Ecological Research

(2002)

17,

705–716

Blackwell Science, LtdOxford, UKERE

Ecological Research0912-38142002 Ecological Society of Japan

176November 2002

527Clonal plants and species diversity

M. Song et al.

10.1046/j.0912-3814.2002.00527.x

Original Article705716BEES SGML

*Author to whom correspondence should beaddressed. Email: dongming@95777.com

Received 8 August 2001. Accepted 22 May 2002.

Importance of clonal plants and plant species diversity in the Northeast China Transect

M

INGHUA

S

ONG

,

M

ING

D

ONG

*

AND

G

AOMING

J

IANG

Laboratory of Quantitative Vegetation Ecology, Institute of Botany, The Chinese Academy of Sciences, Beijing 100093, China

In plant communities, the internal (genet-level) control mechanisms on a spatio-temporal scale ofclonal plants impose strong constraints on spatial pattern as well as on competitive relations and,thus, species coexistence. Therefore, the presence of clonal species within a plant community affectsspatio-temporal dynamics and plant species diversity. We examined the distribution of plants withdifferent clonal growth forms in the Northeast China Transect (NECT) and correlated plant speciesdiversity with the importance of clonal plants, and the importance of phalanx and guerilla clonalplants. Phalanx clonal plants were more abundant in western communities where the altitude washigher and both the soil nitrogen contents and precipitation were relatively low. Whereas guerillaclonal plants were more abundant in the middle of the NECT where the precipitation, mean annualtemperature and photosynthetically active radiation were relatively high. In the relatively productivetemperate typical steppe, plant species diversity was negatively correlated with the importance ofphalanx clonal plants and positively correlated with the importance of guerilla clonal plants. Inrelatively unproductive temperate desert steppe, plant species diversity was positively correlatedwith the importance of both phalanx and guerilla clonal plants.

Key words:

clonal growth forms; clonal plants; guerilla; habitat conditions; phalanx; plant speciesdiversity.

INTRODUCTION

Clonal growth is one of the most importantvegetative reproduction means and it can producenew genetically identical descendant (ramets) (deKroon & van Groenendael 1997). Plants usingmodes of clonal growth can be very successful andcan dominate many ecosystems (Callaghan

et al

.1992; Prach & Pysek 1994; Klimes

et al

. 1997). Theprocesses that govern clonal growth may affect thestructure, species composition (van Groenendael &de Kroon 1990a,b) and, thus, community biodiver-sity of a large part of the vegetation.

Clonality imposes strong constraints on thespatial pattern and competitive relations of plantcommunities (Herben

et al

. 1993a,b; Law

et al

.1993; Oborny & Bartha 1995). On the one hand,

clonal species have characteristics such as largeshoot systems, high storage capacities and fastvegetative spreading abilities (Begon

et al

. 1986;de Kroon & van Groenendael 1997) that make itpossible for these plants to rapidly colonize avail-able space and compete for resources and manyother plant species may be out-competed, result-ing in a marked poverty in this species-rich com-munity (Bobbink & Willems 1987; Callaghan

et al

. 1997; de Kroon & Bobbink 1997; Herben &Hara 1997). However, clonality can also constrainspecies coexistence in relation to a trade-offbetween mobility and local persistence (Oborny &Bartha 1995). Clonal plants have internal (genet-level) control mechanisms on a spatial-temporalscale, including morphological and physiologicalplasticity, density-dependent controls on meristemactivity, physiological integration, regulation inthe timing of shoot birth, vegetative growth andsexual reproduction regulation, which alleviateclone competition and facilitate species coexist-ence (de Kroon 1993; Dong & de Kroon 1994;Oborny & Bartha 1995). Therefore, the presence

706 M. Song

et al

.

of clonal species in a plant community widens thepotential mechanisms for community organization(Oborny & Bartha 1995; Herben & Hara 1997).

The architecture of clonal plants may alsostrongly affect community species diversity(Herben & Hara 1997). The occurrence of dif-ferent growth strategies may contribute not onlyto the competitive balance, but also to irreversiblechanges in a multispecies plant community(Winkler & Schmid 1995). Guerilla clones tend toshow either a foraging strategy (wander by runnersselectively through the habitat and establishramets predominantly in high quality patches) ora conservative strategy (restrict clonal proliferationunder resource deprivation), while phalanx clonestend to have a consolidation strategy (promotethe local persistence of the clone) (Harper 1985;Callaghan 1988; de Kroon & Knops 1990; deKroon & Schieving 1990). In guerilla-strategyclones, loosely aggregated ramets increase thechance of encountering neighbors that belong toanother species. In phalanx-strategy clones, thetightly aggregated ramets increase the frequencyof intraclonal contacts (Lovett Doust 1981;Schmid & Harper 1985). Therefore, clonal plantswith different growth forms may have different‘species combination’ abilities within a plant com-munity. Moreover, density regulation mechanismsdiffer among phalanx and guerilla species (Schmid& Harper 1985). Phalanx plants were superior inhomogeneous and densely populated habitats(Dietz & Steinlein 2001) and appear to be betteradapted to stressful conditions under intense com-petition (Humphrey & Pyke 1998). The extremelyhigh ramet density in a phalanx species can pre-vent seedling establishment by the same speciesor by another species, resulting in monodomi-nant patches within the community (Cook 1985;Silander 1985). However, the guerilla-type plantsare favored under spatially heterogeneous dis-turbed habitats (Dietz & Steinlein 2001) becausethey have the ability to colonize gaps and invadeopen space, and tend to produce a fine-scale mix-ture of species. Therefore, plants with differentclonal growth forms may exert a different influenceon the plant species diversity within a community.

Distribution of clonal species strongly dependson habitat conditions (Herben & Hara 1997).Clonal plants are present in some of the most

species-rich communities in the world and are alsofound in areas of very low productivity (Kull &Zobel 1991; Willems

et al

. 1993; de Kroon &Bobbink 1997; Grace & Pugesek 1997). The pio-neering model of Bell (1984) and a cellular autom-aton model showed that the interaction betweenguerilla and phalanx species was different underdifferent habitat conditions, resulting in differentcommunity spatial patterns (Bell 1984; Winkler& Schmid 1995; Herben & Hara 1997). Underproductive conditions, competitive relations inclone communities are likely to be hierarchical(transitive), which usually results in a clonal spe-cies monodominant stand. Whereas under lessproductive conditions, non-transitivity in compet-itive relations promotes species coexistence and, inthe long run, increases diversity (Hara 1994).

Spatio-temporal dynamics and species coexist-ence in plant communities dominated by clonalplants appear to be determined by a combinationof clonal architecture, ramet-level interactions andhabitat conditions (stress and disturbance) (Dietz& Steinlein 2001). The present investigation aimsto: (i) describe the distribution of clonal plants,including phalanx and guerilla clonal plants, alongthe Northeast China Transect (NECT); and (ii) tounderstand the relationship between the impor-tance of clonal plants and plant species diversitywithin plant communities.

METHODS

Study areas

Investigations were conducted along the NECT.The NECT is a transect designated by the GlobalChange and Terrestrial Ecosystem Program(GCTE) and recognized by the InternationalGeographical and Biological Plan (IGBP) as one ofthe major global transects (GCTE Core ProjectOffice 1994). The transect extends from thenorthern Changbai Mountains of Jilin Provincethrough the Songliao Plain to the plateau of InnerMongolia, China (112

∞-

130

∞

30

¢

E and 43

∞

30

¢-

44

∞

30

¢

N). Altitudes range from 120 m to1700 m. From east to west, there are decreasinggradients of precipitation and temperature as wellas variations in the plant communities and soilnitrogen contents and photosynthetically active

Clonal plants and species diversity 707

radiation (PAR) in the herbaceous layers wheremost of the clonal plants grow (Zhang

et al

. 1997;Jiang

et al

. 1999). Six types of plant communitiesfrom east to west in NECT have been distin-guished as follows (Jiang

et al

. 1999).

1 Montane temperate coniferous-broad-leavedmixed forest (dominated by

Pinus koraiensis

Sieb. et Zucc. and

Abies fabri

(Most.) Craib; therepresentative clonal species were

Carex pedifor-mis

L.,

Cardamine schulziana

Baehne.,

Thalictrumtuberiferum

Maxim. and

Gymnocarpium jessoense

(Koidz.) Koidz.).2 Temperate deciduous-broad-leaved forest

(dominated by

Quercus mongolica

Fisch. and

Juglans mandshurica

Maxim.; the representativeclonal species were

Iris uniflora

Pall. ex Link,

Carex planiculmis

Kom.,

Pteridium aquilinum

(L)Kuhn and

Diarrhena manshurica

Maxim).3 Temperate forest-steppe ecotone (mostly culti-

vated with wheat, corn and soybean, etc.; therepresentative clonal species were

Pteridiumaquilinum

(L) Kuhn. var.

latiusculum

(L),

Puc-cinellia tenuiflora

(Griseb.) Scrib. et Merr.,

Saus-surea amara

DC.,

Leymus chinensis

(Trin.) Tzvel.,

Carex enervis

C.A. May and

Phragmites australis

(Clav.) Trin.).4 Temperate meadow steppe (dominated by

Poten-tilla

spp.; the representative clonal species were

Lespedeza dahurica

(Laxm.) Schindl.,

Cleistogenessquarrosa

(Trin.) Keng,

Arundinella hirta

(Thunb.) Raddi and

Potentilla acaulis

(L)).5 Temperate typical steppe (dominated by

Aneurolepidium chinense

(Trin.) Kitag.,

Stipabaicalensis

Roshev.,

Stipa grandis

P. Smirn. and

Stipa krylovii

Roshev.; the representative clonalspecies were

Potentilla acaulis

L.,

Artemisiafrigida

Willd.,

Koeleria cristata

L., Festuca ovinaL., Cleistogenes squarrosa (Trin.) Keng,

Leymuschinensis

L., Agropyron cristatum (L) Gaertn.,

Stipa grandis

P. Smirn.,

Stipa Krylovii

Roshev.,

Carex duriuscula

C.A. Mey.,

Allium tenuissimum

L.,

Allium polyrrhizum

Turcz. and

Asparagus dau-ricus

Fisch. ex Link).6 Temperate desert steppe (dominated by

Car-agana microphylla

Lam.,

Artemisia frigida

Willd.and

Neopallasia pectinata

(Pall.) Poljak.; therepresentative clonal species were

Stipa gobica

Roshev.,

Cleistogenes songgorica

(Roschev.) Ohwi,

Leymus secalinum

(Georgi) Kitag,

Allium mongoli-cum

Regel and

Artemisia frigida

Willd.).

Field investigation

The field investigation was conducted from 14July to 1 August 1997. Measurements werestarted at the eastern end and ended at the westernend of the NECT. The geographic position of everyinvestigation site was recorded using a MagllaGPS Field PRO VTM (Garmin, Kansas, USA).Twenty-nine study sites were chosen along theNECT. The distance between any two adjacentinvestigation sites was 49 km. In the forest com-munities, plants in the tree layer (the top layer ofa forest community, where only tree species arefound), the shrub layer (the second highest layerof a forest community, where only woody speciesare found) and the herb layer (the lowest layer ofa forest community, where herbaceous species arefound) were sampled using quadrats measuring20 m

¥

30 m, 2 m

¥

2 m and 1 m

¥

1 m, respec-tively. In the herbaceous communities, theplants were sampled using quadrats measuring1 m

¥

1 m. There were six replicate quadrats foreach of the quadrat types at each investigation site.The number of species (species richness) in eachquadrat was recorded. Plant height and plant coverwere also measured. Species frequencies wereevaluated using the replicate quadrats and another10 samples from the same vegetation type, in orderto deal with heterogeneity within the habitats. Wecollected climatic data from 110 weather stationson the NECT. The range of soil nitrogen contentswas taken from Zhu and Wen (1990) according tothe soil types. The mean values of soil nitrogencontents of different soil types were used to evalu-ate the soil nitrogen contents of each investigationsite.

Plant growth forms

Information on clonal growth mostly came fromexcavation and observation, and other informationwas extracted from

Floras of China

(The EditoralCommittee of Flora of China of the Chinese Acad-emy of Sciences 1979–99), Chen (1987),

Sketchesand Descriptive Features of High Plants in China

(Institute of Botany, Chinese Academy of Sciences

708 M. Song

et al

.

1974) and de Kroon & van Groenendael (1997).Clonal species with different abilities of horizontaldispersal, that is, those corresponding to theguerilla or phalanx type of growth (Lovett Doust1981; Begon

et al

. 1986), were evaluated. Plantswith relatively long internode or rhizome lengthsand a strong tendency to continue in the previousdirection of growth with little branching wereclassified as guerilla clonal plants. These plantscan spread rapidly and are capable of producingvegetative offspring at a distance of 0.5 m or moreduring 1 year and of forming a nearly linear chainof widely spread daughter ramets, includingrhizomatous and stoloniferous ramets. Plantswith comparatively short internode or rhizomelengths and non-directionality were considered tobe phalanx clonal plants. These plants usuallyspread slowly and formed roughly circular clones,including bulbous, tuberous, earthnut, tilleringand spouting clones (Lovett Doust 1981; Leakey1981; Bell 1984; Harper 1985; Sackville-Hamilton

et al

. 1987; Cowie

et al

. 1995).

Data analysis

For each species, relative frequency (RF), relativeheight (RH) and relative cover (RC) were derivedfrom the plant frequency, plant height and plantcover of each species. Relative importance (RI

i

)of the

ith

species was calculated by dividingthe sum of RF, RH and RC of the

ith

speciesby three. Shannon–Wiener index (H

iv

), a mea-surement of plant species diversity of commu-nity, was determined for each of the communitiesbased on the relative importance of each species:H

iv

= S

Rii ln(RIi) (Barbour et al. 2001). Mean-while, cover of the herbaceous layer, species rich-ness and the relative importance of clonal plants,as well as guerilla and phalanx clonal plants, werecalculated.

Along the NECT from east to west, the six typesof plant communities were grouped into: (i)natural forest communities including the montanetemperate coniferous broad-leaved mixed forestand the temperate deciduous broad-leaved forest;(ii) semi-natural herbaceous communities includ-ing the temperate forest-steppe ecotone and thetemperate meadow steppe; and (iii) natural herba-ceous communities including the temperate typi-cal steppe and the temperate desert steppe. Few

clonal tree species occurred along the NECT, thusalmost all clonal plants grew in the herbaceouslayer, with a few occurring in the shrub layer (Songet al. 2001). In the natural forest communities, theundergrowth of the montane temperate coniferousbroad-leaved mixed forest and the temperatedeciduous broad-leaved forest received relativelylow PAR and was a less productive habitat forspecies growing in the herbaceous layer, wheremost of the clonal plants occurred (Table 1). In thesemi-natural herbaceous communities, the tem-perate forest-steppe ecotone possesses higher soilnitrogen content and is a more productive habitatfor clonal plants than the temperate meadowsteppe. In the natural herbaceous communities,the temperate typical steppe possesses highercumulative temperature (>10∞C), higher meanannual temperature, higher precipitation andhigher soil nitrogen content than the temperatedesert steppe. Therefore, the temperate typicalsteppe is a more productive habitat for clonalplants. Characteristics of the communities, such asspecies richness, plant cover in the herbaceouslayer and Shannon–Wiener index were correlatedwith distance to the east end of the NECT. A one-way ANOVA was used to compare the difference inenvironment factors and plant cover in the herba-ceous layers between the six communities. Step-wise regression was used to discover the relativeimportance of plant species with different clonalgrowth forms to habitat conditions along theNECT. Variables such as the relative importancevalue of plants with different growth forms, alti-tude, mean annual temperature, annual precipita-tion, soil nitrogen content and photosyntheticallyactive radiation, whose distributions were not nor-mal, were log transformed. The log-transformedrelative importance of plants with different growthforms was related to the log-transformed values ofenvironment factors (altitude, mean annual tem-perature, annual precipitation, soil nitrogen con-tent and photosynthetically active radiation) usinga stepwise regression. Using diagnosis of multi-collinearity and homoscedasticity among vari-ables, we determined the regression equations aftereliminating insignificant factors. Rank correlationanalysis was used to analyze the relationshipbetween the Shannon–Wiener index and the rela-tive importance of plant species with differentclonal growth forms.

Clonal plants and species diversity 709T

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T),

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n an

nual

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pera

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(∞C

); (P

), an

nual

pre

cipi

tati

on (

mm

); (N

), to

tal

nitr

ogen

ous

cont

ent

in s

oil

(%);

(PA

R),

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osyn

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ical

ly a

ctiv

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diat

ion

on t

he fl

oor

( mm

olm

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S),

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tane

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k br

own

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GB

S),

Mon

tane

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y br

own

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E),

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n ea

rth;

(D

MS)

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rk m

eado

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(CS)

, che

stnu

t so

il; (

BS)

, bro

wn

soil

; (M

TC

BM

F), M

onta

ne t

empe

rate

con

ifer

ous-

broa

d-le

afed

mix

ed fo

rest

; (T

DB

F), t

empe

rate

dec

iduo

us-b

road

-lea

fed

fore

st;

(TFS

E),

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pera

te f

ores

t-st

eppe

eco

tone

; (T

MS)

, te

mpe

rate

mea

dow

ste

ppe;

(T

TS)

, te

mpe

rate

typ

ical

ste

ppe;

(T

DS)

, te

mpe

rate

des

ert

step

pe.

710 M. Song et al.

RESULTS

Distribution of community characters along the Northeast China Transect

Along the NECT, species richness, plant cover inthe herbaceous layer and the Shannon–Wienerindex varied greatly (Fig. 1). Species richness washighest in the temperate typical steppe where itabruptly increased up to a peak value and thendecreased rapidly (Fig. 1a). Plant cover in the her-baceous layer was low in the montane temperateconiferous broad-leaved mixed forest and the tem-perate deciduous broad-leaved forest. Plant coverwas higher in the temperate forest-steppe ecotone

than in the temperate meadow steppe, and washigher in the temperate typical steppe than inthe temperate desert steppe (Table 2), showing asimilar correlation to the productivity of thecommunities.

Relationship between the relative importance of plant species with different growth forms to habitat conditions

The relative importance of clonal plants and non-clonal plants as well as of guerilla and phalanxclonal plants was significantly related to habitatconditions (Table 3). Clonal plants and non-clonalplants respond to environmental factors differ-ently. The relative importance of clonal plants waspositively related to altitude and PAR, whereas itwas negatively related to total soil nitrogen con-tent (Table 3). Relative importance of non-clonalplants was negatively related to altitude and PARand positively related to total soil nitrogen content(Table 3). When phalanx or guerilla clonal plantswere considered separately, they differed in theirresponse to environmental factors. The relativeimportance of phalanx clonal plants was positivelyrelated to altitude and negatively related toannual precipitation and total soil nitrogen con-tent. When only guerilla clonal plants were con-sidered, relative importance was positively relatedto annual precipitation and PAR (Table 3).

Relationship of plant species diversity to the importance of clonal plants

In the montane temperate coniferous broad-leavedmixed forest and the temperate deciduous broad-leaved forest, the Shannon–Wiener index was lin-early positively correlated to the relative impor-tance of all clonal plants and to phalanx clonalplants. The positive correlation between theShannon–Wiener index and the relative impor-tance of guerilla clonal plants was not significant(Fig. 2).

In the temperate forest-steppe ecotone, theShannon–Wiener index was significantly nega-tively correlated with the relative importance ofclonal plants and guerilla clonal plants. The rela-tionship between the Shannon–Wiener index andthe relative importance of phalanx clonal plantswas positive. In the temperate meadow steppe,

Fig. 1. Distribution of (a) species richness, (b) plantcover in the herbaceous layer and (c) Shannon–Wienerindex of plant communities along the Northeast ChinaTransect (NECT). (D), distance (km) from the investi-gation site to the east end of the NECT. See Table 1 forthe investigation sites and their corresponding plantcommunities.

Spe

cies

ric

hnes

s

Sha

nnon

–Wie

ner

inde

x

Pla

nt c

over

of h

erba

ceou

s la

yer

(a)

(b)

(c)

35

30

25

20

15

10

140

120

100

80

60

40

20

3.5

3

2.5

2

1.5

1

0.5

00 300 600 900 1200 1500 1800

0

5

0

D (km)

Clonal plants and species diversity 711

the Shannon–Wiener index was positively signifi-cantly correlated with the relative importance ofclonal plants as well as with phalanx clonal plants,but was not significantly correlated with guerillaclonal plants (Fig. 2).

In the temperate typical steppe, the Shannon–Wiener index was significantly negatively corre-lated with the relative importance of phalanxclonal plants and positively correlated with therelative importance of guerilla clonal plants. In thetemperate desert steppe, the Shannon–Wienerindex was significantly positively correlated withthe relative importance of clonal plants. When

only phalanx or guerilla clonal plants were consid-ered, the Shannon–Wiener index was positivelycorrelated with the relative importance of bothphalanx and guerilla clonal plants (Fig. 2).

DISCUSSION

The distribution of clonal plant species stronglydepended on habitat conditions, and clonal plantshad a different contribution to plant speciesdiversity depending on the plant community. Therelationship of plant species diversity to plant

Table 2 Comparison of environmental factors and plant cover of the herbaceous layer among the six communities

Vegetationtypes

Elevation(m)

Mean annualtemperature

(∞C)

Annualprecipitation

(mm)

Totalnitrogenous

contentin soil(N%)

Photosyntheticallyactive radiation(mmol m-2 s-1)

Plant cover in the

herbaceouslayer(%)

MTCBMF 525.00 ± 35.00a 4.40 ± 0.05bc 503.90 ± 0.80b 0.27 ± 0.01d 269.50 ± 38.5a 29.90 ± 3.72a

TDBF 380.67 ± 64.67a 4.01 ± 0.04b 554.77 ± 7.22b 0.22 ± 0.03c 307.67 ± 58.92a 34.69 ± 2.11a

TFSE 285.29 ± 54.65a 5.13 ± 0.43bc 465.80 ± 10.59b 0.43 ± 0.01e 1760.00 ± 66.48b 55.08 ± 2.14c

TMS 295.50 ± 50.87a 6.34 ± 0.11c 309.70 ± 4.08a 0.28 ± 0.05d 2012.50 ± 102.34b 45.73 ± 5.02b

TTS 1031.11 ± 45.80b 3.39 ± 0.52b 307.62 ± 4.55a 0.14 ± 0.01b 2142.22 ± 85.22b 61.68 ± 6.98c

TDS 1113.25 ± 50.62b 1.40 ± 0.09a 226.63 ± 14.25a 0.05 ± 0.00a 2180.00 ± 114.52b 29.38 ± 4.31a

(MTCBMF), The montane temperate coniferous broad-leaved mixed forest; (TDBF), the temperate broad-leaved forest; (TFSE), thetemperate forest-steppe ecotone; (TMS), the temperate meadow steppe; (TTS), the temperate typical steppe; (TDS), the temperate desertsteppe.

Different letters show significant differences at P < 0.05.

Table 3 The relationship between community characteristic values and habitat conditions

Community characteristic values Stepwise regression equations

Relative importance of clonal plants (Ic)Standardized correlation coefficient

Ic = 2.31 ¥ 10-4al - 3.64 ¥ 10-2N + 1.32-4PAR + 0.14(0.40) (-0.31) (0.38)(R2 = 0.64, P = 0.003, N = 29)

Relative importance of non-clonal plants (In)Standardized correlation coefficient

In = -2.31 ¥ 10-4al + 3.64 ¥ 10-2N - 1.32 ¥ 10-4PAR + 0.86(-0.40) (0.31) (-0.38)(R2 = 0.64, P = 0.003, N = 29)

Relative importance of phalanx clonal plants (Ip)Standardized correlation coefficient

Ip = 3.18 ¥ 10-4al - 5.03 ¥ 10-4P - 5.66 ¥ 10-2 N + 0.39(0.60) (-0.27) (-0.39)(R2 = 0.78, P = 0.0001, N = 29)

Relative importance of guerilla clonal plants (Ig)Standardized correlation coefficient

Ig = 1.02 ¥ 10-5P + 1.83 ¥ 10-4PAR - 0.48(0.73) (0.77)(R2 = 0.55, P = 0.007, N = 29)

(al), altitude (m); (P), annual precipitation (mm); (N), soil nitrogen content (%); (PAR), photosynthetically active radiation(mmol m-2 s-1); (R2), adjusted R-square; (P), significance level (P <0.05); (N), number of sample sites.

712 M. Song et al.

Fig. 2. Correlations of the Shannon–Wiener index to the relative importance of all clonal plants (Ic), the relativeimportance of phalanx clonal plants (Ip) and the relative importance of guerilla clonal plants (Ig) in (a–c) the montanetemperate coniferous broad-leaved mixed forest (MTCBMF), (d–f ) the temperate broad-leaved forest (TDBF), (g–i)the temperate forest-steppe ecotone (TFSE), (j–l) the temperate meadow steppe (TMS), (m–o) the temperate typicalsteppe (TTS) and (p–r) the temperate desert steppe (TDS).

E

Hiv = 0.87Ip + 0.94

(R 2 = 0.76,n = 14,P = 0.0001)

FD

Hiv = 0.55Ic + 3.40

(R 2= 0.30,n = 14,P = 0.043)

0

3

6

9

12

15

TD

BF

H

Hiv = 0.59Ip + 4.46(R

2 = 0.39,n = 21,P < 0.002)

I

Hiv = –0.72Ig + 18.9

(R 2 = 0.52, n = 21, P = 0.0001)

)

G

Hiv = –0.69Ic + 18.6(R

2= 0.48,n = 21,P = 0.001)

0

5

10

15

20

25

TF

SE

K

Hiv = 0.58Ip + 2.73

(R 2= 0.34,n = 12,P = 0.04)

LJ

Hiv = 0.53Ic + 3.05

(R 2 = 0.29,n = 12,P = 0.05)

0

3

6

9

12

15

TM

S

N

Hiv = –0.61Ip + 23.32

(R 2= 0.37,n = 28,P = 0.001)

O

Hiv = 0.60Ig + 5.87

(R 2 = 0.35,n = 28,P = 0.001)

M

0

6

12

18

24

30

TT

S

Q

Hiv = 0.63Ip + 2.29(R

2 = 0.46,n = 12,P = 0.015)

0 6 12 18 24 30

R

Hiv = 0.56Ig + 2.85

(R 2 = 0.31,n = 12,P = 0.05)

0 6 12 18 24 30

P

Hiv = 0.63Ic + 2.41

(R 2= 0.40,n = 12,P = 0.028)

0

3

6

9

12

15

0 6 12 18 24 30

TD

S

Ran

k of

Sha

nnon

–Wie

ner

inde

x v(

Hiv)

Rank of relative importanceof phalanx clonal plnats

Rank of relative importanceof guerilla clonal plants (Ig)

Rank of relative importance of clonal plants (Ic)

A

Hiv = 0.77IC + 1.27

(R 2 = 0.59,n = 10,P = 0.009)

0

2

4

6

8

10

12T

MC

BM

F

B

Hiv = 0. 98Ip + 0.20

(R 2 = 0.90,n = 10,P = 0.0001)

C

Clonal plants and species diversity 713

clonality was directly related to clonal growthforms and habitat conditions (de Kroon &Bobbink 1997; Grace & Pugesek 1997). In gen-eral, clonal plant species were more abundant andmore important in the western plant communities(habitats) of the NECT, where the altitude washigher and both soil nitrogen contents andprecipitation were relatively low (Song et al.2001). This preference of clonal plants confirmsthat clonal growth in plants is, in general, adaptiveunder stressful conditions (Grime 1979; Tiffney &Niklas 1985; de Kroon et al. 1992; Grace 1993).Phalanx and guerilla clonal plants differed inresponse to habitat conditions. The regressionequation reveals the strong ability of phalanxclonal plants to grow in stressful environments. Incontrast, however, the performance of guerillaclonal plants suggests that the best habitats wereplant communities allocated in the middle of theNECT, where precipitation, temperature and PARwere relatively high. The difference between thelocation of phalanx and guerilla clonal plants withrespect to optimal locations on the NECT may bedue to different strategies in utilizing resources(Harper 1985; Callaghan 1988; de Kroon &Schieving 1990). Phalanx clonal plants areresource-deprived (Bell 1984). Resource capture ofphalanx clones with a consolidation strategyappears to be a more stochastic activity, primarilydependent on temporal variation in the availabilityof resources in chronically unproductive habitats.Guerilla growth appears to be resource exploited(Grime 1979; Bell 1984; Harper 1985; Callaghan1988; de Kroon & Knops 1990; de Kroon &Schieving 1990). Under either a foraging or con-servative strategy, guerilla clonal plants bringabout a continuous spatial re-arrangement of theabsorptive surfaces, which allows the plants toadjust to changes in the distribution of resourcesduring the growing season.

The founder controlled guerilla plants tend tohave a wider range of involved parameter values(growth architecture parameters of individualplant) of species coexistence and tend to form afine-scale mixture of species (Yodzis 1978; Leps &Stursa 1989; Herben & Hara 1997). Differences inthe strategies used by phalanx and guerilla plantsto utilize resources and differences in the mecha-nisms used to control competition produce dif-ferent community spatial patterns (Schmid 1986;

Oborny & Bartha 1995; Herben & Hara 1997).Guerilla clonal plants often show strong spatialspreading that leads to the formation of char-acteristic structures of space occupation and, con-sequently, characteristic gap structures that areavailable for occupation by other species (Bell1984; Grubb 1977; Cain et al. 1991). This facili-tates the coexistence of different species withinthe community (Glenn & Collins 1990; Bartha1992; Herben et al. 1993a,b). Thus, guerilla clonalplants increase or maintain the number of speciesin both productive and unproductive habitats,resulting in an increase in community diversity.With respect to the phalanx growth form, rametdensity in phalanx species is extremely high (Cook1985), which prevents seedling establishment byother species (Silander 1985; Silvertown et al.1992) and creates monodominant patches of clonalspecies within the community. In unproductiveand/or stressful habitats, where few other plantspecies can grow, the presence of phalanx clonalplants with a strong ability to adapt to poor-resource conditions may increase communitydiversity. In contrast, in relatively productivehabitats with dense vegetation and strong compe-tition, the presence of phalanx clonal plants mayimpoverish the species-rich community by out-competing other plant species, resulting in amarked decrease in community diversity (Bobbink& Willems 1987; Bobbink et al. 1988). In prac-tice, clonal plants with different growth forms(e.g. phalanx and guerilla) often coexist. The cor-relation of community diversity to the importanceof all clonal plants is the result of the integrationof the correlations between community diversityand the importance values of clonal plants withdifferent growth forms, such as phalanx and gue-rilla plants.

In summary, the occurrence of clonal and non-clonal plants, phalanx and guerilla clonal plantswas markedly different in the NECT, correspond-ing to the different strategies and internal controlmechanisms used by the plants. The performanceof clonal plants in communities affects plantspecies diversity. The relationship of plant speciesdiversity to the importance of clonal plants wasdirectly related to the clonal growth form(‘phalanx’ and ‘guerilla’), their control mechanismsfor competition and the habitat conditions. As aresult, the presence of clonal species within a

714 M. Song et al.

community enriches the classical communitytheory that the number of species coexisting atequilibrium cannot exceed the number of limitingresources. The internal control mechanisms ofclonal plants alleviate clone competition andfacilitate species coexistence. Therefore, clonalplants have a great potential to influence commu-nity organization.

ACKNOWLEDGEMENTS

This research was financially supported by theChinese Academy of Sciences (KSCX1-08-02), theNational Key Basic Research Special FoundationProject of China (G2000018607) and the NationalScience Fund for Distinguished Young Scholars ofChina (39825106).

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