Journal of Ecology

2003

91

, 58–67

© 2003 British Ecological Society

Blackwell Science, Ltd

Are trade-offs in allocation pattern and root morphology related to species abundance? A congeneric comparison between rare and common species in the south-western Australian flora

PIETER POOT and HANS LAMBERS

School of Plant Biology, Faculty of Natural and Agricultural Sciences, The University of Western Australia, 35 Stirling Highway, Crawley WA 6009, Australia

Summary

1

Many narrowly endemic species are restricted to distinctive edaphic environments.The adaptations that make these species successful in their restricted habitat mayincur a cost, and decrease their success in more common habitats. We compared growth,biomass allocation and root morphology of two narrowly endemic

Hakea

species (Pro-teaceae) of Mediterranean south-western Australia with those of five more widespreadcongeners, in a glasshouse study. The rare

Hakea

species occur in endangered winter-wet shrublands that grow on skeletal (0–20 cm deep) soils overlying massive ironstonerock, whereas their common congeners occur nearby on deeper wetland and non-wetland soils.

2

The ironstone endemics differed consistently from their widespread congeners insome important root characteristics. During early development they allocated relativelymore biomass to their roots, and had a higher specific root length due to a lower averageroot diameter and a lower root mass density. Therefore, when compared at the sameplant mass, the ironstone endemics had a considerably greater total root length.

3

The ironstone endemics also favoured root growth in deeper layers of the substrate:they invested up to 64% of their root mass in the bottom 10 cm of 40-cm-deep pots, vs.35% for common species. Only in the ironstone endemics did the extension of the mainroot axis continue at the same rate after reaching the bottom of the pot.

4

We suggest that the observed differences are the consequence of evolutionary trade-offs, and represent specializations of the endemic species to increase the chances of gettingaccess to water before the onset of severe summer drought in these habitats. However,while adaptive in a shallow-soil habitat, these traits may reduce success on deeper soilsby compromising both below-ground and above-ground competitive abilities.

Key-words

: biomass allocation, endemic,

Hakea

, ironstone community, root morphology,shallow soils, specialization, trade-off

Journal of Ecology

(2003)

91

, 58–67

Introduction

Many explanations have been offered for the rarity ofdifferent plant species, but no single unifying theory orhypothesis has emerged (e.g. reviews in Drury 1974;Kruckeberg & Rabinowitz 1985; Fiedler 1986; Pate &Hopper 1993; Murray

et al

. 2002). Some authors havetherefore argued that the quest for general principlesin this area is premature, and that all species may be

idiosyncratic (e.g. Fiedler 1986). Others consider this questfundamental for managers of threatened species, andargue that there are promising lines of research worthpursuing (Pate & Hopper 1993; Murray

et al

. 2002).A relatively large number of rare plant species are

closely associated with some distinctive environmentalfeature that is usually edaphic; local endemics that areassociated with unusual substrates like gypsum, serpen-tine, limestone, alkaline and heavy-metal soils are wellknown to field botanists all over the world (Kruckeberg& Rabinowitz 1985, references therein). There is, how-ever, little evidence to support the view that theseedaphic endemics require the chemical, physical or

Correspondence: Pieter Poot (tel. + 61 89380 2491, fax + 6189380 1108, e-mail ppoot@agric.uwa.edu.au).

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Hakea

species

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biological features of their specific substrate. Many ofthem can grow and complete their life cycles in glass-houses and common gardens and even in neighbouringcommunities, as long as competition with surroundingvegetation is prevented. Rather, the edaphic endemicshave the ability to resist the local, sometimes toxic, con-ditions better than many widespread species.

It is hypothesized that in the more common habitatsedaphic endemics would be outcompeted due to thehigh costs of the specific adaptations to their ‘own’environment (Kruckeberg & Rabinowitz 1985). Withinthis context, edaphic endemics may be hypothesized tobe genetically fixed specialists. Strong selection pres-sures may have reduced genetic variation for the traitsinvolved in the anatomical, morphological or physio-logical adaptations necessary for survival in theirextreme environments. In other habitats these relativelyfixed traits may be maladaptive and incur a fitness cost.

What evidence do we have for the costs of such spe-cialization? Most edaphic endemics only occur withvery low frequency, if at all, in different environments.This strongly suggests that, as in most cases at leastsome of the seeds of these plants will reach the sur-rounding communities and germinate, they cannotestablish or are inferior competitors. Several researchershave argued that narrow endemics only occur in habitatsin which competition is of minor importance (Gankin &Major 1964; Baskin & Baskin 1988; Medail & Verlaque1997; Walck

et al

. 1999). Much ecological and geneticresearch in this area has concentrated on comparingnarrowly endemic species with their widespread con-geners, to take dissimilar life history characteristicsand evolutionary histories into account (Karron 1987).Walck

et al

. (1999) showed that the rock outcrop narrowendemic

Solidago shortii

had a lower relative competit-ive ability than its widespread congener

S. altissima

and the common competitor

Festuca arundinacea

. Ina comparison of three pairs of congeners, each pairconsisting of a common weed and a serpentine narrowendemic, Hart (1980) showed that the endemics hadlower relative competitive abilities when grown on non-serpentine soil. Results of several other studies suggestmore indirectly that endemics have lower competitiveabilities than widespread congeners, due to slower growthrates or smaller sizes (e.g. Prober 1992; Robson & Maze1995). Although a few congeneric comparisons reportedno differences in competitive abilities between rare andcommon species (Gottlieb & Bennett 1983; Snyder

et al

.1994), the majority of evidence suggests that edaphicendemics are poor competitors, at least in environmentsdifferent from those they characteristically occupy.Most competition experiments, however, do not provideinformation on the underlying causes of differences incompetitive ability (Connolly

et al

. 2001).In this study we aim to identify ecophysiological rea-

sons for narrow endemism in a unique, presumablyedaphically determined, plant community in Mediter-ranean south-western Australia. The largely perennialvegetation in these critically endangered ‘ironstone’

communities grows on reddish, shallow (0–200 mmdeep), winter-wet soils, overlaying massive ironstonerock (Gibson

et al

. 2000). More than 20 plant taxa areendemic to, or have their distribution centred on, thesehabitats. During winter, these plants have to withstandvariable periods of waterlogging, whereas during summerthe shallow soils dry out quickly, leading to extremedrought. We hypothesize that the ironstone commun-ities are ‘shaped’ by physical constraints (extremelyshallow soils), necessitating drought-avoidance ordrought-tolerance strategies. Especially during earlyseedling establishment, there is probably strong selec-tion for characteristics that give access to water sourcesvia cracks or crevices in the ironstone rock, beforethe first summer drought starts. Therefore, we wouldexpect ironstone endemics to show a strong emphasison root growth and root foraging.

We have taken a comparative approach, in which wecompare two ironstone endemics of the genus

Hakea

(Proteaceae) with five widespread congeners. By com-paring the species in a common environment (glass-house) on a common substrate (river sand), we aimedto determine whether there were any inherent dif-ferences between the rare and widespread species ingrowth, biomass allocation, root distribution andmorphology that might explain their contrastingabundance. The generality of this study was enhancedby using two rare endemics from two separate commun-ities, two populations for each species, and a rangeof widespread species originating from ecologicallydistinct wetland and non-wetland habitats on deepersoils.

Materials and methods

Hakea

species (Proteaceae) are woody perennials thatrange in size from shrubs to small trees. Mediterraneansouth-western Australia is the major centre of diversityfor this genus, with approximately 70% of

Hakea

spe-cies endemic to this region (Groom & Lamont 1996).We studied seven south-west Australian

Hakea

speciesthat differed in abundance and originated from threecontrasting habitats: endangered ironstone winter-wetlands, ‘other’ winter-wetlands, and non-wetland

Eucalyptus

woodlands (Fig. 1, Table 1). Plants fromtwo populations were used for each species.

Only scattered remnants of the unique ironstonecommunities are left on the southern Swan and ScottRiver Coastal Plains (Fig. 1). Of an estimated originalarea of

c.

3900 ha, only

c.

420 ha have escaped the mas-sive clearing of these coastal plains. For a more detaileddescription of the floristics, climate and soils of theironstone communities and their many endemic speciessee Gibson

et al

. (2000) and references therein.

H. oldfieldii

is locally common on the southern Swanironstone communities. Outside these communitiesit is absent or very rare. Current information on its

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distribution (Florabase, Department of Land Manage-ment and Conservation, Western Australia, http://www.calm.wa.gov.au/science/florabase.html) indicatesa few disjunct populations located hundreds of kilometresinland from the ironstone sites. However, the taxo-nomic status of these populations is still uncertain.

H.tuberculata

is locally common on the Scott ironstone com-munities and has a few disjunct small populations nearAlbany some 250 km to the east (see Coates & Hamley1999). Both ironstone species have priority status.

H. ceratophylla

and

H. varia

are both commonspecies that typically occur on winter-wetlands in south-western Australia. They also occur on very few of theremnant ironstone communities but are rare in thishabitat. For both these species seeds were collectedfrom two nature reserves (Ruabon Nature Reserve andYoongarillup Nature Reserve) on the southern Swancoastal plain in the vicinity of the ironstone commun-ities (Fig. 1). Both reserves contain a variety of damp-lands and sumplands with deeper sandy soils (> 0.8 m)overlying a hardpan.

H. linearis

is the least widespreadof the three ‘winter-wet’ species occurring in seasonallywet flats. One of the populations used for this specieswas a remnant stand along a roadside verge on thesouthern Swan coastal plain. The other population waslocated in the swampy catchment valley of a eucalypt

forest on the nearby Blackwood Plateau. This popula-tion occurs on deep sandy soils.

H. lissocarpha

and

H. cyclocarpa

are both commonspecies that occur on lateritic soils in the undergrowthof eucalypt woodlands on the Darling and BlackwoodPlateaux. Neither species occurs in winter-wet situations.

The phylogenetic status of the different

Hakea

spe-cies is still under consideration. However, under thecurrent classification system (Barker

et al

. 1999) thecomparison presented in this study is unbiased, as noneof the species within a specific habitat are classified inthe same taxonomic subgroup.

, ,

For each of the seven

Hakea

species, woody folliclescontaining the seeds were sampled in the field duringMarch and April 2000. Two populations at least 10 kmapart were sampled per species, and for each populationfollicles were collected from at least five plants. Within2 weeks at room temperature all follicles had dehiscednaturally. Forty randomly selected seeds per populationwere placed just under the surface of native low-nutrientpotting mix (Kings Park and Botanic Garden) in smallplastic pots (four seeds per pot). The potting mix hadinitially been watered with a diluted fungicide solution(Previcur; group Y fungicide) to prevent damping off.All pots were placed in a glasshouse at the University ofWestern Australia campus at the end of April 2000.

After 4 weeks of growth the seedlings were transplantedindividually into free-draining PVC pots containingwashed river sand. The pots were 40 cm deep and 9 cmwide. The sand was covered with a layer of small aquariumstones to prevent excessive evaporation from the soil sur-face. Pots were placed randomly on three neighbouringbenches in a temperature-controlled glasshouse (20

°

C/15

°

C, day/night, light intensities 65% of ambient). Everyother day pots were flushed with a low concentrationnutrient solution (cf. low nutrient availabilities in south-west Australian habitats) of the following composition(

µ

M): 400 NO

–3

, 204 K

+

, 200 Ca

2+

, 154 SO

2–4

, 54 Mg

2+

,40 Fe-EDTA, 4 PO

3–4

, 2.4 BO

3–3

, 0.24 Mn

2+

, 0.10Zn

2+

, 0.030 MoO

42–

, 0.018 Cu

2+

. We allowed 3 weeks foradjustment of the plants to the new growth conditions,prior to commencement of the experiment.

Table 1 The experimental species and their codes. For each species two populations were used (see Fig. 1)

Rare species with their distribution centred on the winter-wet ironstone communities(1) Hakea oldfieldii Benth. (HO)(2) Hakea tuberculata R. Br. (HT)

Common species typically occurring on winter-wet communities in general(3) Hakea ceratophylla (Smith R. Br.) (HCE)(4) Hakea varia R. Br. (HV)(5) Hakea linearis R. Br. (HL)

Common species occurring on non-wetland lateritic soils (Eucalyptus woodland)(6) Hakea lissocarpha R. Br. (HLS)(7) Hakea cyclocarpa Lindl. (HC)

Fig. 1 Approximate locations in south-western Australia ofthe two separate populations used for each species. Thenumbers refer to the species as shown in Table 1.

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Hakea

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Plants were grown in the glasshouse for a total of188 days during which a growth analysis was performed.Because of the high variability in germination time,both within and between species, we harvested plantsaccording to their individual germination dates. ‘Con-trol’ plants were harvested at days 62, 125 and 188 aftergermination (five plants per population per harvest).Ten further plants per population were waterloggedfrom day 62 to day 125. Half of these plants were harv-ested at day 125, whereas the other half were left tocontinue to grow under ‘control’ conditions beforethey were harvested on day 188. The specific effects ofthe waterlogging treatment are presented elsewhere(Poot & Lambers 2003).

Roots were rinsed with water to remove all sand. Atall harvests, fresh and oven-dry masses of roots, stemsand leaves were determined after drying for 48 h at70

°

C. Total leaf area was computer scanned and ana-lysed using the Win Rhizo V3.9 software (RegentInstruments, Quebec, Canada). Total length of themain root axis was recorded when straightened. Thelatter was especially necessary at the last harvest as allplants had reached the bottom of the pot. At the initialharvest, roots were stained with diluted basic fuchsinand computer scanned as above, to determine totalroot length, volume and average root diameter. Later inthe experiment roots of all species had developed manyspecialized bottlebrush-like root structures (clusterroots) and a root scan analysis was not possible. At thefinal harvest the distribution of the roots in the pot wasexamined by harvesting the roots at four root depthclasses (0–10, 10–20, 20–30 and 30–40 cm).

Data were analysed with the general linear models pro-cedure of the statistical package Genstat (Genstat 4.2Committee 2000). Two separate models were run toanalyse the data from both individual species and hab-itat perspectives. In the species model, the factor pop-ulation was nested within species, and either a one-way

, with species as fixed factor, or a two-way

with time and species as fixed factors in the model, were

performed. In the habitat model, the variation betweenspecies was further subdivided into variation betweenhabitats and between species within a habitat. Datawere natural log or arcsin transformed where necessaryto ensure normality and homogeneity of variances.

Results

Total plant dry mass at the initial harvest (day 62)was positively correlated with seed mass (

r

2

= 0.56,

P

= 0.002), with the rare ironstone species havingsomewhat smaller masses, especially when comparedwith species from the non-wetland habitat (Fig. 2,Table 2). However, in these young seedlings, cotyle-dons constitute a significant part of total plant mass,

Table 2 Dry mass (mg) of different organs, at the initial harvest (62 days after germination), for seven Hakea species (HO, HT,HCE, HV, HL, HLS and HC) originating from ironstone, winter-wet and non-wetland habitats. Values are means from twopopulations per species. Probability (P) values were obtained after a one-way nested with ln transformed data, with eitherspecies (Spec) or habitat (Hab) as fixed factor and population as nested factor in the model (n = 5 per population). Forpresentation purposes, LSD values are given for the untransformed data. The population effect was not significant for any of theparameters. ***P < 0.001, **P < 0.01, *P < 0.05, NS = not significant. Species codes are as given in Table 1

Ironstone Winter-wet Non-wetland Statistics

HO HT HCE HV HL HLS HC LSD Spec P Hab P

Leaf 88 54 74 110 98 106 125 11 *** NSStem 13 13 20 38 22 19 23 10 *** NSRoot 52 39 30 39 44 54 58 11 ** NSCotelydon 9.3 8.9 26 11 9.6 22 55 5.9 *** NSTotal 162 115 150 198 173 201 260 24 *** NS

Fig. 2 Relationship between plant dry mass at the initialharvest, 62 days after germination, and average seed mass, forHakea species originating from contrasting habitats: ironstoneendemics (filled symbols), common winter-wet species (opensymbols), common non-wetland species (grey symbols). Eachsymbol represents the mean ± SE (n = 5) of a population ofa species. Two populations per species were used. The linerepresents a linear regression (y = 143.5 + 1.46, r2 = 0.56).Species codes are as given in Table 1.

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especially in the larger-seeded species (e.g. up to 23% ofthe total in

H. cyclocarpa

). The relationship betweenseed mass and non-cotyledonous plant mass was muchless clear (

r

2

= 0.25,

P

= 0.068).The ironstone endemics allocated a significantly

larger percentage of dry mass to their roots (Fig. 3a,Table 3). The larger investment of the endemics in rootswas at the expense of allocation to the stem (both iron-stone species), and to a lesser extent to the leaves (

H.tuberculata

, see Table 2). Differences in absolute leafand root mass between species were not related tohabitat group.

Despite the absence of differences in absolute rootmass between the habitat groups (Table 2), there weresubstantial differences in other root characteristics.The ironstone species produced almost twice as muchroot length for each unit of root mass, i.e. they had aconsiderably greater specific root length (SRL) thanthe winter-wet species (Fig. 3b), and twice as manyroot tips (Table 3). Species from the non-wetland hab-itat had intermediate values for these parameters.

When the SRL data for all species within a habitatgroup were pooled, the ironstone endemics differed sig-nificantly from species in both of the other habitatgroups (LSD test after one-way

for the habitatmodel,

P

< 0.05).A difference in SRL can be caused by differences in

either root tissue density or root diameter. In

H. old-fieldii

, the higher SRL was mainly caused by the lowertissue density of the roots (Table 3). In

H. tuberculata

itwas due to a combination of a relatively low root tissuedensity and a smaller root diameter, neither of these para-meters being significantly different on their own (Table 3).

The two later harvests were conducted to study theontogeny of several plant characteristics. Table 4 sum-marizes the statistics for a species model to comparethe seven species separately, and a habitat model tocompare the three habitat groups.

Table 3 Root characteristics at the initial harvest (62 days after germination), for seven Hakea species originating from ironstone,winter-wet and non-wetland habitats. Values are means from two populations per species. Probability (P) values were obtainedafter a one-way nested , with either species (Spec) or habitat (Hab) as fixed factor and population as nested factor in the model(n = 5 per population). The population effect was not significant for any of the parameters. For presentation purposes, LSD values aregiven for the untransformed data. ***P < 0.001, **P < 0.01, *P < 0.05, NS = not significant. Species codes are as given in Table 1

Ironstone Winter-wet Non-wetland Statistics

HO HT HCE HV HL HLS HC LSD Spec P Hab P

Root mass ratio (percentage of total dry mass)

32 34 20 20 26 26 22 5 ** *

Total root length (m) 4.6 3.1 1.6 2.1 1.9 3.3 3.7 1.2 ** *Number of root tips† 812 559 231 331 267 571 695 238 *** *Specific root length (m g−1 dry mass) 90 77 54 56 45 58 64 23 * *Root diameter (mm) 0.54 0.56 0.61 0.58 0.59 0.61 0.61 – NS *Root tissue density (kg dry

mass m−3 root)48 60 64 70 85 60 56 6 *** NS

†P values are for ln transformed data.

Fig. 3 Relationship between (a) plant dry mass and root mass, and (b) root mass and total root length, at the initial harvest, forHakea species originating from contrasting habitats (see legend to Fig. 2). Each point represents an individual plant. Twopopulations per species were used (n = 5 per population). Lines represent significant (P < 0.001) linear regressions for allindividuals originating from one of three habitat groups. Species codes are as given in Table 1. Equations of linear regressions: (a)y = 4.53 + 0.296x, r2 = 0.89 (ironstone endemics; solid line); y = 6.99 + 0.176x, r2 = 0.53 (winter-wet species; dashed line); y =− 1.88 + 0.251x, r2 = 0.67 (non-wetland species; dotted line); (b) y = −0.416 + 0.0940x, r 2 = 0.65 (ironstone endemics; solid line);y = 0.509 + 0.0349x, r 2 = 0.42 (winter-wet species; dashed line); y = −0.896 + 0.0784x, r 2 = 0.74 (non-wetland species; dotted line).

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© 2003 British Ecological Society, Journal of Ecology, 91, 58–67

Although there were some clear differences betweenthe species in the total amount of dry mass attained atthe different harvests, this was not related to habitat(Table 4). Similarly, despite differences in leaf and rootrelative growth rates between the species (seespec × time for leaf and root mass in Table 4), thesewere not related to the specific habitat groups (seehab × time, Table 4).

The initial difference in root mass ratio (RMR)between the habitat groups disappeared with time(Fig. 4a, significant hab × time for RMR in Table 4).Species from the winter-wet habitats (especially H. lin-earis and H. varia) increased their RMR during thefirst time interval considerably more than the otherspecies. This was mainly due to their relatively lowshoot RGR during this period (not shown). At the lastharvest, the differences in RMR were species-specificrather than habitat-specific.

Due to the development of numerous cluster rootsafter the first harvest, we could not monitor the devel-opment of SRL over time. Although there were cleardifferences between the species in the number and sizeof root clusters, there was no relationship with the hab-itat from which the species originated (data not shown).

During the whole growth period the ironstone spe-cies allocated less dry mass to their stems (lower stemmass ratio), than the winter-wet species (Table 4). Thenon-wetland species had intermediate values. Most ofthe significant population effects (Table 4) were asso-ciated with stem length and plant height, and weremainly caused by differences between the two popula-tions of H. varia. Although both populations of H.varia had a relatively high allocation to stems they dif-fered considerably.

Despite the equal relative investment in roots at thelast harvest, the ironstone species had longer main root

Table 4 Statistical analyses of ontogenetic changes in plant characteristics, for two populations of seven Hakea species,originating from ironstone, winter-wet and non-wetland habitats. Plants were harvested 62, 125 and 188 days after germination.Values indicate the percentage of the total variation (sums of squares) attributable to that factor. Two statistical models werefitted. In the species model, a two-way was used with species and time as fixed factors, and population as a nested factorwithin species. In the habitat model the variation between species was further subdivided into a habitat and a species component.Note that for this last model, only the main effect of habitat and the interaction between habitat and time is shown. The data forthe organ mass ratios were arcsin transformed before testing. All other data were ln transformed before testing. ***P < 0.001, **P< 0.01, *P < 0.05, NS = not significant

Model:

Species Habitat

Spec Spec Pop TimeSpec × Time

Spec Time Pop Hab

Hab × Time Error Total

d.f. 6 7 2 12 14 2 4 166 207Dry mass

Root 1.7*** 0.1NS 96*** 0.4NS 0.5NS 0.8NS 0.0NS 3.3 471Leaf 6.0*** 0.2NS 89*** 2.1*** 0.4NS 4.1NS 0.1NS 3.1 381Stem 6.7** 0.8** 87*** 2.1*** 0.3NS 4.5NS 0.8NS 4.2 408Total 4.2*** 0.2NS 93*** 0.8NS 0.4NS 2.8NS 0.3NS 2.8 377

Mass ratiosRoot 31*** 2.0NS 34*** 13*** 2.3NS 14NS 9.5* 20 2.13Leaf 28* 4.9* 1.5NS 35*** 3.4NS 15NS 10NS 30 1.11Stem 57** 7.9*** 0.3NS 11.2*** 1.6NS 44* 3.1NS 22 0.79

Plant height 17* 2.9*** 69*** 3.2** 0.8NS 9.3NS 0.8NS 8.9 61Rooting depth 10.7** 1.2NS 69*** 3.3* 1.3NS 9.7* 2.7** 16 42.7

Fig. 4 Ontogenetic development of (a) root mass ratio, and (b) length of the main root axis, for Hakea species originating fromcontrasting habitats (see legend to Fig. 2). Each point represents the mean of two populations (n = 5 per population). Barsrepresent least significant differences as calculated by one-way s with species as fixed factor, and population as a nestedfactor within species, in the model. Species codes are as given in Table 1.

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axes (Fig. 4b, rooting depth in Table 4). This differencemainly appeared during the second growth period.After reaching the bottom of the pots, the winter-wetand non-wetland species decreased the rate of exten-sion of their main root considerably, whereas the iron-stone species did not (Fig. 4b).

At the final harvest the rare ironstone species hadlocated a much larger proportion of their roots in thebottom 10 cm of the pots (Fig. 5a): an average of 64%vs. 35% for non-ironstone species. Plants that had beenwaterlogged between the first and second harvest, andwere subsequently treated as well-drained controls,showed a similar pattern to those that were well-drained throughout (Fig. 5b). Although root growthwas greatly reduced during the waterlogging period(see Poot & Lambers 2003), ironstone species had alarger percentage of their root mass in the bottom ofthe pots (37% vs. 11%).

Discussion

The two geographically restricted Hakea species, ori-ginating from separate ironstone community remnants,clearly differed from their widespread congeners.During the early stages of seedling development theyallocated more biomass to roots, and their roots hada higher specific root length. As measurements wereobtained on seedlings with at least partly overlappingtotal plant mass (cf. Figure 3), these differences cannotbe due to ontogenetic or allometric effects.

During later stages of seedling development the iron-stone endemics had invested proportionally more rootmass in the bottom layer of the pot. This might have

been expected on the basis of their initially higher rootmass ratio and specific root length. However, at thisstage the difference in root mass ratio between thehabitat groups had disappeared. Also, the differentialallocation of roots to the bottom of the pot was inde-pendent of total root mass (Fig. 5a), and was asso-ciated with the response of the main root axis whenreaching the bottom of the pot. In all common species,growth of the main root axis was strongly reducedwhen this physical barrier was reached. Presumably,this was associated with the growth and/or initiation ofmore superficial laterals, as the difference in root massratio between the habitat groups decreased rather thanincreased with ontogeny. The behaviour of the com-mon non-ironstone species may be the typical responseof plant roots encountering a rock, hardpan or com-pacted soil layer (e.g. Crossett et al. 1975; Goss 1977;Misra & Gibbons 1996; Thaler & Pages 1999). Physicalconstraints are thought directly to reduce root cellelongation and/or division within the main axis. Thiswould decrease sink strength of the main axis, leavingmore carbohydrates available for existing laterals andfor the initiation of lateral primordia (decreased apicaldominance; Thaler & Pages 1999). In contrast, themain root axis of the ironstone endemics continued toelongate at the same rate after reaching the bottom ofthe pot. Possibly, their roots immediately deflect afterencountering a physical barrier, and thus do not senseit. Alternatively, they do sense it but respond differ-ently. The latter may be mediated by differencesbetween the habitat groups in hormone metabolism. Inmany plant species it has been observed that rootsencountering a compacted soil layer accumulate ethyl-ene (e.g. Sarquis et al. 1991) and abscisic acid (ABA,e.g. Tardieu et al. 1992). The two hormones and theinteractions between them are thought to mediate

Fig. 5 Root fresh mass located in the bottom 30–40 cm of the pot, at the last harvest (188 days after germination), for Hakeaspecies originating from contrasting habitats (see legend to Fig. 2). (a) Plants that were continuously grown under well-drainedconditions. (b) Plants that were grown for 63 days under waterlogged conditions, after which pots were drained and the plantswere allowed to recover for another 63 days. Each point represents an individual plant. Two populations per species were used(n = 5 per population). Lines represent significant (P < 0.05) linear regressions for all individuals originating from one of threehabitat groups. Species codes are as given in Table 1. Equations of linear regressions: (a) y = −0.496 + 0.686x, r 2 = 0.95 (ironstoneendemics; solid line); y = 0.019 + 0.333x, r 2 = 0.62 (wetland species; dashed line); y = −0.614 + 0.403x, r 2 = 0.82 (non-wetlandspecies; dotted line); (b) y = 0.297 + 0.338x, r 2 = 0.28 (ironstone endemics; solid line).

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other well-known responses to soil compaction, suchas a decrease in stomatal conductance, and decreasedroot and leaf growth (Hussain et al. 2000).

Because we used two populations of each species, andeach gave similar results, the differences between theironstone endemics and their common congeners arespecies-specific, rather than population-specific. Thisshows that these differences have a genetic basis andstrongly suggests that there is a selective advantage inhaving a high root mass ratio, a large total root lengthand a high allocation to deep roots during the earlyestablishment phase of Hakea seedlings on an iron-stone soil.

What might this advantage be? In Mediterraneanecosystems plant populations have to withstand severesummer droughts. Natural regeneration generallytakes place during the first winter after a summer fire,and thus seedlings may experience their first droughtwithin a few months of emergence (e.g. Lamont &Groom 1998 for south-west Australian Proteaceae).Drought-related mortality is therefore a major compon-ent of the demography of seedlings in Mediterraneanhabitats (e.g. Frazer & Davis 1988; Enright & Lamont1989; Richards et al. 1997). In south-western Aus-tralia, the most severe drought is experienced by plantsin shallow soil overlying rocky hills and ridges (e.g.Mishio 1992; Groom & Lamont 1995). Althoughthe ironstone communities are situated at the basesof scarps in relatively flat country, the shallowness oftheir soils would make them extremely susceptibleto drought. Plants in these communities would not beable to survive if they could only access superficialwater and species present would be restricted to droughtavoiders (annuals), highly specialized resurrection plants(e.g. Gaff 1981) or plants having water-storage capabil-ities (e.g. Calothamnus tuberosus, Pate & Dixon 1982).However, the amount of perennial vegetation on theironstone communities strongly suggests that thereare alternative water sources. These are most likelyaccessed via cracks and fissures in the underlying iron-stone rock. We therefore suggest that in an ironstoneenvironment, seedling survival depends on the detec-tion of cracks and fissures to access water before thestart of the summer drought. With their relatively highallocation to roots and their greater specific rootlength, the ironstone endemics can explore a muchlarger soil volume for both water and for cracks thatmay lead to water.

What might be the advantages in this environment ofinvesting in roots in deeper layers or more distally fromthe base of the plant? On the shallow ironstone soil theroot of a germinated seedling would quickly encounterthe ironstone hardpan. Presumably, the main root ofthe ironstone endemic would deflect and then continueto grow laterally at the same rate. While growing over

the surface of the hardpan, the root of the ironstoneplant would form many laterals, thereby maximizing itschances of encountering cracks or fissures. In contrast,the widespread species would, on the basis of this study,be expected to slow the extension of their main rootafter hitting the hardpan, which then would trigger theinitiation of laterals. Clearly the total rock surface areathat would be explored by the widespread specieswould be much less than that of the ironstone endemics.In addition, root anchorage on a shallow soil would bemuch more stable with a wider spread of distal roots.We suggest that the higher root mass ratio and specificroot length, as well as the preferential allocation ofroot mass to deeper soil layers, reflects the specific root-foraging strategy of the ironstone endemics. Thesetraits therefore may offer the major explanation for theirsuccess in this habitat.

In a companion study, we have shown that the iron-stone endemics exhibited similar tolerances to water-logging as the common winter-wet species (Poot &Lambers, 2003). However, the non-wetland speciesshowed stronger growth reductions upon waterlogging,which may further compromise their survival in iron-stone communities.

On deeper soils, the specific adaptations of the iron-stone endemics may well be maladaptive. In most soils,the majority of the nutrients occur in the top layers.The ironstone Hakea species we used would probablyinvest far more root biomass in deep layers, as was seenin the current experiment, than strictly necessary. Thismay seriously compromise their ability to competewith other species for nutrients and water in the rel-atively rich upper layers of the soil. In addition, theirinitially large allocation to roots may compromise theirabove-ground competitive ability. The latter may notbe important in the relatively open ironstone commu-nities, but may be essential in communities with higherplant densities and less open space. This may explainwhy the species originating from the densest com-munities (winter-wetlands) were tallest (data not shown)and invested most biomass in their stems, when com-pared with species from the relatively open ironstonecommunities and understorey of Eucalyptus woodlands.

The data presented in this paper strongly suggest thatironstone endemics are specialists. Their specific adap-tations to their local environment may be directlyresponsible for their low competitive abilities in otherenvironments. The consequences of trade-offs in wholeplant biomass allocation (investment in root or shoot),and within root biomass allocation (high or low spe-cific root length; formation of predominantly basal ordistal laterals) may cause them to be well adapted to

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© 2003 British Ecological Society, Journal of Ecology, 91, 58–67

their own environment, but maladapted to others. Asmany edaphic endemics occur in relatively open, shal-low, rocky and water-stressed environments the aboveexplanation may also apply to many other species (e.g.Kruckeberg & Rabinowitz 1985; Baskin & Baskin1988; Pate & Hopper 1993; Medail & Verlaque 1997).In a comparison of a narrowly endemic rock outcropSolidago and a common Solidago, Walck et al. (1999)also showed that the endemic species had a higher rootmass ratio, and they argued that this would add to itssuccess in its own water-stressed habitat. In many otherstudies of narrowly endemic plant species and theirwidespread congeners, root mass ratio was not deter-mined, or differences in root mass ratio were not found(e.g. Hart 1980; Gottlieb & Bennett 1983; Prober 1992;Snyder et al. 1994; Robson & Maze 1995). However,root mass ratio is obviously not static, but changes withplant size, and may have to be followed over a longerperiod for differences to be observed. Also, to ourknowledge, none of the congeneric comparisonsbetween rare and common species determined totalroot length, specific root length and other aspects ofroot morphology. Clearly, total root length is a betterpredictor of explorable soil volume and therefore of thecapacity of roots to absorb nutrients and water and tofind cracks, than absolute root mass.

Acknowledgements

We thank Roy Bakker, Lieve Bultynck and Julia Mattnerfor their assistance during the set-up and harvestingphase of this experiment, Kingsley Dixon and NeilGibson for their enthusiasm and helpful discussions atthe start of the project, and Erik Veneklaas for themany helpful discussions and the critical comments onan earlier version of the manuscript. This research wassupported by an Australian Research Council SPIRTgrant to Pieter Poot, with additional financial supportfrom Kings Park and Botanic Garden.

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Received 25 April 2002 revision accepted 14 October 2002