Trace element stoichiometry of marine plankton & its effect ... - IMBER

Twining et al. 2003
Trace element stoichiometry of marine plankton & its
effect on carbon trophic dynamics
Maria T. Maldonado
Earth & Ocean Sciences, University of British Columbia, Vancouver, Canada

Talk Outline
1. Technical challenges hll in determining dt ii plankton trace metal tl
stoichiometry
2. Overview of “bulk plankton” metal stoichiometry
3. Phytoplankton‐specific metal stoichiometry
‐ evolutionary, taxonomic, environmental influences
4. Transfer efficiencies of metals to upper trophic levels.
5. Metal stoichiometry & links to the marine C cycle
‐ bacteria/phytoplankton/zooplankton
‐ C fixation, calcification & C remineralization
6. Ecological implications phytoplankton metal stoichiometry
7. Conclusions
Armbrust (2009)

Technical challenges determining plankton trace metal stoichiometry
‣Separating living from detrital/lithogenic material; contribution of
various organisms to a given size classes
‐ Laboratory (cellular stoichiometry) vs. field estimates (bulk)
‣ Intracellular vs. extracellular trace metals; i.e. uptake vs. adsorption
‣Normalizing cellular trace metal concentrations: P vs. C
‣Measurements are time consuming and potentially expensive
ICPMS: multi-element in situ & lab; (extra- intra-cellular wash; lithogenic
ICPMS: multi-element in situ & lab; (extra-, intra-cellular wash; lithogenic
contamination)
SXRF: metal stoichiometry and mapping of individual cells in situ & lab
Radiotracers: physiological studies (uptake, recycling, storage...)

Synchroton X‐ray fluorescence microprobe
Light, epifluorescence micrographs
& SXRF false-color element maps
using estimates
of cell volume to
calculate cell C
Fluorescence spectra
of a diatom
Iron content of Thalassiosira weissflogii
Twining et al. 2003, 2004, 2008

What to use to normalize the trace metal data, using P or C
- Trace metals & C cycle: normalize to cellular C
- Geochemists prefer normalizing to P
- P content is very plastic (Sterner & Elser 2002)
- P is not the best proxy for biomass
Trend: different Cu:P quotas for green vs. red algae disappears if normalized to C
Species
C:P
(mol:mol)
Cu:P
(mmol:mol)
Cu:C
(μmol:mol)
Mean Cu:P
(mmol:mol)
Mean Cu:C
(μmol:mol)
Chlorophyceae 198 ±35 0.45 ± 0.31 2.17 ±1.19
Prasinophyceae 200 ± 9 0.55 ± 0.06 2.77 ±0.2 0.5 2.47
Dinophyceae 117 ±31 0.29 ± 0.24 2.26 ±1.62
Prymnesiophyceae 70 ± 8 0.09 ± 0.03 1.32 ±0.56
Bacillariophyceae 62 ±22 0.17 ±0.09 2.8 ±1.4 0.18 2.13
Data from Ho et al. 2003

Talk Outline
1. Technical challenges hll in determining dt ii plankton trace metal tl
stoichiometry
2. Overview of “bulk plankton” metal stoichiometry
3. Phytoplankton‐specific metal stoichiometry
‐ evolutionary, taxonomic, environmental influences
4. Transfer efficiencies of metals to upper trophic levels.
5. Metal stoichiometry & links to the marine C cycle
‐ bacteria/phytoplankton/zooplankton
‐ C fixation, calcification & C remineralization
6. Ecological implications phytoplankton metal stoichiometry
7. Conclusions
Armbrust (2009)

Overview of “bulk plankton” metal stoichiometry (lab vs. field)
Study
(mol:mol)
Compiled by
Bruland et al. 1991
P Fe Zn Cu Mn Ni Cd Co
1000 5 2 0.4 0.4 0.4 0.4
Kuss & Kremling 1000 5 2 0.4 2 1 0.5 0.2
1999
Twinning et al. 2004 1000 1.8 5.4 0.26 0.61 0.21
Ho et al. 2003 1000 7.5 0.8 0.38 3.28 0.22 0.19
Copepods, Ho et al.
2007
1000 13 3.6 1.1 0.33 0.071
Mean 6.5 2.8 0.57 1.25 0.56 0.37 0.15
Range (X‐fold) 7.2 6.8 2.9 12.6 4.5 2.4 2.8
MEAN stoichiometric values vary 2-13 fold

Size‐fractionation of metal stoichiometry in the field
• Metal content (Al, Ti, Mn, Fe, Co, Ni, Cu, Zn) decreases as size of organisms
increases (Ho et al. 2007)
a) Higher SA to volume ratio in the smaller fractions, potential for more
extracellular trace metals
Ho et al 2007
Me g wt -1 )
(μg M
10 -60 m
60 -150 m > 150 m

But there is significant variability within the mean values….
Two ends of each box represents
the 25 & 75 percentiles for all data
Under identical growth
conditions, difference
among species (~20 fold,
exception Cd) ) reflects:
1. Unique cell biochemistry
2. Ability to take up Me
+
3. Ability to store Me +
Ho et al. 2003

Talk Outline
1. Technical challenges hll in determining dt ii plankton trace metal tl
stoichiometry
2. Overview of “bulk plankton” metal stoichiometry
3. Phytoplankton‐specific metal stoichiometry
‐ evolutionary, taxonomic, environmental influences
4. Transfer efficiencies of metals to upper trophic levels.
5. Metal stoichiometry & links to the marine C cycle
‐ bacteria/phytoplankton/zooplankton
‐ C fixation, calcification & C remineralization
6. Ecological implications phytoplankton metal stoichiometry
7. Conclusions
Armbrust (2009)

Phytoplankton‐specific metal stoichiometry
Taxonomic trends (Quigg et al. 2003 & Ho et al. 2003) (~ 20 fold difference):
• Green superfamily (chl b): high Fe (higher PSI:PSII ratio) , Cu & Zn
• Red superfamily (chl c): high Cd, Co & Mn
• Prokaryotic autotrophs: high Fe, Mo, Co
Geographic trends:
• Coastal phytoplankton higher Fe quotas (~2 ‐ 4 fold) than oceanic
(Sunda and Huntsman 1995, Maldonado and Price 1996)
Environmental trends:
• Metal concentrations:
– Change in [Me’] by 100 X changes quota by 2‐2020 fold
– Trace metal substitutions (ie. Zn, Co & Cd), 2‐5 fold
• Light:
– Increase metal tlquotas under low light high h (10 fold or greater) )(Finkel et al. 2006)
• Macronutrient interactions (N &P): 2‐10 fold;

Taxonomic patterns of phytoplankton metal stoichiometry
Clear differences
among taxonomic
groups
For modellers, using
functional groups
seems appropriate
Growth conditions also
important.
t
Ho et al. 2003

Interactions between trace metals and acquisition of N, C and P
Price and Morel 2003
-Fe limitation, high Si:N diatom (Hutchins & Bruland 98; Takeda 98; Marchetti & Harrison 2007)
-Fe limitation, high cellular P (~1.5 fold, Price 2005)

Talk Outline
1. Technical challenges hll in determining dt ii plankton trace metal tl
stoichiometry
2. Overview of “bulk plankton” metal stoichiometry
3. Phytoplankton‐specific metal stoichiometry
‐ evolutionary, taxonomic, environmental influences
4. Transfer efficiencies of metals to upper trophic levels.
5. Metal stoichiometry & links to the marine C cycle
‐ bacteria/phytoplankton/zooplankton
‐ C fixation, calcification & C remineralization
6. Ecological implications phytoplankton metal stoichiometry
7. Conclusions
Armbrust (2009)

Metal assimilation efficiency by copepods feeding on phytoplankton (ie.
diatoms)
1. Phytoplankton cellular trace metal partitioning: extracellular, cytoplasmic & membrane bound
2. Cytoplasmic trace metal pool increases by ~ 10% during stationary phase
Cu
Fe
Co
(Reinfelder & Fisher 1991, Hutchins & Bruland 1994, Chang & Reinfelder 2000)

Metal assimilation efficiency by juvenile fish feeding on copepods
Copepods trace metal partitioning: soft‐tissue & exoskeleton
Elements in the soft tissue control assimilation efficiency by juvenile fish
(Reinfelder & Fisher 1994)

Talk Outline
1. Technical challenges hll in determining dt ii plankton trace metal tl
stoichiometry
2. Overview of “bulk plankton” metal stoichiometry
3. Phytoplankton‐specific metal stoichiometry
‐ evolutionary, taxonomic, environmental influences
4. Transfer efficiencies of metals to upper trophic levels.
5. Metal stoichiometry & links to the marine C cycle
‐ bacteria/phytoplankton/zooplankton
‐ C fixation, calcification & C remineralization
6. Ecological implications phytoplankton metal stoichiometry
7. Conclusions
Armbrust (2009)

Metal effects on C fixation and calcification rates (POC / PIC)
‐ Low Fe decreases growth rate & calcification rates BUT low Zn only
decreases growth rates
Fe
Zn
(Schulz et al. 2004)

Trace metal effects on the marine C cycle:
Remineralization and C trophic transfer
HETEROTROPHIC BACTERIA:
- higher Fe:C ratios than phytoplankton
- Fe limitation lowers their growth efficiency
Fe case study
Tortell et al. 1996

Trace metal effects on the marine C cycle:
Remineralization and C trophic transfer
PROTOZOANS
Fe case study
- require 2-3 fold more Fe
than phytoplankton
-their growth efficiency
decreases under low Fe
(34 vs. 16 %), despite
faster filtration rates and
ingestion rates of C
Phytoplankton
iron-deficient ~ 3
(Maldonado & Price 1996)
- Fe recycling was higher
when Fe limited (60 vs.
85%)
(Chase & Price 1997)

Changes in relative trophic position –prey selectivity
Fe case study
Ochromonas
MIXOTROPHS
- Ingesting bacteria:
an effective way to obtain Fe when Fe
is low (additional bacterial C benefits)
control
- Higher growth efficiency
when assimilating bacterial Fe
vs. assimilating dissolved Fe
- Ingestion rates & clearance rates
faster for Fe limited Ochromonas
o Fe supplied as dissolved or bacterial Fe
control T. pseudonana with bacterial Fe
(Maranger et al. 1998)

Talk Outline
1. Technical challenges hll in determining dt ii plankton trace metal tl
stoichiometry
2. Overview of “bulk plankton” metal stoichiometry
3. Phytoplankton‐specific metal stoichiometry
‐ evolutionary, taxonomic, environmental influences
4. Transfer efficiencies of metals to upper trophic levels.
5. Metal stoichiometry & links to the marine C cycle
‐ bacteria/phytoplankton/zooplankton
‐ C fixation, calcification & C remineralization
6. Ecological implications phytoplankton metal stoichiometry
7. Conclusions
Armbrust (2009)

Why do pennate diatoms dominate iron‐induced blooms
High
[Nitrate] µM
Low
Alaska
SERIES
July 29 th , 2002
Day 20
Patch size = 700 km
2
Eifex 2004 www.awi.de/.../Pics/planktonInside-g.gif
Pseudo‐nitzschia spp.
Courtesy of Jim Gower, Boyd Institute et of Ocean al. 2004 Sciences, Nature Canada

Ecological implications of phytoplankton metal stoichiometry
Iron requirements in oceanic pennate vs. centric diatoms
a
300
250
200
150
100
Oceanic Pennates, Pseudo-nitzchia spp.
Oceanic Centrics, Thalassiosira spp.
High Fe
Quota
High Fe-Q
(mol Fe mol C -1 )
b
50
0
14
12
10
8
6
4
• Pennates have higher h maximum
Fe quotas than Centrics
• Pennates & Centrics have
similarly low minimum Fe requirements
Fe-Qhigh : Fe-Qlow F
Low Fe Quota
Low Fe-Q
(mol Fe mol C -1 )
c
2
0
60
Oceanic Pennate diatoms (Pseudo-
nitzschia spp.) have a higher h Fe storage
Low Fe‐Q
40
20
0
capacity than oceanics (Thalassiosira spp.)
High Fe‐Q :
P. heimii type 1 (UBC403)
P. cf. heimii type 2 (UBC303)
P. dolorosa (UBC203)
P. cf. turgidula (UBC103)
T. oceanica (1003)
T. parthenela (Thal 9)
T. subtilis (50 Ait)
P. multiseries (Orø13)
P. cf. calliantha (NWFSC186)
T. pseudonana (3H)
T. weissflogii (Actin)
Marchetti et al. L&O 2006

Iron storage molecule ferritin discovered in Pseudo‐nitzschia
monomer
multimer (24mer)
• Exhibits ferroxidase
activity
• Stores > 600 atoms in vitro
multimer
(24mer) Marchetti et al. 2009

light
Exudation
Primary Production
POM
(particulate organic matter)
Dissolved Organic Matter
DOM
Viral
lysis
Consumption
Excretion
Grazers
Consumption
C-Link
Bacteria
Euphotic zone
mixing
Excretion
nutrient release
Remineralization
nutrient / CO 2 release
C-Sink
Phytoplankton
Sinking
POM Export
nutrients
POM export
Fecal pellets (egestion),
sloppy feeding
Deep Ocean
sediments

Conclusions
• Metal stoichiometry measurements are difficult, methods are evolving
• Choice of biomass proxy for normalization is important
t
• Using functional phytoplankton p groups in models is good approach
• Environmental influences must be considered
• The transfer of metals across trophic levels appears well constrained
• Trace metal stoichiometry may affect production, consumption &
remineralization pathways
• Understanding of metal stoichiometry can provide insights into ecological
dynamics