Patterns in phytoplankton size structure: abundance,
biomass and production in coastal and open-ocean waters
Emilio Marañón  Universidad de Vigo  Vigo (Spain)
Thanks to:
Pedro Cermeño, María Huete-Ortega, Daffne C. López-Sandoval, Tamara
Rodríguez-Ramos, Cristina Sobrino, José M. Blanco, Jaime Rodríguez
Primary production in the ocean. The 45th Liège Colloquium, Liège (Belgium), 13-17 May 2013.
Session on Field estimates of primary production. Keynote talk
The importance of phytoplankton cell size
Figure from Finkel et al. 2010 JPR
Many key phytoplankton processes are affected by cell size:
• Growth and metabolic rate
• Resource acquisition and use
• Susceptibility to predation and sinking
The importance of phytoplankton cell size
Phytoplankton dominated by:
Property
Small cells
Large cells
Dominant trophic pathway
Photosynthesis-to-respiration ratio
f-ratio and e-ratio
Main fate of primary production
Microbial food web
~1
5–15%
Recycling
in the upper layer
Herbivorous food chain
>1
>40%
Export toward deep
waters
% picophytoplankton chl a
% microphytoplankton chl a
Hirata et al 2011 Biogeosci.
Outline
• Phytoplankton size structure: importance of resources vs. temperature
• Variability in total and size-fractionated production to biomass ratio
• Size-scaling of phytoplankton abundance and metabolic rate
• Mechanisms underlying the size-dependence of phytoplankton growth
Outline
• Phytoplankton size structure: importance of resources vs. temperature
• Variability in total and size-fractionated production to biomass ratio
• Size-scaling of phytoplankton abundance and metabolic rate
• Mechanisms underlying the size-dependence of phytoplankton growth
Data compilation: 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
General relationship between total and size-fractionated chl a
-1
Size-fractionated Chl a (µg L )
100
picophytoplankton 0.2-2µm
nanophytoplankton 2-20µm
microphytoplankton >20µm
10
1
0.1
0.01
0.001
All data (n = 500)
0.0001
0.01
0.1
1
10
100
Total Chl a concentration (µg L-1)
Marañón et al. 2012 L&O
Does temperature have a direct effect on size structure?
Data conform to a single overall relationship –
irrespective of temperature
% Microphytoplankton Chl a
100
80
100
60
cold
temperate
warm
80
60
40
40
20
20
0
0
1
2
0
0
5
10
15
20
Total Chl a concentration (µg L-1)
25
Locations
Temperature vs.
% microphytoplankton Chl a
% Microphytoplankton Chl a
100
12
2
10
80
14
3
27
8
4
60
25
29
28
32
6
13
40
26
15
11
20
7 17
1
19 20
9
21
16
22
23 5
0
-5
0
5
10
31
24
18
33
30
15
20
Temperature (°C)
Marañón et al. 2012 L&O
25
30
35
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
Marguerite Bay, Antarctic Peninsula, winter
Marguerite Bay, Antarctic Peninsula, summer
Southern Ocean, Atl. sector, spring ice edge zone
Southern Ocean, Atl. sector, marginal ice zone
Southern Ocean, Atl. sector, polar front
SOIREE Fe addition exp. (Southern Ocean), inside
SOIREE Fe addition exp., outside
SOFeX iron addition exp. (Southern Ocean), inside
SOFeX iron addition exp., outside
Kerguelen Plateau, Fe-fertilised waters
Kerguelen Plateau, HNLC water
SEEDS Fe addition exp. (subarctic W Pacific), inside
SEEDS Fe addition exp., outside
SERIES iron addition exp. (Gulf of Alaska), inside
SERIES iron addition exp., outside
Okhotsk Sea (western Pacific Ocean), Oct 1993
Okhotsk Sea, Nov 1993
NE subarctic Pacific, late summer
NE subarctic Pacific, late winter
NE subarctic Pacific, late spring
NW subarctic Pacific, summer
NW subarctic Pacific, autumn
NW subarctic Pacific, winter
Ría de Vigo (NW Iberian peninsula), winter
Ría de Vigo, upwelling season
Gulf of Tehuantepec (SW Mexico), Jan-Feb 1999
Gulf of Tehuantepec, Jan-Feb 1989
Johor Strait (Singapore), May-Jul 1998
Iskenderun Bay (NE Mediterranean Sea, Jul 2003
North & South Atl. subtropical gyres
Arabian Sea during the 1995 monsoon (Aug-Sep)
IronEx II Fe addition exp., inside
IronEx II Fe addition exp., outside
Locations
Temperature vs.
% microphytoplankton Chl a
% Microphytoplankton Chl a
100
12
2
10
80
14
3
27
8
4
60
25
29
28
32
6
13
40
26
15
11
20
7 17
1
19 20
9
21
16
22
23 5
0
-5
0
5
10
31
24
18
33
30
15
20
Temperature (°C)
Marañón et al. 2012 L&O
25
30
35
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
Marguerite Bay, Antarctic Peninsula, winter
Marguerite Bay, Antarctic Peninsula, summer
Southern Ocean, Atl. sector, spring ice edge zone
Southern Ocean, Atl. sector, marginal ice zone
Southern Ocean, Atl. sector, polar front
SOIREE Fe addition exp. (Southern Ocean), inside
SOIREE Fe addition exp., outside
SOFeX iron addition exp. (Southern Ocean), inside
SOFeX iron addition exp., outside
Kerguelen Plateau, Fe-fertilised waters
Kerguelen Plateau, HNLC water
SEEDS Fe addition exp. (subarctic W Pacific), inside
SEEDS Fe addition exp., outside
SERIES iron addition exp. (Gulf of Alaska), inside
SERIES iron addition exp., outside
Okhotsk Sea (western Pacific Ocean), Oct 1993
Okhotsk Sea, Nov 1993
NE subarctic Pacific, late summer
NE subarctic Pacific, late winter
NE subarctic Pacific, late spring
NW subarctic Pacific, summer
NW subarctic Pacific, autumn
NW subarctic Pacific, winter
Ría de Vigo (NW Iberian peninsula), winter
Ría de Vigo, upwelling season
Gulf of Tehuantepec (SW Mexico), Jan-Feb 1999
Gulf of Tehuantepec, Jan-Feb 1989
Johor Strait (Singapore), May-Jul 1998
Iskenderun Bay (NE Mediterranean Sea, Jul 2003
North & South Atl. subtropical gyres
Arabian Sea during the 1995 monsoon (Aug-Sep)
IronEx II Fe addition exp., inside
IronEx II Fe addition exp., outside
Locations
Temperature vs.
% microphytoplankton Chl a
% Microphytoplankton Chl a
100
12
2
10
80
14
3
27
8
4
60
25
29
28
32
6
13
40
26
15
11
20
7 17
1
19 20
9
21
16
22
23 5
0
-5
0
5
10
31
24
18
33
30
15
20
Temperature (°C)
Marañón et al. 2012 L&O
25
30
35
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
Marguerite Bay, Antarctic Peninsula, winter
Marguerite Bay, Antarctic Peninsula, summer
Southern Ocean, Atl. sector, spring ice edge zone
Southern Ocean, Atl. sector, marginal ice zone
Southern Ocean, Atl. sector, polar front
SOIREE Fe addition exp. (Southern Ocean), inside
SOIREE Fe addition exp., outside
SOFeX iron addition exp. (Southern Ocean), inside
SOFeX iron addition exp., outside
Kerguelen Plateau, Fe-fertilised waters
Kerguelen Plateau, HNLC water
SEEDS Fe addition exp. (subarctic W Pacific), inside
SEEDS Fe addition exp., outside
SERIES iron addition exp. (Gulf of Alaska), inside
SERIES iron addition exp., outside
Okhotsk Sea (western Pacific Ocean), Oct 1993
Okhotsk Sea, Nov 1993
NE subarctic Pacific, late summer
NE subarctic Pacific, late winter
NE subarctic Pacific, late spring
NW subarctic Pacific, summer
NW subarctic Pacific, autumn
NW subarctic Pacific, winter
Ría de Vigo (NW Iberian peninsula), winter
Ría de Vigo, upwelling season
Gulf of Tehuantepec (SW Mexico), Jan-Feb 1999
Gulf of Tehuantepec, Jan-Feb 1989
Johor Strait (Singapore), May-Jul 1998
Iskenderun Bay (NE Mediterranean Sea, Jul 2003
North & South Atl. subtropical gyres
Arabian Sea during the 1995 monsoon (Aug-Sep)
IronEx II Fe addition exp., inside
IronEx II Fe addition exp., outside
Locations
Temperature vs.
% microphytoplankton Chl a
% Microphytoplankton Chl a
100
12
2
10
80
14
3
27
8
4
60
25
29
28
32
6
13
40
26
15
11
20
7 17
1
19 20
9
21
16
22
23 5
0
-5
0
5
10
31
24
18
33
30
15
20
Temperature (°C)
Marañón et al. 2012 L&O
25
30
35
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
Marguerite Bay, Antarctic Peninsula, winter
Marguerite Bay, Antarctic Peninsula, summer
Southern Ocean, Atl. sector, spring ice edge zone
Southern Ocean, Atl. sector, marginal ice zone
Southern Ocean, Atl. sector, polar front
SOIREE Fe addition exp. (Southern Ocean), inside
SOIREE Fe addition exp., outside
SOFeX iron addition exp. (Southern Ocean), inside
SOFeX iron addition exp., outside
Kerguelen Plateau, Fe-fertilised waters
Kerguelen Plateau, HNLC water
SEEDS Fe addition exp. (subarctic W Pacific), inside
SEEDS Fe addition exp., outside
SERIES iron addition exp. (Gulf of Alaska), inside
SERIES iron addition exp., outside
Okhotsk Sea (western Pacific Ocean), Oct 1993
Okhotsk Sea, Nov 1993
NE subarctic Pacific, late summer
NE subarctic Pacific, late winter
NE subarctic Pacific, late spring
NW subarctic Pacific, summer
NW subarctic Pacific, autumn
NW subarctic Pacific, winter
Ría de Vigo (NW Iberian peninsula), winter
Ría de Vigo, upwelling season
Gulf of Tehuantepec (SW Mexico), Jan-Feb 1999
Gulf of Tehuantepec, Jan-Feb 1989
Johor Strait (Singapore), May-Jul 1998
Iskenderun Bay (NE Mediterranean Sea, Jul 2003
North & South Atl. subtropical gyres
Arabian Sea during the 1995 monsoon (Aug-Sep)
IronEx II Fe addition exp., inside
IronEx II Fe addition exp., outside
% Chl a in each size class depends on primary productivity,
e.g. resource utilization rate
80
60
100
Pico
% Nanophytoplankton Chl a
cold
temperate
warm
40
20
0
Nano
80
60
40
20
0
0
500
% Microphytoplankton Chl a
% Picophytoplankton Chl a
100
1000
0
1500
100
500
Micro
80
60
100
80
40
60
40
20
20
0
0
0
0
500
100
1000
200
1500
Total primary production (µg C L-1 d-1)
1000
1500
A summary of phytoplankton size structure in the ocean
Temperature
HIGH
LOW
Resource utilization rate
COLD
TEMPERATE
WARM
• Summer bloom in
Antarctic Peninsula
• NW Iberian coast,
upwelling season
• Coastal, nutrient-rich
waters in warm seas
• Fertilised patch,
Fe addition expts in
Southern Ocean
• Fertilised patch,
SERIES experiment
(Gulf of Alaska)
• Fertilised patch,
IronEx II (Eq. Pacific)
• Antarctic peninsula in
winter (light limitation)
• NW Iberian coast,
winter (light limitation)
• Subtropical gyres
(macronutrient
limitation)
• Southern Ocean
HNLC waters in
summer (Fe limitation)
• Eastern subarctic N
Pacific (Fe limitation)
• Eq. Pac., HNLC
waters (Fe limitation)
Small cells dominate
Large cells dominate
Outline
• Phytoplankton size structure: importance of resources vs. temperature
• Variability in total and size-fractionated production to biomass ratio
• Size-scaling of phytoplankton abundance and metabolic rate
• Mechanisms underlying the size-dependence of phytoplankton growth
Phytoplankton production (P) and biomass (B) in openocean and coastal waters: what is the variability of P/B?
Mean coastal µ = 1.30 d-1
Mean open-ocean µ = 0.34 d-1
y = 1.58 x - 1.21
r2 = 0.65, n = 70
3.0
2.5
-3
-1
PP (mgC
m d
Log Log
surface
PP (mgC
m-3) d-1)
3.5
Ría de Vigo
(2001-2002)
AMT
(1995-1996)
2.0
1.5
slope = 1.58
1.0
0.5
Open ocean
Coastal
0.0
-0.5
0.5
1.0
1.5
2.0
2.5
3.0
Log Log
surface
phyto
biomass
(mgC
Phyto
biomass
(mgC
m-3)m-3)
Marañón et al. in prep.
 Low nutrient supply in open-ocean waters limits the growth and
physiological state of phytoplankton, not only their standing stock
Chl a map from MODIS Aqua (NASA)
Huete-Ortega et al. 2012 J Mar Sys
Chl a mg m-3
Trynitrop 2007
Nitrate µM
Temp °C
The equatorial upwelling causes an increase in
phytoplankton biomass turnover rate
Trynitrop 2007
6
25
5
20
4
15
3
2
10
5
-10
1
0
-5
0
5
10
15
20
25
Latitude
Latitud
Biomasa total
Biomass
Primary
production
Producción
total
Production/Biomass
Tasa de crecimiento total
Chl a map from MODIS Aqua (NASA)
Huete-Ortega et al. 2012 J Mar Sys
30
0.24
0.22
0.20
0.18
0.16
0.14
0.12
0.10
0.08
0.06
0.04
-1
7
Turnover
rate (d )
Tasa
total recambio
30
-1
-1
Biomasa
total (g C L )
Phytocarbono
biomass
-1
Tasa
fijaciónproduction
carbono total (g C L d )
Primary
The equatorial upwelling causes an increase in
phytoplankton biomass turnover rate
Large phytoplankton sustain high Cspecific production in nutrient-rich waters
J
A
S
O
N Temperature
D
J
F
(°C)
Depth (m)
12
13
14
15
16
17
M
A
M
J
J
A
M
J
J
A
A
M
M
JJ
JJ
18
-10
-20
-30
-40
J
A
S
O
N
D
J
F
M
Nitrate (µmol kg-1)
0 1 2 3 4 5 6 7 8 9 10 11 12 13
Depth (m)
0
-10
-20
-30
JJ
AA
SS
O
O
N
DD
JJ
FF
M
M
Cermeño et al. 2005 MEPS
Outline
• Phytoplankton size structure: importance of resources vs. temperature
• Variability in total and size-fractionated production to biomass ratio
• Size-scaling of phytoplankton abundance and metabolic rate
• Mechanisms underlying the size-dependence of phytoplankton growth
Regularity in normalized biomass size-spectra (NBSS) and
size-abundance spectra (SAS) in open-ocean waters
Bacteria, phyto- and zooplankton
NBSS slope  -1
35°N 56°W
Bact
Phytoplankton
SAS slopes between -1.3 and -1.1
Phyto
Zoo
32°N 55°W
Huete-Ortega et al. 2012 Proc Roy Soc B
Quiñones et al. 2003 Prog Oceanogr
The metabolic theory of ecology predicts that biomassspecific metabolic rates decrease with body size
slope 3/4
Brown et al. 2004 Ecology
Log mass-specific metabolic rate (or µ)
Ln(Biomass production rate per individual)
The ¾-power rule: individual metabolic rate  M3/4 (Kleiber, 1932)
 Mass-specific metabolic rate (or growth rate)  M-1/4
slope = -1/4
Log body size
A quantitative illustration of the ¾-power rule
If the average Lilliputian was as tall as Gulliver’s
middle finger (ca. 7 cm) and assuming Gulliver was
1,80 m tall:
1 Gulliver = (180/7)3 = 17600 Lilliputians
So, how much food should the Lilliputians give him?
The Emperor of Lilliput decreed:
“…the said Man Mountain shall have a daily
allowance of meat and drink sufficient for the
support of 1724 of our subjects."
1724=17600b
 b=log(1724)/log(17600)=0.76!!
Kleiber (1967)
Gulliver’s Travels (Swift, 1726)
Early estimates suggested a slope value higher than ¾…
-1
Log10 pg C cell d
-1
6
4
2
Size-fractionated production and
biomass data from different locations
0
b = 1.03
-2
-4
-1
0
1
2
3
4
5
Log10 µm3 cell-1
Marañón et al. 2006 L&O
Data obtained from the literature
Marañón 2008 J Plankton Res
…and more accurate measurements confirm that the slope is
approximately 1 (isometric size-scaling)
Trynitrop 2007
Chl a map from MODIS Aqua (NASA)
Huete-Ortega et al. 2012 Proc Roy Soc B
 phytoplankton metabolism does not follow the ¾-power rule
Linking the size-scaling of abundance and metabolic rate
Assuming populations grow until resources are limiting, in steady-state we will have
(Enquist et al 1998) that Nmax = R/Q, where N is abundance, R is resource supply
rate and Q is the individual rate of resource use (e.g. metabolic rate).
Let S be body size. If R  S0 and Q  Sb then Nmax  S-b  reciprocal size-scaling of
abundance and metabolic rate.
slope : 1.16±0.09
slope : -1.15±0.09
Huete-Ortega et al. 2012 Proc Roy Soc B
Summary so far:
• Phytoplankton size-structure depends on the rate of resource use
• Phytoplankton biomass turnover rates respond to nutrient supply
• Microphytoplankton can sustain high growth rates
• In near steady-state ecosystems, the size-scaling of abundance
reflects the size-scaling of metabolic rate
• Phytoplankton metabolism does not follow the ¾-power rule
Outline
• Phytoplankton size structure: importance of resources vs. temperature
• Variability in total and size-fractionated production to biomass ratio
• Size-scaling of phytoplankton abundance and metabolic rate
• Mechanisms underlying the size-dependence of phytoplankton growth
Phytoplankton cultures grown under identical conditions
show near-isometric size-scaling of metabolic rates
104
102
-1
Diatoms
Dinoflagellates
Coccolithophores
Cyanobacteria
Chlorophytes
Others
-1
103
101
100
10-1
10-2
10-3
Respiration (pmolO2 cell d )
-1
104
-1
Photosynthesis (pgC cell h )
105
slope = 0.90
10-4
10-2 10-1 100 101 102 103 104 105 106 107
Cell size (µm3)
103
102
101
100
10-1
10-2
10-3
slope = 0.91
10-4
10-2 10-1 100 101 102 103 104 105 106 107
Cell size (µm3)
López-Sandoval et al. in prep.
A closer look reveals that in fact the size-scaling of
phytoplankton growth and production is unimodal
Mass-specific production rate (h-1)
Maximum growth rate (d-1)
1.2
0.25
1.0
0.20
Diatoms
Dinoflagellates
Coccolithophores
Cyanobacteria
Chlorophytes
Others
P (h )
-1
-1
µmax (d )
0.8
C
0.6
0.15
0.10
0.4
0.2
0.05
0.0
0.00
10-2 10-1 100 101 102 103 104 105 106 107
10-2 10-1 100 101 102 103 104 105 106 107
Cell size (µm3)
Cell size (µm )
3
Marañón et al. 2013 Ecol Lett
Unexpected size-scaling of nutrient maximum uptake rate
(VmaxN)
104
104
Diatoms
Dinoflagellates
Coccolithophores
Cyanobacteria
Chlorophytes
Others
100
10-1
10-2
10-3
10-4
-1
102
-1
103
101
VmaxN (pgN cell h )
-1
101
VmaxN (pgN cell h )
102
-1
103
slope = 0.97
10-5
10-2 10-1 100 101 102 103 104 105 106 107
3
Cell size (µm )
Theoretically, it was expected that
Vmax  (cell size)2/3, which would mean
that volume-specific Vmax  (cell size)-1/3.
In contrast, our data suggest that volumespecific Vmax is size-independent
100
10-1
10-2
10-3
10-4
slope = 1.15
10-5
10-3 10-2 10-1 100 101 102 103 104 105
QminN (pgN cell-1)
As cell size increases, the ability to take up
nutrients increases faster than requirements
Marañón et al. 2013 Ecol Lett
An illustration of the importance of using different sizescaling exponents for nutrient uptake
Uptake rate
(fgN cell-1 h-1)
Cell volume
(µm3)
VmaxV1
1
0.1
Difference
VmaxV0.66
1
10-fold
10
1
5
5-fold
100
10
22
2-fold
1000
100
100
-
10000
1000
457
2-fold
100000
10000
2089
5-fold
1000000
100000
9549
10-fold
e
Ov
res
n
tio
a
tim
ere
d
Un
n
tio
a
m
s ti
Potential mechanisms underlying the size-scaling of
phytoplankton metabolism and growth
Size range
Trend in µ
with cell size
<10-50 µm3
--
Relevant properties
and processes
N-rich cells
Non-scalable components
Low VmaxN:QminN
Up to 50-200 µm3
Increasing
Increasing space for catalysts
Increasing VmaxN:QminN
From 50-200 µm3
upwards
Decreasing
Increasing intracellular distances
Reduced light absorption
>103-104 µm3
--
High VmaxN:QminN
High QmaxN:QminN
Limited by assimilation
Thank you.
Emilio Marañón – Universidad de Vigo – [email protected]