Tropical plant trait evolution and the consequences for savanna-forest transitions

William A. HoffmannNorth Carolina State University

CollaboratorsAugusto FrancoM. HaridasanErika Geiger

Sybil GotschLucas SilvaDavi Rossatto

The Cerrado

What determines tree cover in savannas?

What determines the distribution of

forest and savanna?

•Dense tree cover•no grass

•Hot, dry, windy microclimate•Frequent fire

•Cool, moist microclimate•Infrequent, mild fire

•Sparse tree cover•Dense grass

Miconia cuspidata

Miconia pohliana

(Forest species)

(Savanna species)

Symplocos mosenii(Forest species)

Symplocosrhamnifolia

(Savanna species)

Large areas of the tropics have climates in which either savanna or forest vegetation in possible

Staver et al (2011)

Cerling et al 1997 Nature 389:153-158

C4 grasses became abundant only in the past 8 million years

Simon et al 2009

Savanna trees and shrubs began to arise from forest ancestors approximately 10 million years ago.

There have been at least 115 independent origins of savanna trees or shrubs

Black = forest taxaRed = savanna taxa

Hoffmann (unpublished)

Main questions

• What selective pressures have shaped the evolution of tree species in savanna?

• What are the consequences of savanna tree adaptations for ecosystem properties and vegetation dynamics?

The multiple, independent origins of savanna lineages is ideal for comparative studies

Black = forest taxaRed = savanna taxa

Savanna Forest

Hei

ght a

t mat

urity

(m)

0

2

4

6

8

10

Savanna Forest

Leaf

Are

a In

dex

0.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

Note that this is a comparison of forest and savanna species.Savanna Forest

See

dlin

gro

ot:s

hoot

ratio

0

1

2

3

4

Savanna and forest species differ substantially in traits that have large implications for ecosystem structure and dynamics

Savanna Forest

Bar

k th

ickn

ess:

stem

radi

us

0.0

0.1

0.2

0.3

Savanna ForestDia

met

er g

row

th ra

te (m

m y

r-1)

0

1

2

3

4

5

6

53% of the evolutionary transitions from forest to savanna were associated with a shift to a smaller growth form.

Question 2:

What are the consequences of these adaptations for ecosystem properties and vegetation dynamics?

Savanna species Forest species

Pos

t-fire

sur

viva

l (%

)

0

20

40

60

80

100

Savanna and forest species survive fire equally well

The fire trap (Bell 1984)

Long time without fire

Fire

The fire trap (Bell 1984)

Short time without fire

Long time without fire

Fire

The fire trap (Bell 1984)

Short time without fire

Long time without fire

FireFire

The fire trap (Bell 1984)

Short time without fire

Long time without fire

Fire

The fire trap (Bell 1984)

Short time without fire

Long time without fire

FireFire

An analogous threshold exists for ecosystems

An analogous threshold exists for ecosystems

Short timewithout fire

An analogous threshold exists for ecosystems

Short timewithout fire

Fire

An analogous threshold exists for ecosystems

Short timewithout fire

Long timewithout fire

Fire

An analogous threshold exists for ecosystems

Short timewithout fire

Long timewithout fire

Fire Fire

CONTROL

WATER

NUTRIENTS

WATER + NUTRIENTS

10m x 70m plots

Resource manipulation experiment

Water availabilityNot irrigated Irrigated

Gro

wth

rate

(mm

yr-1

)

0

1

2

3

4No added nutrientsAdded nutrients

Tree growth is more strongly limited by nutrients than by water

High-resource sites permit more rapid canopy closure

Time since fire (y)

Cano

py co

ver

High resource site

Low resource site

At what point is each thresholds reached?

• How big must a tree be to avoid topkill?• How dense must the canopy be to substantially

reduce flammability?

Hoffmann et al (2012) Ecology Letters

Bark thickness (mm)0.1 1 10 100

Ste

m s

urvi

val (

%)

0

20

40

60

80

100Low fire intensity

Hoffmann et al (2012) Ecology Letters

Bark thickness (mm)0.1 1 10 100

Ste

m s

urvi

val (

%)

0

20

40

60

80

100Low fire intensity

A growing stem becomes fire resistant when its bark thickness exceeds 6 mm

Hoffmann et al (2012) Ecology Letters

Bark thickness (mm)0.1 1 10 100

Ste

m s

urvi

val (

%)

0

20

40

60

80

100Low fire intensity

5.9 mm

A growing stem becomes fire resistant when its bark thickness exceeds 6 mm

Hoffmann et al (2012) Ecology Letters

Bark thickness (mm)0.1 1 10 100

Ste

m s

urvi

val (

%)

0

20

40

60

80

100Low fire intensityHigh fire intensity

5.9 mm 9.1 mm

-30 -10 10 30Distance (m)

Microclimate •Wind speed•Relative humidity•Temperature

Fuels •Mass•Moisture•Bulk density

BehavePlus 5(fire behavior model)

Hoffmann et al (2012) Austral Ecology

Win

d sp

eed

(km

hr-1

)

0.0

0.5

1.0

1.5

2.0

2.5

Min

. rel

ativ

e hu

mid

ity (%

)

35

40

45

50

55

Distance (m)-30 -20 -10 0 10 20 30

Max

air

tem

p.(C

)

202122232425262728

Distance (m)-30 -20 -10 0 10 20 30

Fine

fuel

moi

stur

e (%

)

68

1012141618

Flam

e le

ngth

(m

)

0.00.20.40.60.81.01.21.4

Fire

line

inte

nsity

(k

W m

-2)

0

100

200

300

400

Distance (m)-30 -20 -10 0 10 20 30

Rat

e of

spr

ead

(Km

hr-

1)

0.00

0.05

0.10

0.15

0.20

Fire simulations with BehavePlus

Distance along transect (m)-30 -20 -10 0 10 20 30

Fuel

bul

k de

nsity

(kg

m-3

)

0

10

20

30

Flammability of savanna is determined primarily by the presence of grass

The canopy density at which grasses are excluded is a critical transition between savanna and forest.

Tree LAI0 1 2 3 4 5

Gra

ss L

AI

0

1

2

3

4

Thus we have two critical thresholds

• A tree reaches a fire-resistance threshold when it accumulates a bark thickness of about 6 mm.

• The ecosystem reaches a fire-suppression threshold when it attains a leaf area index of about 3.

Stem diameter (cm)1 10 100

Bar

k th

ickn

ess

(cm

)

0.01

0.1

1

10Savanna speciesForest species

As savanna trees grow, they accumulate bark thickness more quickly than forest species

Stem diameter (cm)1 10 100

Bar

k th

ickn

ess

(cm

)

0.01

0.1

1

10Savanna speciesForest species

As savanna trees grow, they accumulate bark thickness more quickly than forest species

Threshold bark thickness

Stem diameter (cm)1 10 100

Bar

k th

ickn

ess

(cm

)

0.01

0.1

1

10Savanna speciesForest species

As savanna trees grow, they accumulate bark thickness more quickly than forest species

Threshold bark thickness

4.7 cm 10.2 cm

Recall that forest species grow more quickly than savanna species when growing in the same environment

Savanna ForestDia

met

er g

row

th ra

te (m

m y

r-1)

0

1

2

3

4

Savanna species Forest speciesFire interval required to ensure <50% topkill

8 years 14 years

5-year mean return interval

25 years 108 years

2-year mean return interval

510 years 32800 years

Expected total time under stochastic fire regime

Under a typical fire regime a forest tree has little chance of reaching maturity in savanna

But, there is safety in numbers

•Dense tree cover•no grass

•Hot, dry microclimate•Frequent fire

•Cool, moist microclimate•Infrequent, mild fire

•Sparse tree cover•Dense grass

Forest species have greater leaf area than savanna species when growing in the same environment

Diameter (cm)0.1 1 10

Leaf

are

a (m

2 )

0.0001

0.001

0.01

0.1

1

10

100

Savanna speciesForest species

Forest species permit more rapid canopy closure

0

1

2

3

4

5

6

Time (years)

Leaf

are

a in

dex

Site occupied by forest species

Site occupied by savanna species

Forest species permit more rapid canopy closure

0

1

2

3

4

5

6

Time (years)

Leaf

are

a in

dex

Site occupied by forest species

Site occupied by savanna species

Threshold canopy density

Forest species permit more rapid canopy closure

0

1

2

3

4

5

6

Time (years)

Leaf

are

a in

dex

Site occupied by forest species

Site occupied by savanna species

Threshold canopy density

Distance along transect (m)-30 -20 -10 0 10 20 30

Dia

met

er g

row

th ra

te (m

m y

r-1)

0

2

4

6

8

10

12

14

16

Forest species

Savanna species

Conclusions•Many indepedent origins of savanna trees •Fire has exerted strong selection on traits •Nutrients, not water, limits tree growth in these mesic savannas.•Two critical thresholds govern savanna-forest dynamics:

(1) bark thickness at which a stem becomes fire resistant.(2) canopy density at which grasses are excluded

• Reaching a forest state requires forest species, but these are particularly constrained by the high frequency of fire

Vegetation models should

•Represent fire and its feedbacks with vegetation•Represent topkill and reprouting •Represent of savanna and forest tree functional types OR tradeoffs involving bark, carbohydrate storage, shade tolerance, canopy density. •Not assume that tree cover in mesic savannas are water limited.•Robustly simulate savannas over large areas in response to water deficits, multiple nutrient deficiencies, seasonal flooding, and physical soil constraints.