate of Phaeocystis sp. carbon biomass: methodological problems related to the mucilaginous nature of the colonial matrix. J. Phycol. (2000) 36:1049–1056.[CrossRef][Web of Science]
Moline M. A., Schofield O., Boucher N. P. Photosynthetic parameters and empirical modeling of primary production: a case study on the Antarctic Peninsula shelf. Antarctic Sci. (1998) 10:45–54.
Olson R. J., Sosik H. M., Chekalyuk A. M., et al. Effects of iron enrichment of phytoplankton in the Southern ocean during late summer: active fluorescence and flow cytometric analyses. Deep-Sea Res. II (2000) 47:3179–3200.
Peloquin J. A., Smith W. O. Jr. Phytoplankton blooms in the Ross Sea, Antarctica: Interannual variability in magnitude, temporal patterns, and composition. J. Geophys. Res. (2007) 112. doi10.1029/2006JC003816.
Peperzak L., Duin R. M. N., Colijn F., et al. Growth and mortality of flagellates and non-flagellate cells of Phaeocystis globosa (Prymnesiophyceae). J. Plankton Res. (2000) 22:107–119.
Platt T., Jassby A. D. The relationship between photosynthesis and light for natural assemblages of coastal marine phytoplankton. J. Phycol. (1976) 12:421–430.[CrossRef][Web of Science]
Raven J. A. The twelfth Tansley lecture—small is beautiful—the picophytoplankton. Funct. Ecol. (1998) 12:503–513.[CrossRef]
Robinson D. H., Arrigo K. R., DiTullio G. R., et al. Evaluating photosynthetic carbon fixation during Phaeocystis antarctica blooms. In: Biogeochemistry of the Ross Sea—DiTullio G. R., Dunbar R. B., eds. (2003) Washington, DC: American Geophysical Union. 179–196.
Rousseau V., Valout D., Casotti R., et al. The life cycle of Phaeocystis (Prymnesiophyceae): evidence and hypotheses. J. Mar. Syst. (1994) 5:23–40.[CrossRef]
Sarmiento J. L., Monfray P., Maier-Reimer E., et al. Sea-air CO2 fluxes and carbon transport: a comparison of three ocean general circulation models. Global Biogeochem. Cycles (2000) 14:1267–1282.[CrossRef][Web of Science]
Schoemann V., Becquevort S., Stefels J., et al. Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J. Sea Res. (2005) 53:43–66.[CrossRef]
Sedwick P. N., DiTullio G. R. Regulation of algal blooms in Antarctic shelf waters by the release of iron from melting sea ice. Geophys. Res. Lett. (1997) 24:2515–2518.[CrossRef][Web of Science]
Sedwick P. N., DiTullio G. R., Mackey D. J. Iron and manganese in the Ross Sea, Antarctica: seasonal iron limitation in Antarctic shelf waters. J. Geophys. Res. (2000) 105:11321–11336.[CrossRef]
Sedwick P., Garcia N., Riseman S., et al. Evidence for high iron requirements of colonial Phaeocystis antarctica at low irradiance. Biogeochemistry (2007) 83:83–97.
Shields A. R., Smith W. O. Jr. An examination of the role of colonial Phaeocystis antarctica in the microbial food web of the Ross Sea. Polar Biol. (2008) 31:1091–1099.[CrossRef][Web of Science]
Smith W. O. Jr, Asper V. A. The influence of phytoplankton assemblage composition on biogeochemical characteristics and cycles in the southern Ross Sea, Antarctica. Deep-Sea Res. I (2001) 48:137–161.[CrossRef]
Smith W. O. Jr, Dennett M. R., Mathot S., et al. The temporal dynamics of the flagellated and colonial stages of Phaeocystis antarctica in the Ross Sea. Deep-Sea Res. II (2003) 50:605–617.[CrossRef]
Smith W. O. Jr, Shields A. R., Peloquin J. A., et al. Interannual variations in nutrients, net community production, and biogeochemical cycles in the Ross Sea. Deep-Sea Res. II (2006) 53:815–833.[CrossRef]
Sunda W. G., Huntsman S. A. Interrelated influence of iron, light and cell-size on marine phytoplankton growth. Nature (1997) 390:389–392.[CrossRef][Web of Science]
Tagliabue A., Arrigo K. R. Anomalously low zooplankton abundance in the Ross Sea: an alternative explanation. Limnol. Oceanogr. (2003) 24:686–699.
Tang K. W., Smith W. O. Jr, Elliott D. T., et al. Colony size of Phaeocystis antarctica (Prymnesiophyceae) as influenced by zooplankton grazers. J. Phycol. (2008) 44:1372–1378.[CrossRef][Web of Science]
van Hilst C. M., Smith W. O. Jr. Photosynthesis/irradiance relationships in the Ross Sea, Antarctica and their control by phytoplankton assemblage composition and environmental factors. Mar. Ecol. Prog. Ser. (2002) 226:1–12.[CrossRef]
Veldhuis M. J. W., Cloijn F., Admiraal W. Phosphate utilization in Phaeocystis pouchetii (Haptophyceae). Mar. Ecol. (1991) 12:53–62.[CrossRef]
Veldhuis M. J. W., Brussard C. P. D., Noordeloos A. A. M. Living in a Phaeocystis colony: a way to be a successful algal species. Harm. Algae (2005) 4:841–858.[CrossRef]
Verity P. G., Villareal T. A., Smayda T. J. Ecological investigations of blooms of colonial Phaeocystis pouchetii. II. The role of life-cycle phenomena in bloom termination. J. Plankton Res. (1988) 10:219–248.
Wassmann P., Ratkova T., Reigstad M. The contribution of single and colonial cells of Phaeocystis pouchetii to spring and summer blooms in the north-eastern North Atlantic. Harm. Algae (2005) 4:823–840.[CrossRef]
Webb W. L., Newton M., Starr D. Carbon dioxide exchange of Alnus rubra: a mathematical model. Oecologia (1974) 17:28l–291.
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