COMMENTARY
Diatom traits regulate Southern Ocean silica leakage Philip W. Boyd1 Institute for Marine and Antarctic Studies, University of Tasmania, Hobart 7005, Tasmania, Australia
Ocean circulation is a remarkable interconnecting conduit, such that biological processes occurring in the remote Southern Ocean can influence the regulation of productivity in Northern Hemisphere waters. Marine phytoplankton, despite their small size, play a disproportionately important role in setting the stoichiometric relationship between elements such as nitrogen, phosphorus, carbon and silicon in the global ocean (1, 2). In turn this ecological stoichiometry helps to set the ultimate limiting nutrient(s) for primary productivity (2, 3). To date, investigation of stoichiometric effects has mainly been centered on low latitude waters (3, 4). However, the Southern Ocean plays a fundamental role in setting the productivity of distant waters, such as the Equatorial Pacific (5), by controlling the leakage of waters with high Silicic acid:Nitrate ratios—the so-called silicic acid leakage hypothesis (SALH) (6, 7). In PNAS, Assmy et al. (8) provide unprecedented detail of how the ecological traits of different polar diatom species contribute to the regulation of ocean nutrient stoichiome-
try. Thus, diatom floristics help to control the leakage of silicic acid, relative to that of nitrate, into the global ocean, which sets the magnitude of Northern Hemisphere diatom productivity, export, and hence carbon sequestration. Assmy et al. (8) are able to reveal the potent linkages between Southern Ocean ecology and regional biogeochemistry because they conducted a transdisciplinary 35-d study [European Iron Fertilization Experiment (EIFEX)] on a scale of 100 km. Such mesoscale iron enrichments represent some of the largest ecological manipulation experiments globally (9). Thus, they are of sufficient scale, scope, and longevity to provide a holistic view of how environmental manipulations drive a diverse range of biological responses. Such responses consequently transform many ecological processes, each with characteristic biogeochemical signatures. When these ecological responses are placed in a wider biogeochemical context, and animated by ocean circulation, the global implications for ocean biogeochemistry become evident. Until EIFEX
Fig. 1. Species composition of Southern Ocean diatom blooms regulates silicic acid leakage to the global ocean. (A) Diatoms with a suite of traits characterized by Chaetoceros spp. dominate the initial phases of the iron-fueled bloom and avoid predation by growing fast. Consequently, their abundances exceed the threshold for particle aggregation and these C- and N-rich cells sink out. (B) Diatoms with traits characterized by Fragilariopsis spp. dominate the latter bloom phases, with slow growth rates (similar to their predators) compensated for by silica body armor and ensuring that they accumulate in surface waters (but do not exceed the aggregation threshold that leads to rapid sedimentation). Together these strategies help define the ecological stoichiometry of individual blooms and (C) help regulate the Si:N stoichiometry of Subantarctic mode water flowing northward. The diatom images in panels A and B are courtesy of the Alfred Wegener Institute, and the Southern Ocean circulation schematic in panel C is redrawn from (20) and is courtesy of the Royal Society of Tasmania. 20358–20359 | PNAS | December 17, 2013 | vol. 110 | no. 51
(8), our understanding of the SALH (6, 7) centered around a generic relationship between polar diatoms and the role that iron supply plays on altering their silicic acid: nitrate uptake ratio, and hence the consequent supply of excess silicic acid, relative to nitrate, to more northerly waters (6, 7). During EIFEX (8), the team tracked how the contribution of the dominant diatom species during the ironstimulated bloom changed over time, and significantly they pinpointed the fate of the main blooming diatom species. These trends, when related to temporal changes in both nutrient consumption and elemental composition of the diatom community, give us new insights into how the makeup of the diatom community (i.e., floristics) sets the degree of coupling between carbon, nitrogen, and silicon biogeochemistry. Furthermore, Assmy et al. (8) use a revolutionary concept proposed by one of the coauthors, “the watery arms race,” (10) to provide the underlying survival strategies that support this diverse diatom community. In brief, Smetacek (10) hypothesized that the wide range of geometries and elemental compositions evident in polar diatoms reflect different strategies to avoid predation. In the Southern Ocean, abundant silicic acid may have resulted in the evolutionary development of “silica body armor” to deter grazers (11). Such armor requires a large amount of silica per diatom (8, 11) and hence when ecological stoichiometry gets altered at a cellular level, it is of regional (and later global) significance due to ubiquitous nature of these diatom groups that often bloom. Hence, Assmy et al. (8) advance our understanding of the nuances of the SALH (6, 7) by invoking a fundamental diatom trait (grazer avoidance through ecological stoichiometry), which has subsequent effects on the Si:N ratio of northward flowing waters (7). It is notable that the ecological traits of a range of different species, which evolved in the specialized Southern Ocean environment, can have such Author contributions: P.W.B. wrote the paper. The author declares no conflict of interest. See companion article on page 20633. 1
E-mail: [email protected].
www.pnas.org/cgi/doi/10.1073/pnas.1320327110
Boyd
driven by trait-based succession, with Fragilariopsis spp. doubling in biomass rather than simply persisting, as reported by Assmy et al. (8), later in the bloom. This enhanced biomass probably resulted jointly from the capacity for iron storage, iron-mediated decreases in sinking rate (16), and body armor (Fig. 1).
EIFEX (8) details one example of diatom bloom dynamics within the Antarctic Circumpolar Current (ACC). The cumulative effect of blooms, with differing ecological stoichiometries, across the ACC will strongly influence the degree of coupling between C, N, and Si biogeochemistry and consequently affect C sequestration efficiency (9) and/or the Si:N ratio of waters leaking northward within sub-Antarctic mode water (6, 7). The initial diatom seed stocks and the interplay of physiological traits that characterize each
diatom species will determine which type of diatom species (co)dominates individual blooms (Fig. 1). As pointed out by Assmy et al. (8), the ACC with its continuous westward circumpolar flow is a conveyor belt seeded with a wide range of diatom species— from neritic to oceanic provenances—all primed to respond opportunistically to the supply of the scarce micronutrient iron. Each diatom species can dominate (Fragillariopsis spp.) (9, 16) or codominate (8, 9) blooms. The important ecological and biogeochemical roles of diatom species succession has also been reported for Southern Ocean waters that are naturally high in iron (17), as well as in Northern Hemisphere oceanic (13) and coastal (18) waters, suggesting it is a widespread trend. As is becoming evident across the global ocean, the concept of a functional group— such as coccolithophores—breaks down whenever their responses to environmental forcing are probed, such as in laboratory culture studies (19). This appears to be equally true for diatoms, a point well made by Assmy et al. (8) and others during naturally occurring blooms (17, 18) and mesoscale iron enrichment studies (13). Unlike laboratory culture experiments, such field studies also reveal the wider regional and global ramifications, such as the SALH, of diatom floristics on ocean biogeochemistry.
1 Falkowski PG, Barber RT, Smetacek V (1998) Biogeochemical controls and feedbacks on ocean primary production. Science 281(5374):200–207. 2 Sarmiento JL, Gruber N, Brzezinski MA, Dunne JP (2004) Highlatitude controls of thermocline nutrients and low latitude biological productivity. Nature 427(6969):56–60. 3 Deutsch C, Sarmiento JL, Sigman DM, Gruber N, Dunne JP (2007) Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445(7124):163–167. 4 Ward BA, et al. (2013) Iron, phosphorus, and nitrogen supply ratios define the biogeography of nitrogen fixation. Limnol Oceanogr 58(6):2059–2075. 5 Pichevin LE, et al. (2009) Enhanced carbon pump inferred from relaxation of nutrient limitation in the glacial ocean. Nature 459(7250):1114–1117. 6 Matsumoto K et al. (2002) Silicic acid leakage from the Southern Ocean: A possible explanation for glacial atmospheric pCO2. Global Biogeochem Cycles, 10.1029/2001GB001442. 7 Matsumoto K, Sarmiento JL (2008) A corollary to the silicic acid leakage hypothesis. Paleoceanography, 10.1029/2007PA001515. 8 Assmy P, et al. (2013) Thick-shelled, grazer-protected diatoms decouple ocean carbon and silicon cycles in the iron-limited Antarctic Circumpolar Current. Proc Natl Acad Sci USA 110:20633–20638. 9 Boyd PW, et al. (2007) A synthesis of mesoscale iron-enrichment experiments 1993-2005: key findings and implications for ocean biogeochemistry. Science 315:612–617. 10 Smetacek V (2001) A watery arms race. Nature 411(6839):745.
11 Hamm CE, et al. (2003) Architecture and material properties of diatom shells provide effective mechanical protection. Nature 421(6925):841–843, 10.1038/nature01416. 12 Litchman E, Klausmeier CA (2008) Trait-based community ecology of phytoplankton. Ann Rev Ecol. Evol Syst 39:615– 639. 13 Boyd PW, et al. (2005) The evolution and termination of an ironinduced mesoscale bloom in the northeast subarctic Pacific. Limnol Oceanogr 50(6):1872–1886. 14 Strzepek RF, et al. (2011) Adaptive strategies by Southern Ocean phytoplankton to lessen iron limitation: Uptake of organically complexed iron and reduced cellular iron requirements. Limnol Oceanogr 56(6):1983–2002. 15 Marchetti A, et al. (2009) Ferritin is used for iron storage in bloomforming marine pennate diatoms. Nature 457(7228):467–470. 16 Waite A Nodder S (2001) The effect of in situ iron addition on the sinking rates and export flux of Southern Ocean diatoms. Deep Sea Res Part II Top Stud Oceanogr 48(11-12):2635–2654. 17 Queguiner B (2013) Iron fertilization and the structure of planktonic communities in high nutrient regions of the Southern Ocean. Deep-Sea Res II 90: 43–54. 18 Riebesell U (1991) Particle aggregation during a diatom bloom. II. biological aspects. Mar Ecol Prog Ser 69:281–291. 19 Boyd PW, et al. (2010) Environmental control of open-ocean phytoplankton groups: Now and in the future. Limnol Oceanogr 55(3):1353–1376. 20 Rintoul SR (2000) Southern Ocean currents and climate. Papers Proc Royal Soc Tasmania 133:41–50.
Assmy et al. provide unprecedented detail of how the ecological traits of different polar diatom species contribute to the regulation of ocean nutrient stoichiometry.
PNAS | December 17, 2013 | vol. 110 | no. 51 | 20359
COMMENTARY
fundamental importance on both regional and global productivity. Despite the appeal of the proposed “evolutionary arms race” (8), Assmy et al. stop short of considering the importance of other physiological traits that help characterize this diverse range of diatom species. Studies of physiological traits and how tradeoffs between traits (e.g., resource acquisition versus predator avoidance) are a growing research theme (12). Also, had Assmy et al. (8) looked more closely at mesoscale iron enrichment studies in other iron-poor regions, they would have noted similar trends with respect to temporal succession during diatom blooms (13). For example, during the Subarctic Ecosystem Response to Iron Enrichment Study bloom in the northeast subarctic Pacific, Chaetoceros spp. dominated the early bloom phases and were succeeded by Thalassiothrix spp. after Chaetoceros sank to depth (13), a trend conspicuous during EIFEX (8). Fig. 1 links the wider concepts of physiological traits and tradeoffs with observed temporal trends of diatom species succession in subarctic (13) and Southern Ocean ironstimulated blooms (8). Important adaptive strategies, in addition to predator avoidance, include growth rate and iron requirements (14), capacity for intracellular iron storage (pennates vs. centric diatoms) (15), cell sinking rate (13, 16), and how prone cells are to species-specific aggregation (13). As observed for the ratio of silicic acid:nitrate uptake, iron supply influences most of these characteristics (13, 14). Hence, the trends from EIFEX (8) also reflect the interplay of additional strategies in terms of diatom physiology, which set the timing of bloom dominance by different diatom species (growth rate), their fate (rapid growth leads to aggregation then export) (13), and the interplay of factors controlling diatom succession (slow growth rate, ability to store iron, body armor) evident in both subarctic and polar waters. EIFEX (8) provides a valuable example from a Southern Ocean field study of the wider ecological and biogeochemical ramifications of the interplay of physiological traits that will be of particular interest for modelers. During EIFEX, diatom species that contributed to the bloom avoided predation by either growing fast (Chaetoceros spp.) or via body armor (Fig. 1). The longevity of the bloom was
Diatom traits regulate Southern Ocean silica leakage Philip W. Boyd1 Institute for Marine and Antarctic Studies, University of Tasmania, Hobart 7005, Tasmania, Australia
Ocean circulation is a remarkable interconnecting conduit, such that biological processes occurring in the remote Southern Ocean can influence the regulation of productivity in Northern Hemisphere waters. Marine phytoplankton, despite their small size, play a disproportionately important role in setting the stoichiometric relationship between elements such as nitrogen, phosphorus, carbon and silicon in the global ocean (1, 2). In turn this ecological stoichiometry helps to set the ultimate limiting nutrient(s) for primary productivity (2, 3). To date, investigation of stoichiometric effects has mainly been centered on low latitude waters (3, 4). However, the Southern Ocean plays a fundamental role in setting the productivity of distant waters, such as the Equatorial Pacific (5), by controlling the leakage of waters with high Silicic acid:Nitrate ratios—the so-called silicic acid leakage hypothesis (SALH) (6, 7). In PNAS, Assmy et al. (8) provide unprecedented detail of how the ecological traits of different polar diatom species contribute to the regulation of ocean nutrient stoichiome-
try. Thus, diatom floristics help to control the leakage of silicic acid, relative to that of nitrate, into the global ocean, which sets the magnitude of Northern Hemisphere diatom productivity, export, and hence carbon sequestration. Assmy et al. (8) are able to reveal the potent linkages between Southern Ocean ecology and regional biogeochemistry because they conducted a transdisciplinary 35-d study [European Iron Fertilization Experiment (EIFEX)] on a scale of 100 km. Such mesoscale iron enrichments represent some of the largest ecological manipulation experiments globally (9). Thus, they are of sufficient scale, scope, and longevity to provide a holistic view of how environmental manipulations drive a diverse range of biological responses. Such responses consequently transform many ecological processes, each with characteristic biogeochemical signatures. When these ecological responses are placed in a wider biogeochemical context, and animated by ocean circulation, the global implications for ocean biogeochemistry become evident. Until EIFEX
Fig. 1. Species composition of Southern Ocean diatom blooms regulates silicic acid leakage to the global ocean. (A) Diatoms with a suite of traits characterized by Chaetoceros spp. dominate the initial phases of the iron-fueled bloom and avoid predation by growing fast. Consequently, their abundances exceed the threshold for particle aggregation and these C- and N-rich cells sink out. (B) Diatoms with traits characterized by Fragilariopsis spp. dominate the latter bloom phases, with slow growth rates (similar to their predators) compensated for by silica body armor and ensuring that they accumulate in surface waters (but do not exceed the aggregation threshold that leads to rapid sedimentation). Together these strategies help define the ecological stoichiometry of individual blooms and (C) help regulate the Si:N stoichiometry of Subantarctic mode water flowing northward. The diatom images in panels A and B are courtesy of the Alfred Wegener Institute, and the Southern Ocean circulation schematic in panel C is redrawn from (20) and is courtesy of the Royal Society of Tasmania. 20358–20359 | PNAS | December 17, 2013 | vol. 110 | no. 51
(8), our understanding of the SALH (6, 7) centered around a generic relationship between polar diatoms and the role that iron supply plays on altering their silicic acid: nitrate uptake ratio, and hence the consequent supply of excess silicic acid, relative to nitrate, to more northerly waters (6, 7). During EIFEX (8), the team tracked how the contribution of the dominant diatom species during the ironstimulated bloom changed over time, and significantly they pinpointed the fate of the main blooming diatom species. These trends, when related to temporal changes in both nutrient consumption and elemental composition of the diatom community, give us new insights into how the makeup of the diatom community (i.e., floristics) sets the degree of coupling between carbon, nitrogen, and silicon biogeochemistry. Furthermore, Assmy et al. (8) use a revolutionary concept proposed by one of the coauthors, “the watery arms race,” (10) to provide the underlying survival strategies that support this diverse diatom community. In brief, Smetacek (10) hypothesized that the wide range of geometries and elemental compositions evident in polar diatoms reflect different strategies to avoid predation. In the Southern Ocean, abundant silicic acid may have resulted in the evolutionary development of “silica body armor” to deter grazers (11). Such armor requires a large amount of silica per diatom (8, 11) and hence when ecological stoichiometry gets altered at a cellular level, it is of regional (and later global) significance due to ubiquitous nature of these diatom groups that often bloom. Hence, Assmy et al. (8) advance our understanding of the nuances of the SALH (6, 7) by invoking a fundamental diatom trait (grazer avoidance through ecological stoichiometry), which has subsequent effects on the Si:N ratio of northward flowing waters (7). It is notable that the ecological traits of a range of different species, which evolved in the specialized Southern Ocean environment, can have such Author contributions: P.W.B. wrote the paper. The author declares no conflict of interest. See companion article on page 20633. 1
E-mail: [email protected].
www.pnas.org/cgi/doi/10.1073/pnas.1320327110
Boyd
driven by trait-based succession, with Fragilariopsis spp. doubling in biomass rather than simply persisting, as reported by Assmy et al. (8), later in the bloom. This enhanced biomass probably resulted jointly from the capacity for iron storage, iron-mediated decreases in sinking rate (16), and body armor (Fig. 1).
EIFEX (8) details one example of diatom bloom dynamics within the Antarctic Circumpolar Current (ACC). The cumulative effect of blooms, with differing ecological stoichiometries, across the ACC will strongly influence the degree of coupling between C, N, and Si biogeochemistry and consequently affect C sequestration efficiency (9) and/or the Si:N ratio of waters leaking northward within sub-Antarctic mode water (6, 7). The initial diatom seed stocks and the interplay of physiological traits that characterize each
diatom species will determine which type of diatom species (co)dominates individual blooms (Fig. 1). As pointed out by Assmy et al. (8), the ACC with its continuous westward circumpolar flow is a conveyor belt seeded with a wide range of diatom species— from neritic to oceanic provenances—all primed to respond opportunistically to the supply of the scarce micronutrient iron. Each diatom species can dominate (Fragillariopsis spp.) (9, 16) or codominate (8, 9) blooms. The important ecological and biogeochemical roles of diatom species succession has also been reported for Southern Ocean waters that are naturally high in iron (17), as well as in Northern Hemisphere oceanic (13) and coastal (18) waters, suggesting it is a widespread trend. As is becoming evident across the global ocean, the concept of a functional group— such as coccolithophores—breaks down whenever their responses to environmental forcing are probed, such as in laboratory culture studies (19). This appears to be equally true for diatoms, a point well made by Assmy et al. (8) and others during naturally occurring blooms (17, 18) and mesoscale iron enrichment studies (13). Unlike laboratory culture experiments, such field studies also reveal the wider regional and global ramifications, such as the SALH, of diatom floristics on ocean biogeochemistry.
1 Falkowski PG, Barber RT, Smetacek V (1998) Biogeochemical controls and feedbacks on ocean primary production. Science 281(5374):200–207. 2 Sarmiento JL, Gruber N, Brzezinski MA, Dunne JP (2004) Highlatitude controls of thermocline nutrients and low latitude biological productivity. Nature 427(6969):56–60. 3 Deutsch C, Sarmiento JL, Sigman DM, Gruber N, Dunne JP (2007) Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445(7124):163–167. 4 Ward BA, et al. (2013) Iron, phosphorus, and nitrogen supply ratios define the biogeography of nitrogen fixation. Limnol Oceanogr 58(6):2059–2075. 5 Pichevin LE, et al. (2009) Enhanced carbon pump inferred from relaxation of nutrient limitation in the glacial ocean. Nature 459(7250):1114–1117. 6 Matsumoto K et al. (2002) Silicic acid leakage from the Southern Ocean: A possible explanation for glacial atmospheric pCO2. Global Biogeochem Cycles, 10.1029/2001GB001442. 7 Matsumoto K, Sarmiento JL (2008) A corollary to the silicic acid leakage hypothesis. Paleoceanography, 10.1029/2007PA001515. 8 Assmy P, et al. (2013) Thick-shelled, grazer-protected diatoms decouple ocean carbon and silicon cycles in the iron-limited Antarctic Circumpolar Current. Proc Natl Acad Sci USA 110:20633–20638. 9 Boyd PW, et al. (2007) A synthesis of mesoscale iron-enrichment experiments 1993-2005: key findings and implications for ocean biogeochemistry. Science 315:612–617. 10 Smetacek V (2001) A watery arms race. Nature 411(6839):745.
11 Hamm CE, et al. (2003) Architecture and material properties of diatom shells provide effective mechanical protection. Nature 421(6925):841–843, 10.1038/nature01416. 12 Litchman E, Klausmeier CA (2008) Trait-based community ecology of phytoplankton. Ann Rev Ecol. Evol Syst 39:615– 639. 13 Boyd PW, et al. (2005) The evolution and termination of an ironinduced mesoscale bloom in the northeast subarctic Pacific. Limnol Oceanogr 50(6):1872–1886. 14 Strzepek RF, et al. (2011) Adaptive strategies by Southern Ocean phytoplankton to lessen iron limitation: Uptake of organically complexed iron and reduced cellular iron requirements. Limnol Oceanogr 56(6):1983–2002. 15 Marchetti A, et al. (2009) Ferritin is used for iron storage in bloomforming marine pennate diatoms. Nature 457(7228):467–470. 16 Waite A Nodder S (2001) The effect of in situ iron addition on the sinking rates and export flux of Southern Ocean diatoms. Deep Sea Res Part II Top Stud Oceanogr 48(11-12):2635–2654. 17 Queguiner B (2013) Iron fertilization and the structure of planktonic communities in high nutrient regions of the Southern Ocean. Deep-Sea Res II 90: 43–54. 18 Riebesell U (1991) Particle aggregation during a diatom bloom. II. biological aspects. Mar Ecol Prog Ser 69:281–291. 19 Boyd PW, et al. (2010) Environmental control of open-ocean phytoplankton groups: Now and in the future. Limnol Oceanogr 55(3):1353–1376. 20 Rintoul SR (2000) Southern Ocean currents and climate. Papers Proc Royal Soc Tasmania 133:41–50.
Assmy et al. provide unprecedented detail of how the ecological traits of different polar diatom species contribute to the regulation of ocean nutrient stoichiometry.
PNAS | December 17, 2013 | vol. 110 | no. 51 | 20359
COMMENTARY
fundamental importance on both regional and global productivity. Despite the appeal of the proposed “evolutionary arms race” (8), Assmy et al. stop short of considering the importance of other physiological traits that help characterize this diverse range of diatom species. Studies of physiological traits and how tradeoffs between traits (e.g., resource acquisition versus predator avoidance) are a growing research theme (12). Also, had Assmy et al. (8) looked more closely at mesoscale iron enrichment studies in other iron-poor regions, they would have noted similar trends with respect to temporal succession during diatom blooms (13). For example, during the Subarctic Ecosystem Response to Iron Enrichment Study bloom in the northeast subarctic Pacific, Chaetoceros spp. dominated the early bloom phases and were succeeded by Thalassiothrix spp. after Chaetoceros sank to depth (13), a trend conspicuous during EIFEX (8). Fig. 1 links the wider concepts of physiological traits and tradeoffs with observed temporal trends of diatom species succession in subarctic (13) and Southern Ocean ironstimulated blooms (8). Important adaptive strategies, in addition to predator avoidance, include growth rate and iron requirements (14), capacity for intracellular iron storage (pennates vs. centric diatoms) (15), cell sinking rate (13, 16), and how prone cells are to species-specific aggregation (13). As observed for the ratio of silicic acid:nitrate uptake, iron supply influences most of these characteristics (13, 14). Hence, the trends from EIFEX (8) also reflect the interplay of additional strategies in terms of diatom physiology, which set the timing of bloom dominance by different diatom species (growth rate), their fate (rapid growth leads to aggregation then export) (13), and the interplay of factors controlling diatom succession (slow growth rate, ability to store iron, body armor) evident in both subarctic and polar waters. EIFEX (8) provides a valuable example from a Southern Ocean field study of the wider ecological and biogeochemical ramifications of the interplay of physiological traits that will be of particular interest for modelers. During EIFEX, diatom species that contributed to the bloom avoided predation by either growing fast (Chaetoceros spp.) or via body armor (Fig. 1). The longevity of the bloom was
