Does temperature affect phytoplankton size structure in the ocean?

Does temperature affect phytoplankton size structure in the ocean? E. Marañón 1, P. Cermeño 1, M. Latasa 2, R. D. Tadonléké 3 a Universidade de Vigo, Vigo, Spain b Instituto Español de Oceanografía, Gijón, Spain c Institut National de la Recherche Agronomique, Thonon les Bains, France

The importance of phytoplankton size structure Figure from Finkel et al 21 Phytoplankton dominated by: Property Small cells Large cells Dominant trophic pathway Microbial food web Classic food chain Main loss process for phytoplankton Grazing by protists Sinking and grazing by metazoans Photosynthesis-to-respiration ratio ~1 >1 f-ratio and e-ratio 5 15% >4% Main fate of primary production Recycling Export toward deep in the upper layer waters

The size-dependence of nutrient acquisition can explain the biogeography of phytoplankton size classes [DIN] (nm) at which cells become diffusion-limited µ= µ= Marañón 29 % picophytoplankton chl a % microphytoplankton chl a Hirata et al 211

but separating the effects of temperature and nutrients can be difficult because they are strongly correlated in the ocean Surface waters, Pacific Ocean Goes et al. 1999

Recent studies suggest a direct effect of temperature on phytoplankton size structure

The temperature-size rule: cell volume in protists decreases ~2.5% per C of warming (Atkinson et al 23) V difference from V 15 C / V 15 C Temperature difference from 15 C Atkinson et al 23

Objectives To test the hypothesis that temperature per se plays a role in controlling phytoplankton size structure in the ocean To assess the relative importance of temperature versus resources in the control of phytoplankton size structure

Approach To obtain a large data set of measurements of size-fractionated chl a in all combinations of temperature and resource supply conditions Nutrients LOW HIGH COLD Temperature WARM

Approach To obtain a large data set of measurements of size-fractionated chl a in all combinations of temperature and resource supply conditions LOW Nutrients HIGH COLD Temperature WARM

Data compilation: temperature, size-fractionated chl a and primary production in cold (<1 C), temperate (1-2 C) and warm (>2 C) waters Chl a map: SeaWiFS Project/NASA

General relationship between total and size-fractionated chl a Size-fractionated Chl a (µg L -1 ) 1 1.1.1.1.1 picophytoplankton nanophytoplankton microphytoplankton.2-2µm 2-2µm >2µm All data (n = 5).1.1 1 1 Total Chl a concentration (µg L -1 )

Similar patterns in regions with different temperatures Size-fractionated Chl a (µg L -1 ) 1 1.1.1.1.1 picophytoplankton nanophytoplankton microphytoplankton Cold.1.1 1 1 Total Chl a concentration (µg L -1 ) Size-fractionated Chl a (µg L -1 ) 1 1.1.1.1 n = 153 Temperate n = 165.1.1.1 1 1 Total Chl a concentration (µg L -1 ) Size-fractionated Chl a (µg L -1 ) 1 1.1.1.1.1 Warm n = 182.1.1 1 1 Total Chl a concentration (µg L -1 )

% Chl a in each size class strongly dependent on total Chl a % Picophytoplankton Chl a 8 6 4 2 cold temperate temperate warm warm Pico % Nanophytoplankton Chl a 8 6 4 2 Nano 5 1 15 2 25 5 1 15 2 25 % Microphytoplankton Chl a 8 6 4 2 8 6 4 2 Micro y = 92.3 (1 - e -53.4x/92.3 ) r 2 =.78, p <.1, n = 5 1 2 5 1 15 2 25 Total Chl a concentration (µg L -1 )

No relationship between temperature and size-frac. Chl a Pico Nano % Picophytoplankton Chl a 8 6 4 2 % Nanophytoplankton Chl a 8 6 4 2-5 5 1 15 2 25 3-5 5 1 15 2 25 3 Micro % Microphytoplankton Chl a 8 6 4 2-5 5 1 15 2 25 3 Temperature ( C)

% Microphytoplankton Chl a Temperature vs. % microphytoplankton Chl a 8 6 4 2 1 3 4 2 1 8 12 14 32 6 13 26 15 7 11 17 24 31 19 2 18 33 9 21 23 5 3 16 22-5 5 1 15 2 25 3 35 25 Temperature ( C) 27 29 28 Locations 1. Marguerite Bay, Antarctic Peninsula, winter 2. Marguerite Bay, Antarctic Peninsula, summer 3. Southern Ocean, Atl. sector, spring ice edge zone 4. Southern Ocean, Atl. sector, marginal ice zone 5. Southern Ocean, Atl. sector, polar front 6. SOIREE Fe addition exp. (Southern Ocean), inside 7. SOIREE Fe addition exp., outside 8. SOFeX iron addition exp. (Southern Ocean), inside 9. SOFeX iron addition exp., outside 1. Kerguelen Plateau, Fe-fertilised waters 11. Kerguelen Plateau, HNLC water 12. SEEDS Fe addition exp. (subarctic W Pacific), inside 13. SEEDS Fe addition exp., outside 14. SERIES iron addition exp. (Gulf of Alaska), inside 15. SERIES iron addition exp., outside 16. Okhotsk Sea (western Pacific Ocean), Oct 1993 17. Okhotsk Sea, Nov 1993 18. NE subarctic Pacific, late summer 19. NE subarctic Pacific, late winter 2. NE subarctic Pacific, late spring 21. NW subarctic Pacific, summer 22. NW subarctic Pacific, autumn 23. NW subarctic Pacific, winter 24. Ría de Vigo (NW Iberian peninsula), winter 25. Ría de Vigo, upwelling season 26. Gulf of Tehuantepec (SW Mexico), Jan-Feb 1999 27. Gulf of Tehuantepec, Jan-Feb 1989 28. Johor Strait (Singapore), May-Jul 1998 29. Iskenderun Bay (NE Mediterranean Sea, Jul 23 3. North & South Atl. subtropical gyres 31. Arabian Sea during the 1995 monsoon (Aug-Sep) 32. IronEx II Fe addition exp., inside 33. IronEx II Fe addition exp., outside

% Chl a in each size class strongly dependent on primary productivity, e.g. resource utilization rate % Picophytoplankton Chl a 8 6 4 2 cold temperate warm Pico % Nanophytoplankton Chl a 8 6 4 2 Nano 5 15 5 15 % Microphytoplankton Chl a 8 6 4 2 8 6 4 2 2 Micro y = 79.5 (1 - e -2.4x/79.5 ) r 2 =.59, p <.1, n = 165 5 15 Total primary production (µg C L -1 d -1 )

A simple simulation indicates the temperature-size rule can cause only minor changes in size structure log 1 cell abundance (cell ml -1 ) 5 4 3 2 1 control +1 C, -25% cell size +2 C, -5% cell size 2.6 34. 63.4 3. 36.4 6.6 3.7 41.8 54.4 2 µm 2 µm Biovolume (%) pico nano micro -1 1 2 3 4 5 log 1 cell size (µm 3 )

A summary of phytoplankton size structure in the ocean Temperature COLD TEMPERATE WARM Resource utilization rate HIGH LOW Summer bloom in Antarctic Peninsula Fertilised patch, Fe addition expts in Southern Ocean Antarctic peninsula in winter (light limitation) Southern Ocean HNLC waters in summer (Fe limitation) NW Iberian coast, upwelling season Fertilised patch, SERIES experiment (Gulf of Alaska) NW Iberian coast, winter (light limitation) Eastern subarctic N Pacific (Fe limitation) Coastal, nutrient-rich waters in warm seas Fertilised patch, IronEx II (Eq. Pacific) Subtropical gyres (macronutrient limitation) Eq. Pac., HNLC waters (Fe limitation) Small cells dominate Large cells dominate

Conclusions Phytoplankton size structure controlled by rate of resource utilization Role of temperature per se is negligible No universal effect of warming on phytoplankton size structure

Acknowledgements Thanks to P. W. Boyd, A. Clarke, and A. Tsuda for making their data available. Research funded by the Spanish Ministry of Science and Innovation. P E R S E O P E R S E O Macroecological patterns in marine phytoplankton A research project funded by Ministerio de Ciencia e Innovación (CTM28-3999)