Does temperature affect phytoplankton size structure in

Does temperature affect phytoplankton size structure in the ocean?

E. Marañón1, P. Cermeño1, M. Latasa2, R. D. Tadonléké3

aUniversidade de Vigo, Vigo, Spain bInstituto Español de Oceanografía, Gijón, Spain

cInstitut National de la Recherche Agronomique, Thonon les Bains, France

Figure from Finkel et al 2010

The importance of phytoplankton size structure

Phytoplankton dominated by:

Property Small cells Large cells

Dominant trophic pathway Microbial food web Classic food chainMain loss process for phytoplankton Grazing by protists Sinking and grazing

by metazoansPhotosynthesis-to-respiration ratio ~1 >1f-ratio and e-ratio 5–15% >40%Main fate of primary production Recycling Export toward deep

in the upper layer waters

% microphytoplankton chl a% picophytoplankton chl a

[DIN

] (nM

) at w

hich

cel

ls

beco

me

diffu

sion

-lim

ited

The size-dependence of nutrient acquisition can explain the

biogeography of phytoplankton size classes… M

arañ

ón 2

009

Hirata et al 2011

µ=

µ=

…but separating the effects of temperature and nutrients can be difficult because they are strongly correlated in the ocean

Goes et al. 1999

Surface waters, Pacific Ocean

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

V d

iffer

ence

from

V15

°C/ V

15°C

Temperature difference from 15°C

The temperature-size rule: cell volume in protists decreases ~2.5% per °C of warming (Atkinson et al 2003)

Atkinson et al 2003

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

Temperature

Nut

rien

ts

HIG

HLO

W

COLD WARM

Temperature

Nut

rien

ts

HIG

HLO

W

COLD WARM

Approach

To obtain a large data set of measurements of size-fractionated chl a in all combinations of temperature and resource supply conditions

Data compilation: temperature, size-fractionated chl a and primary production in cold (<10°C), temperate (10-20°C) and warm (>20°C) waters

Chl a map: SeaWiFS Project/NASA

Total Chl a concentration (µg L-1)

0.01 0.1 1 10 100

Size

-frac

tiona

ted

Chl

a (µ

g L-1

)

0.0001

0.001

0.01

0.1

1

10

100picophytoplanktonnanophytoplanktonmicrophytoplankton

All data (n = 500)

General relationship between total and size-fractionated chl a

0.2-2µm2-20µm>20µm


0.01 0.1 1 10 100

Size

-fra

ctio

nate

d C

hl a

(µg

L-1)

0.0001

0.001

0.01

0.1

1

10

100picophytoplanktonnanophytoplanktonmicrophytoplankton


0.01 0.1 1 10 100

Size

-fra

ctio

nate

d C

hl a

(µg

L-1)

0.0001

0.001

0.01

0.1

1

10

100

Cold Temperate

Similar patterns in regions with different temperatures

n = 153 n = 165


0.01 0.1 1 10 100

Size

-fra

ctio

nate

d C

hl a

(µg

L-1)

0.0001

0.001

0.01

0.1

1

10

100

Warm n = 182

0 5 10 15 20 25

% P

icop

hyto

plan

kton

Chl

a

0

20

40

60

80

100coldtemperatewarm

0 5 10 15 20 25

% N

anop

hyto

plan

kton

Chl

a

0

20

40

60

80

100


0 5 10 15 20 25

% M

icro

phyt

opla

nkto

n C

hl a

0

20

40

60

80

100

Pico Nano

% Chl a in each size class strongly dependent on total Chl a

coldtemperatewarm

0 1 2

020406080

100

Microy = 92.3 (1 - e-53.4x/92.3)r2 = 0.78, p < 0.001, n = 500

-5 0 5 10 15 20 25 30

% P

icop

hyto

plan

kton

Chl

a

0

20

40

60

80

100

-5 0 5 10 15 20 25 30

% N

anop

hyto

plan

kton

Chl

a

0

20

40

60

80

100

Temperature (°C)

-5 0 5 10 15 20 25 30

% M

icro

phyt

opla

nkto

n C

hl a

0

20

40

60

80

100

No relationship between temperature and size-frac. Chl a

Pico Nano

Micro

Temperature (°C)

-5 0 5 10 15 20 25 30 35

% M

icro

phyt

opla

nkto

n C

hl a

0

20

40

60

80

100

1817

4

16

10

33

23 30

2019

22

14

9

32

29

26

2

21

15

6

8

3124

13

25

1

3 28

7

27

12

11

5

1. Marguerite Bay, Antarctic Peninsula, winter2. Marguerite Bay, Antarctic Peninsula, summer3. Southern Ocean, Atl. sector, spring ice edge zone4. Southern Ocean, Atl. sector, marginal ice zone 5. Southern Ocean, Atl. sector, polar front 6. SOIREE Fe addition exp. (Southern Ocean), inside7. SOIREE Fe addition exp., outside8. SOFeX iron addition exp. (Southern Ocean), inside 9. SOFeX iron addition exp., outside10. Kerguelen Plateau, Fe-fertilised waters11. Kerguelen Plateau, HNLC water12. SEEDS Fe addition exp. (subarctic W Pacific), inside 13. SEEDS Fe addition exp., outside 14. SERIES iron addition exp. (Gulf of Alaska), inside15. SERIES iron addition exp., outside 16. Okhotsk Sea (western Pacific Ocean), Oct 199317. Okhotsk Sea, Nov 199318. NE subarctic Pacific, late summer 19. NE subarctic Pacific, late winter 20. NE subarctic Pacific, late spring21. NW subarctic Pacific, summer22. NW subarctic Pacific, autumn 23. NW subarctic Pacific, winter 24. Ría de Vigo (NW Iberian peninsula), winter 25. Ría de Vigo, upwelling season26. Gulf of Tehuantepec (SW Mexico), Jan-Feb 1999 27. Gulf of Tehuantepec, Jan-Feb 198928. Johor Strait (Singapore), May-Jul 1998 29. Iskenderun Bay (NE Mediterranean Sea, Jul 2003 30. 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

Temperature vs. % microphytoplankton Chl a

Locations

Temperature (°C)

-5 0 5 10 15 20 25 30 35

% M

icro

phyt

opla

nkto

n C

hl a

0

20

40

60

80

100

1817

4

16

10

33

23 30

2019

22

14

9

32

29

26

2

21

15

6

8

3124

13

25

1

3 28

7

27

12

11

5


Locations


Temperature (°C)

-5 0 5 10 15 20 25 30 35

% M

icro

phyt

opla

nkto

n C

hl a

0

20

40

60

80

100

1817

4

16

10

33

23 30

2019

22

14

9

32

29

26

2

21

15

6

8

3124

13

25

1

3 28

7

27

12

11

5


Locations


Temperature (°C)

-5 0 5 10 15 20 25 30 35

% M

icro

phyt

opla

nkto

n C

hl a

0

20

40

60

80

100

1817

4

16

10

33

23 30

2019

22

14

9

32

29

26

2

21

15

6

8

3124

13

25

1

3 28

7

27

12

11

5


Locations


Temperature (°C)

-5 0 5 10 15 20 25 30 35

% M

icro

phyt

opla

nkto

n C

hl a

0

20

40

60

80

100

1817

4

16

10

33

23 30

2019

22

14

9

32

29

26

2

21

15

6

8

3124

13

25

1

3 28

7

27

12

11

5


Locations


Temperature (°C)

-5 0 5 10 15 20 25 30 35

% M

icro

phyt

opla

nkto

n C

hl a

0

20

40

60

80

100

1817

4

16

10

33

23 30

2019

22

14

9

32

29

26

2

21

15

6

8

3124

13

25

1

3 28

7

27

12

11

5

1. Marguerite Bay, Antarctic Peninsula, winter2. Marguerite Bay, Antarctic Peninsula, summer3. Southern Ocean, Atl. sector, spring ice edge zone4. Southern Ocean, Atl. sector, marginal ice zone 5. Southern Ocean, Atl. sector, polar front 6. SOIREE Fe addition exp. (Southern Ocean), inside7. SOIREE Fe addition exp., outside8. SOFeX iron addition exp. (Southern Ocean), inside 9. SOFeX iron addition exp., outside10. Kerguelen Plateau, Fe-fertilised waters11. Kerguelen Plateau, HNLC water12. SEEDS Fe addition exp. (subarctic W Pacific), inside 13. SEEDS Fe addition exp., outside 14. SERIES iron addition exp. (Gulf of Alaska), inside15. SERIES iron addition exp., outside 16. Okhotsk Sea (western Pacific Ocean), Oct 199317. Okhotsk Sea, Nov 199318. NE subarctic Pacific, late summer 19. NE subarctic Pacific, late winter 20. NE subarctic Pacific, late spring21. NW subarctic Pacific, summer22. NW subarctic Pacific, autumn 23. NW subarctic Pacific, winter 24. Ría de Vigo (NW Iberian peninsula), winter 25. Ría de Vigo, upwelling season26. Gulf of Tehuantepec (SW Mexico), Jan-Feb 1999 27. Gulf of Tehuantepec, Jan-Feb 198928. Johor Strait (Singapore), May-Jul 1998 29. Iskenderun Bay (NE Mediterranean Sea, Jul 2003 30. North & South Atl. subtropical gyres31. Arabian Sea during the 1995 monsoon (Aug-Sep) 32. IronEx II Fe addition exp., inside 33. IronEx II Fe addition exp., outside

Locations


Temperature (°C)

-5 0 5 10 15 20 25 30 35

% M

icro

phyt

opla

nkto

n C

hl a

0

20

40

60

80

100

1817

4

16

10

33

23 30

2019

22

14

9

32

29

26

2

21

15

6

8

3124

13

25

1

3 28

7

27

12

11

5


Locations


% P

icop

hyto

plan

kton

Chl

a

0

20

40

60

80

100

% N

anop

hyto

plan

kton

Chl

a

0

20

40

60

80

100

Total primary production (µg C L-1 d-1)

0 500 1000 1500

% M

icro

phyt

opla

nkto

n C

hl a

0

20

40

60

80

100

0 100 200

020406080

100

% Chl a in each size class strongly dependent on primary productivity, e.g. resource utilization rate

Pico Nano

Micro

coldtemperatewarm

y = 79.5 (1 - e-2.4x/79.5)r2 = 0.59, p < 0.001, n = 165

0 500 1000 1500 0 500 1000 1500

A simple simulation indicates the temperature-size rule can cause only minor changes in size structure

log10 cell size (µm3)

-1 0 1 2 3 4 5

log 10

cel

l abu

ndan

ce (c

ell m

L-1)

0

1

2

3

4

5

pico micronano

2 µm

20 µ

m

control

+20°C, -50% cell size+10°C, -25% cell size

2.6 63.434.03.0 60.636.43.7 54.441.8

Biovolume(%)

TemperatureR

esou

rce

utili

zatio

n ra

te

HIG

HLO

W

COLD WARMTEMPERATE

A summary of phytoplankton size structure in the ocean

Small cells dominate

Large cells dominate

• Summer bloom in Antarctic Peninsula

• NW Iberian coast, upwelling season

• Subtropical gyres (macronutrient limitation)

• Fertilised patch, Fe addition expts in Southern Ocean

• Eq. Pac., HNLC waters (Fe limitation)

• Fertilised patch, SERIES experiment (Gulf of Alaska)

• NW Iberian coast, winter (light limitation)

• Coastal, nutrient-rich waters in warm seas

• Fertilised patch, IronEx II (Eq. Pacific)

• Eastern subarctic N Pacific (Fe limitation)

• Antarctic peninsula in winter (light limitation)

• Southern Ocean HNLC waters in summer (Fe limitation)

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.

A research project funded by Ministerio de Ciencia e Innovación

(CTM2008-03999)

P E R S E OP E R S E OMacroecological patterns in marine phytoplankton

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Does temperature affect phytoplankton size structure in