The Evolution of Wood Anatomical

Diversity and its Significance

Pieter Baas

Contents

• A bit of history

• Wood in the living tree

• Wood diversity

• Integration of phylogenetic and

ecological approaches to the

study of xylem evolution

• Wood anatomy and climate change –

proxies for mean annual

temperature in wood structure

• Conclusions

Quercus wood as seen by Grew, Malpighi and Leeuwenhoek - three

functional tree biologists!

Ludwig Radlkofer

(1829—1927)

1883 in Munich: The

next hundred years

belong to the

anatomical method

Sapindaceae taxonomy

& morphology (including

wood anatomy)

Pinus longaeva -bristlecone pine

Hydraulic architectural types

Softwood Diffuse-porous hardwood Ring-porous hardwood

Tropical diffuse-porous tree

(Shorea) and climber (Serjania)

Temperate diffuse-porous (Aesculus) and

ring-porous (Quercus) trees

Dicot

Woods

I.W. Bailey (1884—

1967)

• Xylem evolution

• Fossil woods

• Wood properties

(preservatives)

• Tree pathology

• Wood Identification

• Cambium

• Cell wall structure

• Vestured pits

1918

Bailey & Tupper

Size variation in

tracheary cells = Major

trends in xylem

evolution

“Inspirational”

Pieter Baas and others

or:

“Outdated and

unnecessary” ??

Marc Olson –Botan.

Rev. 2012 (and others) Swamy,

1954

Wood evolution

from vesselless

gymnosperms to

vessel-bearing

angiosperms

Conductivity Strength

Division of labour

Simple and

scalariform

perforations

0%

10%

20%

30%

40%

50%

60%

70%

80%

90%

100%

Cretaceous Eocene Miocene RecentPaleo Oligo Pli

o

What Was The Incidence of Perforation

Plate Types in Geologic Past?

Simple

Scalariform

Cretaceous - Recent

P. Gasson

Photo by S. Noshiro, Perforation Plate in Davidia

Scalariform perforation

& Vestured pits

Do

Vestures

reduce

cavitation

risk?

Zweypfenning

1978

Scalariform

perforations

plotted on the

Soltis tree are

much more

common in

basal clades

vestured

pits (**)

on Soltis tree

0

5

10

15

20

25

30

35

40

45

50

Deserts Tropical

lowlands

seasonal

Tropical

lowlands

everwet

Subtropical-

warm

temperate

Tropical

mountains

Cool

temperate

Boreal-arctic

Mean % vestured pits Mean % exclusively scalariform perforations

Ecological trends in (vestured pits and)

scalariform perforations (purple)

Jansen et al.2004, PNAS

< 5 , 5 - 20, 20 - 40, > 40-- Vessels per sq. mm

North America, Temperate Asia, Europe similar to one another Tropical America, Africa, SE Asia similar to one another

< 50 µm , 50 - 100 µm, 100 - 200 µm, > 200 µm --Mean Vessel Diameter

Regions with high proportions of narrow vessels have low proportions of ‘few vessels per sq. mm’

Present-Day Woods

Wheeler, Baas, Rodgers 2007 IAWA J

Trees / Small Trees / Shrubs

Trees wider diameters than

shrubs.

Shrubs have a higher % of

narrowest vessels

Wide vessels restricted to

trees (almost)

Vessel Mean Tangential Diameter in

Trees n = 4840

Small Trees n = 663

Shrubs n = 630

< 50 µm 50-100 µm 100–200 µm > 200 µm

Triangle of wood functions and trade-offs

NARROW VESSELS

Work of

F. Ewers

J. Sperry

U. Hacke

S. Davis

Summary of functional ecological trends

1. In tropical - temperate - boreal - arctic gradients:

Scalariform perforations become more common

Element length decreases

Vessel diameter decreases

Vestured pits become rarer

2. In mesic - xeric gradients:

Scalariform perforations become very rare

Element length decreases

Vessel diameter decreases

Vestured pits become more common

Confounding for temperature and moisture proxies!

Also clade dependent (phylogeny)

Additional Wood Anatomical Proxies for Warmer Climates

• Storied structure +

• Ring porosity –

• Parenchyma rare or absent –

• Paratracheal parenchyma +

• Marginal parenchyma –

• Septate fibres +

• Homocellular rays –

Wiemann et al. 1999; Wheeler et al. 1993, 2007

Scale matters!

• Within wild Olea europaea in Europe vessel density is positively related with MAT (Téral & Mengüal 1999)

• Within world flora vessel density negatively related with MAT (Wheeler et al. 2007)

Interim Conclusion No. I

• Wood anatomy contains very strong ecologically adaptive signals (temperature, water, etc.)

• Some of these signals (perforation type, vestured/nonvestured pits) also contain very strong phylogenetic signals

• Conclusion: adaptive evolution is driver of wood anatomical diversification

• Research questions have to take into account spatial, temporal, and taxonomic scales

Harissonia (2x)

* Cneorum tricoccon

Dictyoloma

Wood anatomy of

Spathelioideae

very similar to that

of other Rutaceae

H.J. Braun (1963, 1970)- Functional Type Rhamnus

Rationale for Links between

Climate and Wood Evolution

• Photosynthesis ~ Gas Exchange ~ Stomatal opening ~

Transpiration

• High CO2 ~ Low stomatal frequency ~ Lower demands on

conductivity

• Climate ~ water vapour deficit ~ drought stress ~ cavitation

• Conductivity ~ 4th Power Conduit Radius ~ vessel density

• Resistance to flow: perforation plates & pit membranes

• Cavitation resistance (drought stress) : vessel diameter,

vestured pits, pit membrane ultrastructure?

• Cavitation resistance (freeze-thaw cycle): vessel diameter,

scalariform perforations

• Forest Canopy transpiration regulates climate

– Jarmila Pittermann 2010

Wood Anatomy and Climate Change 1: Tree rings

Wood Anatomy and Climate Change 2: Vantage Fossil Wood

example

• Rich Mid-Miocene assemblage (Wheeler & Dillhoff, 2009, IAWA Journal Supplement 7)

• Mean Annual Temperature reconstruction based on qualitative wood anatomical proxies

X

Ginkgo Petrified Forest State Park, WA, USA = Vantage Woods

Vantage Woods 15.5 my,mid-Miocene

MAT = 24.78 + 36.57 (% storied rays) - 15.61 (% marginal parenchyma) - 16.41 (% axial parenchyma rare to absent)

Wiemann, M.C., E.A. Wheeler, S.R. Manchester, & K.M. Portier. 1998. Dicotyledonous wood anatomical characters as predictors of climate. Palaeogeography, Palaeoclimatology, Palaeoecology 139: 83--100. Wiemann, M.C., S.R. Manchester, & E.A. Wheeler. 1999. Paleotemperature estimation from dicotyledonous wood characters. Palaios 14: 460--474.

Estimating MAT oC using wood

physiognomy

If treat Vantage Fraxinus as a tendency to storied rays, MAT estimate of 12.8 oC,

If storied rays absent, the MAT estimate is 12.1 oC

Recent Temperate Deciduous Broad-leaved Forests of China have MAT of 10 -- 14.6

oC

Recent Mixed Mesophytic Forests of China have MAT of 11.4--16.4

oC

33 Dicot Wood Types From Main Vantage Locality

Wang, Chi-Wu. 1961. The Forests of China. Maria Moors Cabot Foundation

Publication No. 5

Northern Hemisphere

Wolfe, J.A. 1978

Amer. Sci. 66; 694-703

60 50 40 30 20 10 0

60

AGE Million years before present (Ma)

Y = Estimates of To:

% leaves with entire

margins, O Isotopes

% E

ntire

-Marg

ined L

eaves

Infe

rred M

AT.

o C

0

30o

Past climate change inferred from leaf

margins and Oxygen isotopes

Vantage woods

MAT

Nutbeds

woods

MAT

Experimental Studies

• Increased temperature results in:

increased wood density

lower vessel diameter

lower flow resistance (lower sap viscosity)

• Increased CO2 results in:

increased growth

decreased wood density

lower vessel diameter

Caution: limitations of short term experiments

Interim Conclusion 2

• Wood anatomy contains wealth of climatic signals from past and present

• Wood anatomical profiles of species assemblages are underutilised as environmental proxies

• Is this the full story??

Air-seeding pressure (MPa)

Perc

en

tag

e l

oss o

f co

nd

ucti

vit

y

Lens et al. 2011. New Phytologist 190: 709-723

Cavitation s

ensititve

Cavitation r

esis

tant

Vulnerability curves vs. P50

Cavitation resistance

R² = 0,891

0

50

100

150

200

250

300

350

400

-3,5 -3 -2,5 -2 -1,5 -1 -0,5 0

PM thickness-P50

A. platanoides P50: -2.29MPa

1000 nm 1000 nm 1000 nm

A. grandidentatum P50: -3.19MPa A. saccharinum P50: -1.26MPa

Lens et al. 2011. New Phytologist 190: 709-723

PM PM

PM

P = 0.004

Acer

R² = 0,9293

0

100

200

300

400

500

600

700

800

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

pit chamber depth-P50

P = 0.001

V

V

V

V

V

V

Lens et al. 2011.

New Phytologist

190: 709-723

Tight correlation between ultrastructural IV pit characters and Mean Cav. Press. in Acer

pit m

em

bra

ne t

hic

kness

pit c

ham

ber

de

pth

(t/b

) square

wo

od

de

nsity

wid

th o

f w

all

thic

kenin

gs in inner

vessel w

alll

dia

me

ter

of

pit m

em

bra

ne p

ore

s

vessel le

ngth

vessel gro

upin

g index

hydra

ulic

cconductivity p

er

xyle

m a

rea

num

ber

of

thic

ken

ing

s o

n inn

er

vessel w

all

pit a

pert

ure

shape

conta

ct

fraction

pit a

pert

ure

fra

ction

vessel ele

ment

length

mesom

orp

hy index

pit fra

ction

log-t

ranfo

rmed v

essel le

ngth

avera

ge p

it n

um

ber

per

vessel

mean v

essel dia

mete

r

vuln

era

bili

ty index

vessel density

Ap: pit a

rea p

er

vessel

2x v

essel w

all

thic

kness

pit m

em

bra

ne d

iam

ete

r

fiber

length

pit correlations

nonpit

correlations

mem

bra

ne p

oro

sity

Conclusions no. 3

• Major breakthroughs in last 10 years about understanding roles of pit membrane ultrastructure and thickness (Choat, Sano, Jansen, Lens, a.o.).

• Experimental evidence for role of other attributes: perforation type, helical wall thickenings, vessel grouping – what is more to come?

• Vessel diameter-vessel density trade-offs exist, but only explain a small fraction of efficiency-safety trade-offs!

• Vessel diameter could be fully dependent on tree size (tapering conduit model of Anfodillo)?

Special IAWA Journal Issue 2013

• Proceedings of COST-Action STREeSS and IAWA/IUFRO meeting in Naples, April 2013

• Twelve papers: reviews, new methods to observe functional traits, and integrative physiological and anatomical studies

• Guest editors Veronica de Micco, Giovanna Battipaglia and Frederic Lens

Thank You and thanks to:

• Frederic Lens

• Peter Gasson

• Elisabeth Wheeler

• Steven Jansen