Functionnal and ecological significance of cavitation in trees

UMR PIAFINRA-Université Blaise Pascal

Clermont-Ferrand

Louuvain, 7-02-2013

Hervé Cochard

A L I M E N T A T I O N A G R I C U L T U R E

E N V I R O N N E M E N T

Salt & Water Stress in Plants

Newry August 2014

Cohesion-Tension Theory (Dixon 1896)

Hours

0 6 12 18 24

le

afle

t

, M

Pa

-3

-2

-1

0

Fd, d

m3 d

m-3 h-1

0.0

0.5

1.0

1.5

vp

d, h

Pa

0

5

10

15

20

Rg

, W

m-2

0

200

400

600

800

1000-a-

-b-

-c-

0

Pxy

lem

, M

Pa

Daily time course of xylem pressure

Ash trees

CAVITATION

Cavitation: a common phenomenon

Cavitation in trees? Positive? Negative?What is its biological significance?

% C

AV

ITA

TIO

N

Sap pressure, MPa

P50

Xylem vulnerability curves to cavitation

P50 = Sap pressure provoking 50% cavitation

Methods to measure cavitation

Acoustic Emissions Tyree et al 1985

Hydraulic conductance lossSperry et al 1988

Air injectionCochard et al 1992

0r0.5

1Centrifuge techniqueAlder et al 1997, Cochard 2002

Dehydration

How vulnerable are tree species to cavitation?

% c

avita

tion

Sto

mat

al C

ondu

ctan

ceMartin St Paul et al (in press)

Highly cavitation-resistant species

Sap pressure, MPa

Quercus ilex

Px-min

Sigmoidal curve

Jacobsen & Pratt 2012

Vitis

Zufferey, et al 2011%

cav

itatio

nS

ap p

ress

ure

, M

Pa

Low cavitation-resistance species

Sto

mat

al C

ondu

ctan

ce

% c

avita

tion

Px-min

Exponential curve

Sap pressure, MPa

Xylem pressure, MPa

-5 -4 -3 -2 -1 0

PL

C

0

20

40

60

80

100

ExponentialSigmoidal

Two ‘strategies’ for tree hydraulics

Sto

mat

al c

on

du

ctan

ce

% c

avita

tion

Sap pressure, MPa

Low cavitation-resistance:- Cavitation forms as soon as Px<0- Cavitation and repair are routine on

a daily basis- Water release by cavitation sustain

stomatal opening & carbon gain

High cavitation-resistance:- Cavitation forms when Px<Pcav

- Stomatal control of cavitation- Cavitation occurs only under intense

drought conditions- Refilling is seasonal

The same species have been found to display both strategies !!!

50/50

Cochard & Delzon 2013

What is the biological significance of cavitation ?

Px-min

Pitfalls in hydraulic methods ?

Xylem pressure, MPa

-5 -4 -3 -2 -1 0

PL

C

0

20

40

60

80

100

ExponentialSigmoidal

Air

deh

ydra

tion

Air

inje

ctio

nC

entr

ifuga

tion

Coniferous Diffuse-porous Ring-porous

Sigmoidal

Exponential

Sigmoidal Sigmoidal

Sigmoidal

Sigmoidal Exponential

ExponentialExponential

Sigmoidal

Literature survey > 1000 curves > 500 species

Cochard et al 2013

Open vessel artifact?Cochard et al 2010

Refilling artifactJacobsen et al 2012

Open vessel artifact?Ennajeh et al 2011

Ind

ire

ct a

nd

inva

sive

met

ho

ds

Need for a Reference technique : X-ray Tomography (HRCT)

Direct observation, non-invasive, non-destructive

High resolution (<1µm), measures density variations

Affordable laboratory systems now available(more invasive)

Experiments using synchrotron light and living trees

S Jansen

B ChoatS Delzon

E Badel

H CochardR Burlett

T Brodribb

Oak

HR-CT

Deh

ydra

tion

unpublished

-2.9 MPa -5.1 MPa-3.5 MPa

Cen

trifu

gatio

n

% c

avita

tion

Px-min

Air injection

% c

avita

tion

OliveSap pressure, -MPa

Torres et al (in press)

HR-CT Px-min

HR-CT

Laurel (Laurus nobilis)

Sap pressure, MPa

% c

avita

tion

Cochard et al (in press)

Px-min

?

Tension sample

Relaxed sample

Tension sample

Relaxed sample

But see Trifilo et al (in press)!

% c

avi

tatio

n

Xylem tension (MPa)

0,4 1,55 3 3,6 4,1

Deg

ree

of e

mbo

lism

(%

)

0

10

20

30

40

50

60

70

A. campestre E. pauciflora

Incr

emen

t of t

he d

egre

e of

em

bolis

m (

%)

0

10

20

30

40

IP CUT IP CUT IP CUT IP CUT IP CUT

b

a

E. pauciflora

- - - - - MPa

Intact

Cut under tension

Intact Cut under

tension

Cut under tensionIntact

unpublished

-3.6MPa

Eucalyptus potted plants

Cutting artifactWheeler et al

Refilling artifactTrifilo et al

% c

avi

tatio

n

Xylem pressure, MPa

-5 -4 -3 -2 -1 0

PL

C

0

20

40

60

80

100

ExponentialSigmoidal

% c

avita

tion

Sap pressure, MPa

Px-min

High cavitation-resistance strategy has been validated(Oak, Eucalypt, Laurel, Olive, Poplar, Acer, Pinus, Abies,Vitis, Pteris)

Low cavitation-resistance strategy still needs to be confirmed

What is the biological significance of cavitation in trees ?

?

Oak

Xylem Pressure, MPa

Sto

mat

al c

on

du

ctan

ce

Stomatal / Hydraulic Coordination

Cochard et al 1996

Xylem pressure, MPa

-3.0 -2.5 -2.0 -1.5 -1.0 -0.5 0.0

% c

avita

tion

0

10

20

30

40

50

60

70

Rel

ativ

e pl

ant w

ater

loss

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1.0

Maize

Wheat

Xylem Pressure, MPa

-6 -5 -4 -3 -2 -1 0

Lea

f ev

apor

atio

n ra

te

0

1

2

3

4

5

% C

avit

atio

n

0

20

40

60

80

100

Cochard 2002

Neghliz, Cochard & Martre unpublished

% C

avit

atio

n

“Stomatal control of cavitation”

Xylem pressure, MPa%

Cav

itat

ion

0-3-6

Sto

mat

al c

ond

uct

aceXerophilous species

0-3-6

Hygrophilous species

0-3-6

Mesophilous species

Sto

mat

al c

ond

uct

ace

Sto

mat

al c

ond

uct

ace

% C

avit

atio

n

% C

avit

atio

n

Xylem pressure, MPa

Xylem pressure, MPa

Stomatal / Hydraulic coordination across species

unpublished

Xylem pressure at 10% Cavitation, MPa

Xyl

em p

ress

ure

at 9

0%

sto

mat

al

clos

ure,

MP

a

Populus x cv ‘peace’

+ABA

-ABA

Cochard, Ridolfi, Dreyer 1996

% C

avita

tion

Distance to apex, cm

% C

avita

tion

Sto

mat

al

con

du

cta

nc

e

Xylem Pressure, MPa

Why trees do their best to avoid cavitation at the cost of less carbon uptake ?

Water-stress

Hydraulic failure kills trees under extreme drought conditions

Fagus sylvatica

Weeks after drought onset

0 2 4 6 8 10 12

% E

mbo

lism

0

20

40

60

80

100

% M

orta

lity

0

20

40

60

80

100

% Mortality% Embolism

Barigah et al 2013

% c

avita

tion

Dry till death experiment

Taux de cavitation

0 20 40 60 80 100

Tau

x d

e m

ort

alit

é

0

20

40

60

80

100

% Cavitation

% M

orta

lity

Critical cavitation level for mortality after extreme drought event:

50% cavitation Gymnosperms(Brodribb & Cochard 2010; Brodribb et al 2011)

90% cavitation Angiosperms(Ulri et al 2013, Barigah et al 2013)

Gymnosperms

Angiosperms

Cavitation can delay mortality

Hydraulic failure-induced mortality

Lethal xylem pressure, MPa

-12 -10 -8 -6 -4 -2 0

Xyl

em p

ress

ure

at 5

0 P

LC

, MP

a

-12

-10

-8

-6

-4

-2

0AngiospermsGymnosperms

Vul

nera

bilit

y to

cav

itatio

n, P

50 M

Pa

0

% C

avita

tion

0

50

100

Drought stress intensity

Decennial Seasonal No droughtCentennial

PcavP50P90<<0

Delzon & Cochard 2014

Sap pressure, MPa

Gymnosperms

Angiosperms

Pmin : Minimum field xylem pressure under drought conditions

Tree safety margin for hydraulic failure-induced mortality

Gymnosperms:Pmin-P50

Angiosperms:Pmin-P90

Safety margins are >0 but constant across forest biomes

Modified from Choat et al. Nature 2012

Global convergence in the vulnerability of forests to drought

Vulnérabilité à la cavitation P50, MPa

-8 -6 -4 -2 0

StipeBrachypodeMéliqueChiendent cRay-grassFlouvePhléoleDactyleFétuqueFromentalChiendent rVulpinBlé récitalMaïsRizPanicGlycérieRoseauBaldingère

Vulnérabilité des Poacées à la cavitation (P50, MPA)

Xerophilous

Mesophilous

Hygrophilous

Crops

Cochard, Picon-Cochard, unpublished

Cavitation resistance in Poaceae (grasses)

Vulnerability to cavitation, P50 MPa

Tixier et al 2013

% c

avita

tion

% c

avita

tion

% c

avita

tion

% c

avita

tion

S Herbette

Melzer et al 2008

Lens et al 2013

“Woody” Arabidopsis (soc1-6 ful7 mutants)

% c

avita

tion

Xylem Pressure (Pmin, MPa)

0

% F

unct

ion

inte

nsity

0

50

100

Cavitatio

n

Tran

spir

atio

nP

ho

tosy

nth

esis

 

Mo

rta

lity

Drought stress intensity

Decennial Seasonal No droughtCentennial

PcavP50P90<<0 Pmidday

Take-home-doggy-bag message

1. Cavitation and repair and not routine in trees (plants?)

2. Coordination between stomatal and hydraulic functions

3. Cavitation forms under intense drought conditions

4. Hydraulic failure can induce tree mortality under extreme drought conditions

5. There is a future for Arabidopsis (in plant hydraulics)

A L I M E N T A T I O N A G R I C U L T U R E

E N V I R O N N E M E N T

http://herve.cochard.free.fr

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to S

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