Trends of the Herbs Ecological Evolution

Chapter 11Trends of the Herbs Ecological Evolution

Sergei N. Sheremet’ev and Yuri V. Gamalei

Abstract The results of analytic research show that the evolution of leaf structureand water balance are completely coincident to global changes of planet climateand hydrology. Taxonomical diversity of herbs and herbaceous biomes is thefunction of paleoclimate variability and plant adaptogenesis to it. Two globaltrends of ecological evolution contrast differing by the composition of herbaceousadaptive types is the next: (a) the line of herbs of chilling plains with dominationthe group of plant species with C3 apoplastic syndrome formed under cold climateinfluence, and (b) the line of herbs of hot plains with domination of plant specieswith C4 apoplastic syndrome. Both trends include the monocots and dicots, andboth are the results of climate changes in Cenozoic. C3 herbs of chilling plains andthe steppe and meadow phytocoenosis formed by them arise as the answer totemperature decrease in great areas of high latitudes. The apoplastic syndrome(transfer from symplastic transport of assimilates suppressed by cold to theirapoplastic transport) is the diagnostic test for this group of herbs. C4 herbs of hotplains and the savanna, desert and solontchak plant vegetation are the adaptiveanswer to aridization of low latitude areas. C4 syndrome (compensation of stomataclosure by the mechanism of CO2 concentration in the leaf tissues) is a special signof this group of herbs. Both types of herbaceous biomes come to change forestbiomes which were strongly decreased in both areas, at low and high latitudes.This tendency is continued in parallels with climate tendency to continentdesiccation and cooling.

S. N. Sheremet’ev (&) � Y. V. GamaleiKomarov Botanical Institute of the Russian Academy of Sciences,Prof. Popov Street 2, St. Petersburg 197376, Russiae-mail: [email protected]

P. Pontarotti (ed.), Evolutionary Biology: Mechanisms and Trends,DOI: 10.1007/978-3-642-30425-5_11, � Springer-Verlag Berlin Heidelberg 2012

189

11.1 Introduction

Last years have appeared and intensively developed databases on the Internet,containing the information on plant taxa age—time of their earliest appearance infossil record. There are data for many families, and in some cases for genera ofangiosperms. The fullest and informative database on the Internet, in our opinion,is the Paleobiology database (PBDB) (http://paleodb.org/cgi-bin/bridge.pl).Possibility to establish age of herbs genera which were earlier objects of researchesof the structural–functional organization (Gamalei 2000) and water relations(Sheremet’ev 2005), has allowed to track changes of structural–functionalproperties of plants in time and to compare this time trends with some majorpaleoclimate changes. Being engaged in this work, we understood neverthelesssome vagueness of such constructions in connection with incomplete clarificationof genera average functioning parameters, and also the data about genera age.However this question, in our opinion, is interesting and demands the preliminaryanalysis and discussion at least.

Global climatic changes, as a rule, are considered in connection with theirinfluence on large biosphere reorganizations and biotic events (Briggs andCrowther 1997; Culver and Rawson 2000; Semikhatov and Chumakov 2004, andothers). Maybe that these changes have left a trace in less considerable manifes-tations, such, as structure and functioning of plant leaves.

11.2 Geological Ages of Some Herbs Generaand Their Functioning

Representatives of the genera whose ages are known (Table 11.1) were the objectsof comparative structural and functional studies (Gamalei 2000; Sheremet’ev2005). Assuming that structural and functional characters have remainedunchanged from the moment when the given taxon arose (Gamalei et al. 2008),one can use the data on the studied genera to construct the time series of the plantstructure and water relations parameters reflecting the accessibility of water for theplants and to trace their relationships with drastic global climatic changes. Weselected the following characters: the transpiration rate, water content of theleaves, partial volume of intercellular spaces in the mesophyll, and water satura-tion deficit (Fig. 11.1). Correlations of these characters with the environmentalmoisture vector have been confirmed by comparative studies along the contem-porary gradients of soil moisture (Sheremet’ev 2005).

The curves of the mean values of the studied characters plotted as functions ofthe genus ages show interrelated variation patterns (Fig. 11.1). The similarity ofthe trends of transpiration rate and water content of the leaves is undoubted; bothparameters increased during the Cretaceous, peaked during the Paleocene, beganto decrease in the late Eocene, and reached the minimum in the Oligocene. Next

190 S. N. Sheremet’ev and Y. V. Gamalei

http://paleodb.org/cgi-bin/bridge.pl

increase began in the mid-Miocene and was followed by next decline in the end ofthat epoch (Figs. 11.1a, 11.1b).

The mesophyll density (Fig. 11.1c) (defined by quantity of intercellular spacesin leaf) is a sign of degree of xeromorphic organizations of herbs—it increases in adirection from humid to arid habitats (Shields 1950; Vasilevskaya 1979; Gamalei1988), that easily confirms by the quantitative data (Sheremet’ev 2005). Thepartial volume of intercellular spaces in the mesophyll, which is generally used asan integrated characteristic of water supply to plants, changed in almost the sameway (as transpiration rate and leaf water content). For obvious reasons, thedirection of changes in water saturation deficit was always opposite (Fig. 11.1d).Therefore, further we would not consider each of these signs separately, takingtranspiration rate for an example and meaning that the same relate to othercharacters.

The dynamics of the structural–functional organization of plants in the con-temporary soil moisture gradient follow habitats water supply conditions. It ispossible to assume that all the four parameters change in time (Fig. 11.1,Table 11.2) can reflect the sequence of changes in the global hydrological cycleduring previous geological epochs, which can be tested using published data.

Table 11.1 The ages of representatives of the genera studied

Genus Stratigraphic interval Intervalboundaries,Ma

Interval middle,Ma

No. of PBDBa

collection

Sanguisorba Early Pleistocene 1.8 0.8 1.3 61,887Valeriana Piacenzian 3.6 2.6 3.1 22,778Vicia Late Miocene–early

Pliocene11.6 3.6 7.6 21,222

Artemisia Early Miocene 23.0 16.0 19.5 47,096Thalictrum Early Miocene 23.0 16.0 19.5 23,906Potentilla Late Oligocene–early

Miocene28.4 16.0 22.2 23,793

Butomus Chattian 28.4 23.0 25.7 26,510Carex Chattian 28.4 23.0 25.7 23,114; 23,663Lycopus Chattian 28.4 23.0 25.7 23,669; 23,781Phalaris Rupelian 33.9 28.4 31.2 35,221; 35,235Polygonum Rupelian 33.9 28.4 31.2 22,844; 22,849Alisma Lutetian 48.6 40.4 44.5 24,106Sagittaria Paleocene 65.5 55.8 60.7 40,426Sparganium Albian 112.0 99.6 105.8 31,174

The first date under which they are mentioned in the paleontological record, interval boundariesafter Ogg et al. 2008a PBDB (http://paleodb.org/cgi-bin/bridge.pl)

11 Trends of the Herbs Ecological Evolution 191

http://paleodb.org/cgi-bin/bridge.pl

11.3 Late Cretaceous–Cenozoic Climateand Plants Functioning

11.3.1 Late Cretaceous–Eocene

The late Cretaceous, Paleocene and Eocene were characterized by a large annualprecipitation on the surface of continents (Fig. 11.2a) (sometimes as large as140–150 cm) because of a combination of many factors, including the continentaltopography, distribution of oceanic currents, a high sea level accompanied by a

Fig. 11.1 Water relations parameters and partial volumes of intercellular spaces in themesophyll of some herbs genera (Table 11.1 and 11.2) as function of time. a Transpiration rate(TR), b leaf water content (WC), c partial volumes of intercellular spaces (PV Ics), d watersaturation deficit (WSD). Grey filling—confidence intervals, Ple—Pleistocene, Pli—Pliocene,Mi—Miocene, Ol—Oligocene, Eo—Eocene, Pa—Paleocene, Cr2—Late Cretaceous, Cr1—Early Cretaceous


Tab

le11

.2T

rans

pira

tion

rate

(TR

,gw

ater

/gdry

mas

s�h),

wat

ersa

tura

tion

defi

cit(

WS

D,%

),le

afw

ater

cont

ent(

LW

C,g

wat

er/g

dry

mas

s)fo

rre

pres

enta

tive

sof

this

stud

y

Gen

usA

ge,

Ma

TR

WS

DL

WC

n� X

SxC

Ln

� XSx

CL

n� X

SxC

L

Sang

uiso

rba

1.3

620

2.21

0.90

0.07

620

12.6

4.7

0.37

620

2.15

0.38

0.03

Val

eria

na3.

122

81.

220.

450.

0622

615

.83.

80.

5022

83.

720.

490.

06V

icia

7.6

290

2.48

1.13

0.13

288

15.8

4.4

0.51

290

2.72

0.49

0.06

Art

emis

ia,

Tha

lict

rum

19.5

1,12

11.

791.

260.

071,

057

26.7

15.9

0.96

1,36

02.

350.

740.

04P

oten

till

a22

.292

01.

740.

930.

0692

021

.26.

50.

4292

01.

790.

300.

02B

utom

us,

Car

ex,

Lyc

opus

25.7

2,00

61.

400.

830.

041,

954

17.2

10.5

0.47

2,00

62.

241.

280.

06P

hala

ris,

Pol

ygon

um31

.257

02.

211.

200.

1057

07

2.1

0.17

570

2.94

0.85

0.07

Ali

sma

44.5

138

3.98

1.01

0.17

138

2.7

1.8

0.29

138

4.98

0.56

0.09

Sagi

ttar

ia60

.713

84.

080.

930.

1613

82.

51.

70.

2913

85.

970.

600.

10Sp

arga

nium

105.

813

82.

200.

680.

1113

815

.24.

60.

7713

84.

890.

470.

08

n—nu

mbe

rof

obse

rvat

ions

,� X

—av

erag

es,

Sx—

stan

dard

devi

atio

ns,

CL

—co

nfide

nce

leve

ls(P

=0.

95)


Fig. 11.2 Transpiration rate (as grey filling confidence corridor) (TR) and global climate of lateCretaceous–Cenozoic: a continental precipitation (after Gibbs et al. 1999); b continentalevaporation (continental precipitation–continental runoff) (after Gibbs et al. 1999); c arid area(white points—computed after maps by Scotese 2003, black points—after maps by Akhmetiev 2004and by Chumakov 2004a, b, zero point—contemporary hyperarid, arid, and semi-arid areas of ice-free land after Middleton and Thomas 1997); d sea level (smoothed curve after Miller et al. 2005);e oxygen isotope ratio in shells of planktonic foraminifera and brachiopods, data averaging by ages(Ogg et al. 2008) from J. Veizer’s database (http://www.science.uottawa.ca/geology/isotope_data/)(Veizer et al., 1999); f Central Europe continental temperature reconstruction (adapted fromMosbrugger et al. 2005)


http://www.science.uottawa.ca/geology/isotope_data/

high temperature of the ocean and land surface, etc (Gibbs et al. 1999). Thisgeological time is characterized as a ‘‘warm biosphere’’ (or a «warm mode» –Frakes et al. 2005) exceptionally favorable for plants (Chumakov 1993, 1997,2004a, b; Akhmetiev 2004). The thermal optimum was accompanied by largeatmospheric precipitation and a comparatively high atmospheric carbon dioxideconcentration (Tajika 1999; Berner and Kothavala 2001; Beerling and Royer 2002;Hansen and Wallmann 2003; Wallmann 2004; Berner 2006; Royer 2006, andothers), however considerable territories of a land have been occupied by arid belts(Chumakov 1997, 2004a, b; Zharkov et al. 2004; Scotese 2003) (Fig. 11.2c).

Often late Cretaceous–Eocene describes as «greenhouse world» (Beerling andWoodward 2001; Zachos et al. 2001; Retallack 2004; Miller et al. 2005; Pearsonet al. 2007). For example, in Eocene (Lutetian) woods in the conditions of enoughwarm and damp climates in high latitudes behind polar circle (70–80�N) grew(Jahren 2007). On this background, a number of cold events (geologically short-term ones—up to 100 thousand years: Miller et al. 2005) are detected (we meanrelatively cold events; temperatures were, possibly, on some degrees abovemodern). Cretaceous climate cooling up to end of Maastrichtian and then in middleEocene up to Oligocene beginning, nevertheless, were continued (Beerling andWoodward 2001; Zachos et al. 2001, and others) (Fig. 11.2e).

The estimation of the structural and functional parameters of plants of the lateCretaceous–Eocene as typical of mesophytes (and maybe hydrophytes) is

0.0

0.2

0.4

0.6

0.8

1.0

0 20 40 60 80 100 120

Time, Ma

Evo

lutio

n ra

te, f

amili

es/M

a

0

5

10

15

20

25

Are

a, ×

106 k

m2

Evolution rate

Area

Fig. 11.3 Evolution rate of angiosperms families (with predominance of herbaceous plants)during late Cretaceous–Cenozoic (computed after Muller 1981; Benton 1993; Martínez-Millán2010 and PBDB; data grouped by epochs) and area of cool temperate climate regions (computedafter maps by Scotese 2003) as function of time


suggested (loose mesophyll promotes high transpiration rate, to accumulation of aconsiderable quantity of water in leaves and to low water saturation deficit)(Fig. 11.1). It is confirmed by the coincidence of the curves of the transpirationrate and global continental precipitation (Fig. 11.2a), and especially waterevaporation from the continent surface (Fig. 11.2b) in this time.

During the Cretaceous–early Eocene, the arid areas considerably decreased(Fig. 11.2c), that corresponds to assumptions about high activity of a hydrologicalcycle in this time (Figs. 11.2a, 11.2b), high sea level (Fig. 11.2d), increasing totalarea of temperate (warm and cool) regions (Scotese 2003), herbs as mesophytes,and hydrophytes functioning (Fig. 11.1).

In the beginning of Eocene, the forest vegetation prevailed in the world andonly in the end of this epoch have appeared and started to develop grasslands inEurasia (Bredenkamp et al. 2002). Therefore, the Paleocene–Eocene beginning ofherbs advancement in an area with cool and warm moderate climates could occuras a part of woody (or shrubby) communities. Perhaps, development and evolutionof herb vegetation mainly was connected with cool temperate climate. Evolutionrate of angiosperm families with predominating of herbs (as number of familiesappeared in some geological epoch divided by duration of this epoch) close cor-responding with Cenozoic dynamics of this climate (Fig. 11.3). Paleocene andEocene dynamics of cool temperate climate was determined by antiphase changesof warm temperate climate, but the next (Oligocene–Pleistocene) cool temperateclimate changes was connected with antiphase dynamics of arid climate. Wideexpansion of herbs ecosystems (as biome) became the general tendency only in aMiocene (see below).

11.3.2 Oligocene

A slow decrease in temperature after the early Eocene climatic optimum wasfollowed by a drastic climatic cooling and large-scale glaciation of the Antarctica(Kennett 1977; Lear et al. 2000; Zachos et al. 2001; DeConto and Pollard 2003a, b;Pollard and DeConto 2003, 2005). Somewhat later, glaciation spread overGreenland (later Eocene–early Oligocene: Eldrett et al. 2007). After that, sym-metric glaciation of both poles occurred (Tripati et al. 2005; Moran et al. 2006).The temperature gradient between the equatorial zone and the poles increased(Nikolaev et al. 1998). The transition from the ‘‘warm biosphere’’ to the ‘‘coldbiosphere’’ was begun (Akhmetiev 2004).

The Oligocene climatic cooling (Figs. 11.2e, 11.2f), which is considered one ofthe most important events in the climatic record (DeConto and Pollard 2003a, b),was accompanied by a decrease in the atmospheric carbon dioxide concentration(Pagani et al. 2005), decrease in precipitation (Fig. 11.2a) and evaporation(Fig. 11.2b), growing aridity of continents (Fig. 11.2c), and lowering the sea level(Fig. 11.2d). Evolution rate of herbaceous plants was decreased up to minimallevel (Fig. 11.3) perhaps as a result of climate cooling, and in consequence of the


Tab

le11

.3T

hefi

rst

appe

aran

cean

dex

pans

ion

ofhe

rbbi

omes

ondi

ffer

ent

cont

inen

ts

Fir

stap

pear

ance

Exp

ansi

onR

efer

ence

C3/C

4C

omm

ent

Nor

thA

mer

ica

Ear

lyO

ligo

cene

(des

ert

herb

ecos

yste

ms)

Lat

eM

ioce

neR

etal

lack

(199

7,20

04)

Not

spec

ified

Pal

eoso

ls

Ear

lyO

ligo

cene

Lat

eO

ligo

cene

orea

rly

Mio

cene

Str

ömbe

rg(2

005)

C3

Col

orad

o,N

ebra

ska,

Wyo

min

g,M

onta

na,

Idah

o.P

hyto

lith

asse

mbl

ages

Lat

eO

ligo

cene

–ea

rly

Mio

cene

Lat

eM

ioce

neR

etal

lack

(199

8)N

otsp

ecifi

edP

aleo

sols

Lat

eO

ligo

cene

-ea

rly

Mio

cene

Str

ömbe

rg(2

002,

2004

)C

3N

ebra

ska.

Phy

toli

thas

sem

blag

es

Ear

lyM

ioce

ne(s

hort

-gra

sspr

airi

e)

Lat

eM

ioce

neR

etal

lack

(199

7,20

04)

Not

spec

ified

Pal

eoso

ls

Ear

lyM

ioce

neL

ate

Mio

cene

Mac

Fad

den

(199

7,20

00)

C3

and

C4

Car

bon

isot

opes

ofto

oth

enam

elof

foss

ilhe

rbiv

ore

mam

mal

s.C

3he

rbbi

omes

befo

reex

pans

ion

ofC

4he

rbbi

omes

inth

ela

teM

ioce

neE

arly

Mio

cene

Lat

eM

ioce

neJa

nis

etal

.(2

000,

2004

);Ja

nis

(200

7)N

otsp

ecifi

edD

iscu

ssio

nof

the

lite

rary

data

Ear

lyM

ioce

neL

ate

Mio

cene

–ear

lyP

lioc

ene

Fox

and

Koc

h(2

003,

2004

)C

4G

reat

plai

ns.

Pal

eoso

ls.

Car

bon

isot

opes

Ear

lyM

ioce

neS

tröm

berg

(200

6)C

3C

olor

ado,

Neb

rask

a,W

yom

ing,

Mon

tana

,Id

aho.

Phy

toli

thas

sem

blag

esM

iddl

eM

ioce

neF

oxan

dK

och

(200

3)C

3G

reat

plai

ns.

Pal

eoso

ls.

Car

bon

isot

opes

Mid

dle

Mio

cene

–lat

eM

ioce

neL

ate

Mio

cene

–ear

lyP

lioc

ene

Kel

logg

(200

1)C

4D

iscu

ssio

nof

the

lite

rary

data

Lat

eM

ioce

neL

ate

Mio

cene

Cer

ling

etal

.(1

997)

C4

Car

bon

isot

opes

ofto

oth

enam

elof

foss

ilhe

rbiv

ore

mam

mal

s.

(con

tinu

ed)


Tab

le11

.3(c

onti

nued

)

Fir

stap

pear

ance

Exp

ansi

onR

efer

ence

C3/C

4C

omm

ent

Lat

eM

ioce

neP

lioc

ene

Axe

lrod

(198

5)N

otsp

ecifi

edP

aleo

bota

nyda

taL

ate

Mio

cene

Pli

ocen

e–P

leis

toce

neT

rave

rse

(200

7)N

otsp

ecifi

edP

aleo

paly

nolo

gyL

ate

Mio

cene

And

erso

n(2

006)

C4

Dis

cuss

ion

ofth

eli

tera

ryda

taL

ate

Mio

cene

Mac

Fad

den

(200

5)C

4T

ooth

mor

phol

ogy

and

carb

onis

otop

esof

toot

hen

amel

offo

ssil

hors

esL

ate

Mio

cene

Mac

Fad

den

and

Cer

ling

(199

4)C

4C

arbo

nis

otop

esof

toot

hen

amel

offo

ssil

herb

ivor

em

amm

als

Lat

eM

ioce

ne(t

allg

rass

prai

rie)

Ret

alla

cket

al.

(200

2)N

otsp

ecifi

edP

aleo

sols

Lat

eM

ioce

neW

ang

etal

.(1

994)

C4

Car

bon

isot

opes

ofto

oth

enam

elof

foss

ilhe

rbiv

ore

mam

mal

sL

ate

Mio

cene

–ear

lyP

lioc

ene

Cer

ling

etal

.(1

998)

C4

Car

bon

isot

opes

ofto

oth

enam

elof

foss

ilhe

rbiv

ore

mam

mal

sE

uras

iaL

ate

Eoc

ene,

Oli

goce

neB

rede

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pet

al.

(200

2)N

otsp

ecifi

edD

iscu

ssio

nof

the

lite

rary

data

Ear

lyM

ioce

neL

ate

Mio

cene

Str

ömbe

rget

al.

(200

7)C

3T

urke

y,G

reec

e,Ir

an.

Phy

toli

ths.

Car

bon

isot

opes

ofpa

leos

ols

and

ofto

oth

enam

els

ofm

amm

als

Mid

dle

Mio

cene

Lat

eM

ioce

neH

oorn

etal

.(2

000)

C3.

C4—

part

iall

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entr

alN

epal

.P

aleo

paly

nolo

gyL

ate

Mio

cene

Lat

eM

ioce

neC

erli

nget

al.

(199

7)C

4P

akis

tan.

Car

bon

isot

opes

ofto

oth

enam

elof

foss

ilhe

rbiv

ore

mam

mal

sL

ate

Mio

cene

Lat

eM

ioce

neJa

nis

etal

.(2

000,

2004

);Ja

nis

(200

7)N

otsp

ecifi

edD

iscu

ssio

nof

the

lite

rary

data

Lat

eM

ioce

neL

ate

Mio

cene

Mor

gan

etal

.19

94C

4P

akis

tan.

Car

bon

isot

opes

ofto

oth

enam

elof

foss

ilhe

rbiv

ore

mam

mal

sL

ate

Mio

cene

–ear

lyP

lioc

ene

Cer

ling

etal

.(1

998)

C4

Pak

ista

n.C

arbo

nis

otop

esof

toot

hen

amel

offo

ssil

herb

ivor

em

amm

als (con

tinu

ed)


Tab

le11

.3(c

onti

nued

)

Fir

stap

pear

ance

Exp

ansi

onR

efer

ence

C3/C

4C

omm

ent

Thr

eeba

sic

epis

odes

ofec

osys

tem

deve

lopm

ent

(see

com

men

t)

Wan

get

al.

(200

6)N

otsp

ecifi

edC

hina

.L

oess

Pla

teau

.P

aleo

paly

nolo

gy.

Lat

eM

ioce

ne(6

.2–5

.8M

a)–s

tepp

e,la

teM

ioce

ne–e

arly

Pli

ocen

e(5

.8–

4.2

Ma)

expa

nsio

nof

fore

stve

geta

tion

,ea

rly

Pli

ocen

e–la

teP

lioc

ene

(4.2

–2.4

Ma)

—st

eppe

Lat

eM

ioce

neE

arly

Pli

ocen

eQ

uade

etal

.(1

989)

C4

Pak

ista

n.P

aleo

sols

.C

arbo

nis

otop

esL

ate

Mio

cene

Ear

lyP

lioc

ene

Ret

alla

ck(1

998)

Not

spec

ified

Pak

ista

n.P

aleo

sols

Lat

eM

ioce

neM

erce

ron

etal

.(2

004)

C3

Afg

hani

stan

.T

ooth

mor

phol

ogy

offo

ssil

mam

mal

sP

lioc

ene

Pli

ocen

eD

ing

and

Yan

g(2

000)

C4

Chi

na.

Loe

ssP

late

au.

Pal

eoso

ls.

Car

bon

isot

opes

Pli

ocen

eP

lioc

ene

Wan

gan

dD

eng

(200

5)C

4C

hina

.T

ibet

anP

late

au.

Car

bon

isot

opes

ofto

oth

enam

elof

foss

ilhe

rbiv

ore

mam

mal

sP

lioc

ene–

Ple

isto

cene

Tra

vers

e(2

007)

Not

spec

ified

Pal

eopa

lyno

logy

Thr

eeep

isod

esof

herb

ecos

yste

mex

pans

ion

(see

com

men

t)

Zhi

shen

get

al.

(200

5)C

4C

hina

.L

oess

Pla

teau

.P

aleo

sols

.C

arbo

nis

otop

es.

Pli

ocen

e(2

.9–2

.7M

a),

Ple

isto

cene

(1.3

–0.9

Ma)

,P

leis

toce

ne–u

okow

ey(0

.6–0

Ma)

Sout

hA

mer

ica

Lat

eO

ligo

cene

Lat

eM

ioce

neJa

nis

etal

.(2

000,

2004

);Ja

nis(

2007

)N

otsp

ecifi

edD

iscu

ssio

nof

the

lite

rary

data

Lat

eO

ligo

cene

Lat

eM

ioce

neM

acF

adde

n(2

000)

C3

and

C4

Car

bon

isot

opes

ofto

oth

enam

elof

foss

ilhe

rbiv

ore

mam

mal

s.C

3he

rbbi

omes

befo

reex

pans

ion

ofC

4he

rbbi

omes

inth

ela

teM

ioce

ne

(con

tinu

ed)


Tab

le11

.3(c

onti

nued

)

Fir

stap

pear

ance

Exp

ansi

onR

efer

ence

C3/C

4C

omm

ent

Ear

lyM

ioce

neL

ate

Mio

cene

Mac

Fad

den

(199

7)C

3an

dC

4C

arbo

nis

otop

esof

toot

hen

amel

offo

ssil

herb

ivor

em

amm

als.

C3

herb

biom

esbe

fore

expa

nsio

nof

C4

herb

biom

esin

the

late

Mio

cene

Mid

dle

Mio

cene

–lat

eM

ioce

neL

ate

Mio

cene

–ear

lyP

lioc

ene

Kel

logg

(200

1)C

4D

iscu

ssio

nof

the

lite

rary

data

Lat

eM

ioce

neL

ate

Mio

cene

Cer

ling

etal

.(1

997)

C4

Car

bon

isot

opes

ofto

oth

enam

elof

foss

ilhe

rbiv

ore

mam

mal

sL

ate

Mio

cene

Lat

eM

ioce

neL

ator

reet

al.

(199

7)C

4A

rgen

tina

.C

arbo

nis

otop

esof

toot

hen

amel

offo

ssil

herb

ivor

em

amm

als

and

ofpa

leos

olca

rbon

ates

Lat

eM

ioce

neM

acF

adde

net

al.

(199

6)C

4A

rgen

tina

.C

arbo

nis

otop

esof

toot

hen

amel

offo

ssil

herb

ivor

em

amm

als

Lat

eM

ioce

ne–e

arly

Pli

ocen

eC

erli

nget

al.

(199

8)C

4C

arbo

nis

otop

esof

toot

hen

amel

offo

ssil

herb

ivor

em

amm

als

Afr

ica

Oli

goce

neO

ligo

cene

Bre

denk

amp

etal

.(2

002)

Not

spec

ified

Dis

cuss

ion

ofth

eli

tera

ryda

taE

arly

Mio

cene

Lat

eM

ioce

neR

etal

lack

(199

8,20

01)

Not

spec

ified

Eas

tA

fric

a.K

enya

.P

aleo

sols

Ear

lyM

ioce

neC

oppe

nsan

dP

ickf

ord

(200

2)N

otsp

ecifi

edE

ast

Afr

ica.

Uga

nda.

Pal

eobo

tany

Mid

dle

Mio

cene

Lat

eM

ioce

neM

orga

net

al.

(199

4)C

4E

ast

Afr

ica.

Ken

ya.

Car

bon

isot

opes

ofto

oth

enam

elof

foss

ilhe

rbiv

ore

mam

mal

sM

iddl

eM

ioce

neL

ate

Mio

cene

Jaco

bs(2

004)

C4

Tro

pica

lAfr

ica

sava

nna.

Pal

eopa

lyno

logy

and

carb

onis

otop

esM

iddl

eM

ioce

neL

ate

Mio

cene

–ear

lyP

lioc

ene

Jani

set

al.

(200

0,20

04);

Jani

s(2

007)

Not

spec

ified

Dis

cuss

ion

ofth

eli

tera

ryda

ta

(con

tinu

ed)


Tab

le11

.3(c

onti

nued

)

Fir

stap

pear

ance

Exp

ansi

onR

efer

ence

C3/C

4C

omm

ent

Mid

dle

Mio

cene

Ret

alla

cket

al.

(199

0);

Dug

asan

dR

etal

lack

(199

3);

Ret

alla

ck(1

992)

Not

spec

ified

Eas

tA

fric

a.K

enya

.P

aleo

sols

,ph

ytol

iths

Mid

dle

Mio

cene

–lat

eM

ioce

neL

ate

Mio

cene

–ear

lyP

lioc

ene

Kel

logg

(200

1)C

4D

iscu

ssio

nof

the

lite

rary

data

Lat

eM

ioce

neL

ate

Mio

cene

Cer

ling

etal

.(1

997)

C4

Car

bon

isot

opes

ofto

oth

enam

elof

foss

ilhe

rbiv

ore

mam

mal

sL

ate

Mio

cene

Ple

isto

cene

Bob

e(2

006)

C4

Eas

tA

fric

a.P

aleo

bota

nyL

ate

Mio

cene

Cer

ling

etal

.(2

005)

C4

Eas

tA

fric

a.C

arbo

nis

otop

esof

toot

hen

amel

offo

ssil

herb

ivor

em

amm

als

Lat

eM

ioce

ne–e

arly

Pli

ocen

eC

erli

nget

al.

(199

8)C

4E

ast

Afr

ica.

Ken

ya.

Car

bon

isot

opes

ofto

oth

enam

elof

foss

ilhe

rbiv

ore

mam

mal

sP

lioc

ene,

Ple

isto

cene

Bob

ean

dB

ehre

nsm

eyer

(200

4)C

4E

ast

Afr

ica.

Too

thm

orph

olog

yof

foss

ilm

amm

als

Pli

ocen

eP

lioc

ene

Ség

alen

etal

.(2

006)

C4

Sou

thW

est

Afr

ica,

Nam

ib.

Car

bon

and

oxyg

enis

otop

esin

foss

ilan

dm

oder

nra

tite

eggs

hell

sA

ustr

alia

Mid

dle

Mio

cene

Lat

eM

ioce

neJo

nes

(199

9)N

otsp

ecifi

edD

iscu

ssio

nof

the

lite

rary

data

Lat

eM

ioce

ne–e

arly

Pli

ocen

eJa

nis

etal

.(2

000,

2004

);Ja

nis

(200

7)N

otsp

ecifi

edD

iscu

ssio

nof

the

lite

rary

data

Wit

hout

indi

cati

ngof

cont

inen

ts

Eoc

ene–

Oli

goce

neL

ate

Mio

cene

Woo

dwar

det

al.

(200

4)C

3D

iscu

ssio

nof

the

lite

rary

data

Ear

lyO

ligo

cene

(des

ert

herb

ecos

yste

ms)

Lat

eM

ioce

neR

etal

lack

(200

1)N

otsp

ecifi

edP

aleo

sols

.Gen

eral

izat

ion

byth

eau

thor

ofhi

sow

nin

vest

igat

ions

ondi

ffer

ent

cont

inen

ts

(con

tinu

ed)


Tab

le11

.3(c

onti

nued

)

Fir

stap

pear

ance

Exp

ansi

onR

efer

ence

C3/C

4C

omm

ent

Oli

goce

neL

ate

Mio

cene

Sag

e(2

005)

C4

Dis

cuss

ion

ofth

eli

tera

ryda

taM

iddl

eM

ioce

neL

ate

Mio

cene

Jaco

bset

al.

(199

9)C

4D

iscu

ssio

nof

the

lite

rary

isot

ope

data

(Nor

ther

nan

dS

outh

ern

Am

eric

as,

Eas

tA

fric

a,P

akis

tan)

Lat

eM

ioce

neB

ond

etal

.(2

005)

C4

Dis

cuss

ion

ofth

eli

tera

ryda

taL

ate

Mio

cene

–ear

lyP

lioc

ene

Cer

ling

etal

.(1

993)

C4

Dis

cuss

ion

ofth

eli

tera

ryda

taL

ate

Mio

cene

Ehl

erin

ger

etal

.(2

002)

C4

Dis

cuss

ion

ofth

eli

tera

ryda

taL

ate

Mio

cene

Ehl

erin

ger

(200

5)C

4D

iscu

ssio

nof

the

lite

rary

data

.S

ynch

rono

usex

pans

ion

onal

lco

ntin

ents

Lat

eM

ioce

neK

eele

yan

dR

unde

l(2

005)

C4

Pal

eoso

lsE

arly

Mio

cene

Kid

der

and

Gie

rlow

ski-

Kor

desc

h(2

005)

Not

spec

ified

Non

mar

ine

diat

omac

eous

sedi

men

ts

Lat

eM

ioce

neK

och

(199

8)C

4D

iscu

ssio

nof

the

lite

rary

isot

ope

data

Ear

lyM

ioce

ne(s

hort

-gra

sspr

airi

e)

Lat

eM

ioce

neR

etal

lack

(200

1)N

otsp

ecifi

edP

aleo

sols

.Gen

eral

izat

ion

byth

eau

thor

ofhi

sow

nin

vest

igat

ions

ondi

ffer

ent

cont

inen

tsSu

mm

ary

C3

C4

Con

tine

ntA

ppea

ranc

eE

xpan

sion

App

eara

nce

Exp

ansi

on

Eur

asia

Ear

lyM

ioce

neL

ate

Mio

cene

Mid

dle

Mio

cene

Lat

eM

ioce

neN

orth

Am

eric

aE

arly

Oli

goce

neL

ate

Oli

goce

neor

earl

yM

ioce

neE

arly

Mio

cene

Lat

eM

ioce

neS

outh

Am

eric

aL

ate

Oli

goce

neL

ate

Mio

cene

Lat

eO

ligo

cene

Lat

eM

ioce

neA

fric

aN

oda

taN

oda

taM

iddl

eM

ioce

neL

ate

Mio

cene

Aus

tral

iaM

iddl

eM

ioce

neL

ate

Mio

cene

Mid

dle

Mio

cene

Lat

eM

ioce

neT

heea

rlie

stes

tim

atio

nsfo

ral

lco

ntin

ents

Ear

lyO

ligo

cene

Lat

eO

ligo

cene

orea

rly

Mio

cene

Lat

eO

ligo

cene

Lat

eM

ioce

ne


Earth aridization, on the other hand. Herbs structural and functional changes weresuch that correspond to mesoxeromorphic and even xeromorphic plant organiza-tion: representatives of these ones had a low water evaporation rate (Fig. 11.1a),lower water content (Fig. 11.1b) of the leaves, denser mesophyll (Fig. 11.1c), andstronger water saturation deficit (Fig. 11.1d).

During Oligocene still there were no open grassland ecosystems similar modernones (see Table 11.3). In the early Oligocene of North America only firstappearance of desert herbs ecosystems (which landscape domination neverthelesswas not fixed) was pointed out (Retallack 1997, 2004; see also: Strömberg 2002,2004, 2005).

11.3.3 Miocene–Holocene

In the late Oligocene, climatic cooling was replaced by warming, but only for ashort time. In the early Miocene, the trend toward cooling became predominantagain (Zachos et al. 2001). It was interrupted by a mid-Miocene (17–14 Ma)climate optimum (see for example Shevenell et al. 2004), which became the lastone during the Cenozoic era. The structural and functional characteristics of plantsbegan changing toward mesomorphic organization again; however, this trendstopped soon. Another cooling, which began 14 Ma ago (Shevenell et al. 2004)(and continues until now), restored the structural and functional characteristicstypical of the Oligocene (Figs. 11.1 and 11.2).

Analyses have demonstrated that the time trends of the characters of plantleaves structure and water relations entirely corresponds to the simultaneousdirections of global climatic and hydrological changes (Fig. 11.2). Two obviousassumptions if the found parallels do not turn out artefacts are arising.

The first assumption that taxon (species or genus) once having appeared with acertain set of properties (or with certain norms of reactions and limits of a variationof structural and functional characters), keeps this set invariable throughout all itshistory. Considerable changes of the structural and functional organization can beconnected only with the origin of a new taxon. Perhaps, the invariance of themorphological organization of a taxon (it is base of morphological taxonomy) alsogo with an invariance of its structural and functional organization (Gamalei et al.2008). Otherwise, it would be impossible to explain why taxon-specific charactersso precisely reflect the specificity of the epoch when the given taxon was formed.The constant characters of each taxon in the varying environment explain thevariability of their geographic ranges, which reflects the pattern of subsequentdevelopment of the ecological niche where the taxon has been formed.

The second assumption that process of adaptogenesis is possible only in time oforigination and formation of a new taxon follows from the first assumption. Whenall characters have formed an equilibrium system, the taxon has been formed andadaptogenesis is completed. The further adaptive possibilities of it taxon (in timesof areal expansions or migrations) are limited by system developed in process of


adaptogenesis structural and functional properties. They are not related to addi-tional adaptive transformations (otherwise, a new taxon appears). The maximumpermissible quantitative deviations are those that do not disturb systemic rela-tionships between characters. There is a variety of the ways and mechanisms ofmigration. An intrazonal network is one of them.

11.4 Origin and Expansion of Grassland Biomes

There are definitions of biomes as large clusters of plant species that are charac-terized by the same life-form, whereas traditional definitions of biomes have alsoincluded either geographic or climatic descriptors (Woodward et al. 2004). In thefirst case, only two herbs biomes are discovering-savanna (mainly tropical her-baceous vegetation with woody canopy up to 30 %) and grassland (mainly tem-perate herbaceous vegetation with woody or/and shrubby canopy less than 10 %)(Woodward et al. 2004). On the other hand, in one of the traditional classificationthere are 14 biomes and 4 biomes of grassy vegetation between them are finding(Olson et al. 2001).

Tropical herbaceous biome is constituted by South American (llanos inVenezuela and Colombia, cerrado in Brazil), African savannas and Australiangrasslands (Allaby, 2006). Temperate grassland biome is constituted by Eurasiansteppes, North American prairies, South American pampas and Patagonian steppe,South African veld (Walter 1985).

By mode of carbon dioxide assimilation all herbs on two major groups aredivided: species with C3 and C4 photosynthesis.

Group of C3 herbs has been compelled to adapt for cold conditions. Thisadaptation were transferring an efflux of an assimilates into apoplast pathway andthan to guard a photosynthesis against suppression by cold because of effluxabsence into symplast pathway (Gamalei 2004; Gamalei et al. 2008). The coldcaused rigidity of actomyosin cytoskeleton, blocking development of plasmodes-mata and symplast. Barrier properties of a tonoplast have been as a result brokenand assimilates began to exude into apoplast. Gathering and return of assimilatesinto symplast—function of specialized «transfer cells». This function compensatesan absence of plasmodesmata and symplast pathway between mesophyll andphloem. Thus, perhaps in the late Eocene–early Oligocene was originated a groupof apoplast dicotyledonous (approximately 20,000 species from 21 families),which test sign-transfer cells (Gamalei 2004).

C4 herbs do not have transfer cells. They test sign-Kranz anatomy and plastiddimorphism. About 7,000 C4 species from 18 families are counted. This groupwas formed at the same time or a bit later (perhaps in the Oligocene, see Tippleand Pagani 2007), but in another climatic zone and in another composition oflimiting conditions of photosynthesis. In this composition an aridity, high tem-perature, and related salinization rather than cold dominates than xylem transportsuppresses and promotes to stomata closing. In the Cenozoic Era the CO2


concentration in the atmosphere is gradually decreasing (Berner 2006) than pho-tosynthesis sharply limits in such conditions. Dysfunction of stomata apparatus ofleaves still more strengthens carbon dioxide starvation. Mechanisms of CO2

concentration inside leaves became necessary. Kranz anatomy and cooperativephotosynthesis (inside 1 or 2 cells, see Voznesenskaya et al. 2006) have been as aresult generated. These characters for apoplastic halophytes and xerophytes arepeculiar. These plants reacted to the factor of CO2 concentration decrease becauseit was combined with not less stressful factors for photosynthesis such as waterdeficit and salinization. Closed stomata because of water deficiency—strong bar-rier to influx of carbon dioxide into the leaves (under whatever CO2 concentrationin the atmosphere).

Stomata apparatus—attribute of xylem transport, its functioning is subordinatedto it in a greater degree, than to photosynthesis. Stomata closing during the hotperiod of day is supervised by water relations and is inevitable reaction to envi-ronment water deficit. Therefore, the climate aridization which peaked in theOligocene and has led to occurrence of hot plains with a high aridity index couldbe the climatic factor that led to origination of C4 herbs. Sometimes C4 species canbe met in other conditions, but these are isolated instances which become at oncesubjects of special publications (see Gamalei et al. 1992). Distribution of C4

photosynthesis mainly in tropics (Ehleringer 2005)—argument that aridity factor ismore important for origination and formation of C4 syndrome. If the reason wasdecrease of carbon dioxide in atmosphere, C4 syndrome undoubtedly became thegeneral property of all land plants. Parallel and independent occurrence of C4

photosynthesis in several families (Kellogg 1998) does not leave doubt that C4

photosynthesis is one of the manifestations of arid adaptogenesis.Thus, approximately at the same time on last big wave of taxonogenesis

two phylogenetic branches of herbs are originated, one (C3) as the answer to aclimate cooling, another (C4) as the answer to climate aridization. Cold openplains (meadows, steppes, tundra, high mountains) occupy C3 species, hot and dryhabitats (savannas, saline soils, deserts) inhabit C4 species.

There are assumptions that origination of C4 photosynthesis occurred in theOligocene (25–33 million years ago) (Kellogg 1998; Sage 2003, 2005, and others),and its wide expansion took place in a late Miocene, 5–7 million years ago (seeTable 11.3). C4 herbs, especially grasses, extend within tropics in grasslandbiomes of Northern and Southern Americas, Africa, Australia (Kovalev 2000;Kellogg 2001). These are plants with pronounced adaptive possibilities and highrates of photosynthesis and growth (Gamalei et al. 1992). In the modern worldwhere C4 taxa are presented less than 2 % of higher plant species, their contri-bution to global primary production constitutes about 25 % (Still et al. 2003;Ehleringer 2005). Approximately, half of 10,000 species of grasses and sedgeshave C4 photosynthesis, whereas among about 2,000 dicotyledonous species thisway of a metabolism is fixed (Ehleringer et al. 2002).

Occurrence of temperate herbs biomes with C3 photosynthesis took place in themiddle or late Eocene or early Oligocene (Zherikhin 1994; Retallack 1997, 2001;Jacobs et al. 1999; Bredenkamp et al. 2002) (Table 11.3). Wide expansion of these


biomes began in the early Miocene (Retallack 1997, 2001, 2004; Jacobs et al.1999; Willis and McElwain 2002) and was combined with intensive radiation ofgrazing mammalian herbivores (Zherikhin 1994; Cerling et al. 1998; Janis et al.2000, 2004; Kemp 2005; MacFadden 2005; Janis 2007) (Table 11.3).

Tropical and paratropical megathermal rainforests that covered more than 50 %of continents in the late Paleocene–early Eocene (Morley 2007), in the modernworld almost completely are replaced by herbaceous vegetation (Ehleringer 2005).Replacement of forests by herbaceous vegetation was probably not unidirectional,but, as shown in a number of works, proceeded by pulsations (Zhisheng et al.2005; Wang et al. 2006). Such replacement could result from increasing of cli-matic zonality and global cooling (Willis and McElwain 2002), destruction offorests by fires (Bond et al. 2005), changes of carbon dioxide concentration inatmosphere (Ehleringer et al. 2002). This tendency becomes stronger as conse-quence of anthropogenic influence.

11.5 Conclusion

Results of the analytical research have shown that dynamics of leaves structure andwater relations of plants corresponds to conceptions about global climate changesand a planet hydrology.

Taxonomical diversity of herbs and herbaceous biomes is the function ofpaleoclimate variability and plant adaptogenesis to it. Two global trends of eco-logical evolution contrast differing by the composition of herbaceous adaptivetypes is the next: (a) the line of herbs of chilling plains with domination the groupof plant species with C3 apoplastic syndrome formed under cold climate influence,and (b) the line of herbs of hot plains with domination of plant species with C4

apoplastic syndrome.Both trends include the monocots and dicots, and both are the results of climate

changes in Cenozoic. C3 herbs of chilling plains and the steppe and meadowphytocoenosis formed by them arise as the answer to temperature decrease in greatareas of high latitudes. The apoplastic syndrome (transfer from symplastic trans-port of assimilates supressed by cold to their apoplastic transport) is the diagnostictest for this group of herbs. C4 herbs of hot plains and the savanna, desert andsolontchak plant vegetation are the adaptive answer to aridization of low latitudeareas. C4 syndrome (compensation of stomata closure by the mechanism of CO2

concentration in the leaf tissues) is a special sign of this group of herbs.Formation of these adaptive types and expansion of the biomes formed by them

occurred almost simultaneously. Both groups derived from primitive apoplasticherbs. Both groups have appeared in the Oligocene which is characterized byclimate cooling and aridization, as a result they are separated territorially. The firstgroup acclimatized to conditions of cold open territories and obtained adaptivefeatures corresponding to the cold environment (transfer cells that compensateabsence of plasmodesmata). The second group adapted for the arid and salted open


spaces with excess of heat and water deficit, that compel stomata be closed in theafternoon and accordingly to get special mechanisms of supplying carbon dioxide(carbon dioxide concentrating—C4 syndrome, or its time deposition—CAM).

Problem of the first—how to provide efflux of an assimilates in cold temperatureconditions at which symplastic transport is impossible. The problem of the second—how to provide photosynthesis by CO2 in hot conditions when stomata is closed andwhen xylem transport is suppressed. For overcoming both problems adaptivemechanisms were discovered but in different groups of taxa. Physiologically, thesemechanisms are incompatible, alternative; and taxonomically these groups of theherbs which have acclimatized to conditions of cold and hot plains are separated.

Both types of herbs biomes began to replace the forest biomes whose areal inthe late Paleogene–Neogene began to reduce both in low and in high latitudes.This tendency, probably, proceeds in parallel with the climatic tendency ofaridization and cooling of continents.

Constancy of taxa characters in combination with inconstancy of climate—thereason of areal mobility. Territorial niche drifts which are connected with globaland local variability of a climate explain migration of taxa after completion offormation period. There is a variety of the ways and mechanisms of migration. Anintrazonal network is one of them.

Acknowledgments Funding for this work was provided by a grant from the Russian Foundationfor Basic Research (10-04-01165-a). We would like to thank Pierre Pontarotti and Marie-HélèneRome for the invitation to contribute to the 15th evolutionary biology meeting at Marseille wherethis work was presented.

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