“Dynamics of stoichiometrical and metabolomical traits under climate change”

Global Ecology UnitCREAF – CSIC – CEAB

Barcelona

Jordi Sardans, Albert Rivas-Ubach, Albert Gargallo-Garriga, Ifigenia Urbina,Jofre Carnicer, Marc Estiarte, Iolanda Filella, Joan Llusià, Romà Ogaya, Josep Peñuelas

Stoichiometry-metabolomic studiesUseful traits to detct and study plant responses to environmental change

Climate change

Sensitivity enough to detect the dynamics of plant responses

PlantMetabolism and stoichiometry shifts

Mechanisms and functions involved in the organism response

Clues to global ecosystem impactsmainly by the effects on trophic webs

Potential improvement of global climate and balance models

Long-time field studies

My first studies of Biogeochemistry in the Global Ecology Unit

Climanani Garraf Site

Prades site

Drought impacts N and P concentrations and contents in Mediterraenan ecosystems

0

10

20

30

40

Protease -Glucosidase

En

zym

e a

cti

vit

y (

g s

ub

stra

te h

yd

roli

zed

g-1

so

il h

-1)

a

ab

b

b

a a

Control

Runoff exclussion

Runoff exclussion plus partial rainfall exclussion

After four years of drought (Mediterranean forest)

Data from Sardans & Peñuelas (2005)Soil Biology and Biochemistry

Four general results observed in all studies

1. Decreases in soil enzyme and root-enzyme activity

2. Decreases of N and P stocks in aboveground biomass3. Increases in total soil N and P stocks but decreses of plant-available stocks4. Changes in plant N:P stoichiometry

-4

0

4

8

Leaves Wood Aboveground

(a) (a)

(b)(b)

Arbutus unedo

50

0

50

a a

b b

Control

Drought

Quercus ilex

Biomass fraction

Total Aboveground

P in

crem

en

t

(k

g h

a-1)

(200

5-1

999

)

0

70

140

210

280

350

Leaves Stem Leaf-Litter

N/P

a

a

bb

bb

Control

Drought

Warming

Erica multiflora

Sardans & Peñuelas (2007)Functional Ecology

Sardans et al. (2008)Global Change Biology

0.05

0.1

So

il S

olu

ble

Pto

tal (

mg

g-1

)

a abb

0.05

0.1S

oil

So

lub

le P

o (

mg

g-1

)

ba a

0-15 cm soil depth

Treatments

0

0.1

0.2

0.3

0.4

C D DD

So

il S

olu

ble

Pi/P

o

a

ab b

Sardans and Peñuelas (2007)Functional Ecology

C/N/P ratio related to several ecosystems process

In freshwater ecosystems

N/P RNA(P-rich)

Growth rate

In terrestrial ecosystems No conclussive results of GR at this moment

Related to species diversity

Relatedto species style of life

Related to soil trophic web structure

Changes in N/P ratio is not a minor question

Growth Rate Hypothesis (GR)Elser et al. (1996)

0

0.05

0.1

So

il so

lub

le K

(mg

g-1

) aab b

0

0.002

0.004

C D DDS

oil

solu

ble

K/t

ota

l K

ab b

0-15 cm soil depth

Treatments

Sardans and Peñuelas (2007)Functional Ecology

But K-stocks were also afected by drought

Sardans et al. (2008)Plant and Soil

0

5

10

15

21

Leaves Stems

a

a

ab bb

b

0

2

4

6

8

10

Leaves Stems

a

b

a

Erica multiflora

Globularia alypum

Ab

so

lute

ab

ov

eg

rou

nd

K a

cc

um

ula

tio

n (

kg

ha

-1)

(19

99

-20

05

)

Plant biomass In soil

Quercus ilex

C

Ca

Fe

K

Mo

N

Na

P S Mg

-1.0 -0.5 0.0 0.5 1.0

PC1 (34%)

-1.0

-0.5

0.0

0.5

1.0

C C C

C

D

D

D

D

-4 -2 0 2 4

PC1 (34% )

-3

-2

-1

0

1

2

3

4

PC

2 (

19

%)

Control

Drought

PC

2 (1

9%)

Drought changes whole foliar elemental composition

C

C

D

D D

W W

W

-4 -2 0 2 4 6

PC1 (42% )

-4

-2

0

2

4

6

PC

2 (

29

%)

C

Drought

Warming

Control

Globularia alypum

C

Ca

Fe

K

M g

M o

N

Na

P S

-1.0 -0.5 0.0 0.5 1.0

PC1 (42%)

-1.0

-0.5

0.0

0.5

1.0

PC

2 (1

9%)

Peñuelas et al. (2008)Pol J Ecol

Soil stocks and biomass concentrations of other several elements (Mo, S or Ca) had been changed by drought

Sardans et a. (2008) Biogeochemistry, Sardans et al. (2008) J. Geophys. Res.

Climate change impact in terrestrial ecosystems stoichiometry: how can we advance?

1.Most studies have been focused on N and P (N/P ratio)

Capture our attention in current studies limitations

What dowe need?

1.More elements such as K, but also Mg, S or Ca among others should be considered

2. Stoichiometric studies of terrestrial plants have been mailny focused on foliar tissues, specially in trees

2. Plants also allocate nutrients to other tissues.We need when possible, take into account whole

plant stoichiometry

3. N/P stoichiometry of higher plants not only depends of the allocation to growth, several other functions can be important sinks for nutrients

3. To gain a global knowledgment of the functional causes underlie stoichiometric shifts in plant

responses to climate change

Sardans et al. (2012a) BiogeochemistrySardans et al. (2012b) Pers Plant Ecol Evol SystSardans and Peñuelas (2012) Plant Physiology

How can improve stoichiometry studiesto be a useful trait to detect dynamics

shifts in terrestrial plant vegetation

Experimental, observationals and review studies (reviews and meta-analysis)

We propose to solve these constrains and advance in the frame of climate change impacts on terrestrial plant communities

Plant functional response

Climate change

Soil resources

Impacts on biotic relationships (competition, herbivorism….)

Change in element use

Changes in gene expresion

Changes in metabolism and molecular structure

Wholel plant stoichiometrical change

1 2

1. Ecometabolomic studies

2. Include other elements such as K.Study the elemental composition and its shifts as a whole

Make the next reasonig

We developed a method to conduct metabolomic analyses with field sampling

Rivas-Ubach et al. (2013)Methods in Ecology and Evolution

We began to use metabolomics analyses in our studies 2

Plants under different climate conditions shift their metabolism. The corresponding metabolomic analysis informs on the molecular causes underlying the shifts in elemental composition

and stoichiometrical ratios

Rivas-Ubach et al. (2012) PNAS

Stoichiometry+

MetabolomicsElemental

Stoichiometry

MetabolomeN/PSugarsAmino acids

S

Spring Season

Preliminary Results

Metabolomic profiling of Quercus ilex.

Seasonal PCA

Drought:

Polyphenolics (antioxidants)Potassium

Oposite responses of roots and leaves

Ecometabolomics : a tool for several ecological estudiesGreat sensitivity to detect plant responses

• When the plant is wounded the metabolome changes

WoundedNo-wounded

Sardans et al. (2013)Plant Biology

Current ecometabolomic-stoichiometric studiesClimate change effects on the populations of the south border of the distribution Area of important European forest species

Fagus sylvatica

Quercus ilex

Pinus uncinata

Stoichiometry and Metabolism on plant-herbivore relationship

Pine processionary mothsThaumetopoea pityocampa

Until this moment the results show that metabolomics can be an useful tool:

1. To give a global view of plant functions involved in plant responses

2.To explain the causes of plant elemental compostion and stoichiometrical shifts under drought

3. To improve the kowledge of the metabolic pathways up– and down-regulated under drought .

4.Is sensitive enough to detect plant molecular and elemental shifts under different environmental conditions through time

5.To know plant responses to herbivore attack

The role of potassium

Data from Catalan National Forestal Inventory

Foliar K content (kg ha-1) Foliar K:C content ratio Foliar K:N content ratio

0.007- 4.31

4.31 – 7.65

7.65 – 12.66

12.66 – 22.43

> 22.43

8.2 – 72.7

72.7 – 92.2

92.2 – 114.2

114.2 – 152.7

> 152.7

0.5897 – 1.6434

1.6434 – 2.0491

2.0491 – 2.5288

2.5288 – 3.4242

> 3.4242

Foliar K concentration (mg g-1)

> 7.62

5.67 – 7.62

4.52 – 5.67

3.41 – 4.52

1.0 – 3.41

Precipitation (L m-2 yr-1)

< 400

400-500

500-600

600-700

700-800

800-900

900-1000

1000-1100

1100-1200

> 1200

50 Km

0

10

20

30

Evergreens Conifers Deciduous

K c

on

ten

t in

fo

liar

bio

mas

s (k

g h

a-1

)

a

aa

b

b

ab

ab

ab

WinterSpring

Summer

Autumn

Sardans et al. (2012)Functional Ecology

K content is related with MAP

Species adapted to dry climate have higher capacity to allocate more K to foliar biomass during summer

2Second: Whole plant elemental composition

Have we neglegted the K limiting role in terrestrial ecosystems?

Sardans et al. (2012)Global Change Biology (in preparation)

0

10

20

30

40

Grasslands Forests

No-limitingLimiting

1

11

3

33

Nu

mb

er o

f s

tud

ies

Vegetation type

75% of field studies have observed that K limits growth of terrestrial plants in field conditions

Review of published data

Climate change effects on global plant elemental composition

Different elements plays different functional and structural functions

C (structure,..)

N (growth, light capture, metabolism functioning,..)

P (growth, energy transfer,…)

K (water economy, internal transport,…)

Mg (light capture,…)

“Biogeochemical niche”

Each species, as a singular evolutionary product,should have an optimum elemental compositionas consequence of optimum function

Consequence of the optimum adaptation to maximize species fitness in determined abiotic and biotic circumstances, i. e. consequence of long-term genetic adaptation (Genotype)

, but also of short-term capacity to respond under certain limits to life-time environmental competition shifts (Phenotype flexibility)

Peñuelas et al. (2010) Global Change Biology

Principal component 1: 35.6%

-3 -2 -1 0 1 2 3

Pri

nci

pa

l co

mp

on

en

t 2:

15

.4%

-6

-4

-2

0

2

4

6

Principal component 1: 35.6%

-1.0 -0.5 0.0 0.5 1.0

Pri

nci

pa

l co

mp

on

en

t 2:

15

.4%

-1.0

-0.5

0.0

0.5

1.0

Na

ZnCu

K

N

Fe

NiAlienNative

-2

0

2

4

6

8

-5 -4 -3 -2 -1 0 1

PC

2 (

22

.7%

)

PC1 (28.6%)

F. excelsior

Q. petrea

Q. canariensis

C. sativaF. sylvatica

Q. humilis x cerrioidesQ. faginea

Q. humilis

Q. cerrioides

Q. suberA. unedo

Q. ilex

P. sylvestris

P. pinea

A. alba

P. halepensis P. pinaster

P. nigraP. uncinata

C

N P

NP

NK PK

S Ca

M g

K

-1.0 -0.5 0.0 0.5 1.0

PC1 (28.6%)

-1.0

-0.5

0.0

0.5

1.0

PC

2 (2

2.7%

)

C

N P

NP

NK PK

S Ca

M g

K (A)

(B)

(C)

Mediterranean

Wet temperate

Alpine

Transition Med-Temp.

Gymnosperms

Angiosperms

200 400 600 800 1000 1200 1400

M AP (L m -2 yr -1)

-10

-5

0

5

10

15

PC

2

PC 2 = - 1.68 + 0.0021 MAP R = 0.26, P < 0.0001

C

N P

N/P

N/K

P/K

S

Ca

Mg

K

-1.0 -0.5 0.0 0.5 1.0

PC1 (27.7%)

-1.0

-0.5

0.0

0.5

1.0

PC

2 (2

0.7%

)

C

N P

N/P

N/K

P/K

S

Ca

Mg

K

-6

-3

0

3

-0.6 0 0.6 1.2

PC

2 (2

0.7%

)

PC1 (27.7%)

P. halepensis (3)

P. pinea (4)

C. sativa (8)

P. pinaster (2) P. nigra (ab)

Q. suber (7)

A. unedo (6)Q. ilex (5)

Angiosperms

Gimnosperms

(1) a

(2) ab(3) b(4) c

(5) d(6) d

(7) e

(8) f

(3) (4) (5)

(1)

(1,2,7,8) (6)a b c

bc

(A)

(B)

Separated throughout PC4

(explaining12% of variability)

“Biogeochemical niche” in action Native and alien species in Hawai

Different forest types in Catalonia

Mediterranean species

Peñuelas et al. (2010)Global Change Biology

Until this moment the results show that the use of more elements that N and P

Give a more global view of the use of resources

Improve the sensitivity in the use of plant elemental composition shift to detect responses to environmental change

N eutrophication threatens to shift the global stoichiometry

4

8

12

16

8.8

17.7

26.4

35.4

1950s 1980s 1990s 2000s1860s 1900s

N:P

ra

tio

(m

ola

r b

as

is)

N:P

ra

tio

(m

as

s b

as

is)

Natural N2 fixation from continents plus oceans

Natural N2 fixation from continents

Redfield’s ratio

0

50

100

150

200

250

300

350

400N from industrial fertilizersN emissions from fuel combustionN

2 fixation of rice and legume crops

Total anthropogenic NTotal anthropogenic P (mineral fertilizers)

Tg

ye

ar-

1

Global N deposition~ 114 Mtones N yr-1

Global P deposition~ 3.3 Mtones N yr-1

ContinentsN:P ~ 47

Oceans N:P ~ 370

Terrestrial plantsN:P ~ 22-30

Plankton and open ocean watersN:P ~ 15-16

63 0.3

51 3

Peñuelas et al. (2012)Global Change Biology

Changing from local to global scale

Number of “Web of Science” studies reporting effects of changes in N:P ratios and its effects on ecosystems

species composition and function

Human induced chsnges on N/P ratios are already altering ecosystems function and biodiversity by the impacts on N/P ratio is already occuring

Peñuelas et al. (2013)

Natre Communications Submitted.

Global P-cycle is being altered by human activity

Peñuelas et al. (2013)Nature Communicatios(Submitted)

Global climate and C-balance models related to global change should include the changes in nutrients balances and stoichiometry

Our first attempt...Projections under different scenarios of the P demands to fixing C emitted by human activities. The models used were TAXIS, HadCM3, IPSL-CM2 , IPSL-CM4-LOOP, CSM, MPI, LLNL,

FRCGC, UMD, UVIC, CLIMBER, BERNCC

Peñuelas et al. (2013)Nature Geoscience (submitted)

Phosphorus and N/P ratio could be gaining role in global capacity to C fixation andconsequently in the global climatic control

Ecometabolomics-stoichiometric studies

A new tool to study plant responses to climate change

Whole elemental composition shiftsWhole metabolome shifts

Sensitive traits to detect dynamic plant responses

Improvement of the knowledge of the functional mechanisms underliying plant responses (growth, storage, defense, antistress….)

Clues on further consequences throughout trophic web

Useful information to improve global elemental budgets (C, N, P,..) and climatic models

Global Ecology UnitCREAF – CSIC – CEAB

Barcelona

Thank you by your attention and…………by no sleepping (if is the case)

From elements toglobal scale