plant stored reserves do not drive resprouting of the lignotuberous shrub erica australis

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Research

Blackwell Science, Ltd

Plant stored reserves do not drive resprouting of the

lignotuberous shrub

Erica australis

Alberto Cruz, Beatriz Pérez and José M. Moreno,

Facultad de Ciencias del Medio Ambiente, Universidad de Castilla-La Mancha, 45071 Toledo, Spain

Summary

• Lignotuberous plants store carbohydrates and mineral nutrients within thelignotuber. Resprouting vigour may depend on stored reserves, as well as on theavailability of soil mineral nutrients and water.• Here the role played by plant reserves and soil resources on the resproutingresponse of

Erica australis

was analysed after clipping plants in 13 different stands,varying in soil resource availability and in plant reserves.• There were significant among-site differences for resprout biomass and maximumlength, but not for resprout number, 1 yr after clipping. Plant reserves at the time ofclipping were not significantly correlated with resprout number, length or biomass.However, resprouting variables were significantly correlated with soil nitrogen orextractable cations, or plant water potentials. Resprout biomass and maximumlength were negatively correlated with lignotuber size.• These findings indicate that the assumption that resprouting vigor in lignotuber-ous plants is primarily dependent on the amount of reserves stored in the lignotubermust be revised, as well as the overall role of lignotubers in resprouting.

Key words:

non-structural carbohydrates, Mediterranean-type ecosystems, nitrogen,starch, fire.

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Author for correspondence:

José M. Moreno

Tel: +34 925268800Fax: +34 925268840 Email: [email protected]

Received:

22 July 2002

Accepted:

24 October 2002

Introduction

The ability of a plant to resprout after its above-ground partsare killed is a main feature of many plants from disturbance-prone, terrestrial ecosystems, like the Mediterranean ones inwhich fire plays a dominant role (Bond & Midgley, 2001).Many plants resprout from special organs, such as thelignotuber, partially buried into the soil, that act as a reservoirof dormant buds, as well as of carbohydrates and mineralnutrient reserves (Mullette & Bamber, 1978; James, 1984;Cruz & Moreno, 2001a). The carbohydrates stored in thelignotuber, or other below-ground parts, are thought to bemobilised during resprouting, thus acting as the main supplyof carbon for regrowth at the early stages after a disturbance(Jones & Laude, 1960; DeSouza

et al

., 1986; Miyanishi &Kellman, 1986; Bowen & Pate, 1993; Van der Heyden &Stock, 1996; Canadell & López-Soria, 1998). The role oflignotuber mineral nutrients (N, P) over resprouting has beenlittle explored, but evidence suggests that they may bemobilised to some extent and can potentially limit regrowth

(Miyanishi & Kellman, 1986; Canadell & López-Soria, 1998).It has often been considered that the vigour of the resproutingresponse after fire would be primarily determined by thedamage caused by heat to the dormant bud bank ininteraction with the pool of reserves previously stored by theplant ( Jones & Laude, 1960; Bowen & Pate, 1993). Forinstance, the level of carbohydrate reserves stored by the plantfluctuates largely during the year and between years (Cruz &Moreno, 2001a), which would explain the variationsobserved in the resprouting vigour depending on the time ofdisturbance (Rundel

et al

., 1987; Malanson & Trabaud,1988). However, a lack of correlation between the amount ofreserves and subsequent regrowth has often been reported(Richards & Caldwell, 1985; Hogg & Lieffers, 1991a,b;Erdmann

et al

., 1993; Sparks & Oechel, 1993). It has beensuggested that not all reserves in the storage organs may bemobilizable (Chapin

et al

., 1990). In addition, undergrounddemands from roots and mycorrhizas may limit mobilizationtowards above ground parts, remaining as strong sinks(Langley

et al

., 2002). It has also been argued that reserves


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may be stored in excess (Van der Heyden & Stock, 1995;Hoffmann

et al

., 2000; Cruz & Moreno, 2001a), hence otherfactors may be limiting. For instance, resprouting vigour ofco-occurring populations of the shrub

Erica australis

wasrelated to variations in the availability of soil resources(mineral nutrients and water) (Cruz

et al

., 2003), presumablydue to differences in resource supply for the regrowth ofresprouting tissues. It is not known whether variations in thelevel of reserves in the below-ground parts of the plantbetween co-occurring populations of the same plant speciescould in fact cause a differential resprouting response in thecase of fire or other defoliating disturbance.

The process of carbohydrate storage depends upon thebalance between photosynthesis and growth and respiration,which, in turn, may depend on soil moisture and nutrientsupply (Chapin

et al

., 1990; Steinlein

et al

., 1993). However,little is known about the factors that control reserve contentof the plant. In arid environments, the process of carbohy-drate storage and use in the roots of

Prosopis glandulosa

waspartially controlled by water content (Wan & Sosebee, 1990).Variations in soil-resource availability might affect theamount of reserves stored by the plant in its below-groundorgans prior to the disturbance. Furthermore, soil-resourceavailability might also determine the relative size of the storageorgan (Cruz & Moreno, 2001b), which in turn, may affectthe capacity of the plant to resprout. Therefore, the relation-ship between stored reserves of carbohydrates or mineralnutrients and resprouting vigour might be indirectly relatedto one another, to the extent that the first might be driven bysoil-resource availability and, eventually, mediated by therelative size of the resprouting organ. Unravelling these inter-actions is important in order to have a clear understanding ofthe mechanisms that control resprouting from lignotuberousspecies in many areas of the world; this is notably so of theMediterranean-type species.

This paper analyses whether the content of carbohydratesand nitrogen of the lignotuber and roots as well as the relativesize of the lignotuber in the shrub

E. australis

drove resprout-ing by this species. Resprouting by

E. australis

and other

Erica

species is a critical component of the regeneration processafter fire in many shrublands of the Mediterranean Region(Mesléard & Lepart, 1989; Calvo

et al

., 1998).

Materials and Methods

Species and study sites

E. australis

L. has a well-developed lignotuber (Moreno

et al

., 1999) from which it resprouts vigorously after fire. It isspread mainly over the western half of the Iberian Peninsula(Rivas-Martínez, 1979), being one of the dominant elemantswhere it grows. We selected 13 sites in the province of Cáceres(central-western Spain) in which

E. australis

was present. Theshrublands of these sites were dominated by

E. australis

,

together with

Cistus ladanifer

L.,

Rosmarinus officinalis

L. or

Erica umbellata

L., among other. The selected sites covered awide range of substrate types in which

E. australis

was present:fluvial sands (A1), granites (G1, G2, G3), quarzits (C1, C2,C3), slates (P1, P2, P3) and ‘rañas’ (Pliocene deposits) (R1,R2, R3). All the sites were selected to be as homogeneous aspossible with respect to elevation, slope and aspect. Maximumdistance between sites was

c.

70 km from N to S, and 25 kmfrom W to E. The climate of the study area is Mediterranean-type, with a mean annual temperature of 15–16

°

C and a meanannual rainfall of

c.

800–1100 mm, mostly concentrated inautumn and spring. The year following plant clipping wasdrier than average, with

c.

69% of average rainfall. The springfollowing clipping was particularly dry, with less than 60 mmrainfall compared to an average of 225 mm in the period1941–1990.

Plant manipulations

At each site we randomly selected six individuals of

E. australis

(78 plants in total). These plants covered a wide rangeof sizes, as assessed by an index of lignotuber area (

La

)(

La

=

π

* D

1

* D

2

/4), obtained from the two largest diametersof the lignotuber perpendicular one to the other (D

1

and D

2

).The lignotuber area index is highly and significantlycorrelated with the size of the whole plant (Moreno

et al

.,1999). The plants included in this study had a mean (

±

SE)lignotuber area of 255.8

±

25.8 cm

2

(from 44 to 1432 cm

2

).In mid-summer (19 and 30 August), the aerial parts of allplants were clipped and removed. This procedure tried tosimulate the effect of removal of above-ground biomasscaused by a fire with null severity and no ash fertilization. Theplants were then fenced with chicken wire to avoid herbivoryby rabbits or ungulates. To diminish differential competitiveinteractions with neighbours, the biomass of all plants in a0.5-m radius circle around each target

E. australis

plant wascut and removed.

Resprouting vigour

Resprouting vigour was monitored three times: in January(4 months after clipping), April (7 months) and September(12 months) of the following year. At each sampling date wecounted the number of resprouts in all plants (RN, number)and measured the length of the longest resprout (resproutmaximum length, RML, cm). From these measurements weestimated resprout biomass (RB, cm), by applying a regressionequation obtained in a different set of plants (ln RB =

−

3.25 + 0.12 * sqrt RN + 1.81 * ln RML;

R

2

= 0.72). A singleRML measurement had probed to be more tightly relatedto resprout biomass than resprout mean length obtainedfrom multiple measurements. Twelve months after clipping(September of the next year), plants from two of the sites (G2and C1) had been browsed, and were discarded for further

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analysis. Consequently, the number of sites from which datawas available was 13 (4 and 7 months after clipping) and 11(12 months after clipping).

Plant carbohydrate and mineral nutrient content

Samples from lignotubers and roots were obtained fromthree plants of

E. australis

at each site, for determinations ofnonstructural carbohydrates and nitrogen concentrations.Previous trials indicate that phosphorus concentrations in thelignotuber were very small and this element was not includedin the study. Sampling was done concurrently with clippingthe target

E. australis

plants. Because of the semidestructivenature of sampling (see below, this section), plants sampledfor TNC and N determinations were not later used inmonitoring of resprouting. Lignotuber samples were obtainedwith a Pressler-type borer. Root samples were obtained fromroots excavated close to the lignotuber. All samples wereimmediately immersed in dry ice, taken to the laboratory andpulverized after being oven-dried. Determinations were madefor glucose (plus fructose), sucrose and starch concentrations,following the enzimatic method proposed by Azcón-Bieto &Osmond (1983) and described in Cruz & Moreno (2001a).The sum of glucose, sucrose and starch was termed totalnonstructural carbohydrates (TNC). Lignotuber and rootsamples were also analysed for nitrogen (N) content in a CHNauto-analyser (Perkin-Elmer 2400 CHN, Shelton, CT, USA).From the three plants sampled at each site we calculated themean population value of TNC, starch and N concentrations,respectively, which were expressed as mg g

−

1

d. wt.No statistically significant correlation was detected between

lignotuber area and TNC or N concentration (for TNC,

r

= 0.25,

P

> 0.05; for N,

r

= 0.15,

P

> 0.05;

n

= 39). Thus,concentrations were not related to plant (lignotuber) size.

Soil resource availability

Soil fertility was evaluated at each site after collecting fivesoil samples (0–10 cm depth) and mixing them into a singlesample (Cruz & Moreno, 2001b). The following analyses weremade: pH (1 : 2.5 soil : water), extractable cation concentration(sum of Na, K, Ca and Mg, after extraction by shaking 5 g ofsoil in 100 ml of ammonium acetate at pH of 7.0, anddetermination of Ca and Mg by atomic absorption and ofNa and K by flame photometry), total nitrogen, in a CHNautoanalyser (Perkin-Elmer 2400 CHN) after total combustion,and available phosphorus, after extraction with sulfuric andhydrochloric acid (Olsen & Summers, 1982).

Soil water availability was evaluated in a comparative way.Shoot predawn water potential (

Ψ

pd

) were measured interminal branches of each four additional, nondisturbed,individuals of

E. australis

per site, with a Scholander-typepressure chamber. Measurements were made during summer(August), at the same time when plants were clipped. The

period without rains lasted for at least 30 d before waterpotential measurements. We used the mean values of predawnwater potentials at each site as comparative indices of wateravailability.

Lignotuber relative size

The biomass, or other measure of the size of the lignotuber,can be expressed as an absolute value. However, the amountof biomass allocated to the lignotuber may also be expressedwith respect to that allocated to other plant structures (leaves,roots, etc.). For the same lignotuber dimension, the capacityto resprout by a plant may depend on the amount of leavesheld prior to the disturbance. This ‘relative’ size of thelignotuber with respect to the biomass of leaves may varybetween populations (Cruz & Moreno, 2001b). It wascalculated by obtaining the mean value of the individuals ofeach population from the

x

–

y

(leaf biomass, lignotuberbiomass) linear regressions. For this, 10 individuals weresampled at each site, from which we obtained the mean valueof the lignotuber biomass (

Lb

), adjusted for the mean value offoliar biomass (

Fb

) (Cruz & Moreno, 2001b), which will bedenoted as

Fb-Lb

. The greater the value of

Fb-Lb

, the greaterthe biomass of the lignotuber with respect to the same foliarbiomass.

Statistical analysis

The significance of differences among-sites for RN, RML andRB were tested separately at each sampling date by ANCOVAtests. In all cases,

La

was used as the covariable. In order tocorrect for normality, before analysis RN was square-roottransformed,

La

was ln transformed, and RML and RB wereln(

x

+ 1) transformed. The significance of differences among-sites for TNC, starch, and N concentrations in lignotubers orroots were tested by one-way ANOVA. The relationshipsbetween mean site values of plant reserve concentrations(N, starch and TNC) and soil resource indices (soil pH, totalN, available P and extractable cation concentrations, and plant

Ψ

pd

) were determined by Pearson correlation.The relationships between resprouting and the potentially

explanatory variables (plant reserve content and soil resources)were ascertained using site as the reference unit. Plants fromeach site may differ in size, and resprouting response is knownto depend on plant size. To avoid a confounding interpreta-tion of site effect caused by variations in plant size, we used atwo-step procedure in order to isolate the effect of a differen-tial plant size. First, we regressed RN, RML and RB on

La

,separately for each sampling date. This determined theamount of variance of the resprouting variables accountedby lignotuber size,

La

being a surrogate of this. Second, wecalculated for each site the mean value of the residuals fromthe previous regressions of the six individuals per site. Themagnitude of the residual indicates whether a plant had a


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more or less vigorous resprouting once it has been correctedby its size. We then calculated the correlation coefficientsbetween the mean values of the residuals of the resproutingvariables for each site and the variables characterizing soilresource availability (soil extractable cations, total nitrogen,available phosphorus and plant

Ψ

pd

) and plant stored carbo-hydrates and mineral nutrients (TNC, starch and N). Meanvalues of plant stored reserves must also be corrected forplant size, in order to be correlated with mean residuals ofresprouting variables. However, no statistically significantcorrelations were detected between carbohydrate or N reservesand plant size (see above, Plant carbohydrate and mineralnutrient content). Consequently, plant concentrations wereused as the size-independent magnitude of plant reserves.

In order to determine the relationship between the res-prouting response and the predisturbance relative lignotuberbiomass, we calculated Pearson correlation coefficients betweenthe resprouting variables (mean site values of the residuals ofthe

La

-RN,

La

-RML and

La

-RB regressions) measured at thedifferent sampling dates and the measure of the relative size ofthe lignotuber at each site (

Fb-Lb

adjusted means).

Results

Plant stored nutrient concentrations and soil fertility

Mean TNC concentrations of

E. australis

in August 1994were almost double in the roots than in the lignotuber (meanof 122 vs. 67 mg g

−

1

d. wt., Fig. 1a–b). Plant TNC concentrationvaried approximately two-fold among the sites, and thesedifferences were statistically significant both in lignotubers(ANOVA,

F

12,26

= 3.44,

P

< 0.01) and roots (ANOVA,

F

12,26

= 2.41,

P

< 0.05). Starch concentrations comprised, onaverage, 44% of TNC in the lignotuber, and 52% in the roots.Starch concentration was more variable among the sites in thelignotubers (almost six-fold) than in the roots (Fig. 1a–b).Indeed, starch concentrations were statistically significantlydifferent among the sites only in the lignotubers (ANOVA,

F

12,26

= 7.43,

P

< 0.001). Plant N concentrations in theroots and lignotubers were low, rarely exceeding 3 mg g

−

1

d. wt. (Fig. 2). Mean N concentrations were statisticallysignificantly different among sites only in the roots (ANOVA,

F

12,26 = 6.37, P < 0.001). The sites also varied with respectto some characteristics of soil resource availability, such astotal nitrogen, available phosphorus, extractable cation con-centration (Cruz et al., 2002) or plant water potentials duringsummer (it ranged from −0.56 to −2.59 MPa). Carbohydrateconcentrations of the lignotuber were not statisticallysignificantly correlated with any of the soil variables, whereas

Fig. 1 Carbohydrate concentrations (TNC: open columns, starch: filled columns; mean ± SE, mg g−1 d. wt.) of (a) lignotubers, and (b) roots of E. australis at the different sites at the time of clipping (mid-summer) (n = 3).

Table 1 Correlation coefficients between the variables indicative of soil resource availability and nitrogen and carbohydrate concentrations in lignotubers and roots of E. australis

Soil fertilityWater availability

Total N Available P Cations pH Ψpd Aug

LignotuberStarch −0.39 −0.16 −0.15 −0.31 −0.26TNC −0.30 −0.25 −0.16 −0.35 −0.34N 0.72 (**) −0.19 0.29 −0.21 −0.11

RootsStarch 0.07 −0.69 (**) −0.11 −0.72 (**) −0.26TNC 0.34 −0.54 −0.25 −0.34 −0.29N 0.15 0.07 −0.01 0.02 −0.06

(n.s) P > 0.05; (*) 0.05 = P > 0.01; (**) 0.01 = P > 0.001; (***) P = 0.001.

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starch concentrations in the roots were statistically significantlyand negatively correlated with soil pH and available phosphorus(Table 1). Nitrogen concentrations into the lignotuber showeda positive and statistically significant correlation with soil totalnitrogen (Table 1).

Number and growth of resprouts

RN reached a maximum for most sites at 7 months after clipping(mean of 153 resprouts per plant), and then declined to amean of 115 resprouts per plant 1 yr after clipping (Fig. 3). Siteeffect for RN was statistically significant at 4 and 12 monthsafter clipping (ANCOVA, P < 0.05, Table 2). RML showed acontinuous increase during the study period, reaching a meanmaximum of 54 cm 1 yr after clipping (Fig. 4). RB, estimated

Fig. 2 Nitrogen concentrations (mean ± SE, mg g−1 d. wt.) of (a) lignotubers, and (b) roots of E. australis at the different sites at the time of clipping (mid-summer) (n = 3).

Fig. 3 Resprout number (RN, mean ± SE, no.) of E. australis at the different sites at (a) 4 months (b) 7 months, and (c) 12 months after clipping (mid-summer) (n = 6).

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from measures of RN and RML, reached a mean of c. 213 gper plant 1 yr after clipping. (Fig. 5). Growth rates of theresprouts showed a consistent pattern of among-site variation,as indicated by the significant differences found at all samplingdates for RML and RB (ANCOVA, P < 0.001, Table 2).

Relationships between number and growth of resprouts and plant resources

Correlation coefficients corresponding to the La-RN, La-RMLand La-RB regressions are shown in Table 3. The amount ofvariance of the different resprouting variables accounted bylignotuber area varied with time, but they were generallymoderate for RN and RB and much lower for RML. Theresiduals from these regressions showed correlation coefficientswith starch, TNC or N concentrations of lignotubers androots which were, in all cases, low and statistically nonsignificant(Table 4). On the contrary, residuals of the resprouting-Laregressions showed some significant correlations with somecharacteristics of soil resource availability, such as extractablecations, total nitrogen or plant water potentials duringsummer (Table 4). The coefficients of such relationships were,in most cases, positive, suggesting a stimulatory effect of alarger availability of soil resources on resprouting. Correlationcoefficients between La-RN residuals and Fb-Lb adjustedmeans were always low and statistically nonsignificant. However,La-RML and La-RB residuals became statistically significantand negatively correlated with the lignotuber relative sizewhen measured 1 yr after clipping (Table 4). This suggeststhat resprout production was not affected by the previousrelative size of the lignotuber, but that the growth of theresprouts was higher in those sites in which the plants carried

Table 2 Results of the ANCOVA tests for significance of the among-site differences in the variables indicative of resprouting vigor of Erica australis (RN, RML and RB), measured at different time (n = 13). La was used as the covariable

ANCOVA

Covariable Site effect

d.f. F P d.f. F P

RN4 months 1 34.48 *** 12 2.46 *7 months 1 57.80 *** 12 0.89 n.s.12 months 1 37.14 *** 10 2.39 *

RML4 months 1 16.16 *** 12 8.14 ***7 months 1 17.01 *** 12 5.29 ***12 months 1 1.31 n.s. 10 5.66 ***

RB4 months 1 31.30 *** 12 7.94 ***7 months 1 50.94 *** 12 4.46 ***12 months 1 18.38 *** 10 3.98 ***

(n.s) P > 0.05; (*) 0.05 ≥ P > 0.01; (**) 0.01 ≥ P > 0.001; (***) P ≤ 0.001.

Fig. 4 Resprout maximum length (RML, mean ± SE, cm) of E. australis at the different sites at (a) 4 months (b) 7 months, and (c) 12 months after clipping (mid-summer) (n = 6).


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a larger number of leaves per unit of lignotuber. Whenresprouting variables were regressed by steps against allpossible explanatory variables, only some variables related tosoil fertility and water availability were selected, along withthe relative size of the lignotuber (Table 5). These resultssuggest that the among-site variation in resprouting vigourwas mostly accounted for by differences in soil resourceavailability and plant structure, rather than by differences inreserve concentrations stored by the plants among the sites.

Discussion

This study documents a significant among-site variability inthe resprouting vigour by E. australis, confirming the resultsobtained in previous studies (Cruz & Moreno, 2001c; Cruzet al., 2002). Indeed, during the first year of resprouting, thedifferent populations of E. australis studied here showed a 2-fold variation in either resprout number or maximum length.As plants were subjected to identical disturbance severity inall cases, that is, complete removal of above-ground parts with-out any other damage to the lignotuber, such variability inresprouting response might be due to a great extent to differ-ences in resource supply among the sites. These resources maybe supplied from the reserves stored by the plant within itsbelow-ground organs, or may be obtained from the soil whenregrowth occurs. In a previous study (Cruz et al., 2002), wefound that a significant amount of variance in resprouting ofE. australis among the sites was accounted for by some variablesrelated to water and nutrient availability in the soil, suggestingthat the amount of resources supplied from the soil may be adetermining factor of resprouting. As the amount of resourcesstored within the plant may also be a function of soil resourceavailability, it was necessary to determine the amount of vari-ance of resprouting specifically explained by each group of resources.

Table 3 Correlation coefficients between the variables indicative of resprouting vigor of E. australis (RN, RML and RB), measured at different time, and the lignotuber area (La, ln cm2). Regressions were calculated at the individual level

Correlation (r)with La n Significance

RN (No) [sqrt]5 months 0.59 78 (***)8 months 0.70 78 (***)13 months 0.58 66 (***)RML (cm) [ln + 1]5 months 0.36 78 (**)8 months 0.50 78 (***)13 months 0.30 66 (*)RB (g) [ln + 1]5 months 0.52 78 (***)8 months 0.67 78 (***)13 months 0.56 66 (***)

(n.s) P > 0.05; (*) 0.05 ≥ P > 0.01; (**) 0.01 ≥ P > 0.001; (***) P ≤ 0.001.

Fig. 5 Resprout biomass (RB, mean ± SE, g) of E. australis at the different sites at (a) 4 months (b) 7 months, and (c) 12 months after clipping (mid-summer) (n = 6). RB was estimated from measurements of RN and RML.


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How much did intersite variations in carbohydrate storage contribute to cause differences in resprouting?

Fluctuation in the carbohydrate content of the resproutingorgans through the year may be responsible for temporalvariations in the subsequent vigour of the resprouting response(Rundel et al., 1987; Malanson & Trabaud, 1988; Castellet al., 1994). However, it has not been established whetherdifferences in carbohydrate content between neighbouringplants may cause differences in their resprouting responsewhen disturbed at the same time. Sparks & Oechel (1993)observed that the capacity of the shrub Adenostoma fasciculatumto produce new resprouts after an experimental fire had nocorrelation with the carbohydrate content in the lignotuber.However, these authors measured the carbohydrate concen-

trations in samples collected 1 yr before burning, so that thestatus of stored reserves in the plant at the time of burning wasunknown. In the present study we found a 2-fold variationamong the sites in the mean values of lignotuber and rootcarbohydrate concentrations of E. australis (almost 6-fold inthe case of lignotuber starch), after measuring the concentrationsjust at the time of clipping the plants. Simple calculationsbased on the range of carbohydrate concentrations measuredhere lead us to the conclusion that an average medium-sizedplant, with a lignotuber biomass of 1500 g, of which c. 66%can be devoted to storage, could have stored in this organfrom 44 to 100 g of TNC, depending on the site. Consideringthat stored carbohydrates are thought to constitute the maincarbon source for regrowth during the early stages ofresprouting, such a variation should have caused a substantially

Table 4 Correlation coefficients between the mean site residuals of the La-RN, La-RML and La-RB relationships, measured at different time, and mean site values of soil resources, plant carbohydrates and nutrient concentrations and lignotuber relative size (Fb-Lb) at each site in several populations of E. australis (4 and 7 months after clipping: n = 13; 12 months after clipping: n = 11)

Soil resource availability Lignotuber stored reserves Root stored reserves Lignotuber relative size

N P Cat pH Ψpd Aug N Starch TNC N Starch TNC Fb-Lb

Residuals of La-RN4 months 0.59 (*) −0.11 0.64 (*) −0.15 0.20 0.33 −0.25 −0.16 0.10 0.28 0.17 −0.057 months −0.11 −0.10 0.56 (*) 0.10 −0.30 −0.18 0.11 0.16 0.05 0.27 0.02 0.4712 months −0.05 −0.44 0.32 −0.01 −0.71 (*) −0.15 0.15 0.19 −0.30 0.23 0.06 0.49

Residuals of La-RML4 months 0.43 0.02 0.42 −0.22 0.51 0.17 −0.28 −0.22 −0.02 0.35 0.19 −0.427 months 0.59 (*) 0.05 0.22 −0.10 0.38 0.19 −0.26 −0.15 0.14 0.26 0.30 −0.2612 months 0.28 0.21 −0.30 −0.25 0.69 (*) 0.14 0.05 0.07 0.31 0.19 0.27 −0.74 (**)

Residuals of La-RB4 months 0.49 −0.06 0.47 −0.32 0.44 0.29 −0.21 −0.12 0.11 0.36 0.19 −0.417 months 0.54 0.04 0.33 −0.09 0.37 0.15 −0.27 −0.16 0.12 0.27 0.28 −0.2112 months 0.30 0.07 −0.21 −0.24 0.50 0.10 0.12 0.15 0.23 0.30 0.25 −0.64 (*)

(*) 0.05 ≥ P > 0.01; (**) 0.01 ≥ P > 0.001.

Independent variables Regression model R2 P

Y = Residuals of La-RN4 months X1: Soil cations Y = −2.79 + 0.03 (X1) 0.40 0.0207 months X1: Soil cations Y = −1.16 + 0.01 (X1) 0.31 0.04712 months X1: Ψpd summer Y = −2.17 – 1.44 (X1) 0.50 0.015

Y = Residuals of La-RML4 months – – – –7 months X1: Soil nitrogen Y = −0.70 + 3.07 (X1) 0.35 0.03412 months X1: Fb-Lb Y = 1.50 – 0.20 (X1) + 0.18 (X2) 0.73 0.006

X2: Ψpd summer

Y = Residuals of La-RB4 months – – – –7 months – – – –12 months X1: Fb-Lb Y = 2.26 – 0.37 (X1) 0.41 0.035

Table 5 Stepwise regression models of the mean site residuals of the La-resprout variables relationships of E. australis measured at different times on some variables related to soil resource availability, plant nutrient concentrations and lignotuber relative size of sites


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different resprouting vigour among the sites studied here.However, once corrected for the differences in lignotuber size,there were no statistically significant correlations between anyof the variables indicating the carbohydrate concentrations ofthe lignotubers or roots at the different sites and those relatedto resprouting vigour. In other words, we found no evidencesuggesting that the significant variation found among thesites in the mean values of starch and total carbohydrateconcentrations in the below-ground organs would be themain responsible factor of the variation observed later in thevariables describing the vigour of the resprouting response.Thus, the amount of resources contained within the plantmay be less relevant than suspected as a driving factor ofresprouting. The populations studied here included a relativelywide range of carbohydrate concentrations. This supports thehypothesis that this species may store reserves, particularly ofcarbohydrates, in greater abundance than needed for supportinga single resprouting event (Cruz & Moreno, 2001a).

What is the role played by the nitrogen reserves contained in the lignotuber on resprouting?

The soils of the study sites are acidic and moderately poorin mineral nutrient (N, P) concentrations. We would expectthat accumulation of nitrogen, or other mineral nutrients,in the lignotubers or roots of E. australis would have beenrelevant for ensuring mineral nutrient supply for regrowth insuch a nutrient-deficient environment. Despite some authorsfinding significant depletion in the pool of mineral nutrientsstored by lignotubers and roots during resprouting episodes(Miyanishi & Kellman, 1986; Canadell & López-Soria,1998), it has not been clearly demonstrated that the mineralnutrients stored by the plants would contribute significantlyto sustain resprout growth. Resprouting plants that inhabitnitrogen-deficient soils, such as in the Mediterranean-typeecosystems of Australia, do not accumulate nitrogen in theirunderground organs in greater amounts than the non-resprouting congeners (Pate et al., 1990). This suggests thatmineral nutrient storage is not very relevant for ensur-ing resprouting. In the case of the nitrogen concentrationsthat we measured in this study for E. australis, they canbe considered as relatively low in comparison with thosedescribed by Shaver (1983) for other woody species fromMediterranean-type areas of California and Chile, and thosereported by Canadell & López-Soria (1998) for the resprouterErica arborea. In addition, the concentrations of this nutrientmeasured at the time of clipping in the lignotubers and rootswere not statistically significantly correlated with theresprouting vigour in the following year. We therefore foundno evidence that lignotubers of E. australis may constitute asignificant source of nitrogen for supporting resprout growth,and a differential nitrogen storage does not seem to be acontributing factor in explaining the variation in theresprouting response by this species.

What is the role played by soil resources on resprouting?

Resprouting variables showed some high and statisticallysignificant correlations with several characteristics of soil resourceavailability, such as total nitrogen content, extractable cationcontent or plant water potential during summer, used here asa relative index of water availability at the sites. Total nitrogenand extractable cation content showed positive correlations withresprout length or number, respectively, suggesting a positiveeffect of soil fertility on resprouting. The positive correlationof plant water potential measured during summer on resproutlength can be interpreted as a positive effect of soil moistureon resprouting. Such effect was reported in a previous studyto be relevant for a short period of time (Cruz et al., 2003),suggesting that early resprouting during drought periodswould be more vigorous in sites with less severe water stress.Paradoxically, in the present study the effect of water potentialcontributed to explain a significant portion of the variation inresprout length not immediately, but 1 yr after clipping. Thisresult might be explained by the severe drought of the springfollowing the treatment implementation, which may havecaused the relative differences in soil moisture among the sitesduring the period of summer drought to be maintainedduring the following year. Plant water potential had asignificant but negative effect over resprout number at thesame sampling date. Resprout number tended to decreaseduring spring, apparently due to ‘self-thinning’. It seems thathigher water availability, by promoting a more vigorousresprout growth, might have caused a more intense reductionin the subsequent number of resprouts.

Resprouting and the relative size of the lignotuber

Resprouting vigour of E. australis seems to be also largelycontrolled by the relative biomass allocation made by theplant to the lignotuber, as growth of the resprouts during thefirst year after clipping was more vigorous at the sites in whichplants carried smaller lignotubers for the same leaf biomass.The relative size of the lignotuber is partially controlled by soilresources, resulting in the plant developing a proportionally largerlignotuber at sites apparently unfavourable for plant growth(Cruz & Moreno, 2001b). This finding suggests that soilresource availability is a powerful driving force of resprouting,either directly, presumably by determining the water andmineral nutrient supply to regrowth, or indirectly, affectingthe relative size of the resprouting organ. However, we did notfind evidence that the concentration of carbohydrate reservesstored by the plant were related to soil resource availability.

Conclusion

This study supports evidence suggesting that early resproutingof co-occurring populations of the Mediterranean-type shrub


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Erica australis is largely driven by the relative size of theresprouting organ (negatively) and the availability of some soilresources (mostly positively), particularly of water. Given therelationships between soil resources and relative size of thelignotuber (Cruz & Moreno, 2001b), it can be concluded thatmoist and moderately fertile soils will favour a more vigorousresprouting, either directly, by causing a higher water andmineral nutrient supply to regrowth, or indirectly, by causinga proportionally larger biomass allocation to leaves per unit oflignotuber. Soil resources showed a less evident relationshipwith the storage process, particularly that of carbohydrates.In any case, the concentration of reserves was unrelated toresprouting vigour. In conclusion this study found thatresprouting is more vigorous the smaller the storage organ.Further, how much this is filled, that is, the concentration ofreserves stored within the lignotuber, is not a relevant driverof resprouting. The role usually attributed to the lignotuber asan organ developed to enhance resprouting is not supportedby this study.

Acknowledgements

Funding was provided by the EC (Project ENV-CT91-320).We thank Dr F. Fernández del Campo and Dr C. Fenoll, andAngeles Muñoz (Departamento de Fisiología Vegetal, UAM)for their advice and for carbohydrate determinations, respectively.We also thank Angel Velasco and Nuria Acevedo for help inthe field.

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plant stored reserves do not drive resprouting of the lignotuberous shrub erica australis

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