Climate Change Treeline

PACE AND PATTERN OF RECENT TREELINE DYNAMICS:RESPONSE OF ECOTONES TO CLIMATIC VARIABILITY

IN THE SPANISH PYRENEES

J. JULIO CAMARERO and EMILIA GUTIÉRREZ

Dept. Ecology, Fac. Biology, University of Barcelona, Avda. Diagonal, 645, 08028 Barcelona, SpainE-mail: [email protected]

Abstract. Treeline ecotones are regarded as sensitive monitors of the recent climatic warming.However, it has been suggested that their sensitivity depends more on changes in tree density than ontreeline position. We study these processes and the effect of climate, mainly air temperature, on treerecruitment and recent treeline dynamics. We selected three relatively undisturbed sites in the SpanishPyrenees, dominated by Pinus uncinata, and analyzed their recent dynamics at local spatial (0.3–0.5ha) and short temporal scales (100–300 years). We wanted to establish whether higher temperaturewas the only climatic factor causing an upward shift of the studied alpine treelines. The data wereport show that treelines were ascending until a period of high interannual variability in mean tem-perature started (1950–95). During the late twentieth century, treeline fluctuation was less sensitive toclimate than was the change in tree density within the ecotone. Tree recruitment and treeline positionresponded to contrasting climatic signals; tree recruitment was favored by high March temperatureswhereas treeline position ascended in response to warm springs. We found a negative relationshipbetween mean treeline-advance rate and March temperature variability. According to our findings,if the interannual variability of March temperature increases, the probability of successful treelineascent will decrease.

1. Introduction

Tree populations at their distribution margins are theoretically very sensitive toclimate variability (Brubaker, 1986). This is the case for latitudinal and altitu-dinal treeline ecotones, where low temperature limits tree growth (Tranquillini,1979). Their value and reliability as monitors of the recent climate warming isbased mainly on studies of tree growth and recruitment within these ecologicalboundaries (Tranquillini, 1979; Payette and Filion, 1985; Slatyer and Noble, 1992;Lescop-Sinclair and Payette, 1995; Paulsen et al., 2000). In this study, we define thealpine forest-tundra ecotone as the area bounded by the treeline (maximum eleva-tion of live individuals with stems at least 2 m high) and the timberline (maximumelevation of a closed forest). Several studies on alpine treeline have documented al-titudinal shift during the first half of the twentieth century followed by tree-densityincrease within the ecotone during the last decades (Kullman, 1979; Rochefort etal., 1994; Szeicz and MacDonald, 1995; MacDonald et al., 1998). There have beenalso reports on treeline recession during recent cold episodes (Kullman, 1996).However, few detailed studies have so far described how climate, and mainly

Climatic Change 63: 181–200, 2004.© 2004 Kluwer Academic Publishers. Printed in the Netherlands.

182 J. JULIO CAMARERO AND EMILIA GUTIÉRREZ

temperature, influences recruitment and treeline-shift at altitudinal forest-tundraecotones. Our main objective was to quantify the treeline-climate relationship ata small spatiotemporal scale (0.3–0.5 ha plot, 100–300 yrs). In order to do this,we focused on changes in treeline elevation and tree recruitment within relativelyundisturbed treeline ecotones in the Spanish Pyrenees. A similar response at all thestudied sites would indicate a common regional effect, most likely a climate factor.We were more interested in tree recruitment because of reports that it was moresensitive to climate variability than tree mortality was (Payette and Filion, 1985;Lloyd, 1997). We suggest that a greater variability in air temperature may be theultimate climate factor favoring an upward shift of alpine mesic treelines.

Like most Eurasian mountains, the Pyrenees provide a unique opportunityto study the effect of two global-change components, i.e., climate warming andland-use modification, on treeline ecotone. Between 1882 and 1970, mean an-nual temperature increased by 0.83 ◦C at the Pic du Midi meteorological station(43◦04′ N, 00◦09′ E, 2862 m a.s.l.) in the Central Pyrenees (Bücher and Dessens,1991). In addition, grazing pressure in this area has been falling since the 1950s,which has led to drastic modification in land use (García-Ruiz and Lasanta-Martínez, 1990). For instance, Bas (1993) estimated a 80% reduction of grazingpressure in a village in the Catalan Pyrenees paralleled by a shift from nomadicto stabling flocks of sheep. These combined processes have caused pronouncedchanges in the structure of the Pyrenean treeline ecotone (Soutadé et al., 1982).

2. Materials and Methods

2.1. STUDY SITES

We reconstructed recent treeline dynamics at the following sites: Ordesa – O,42◦37′ N, 00◦02′ W, 2110–2100 m a.s.l.; Tessó – T, 42◦36′ N, 01◦03′ E, 2360–2330 m; Estanys de la Pera – EP, 42◦28′ N, 01◦38′ E, 2430–2360 m (Figure 1).The mean slope ranged 20◦ (O)–25◦ (T, EP). The three sites represent most of thegeographical variability in the Pyrenean treeline ecotone marked by the W-E cli-mate gradient across the range (W – Atlantic influence; Central area – continentalinfluence; E – Mediterranean influence). The studied ecotones are dominated byPinus uncinata Ram., a shade-intolerant and long-lived (700 yrs.) conifer, whichforms most treelines in the Pyrenees (Ceballos and Ruiz de la Torre, 1979; Boschet al., 1992). The sites O and T have not been affected by local anthropogenic dis-turbances (logging, grazing) during the last 50 years. At these sites recent livestockestimates ranged 2–24 sheep month ha−1 according to Aldezábal et al. (1992) andBas et al. (1994). According to historical documentation, site T has not been in-tensively disturbed since the eighteenth century (Bringue, 1995). Site EP could beregarded as slightly disturbed by grazing (estimated present livestock is ca. 25–50sheep month ha−1).

TREELINE DYNAMICS IN THE PYRENEES 183

Figure 1. Distribution of P. uncinata (black areas) in the Iberian Peninsula and detailed maps of thestudied treelines (O, T, EP). The black rectangles at each site correspond to the approximate locationof the plot.

The climate at the study sites is continental with Atlantic (T site) or Mediter-ranean (O and EP sites) influence. Mean annual temperature and total annualprecipitation range from 2 to 5 ◦C and from 1200 (EP) to 1600 mm (T), re-spectively. Estimated lowest and highest mean monthly temperatures are –4 ◦C(January–February) and 11 ◦C (July). Maximum snow-cover thickness is reachedin winter-spring and ranges from 0.5 (O, EP) to 3 m (T). Snow cover differencesare reflected in the understory vegetation. At site T, we found a community typicalof longer and deeper snow-cover sites dominated by Rhododendron ferrugineumand Vaccinium myrtillus. At sites O and EP, more xeric species were found such asJuniperus communis subsp. alpina, Festuca rubra and Calluna vulgaris.

2.2. FIELD SAMPLING

A rectangular plot (30·100 m, the EP site; 30·140 m, the O and T sites) was markedout at each site in topographically uniform parts of the treeline ecotone. The plothad its longer side parallel to maximum slope and included current treeline andtimberline. The following variables were recorded in the field for every P. uncinata


individual within the plot: location in the plot (x and y coordinates); size (diameterat breast height, height); and growth form (arborescent, flagged-krummholz, andkrummholz). Individuals whose height was equal or less than 0.5 m were regardedas seedlings. All individuals were tagged for their future monitoring.

2.3. DENDROCHRONOLOGICAL METHODS

Germination date was estimated by taking out a core from each live individual’smain stem as close to the ground as possible. This was done for all living individ-uals located within the plot whose height was greater than 0.5 m. All cores weremounted, sanded, and crossdated using standard dendrochronological methodol-ogy (Stokes and Smiley, 1968). Inner-ring dates were corrected for (i) years tocore height and (ii) years to center (missed pith). The correction was made using(i) age-height regression and (ii) age-diameter regression combined with the fittingof a circle template to the ring curvature so as to estimate the distance of the coreto the center. At sites T and EP, we estimated nondestructively the ages of thoseindividuals with height ≤0.5 m by counting the number of branch whorls and budscars on the main stem. This age estimation was validated comparing it with theage obtained counting the tree-rings in basal disks taken from a subsample of treeslocated outside but near the plot. This procedure was not carried out at site Obecause of the multistemmed character of most of the individuals (Camarero andGutiérrez, 1999). A static age structure of live trees is the expression of changein the rate of tree recruitment and mortality over time (Harcombe, 1987). In orderto interpret changes in tree density as a result of tree recruitment dynamics, weassumed that mortality was nearly constant for all cohorts.

To analyze tree recruitment dynamics as related to radial growth, seven residualchronologies from adult P. uncinata growing in high-elevation (2075–2360 m a.s.l.)subalpine forests were used (see also Tardif et al., 2003). These stands are near siteT, and they are a reliable sample of the variability in P. uncinata radial growthin the Spanish Pyrenees (Gutiérrez et al., 1998). Trees were sampled followingstandard dendrochronological techniques, taking at least 2 cores per tree at 1.3 m.These cores were processed in a similar way as the basal ones, but ring widthwas measured using a semiautomatic system (Aniol-CATRAS) with a resolutionup to 0.01 mm. Each ring-width series was standardized using a spline functionwith a 50% frequency response of 32 years (Cook and Peters, 1981). Autoregres-sive modeling was then performed to remove temporal autocorrelation, which wasmostly of first order. Standardization involved transforming the ring-width valueinto a dimensionless index by dividing the observed values by the expected valuesgiven by the spline function (Fritts, 1976). Then the indexed residual series wereaveraged. Following this procedure, long-term (low frequency) trend was removedfrom the tree-ring series. To standardize the tree-ring series we used the programARSTAN (Cook, 1985). Calculation details and chronology statistics can be foundelsewhere (Gutiérrez et al., 1998).


2.4. CLIMATIC INFLUENCE ON TREELINE DYNAMICS

In order to calculate the rate of treeline shift, maximum elevation (y coordinate)of live individuals with stems at least 2 m high (treeline) was determined for 25-yr intervals (maximum treeline elevation). Each plot was divided into 3 altitudinalsubtransects (10-m wide), so as to take the treeline spatial heterogeneity into ac-count. We calculated mean maximum elevation of the treeline and its standarddeviation for 25-yr intervals, using data from the three subtransects per site. Sinceresults did not differ greatly from those obtained using the maximum treeline ele-vation of the entire plot, we used the latter and simpler variable – which in additionwas more related to our interest in the effect of temperature on tree recruitmentwithin the treeline ecotone. The treeline-shift rate (m · yr−1) was calculated bydividing the change in treeline elevation, between successive intervals, by the timeelapsed. On average, a 1-year old seedling took ∼40 years to become a 2-m tree(Camarero, 1999), and we assumed that this time span was constant. The treelineadvanced (rate >0) or remained stable (rate = 0) during all the considered periodsat the studied sites.

In order to study the effect of climate on tree recruitment, the number of pinerecruits within every ten year interval for the 1880–1980 period was calculated.These data were related to monthly mean minimum temperatures (from the Pic duMidi station) averaged for the same 10-yr intervals. Temperature was the most re-liable climatic variable for this station (Bücher and Dessens, 1991). No significanttemporal autocorrelation was detected for recruitment data. In order to quantify theclimatic influence of temperature on treeline dynamics, we used a reconstructionof monthly mean surface-air temperatures (1781–1997) for lake ‘Estany Redó’(42◦39′ N, 00◦46′ E, 2240 m a.s.l.). It was based on lowland instrumental climaterecords (Agustí-Panareda et al., 2000). The temperatures were averaged for 25-yr intervals and related to maximum treeline-advance rate estimated for the sametime intervals during the period of 1775–1995 (1775–99, 1800–24, . . . , 1975–95).In this case we attempted to avoid circular inference by using climate data insteadof dendroclimatic reconstruction. In all the cases, Spearman’s rank correlation co-efficient (rs) was used. If in any paired comparison one or two variables showeda significant (P ≤ 0.05) temporal trend their correlation value was not taken intoaccount.

3. Results and Discussion

The main changes suggested by repeated historical photographs taken along thetwentieth century (Figure 2) were: (i) increase in tree size and density withinthe treeline ecotone; (ii) reduced or even null altitudinal ascent of the treeline.A similar trend was observed in all the studied treeline ecotones. It could suggesta common regional cause such as climate. The data in Figure 3 show this tendency


Figure 2. Structural changes at a treeline ecotone in the Spanish Pyrenees during the twentiethcentury. The most prominent change is the increase in tree size and density across the treelineecotone. Maximum treeline elevation has not increased (white line). These two photographs weretaken in 1909 (Lucien Briet, Musee Pyreneen, Lourdes) and 1997 (J. L. Acın Fanlo) at Punta Diazas(42◦38′ N, 00◦03′ W, Ordesa y Monte Perdido National Park), near site O.

at site T. Firstly, there has been a recent increase in tree establishment and densitywithin the ecotone, specially during the period of 1900–49. Secondly, the treelineascended greatly during the last half of the nineteenth century, reached maxi-mum elevation at the beginning of the twentieth century and then remained stablethroughout the rest of that century. Mean treeline elevation followed a paralleltrend and remained approximately stable during the past century. Maximum spatial


Figure 3. Spatiotemporal variability in tree density and treeline position (maximum elevation oflive individuals with stems at least 2 m high) within the alpine forest-tundra ecotone at site T. Thefigure shows the same plot (30 m · 140 m; the y axis follows the altitudinal gradient upslope – thearrow points upslope) during different time periods (1750–1849, . . . , 1950–97). Various limits areshown: uppermost treeline (MAX – gray thick line) of all individuals present during each period,mean treeline (AVG – black thick line – average of maximum elevation of the treeline formed onlyby individuals established during each 25-yr interval) and its standard deviation (±SD – black thinline). Each filled black symbol represents an individual that established and became a tree (live indi-viduals with stems at least 2 m high) during the period indicated above. Unfilled symbols representtrees established during periods previous to the one indicated above. Different symbols representtree-establishment periods (e.g., circles = 1750–1849). Current timberline is at y = 40 m.


heterogeneity (standard deviation) of mean treeline elevation increased during theperiod of 1850–99 and decreased during that of 1950–97. That pattern might bethe result of the high tree-recruitment rate during that period as well as during theprevious decades. Overall, these changes agree with those observed in repeatedhistorical photographs, i.e., increase of tree density within the ecotone but minoror null treeline shifts (Figure 2). During the first half of the twentieth century, thespatial clustering of pine recruits was greater at short distance (less than 9 m) thanduring the second half (Camarero et al., 2000a). These patterns developed at a timecharacterised by very warm springs and summers and low temperature variabilityduring the first half of the twentieth century, but warm fall-winter seasons andhigh interannual temperature variability during the second half of the last century(Bücher and Dessens, 1991; Manrique and Fernández-Cancio, 2000).

These contrasting climatic trends were also reflected in the temporal variabilityin radial growth (Tardif et al., 2003). High-elevation subalpine P. uncinata stands inthe Central Pyrenees showed two contrasting patterns of radial growth during thetwentieth century (Figures 4A–C). The first half of that century was characterisedby: (i) low interannual variability (low frequency of wide and narrow rings, Fig-ure 4A, low moving standard deviation of mean radial-growth index, Figure 4C),(ii) reduced similarity in growth among sites (low mean inter-site correlation,Figure 4B). A reverse pattern was found during the last half of the twentieth andduring the nineteenth century. Pine recruitment at treeline was very high during theperiods of 1925–49 (site T) and 1950–74 (sites O and EP; Figure 4D). Conversely,the treeline-advance rate was null during the last half of the twentieth century andit reached maximum values at the end of the nineteenth century (1850–74, sitesO and T) or at the beginning of the twentieth century (1900–24, site EP; Fig-ure 4E and Table I). The mean ‘regional’ maximum treeline-advance rate reachedits highest values during the periods of 1850–74 and 1900–24. If these data wereanalyzed subdividing each plot into three 10-m wide transects running along theslope (n = 9 transects per site), the results varied slightly. During the period of1900–49, mean treeline-advance rate reached its highest value at sites T and EP.Furthermore, during the period of 1925–49 most of the subtransects showed alti-tudinal shift above maximum treeline elevation reached during previous periods(Table I). However, and also during the last 50 years, most of the subtransects didnot show any altitudinal ascent.

Climate affected tree recruitment and treeline-advance rate in different ways(Figure 5). Tree recruitment was favored by high monthly mean minimum temper-ature during March–April, July, and October (Figure 5A). The positive effect ofwarm spring and fall could be related to the increase in seedling mortality due tofrost during those seasons. However, such relationships may be more complex. Forinstance, high temperature in spring could speed up snowmelt, and lead to moredrying of soils in summer. This would intensify the negative effect of summerdrought on seedling survival (Puig, 1982; Lloyd, 1997). Other climatic factors,such as winter-spring snow cover, could improve reproductive success at treeline


Figure 4. Relationship between radial-growth (A–C), tree recruitment (D) within three treeline eco-tones (sites O, T, EP), and maximum treeline-advance rate (E) within these sites in the CentralPyrenees. (A) Relative frequency (percentage) of wide (> +1.5 SD; values above 0) and narrow(–1.5 SD<; values below 0) annual ring-width indices in seven subalpine P. uncinata stands. Max-imum and constant sample size reached around 1850 (n = 177 cores). (B) Mean (±SD) fixed(big dots) and moving (small dots) correlations (Pearson’s r; n = 21) between the seven residualchronologies every 25-yr period. (C) Mean (10-yr moving average) and standard deviation (SD,25-yr moving average) of annual ring-width indices in seven stands. (D) Tree-recruitment at treelineecotones (O, T, EP sites). (E) Maximum treeline-advance rate at these sites (bars) and estimate of thevariability of mean annual temperature (line; CV, coefficient of variation for each period based ontemperature reconstructed for the nearby ‘Estany Redo’ lake, 1781–1995). Note that tree recruitment,treeline-advance rate, and the CV of temperature are given for 25-yr periods except for the first andlast ones. Treeline-advance rate at site T during the period of 1850–74 was 4 m · yr−1. The colors ofbars correspond to the different treeline sites in (D) and (E).


Tabl

eI

Mea

n,st

anda

rdde

viat

ion

(±S

D)a

ndm

axim

umtr

eeli

ne-a

dvan

cera

te(m

·yr−

1,i

npa

rent

hese

s)at

thre

eal

titu

dina

ltr

eeli

neec

oton

esin

the

Cen

tral

Pyr

enee

s(O

,T,

and

EP

site

s)du

ring

the

last

150

year

s.T

hefi

fth

colu

mn

show

sm

ean

max

imum

rate

(±SD

)of

tree

line

adva

nce

aver

agin

gth

eva

lues

for

the

thre

esi

tes

(‘re

gion

al’

mea

n).

The

last

colu

mn

show

sre

lativ

efr

eque

ncy

(%)

ofsu

bstr

anse

cts

(n=

9)sh

owin

gal

titud

inal

asce

ntdu

ring

each

peri

od.

Mea

nva

lue

and

stan

dard

devi

atio

nw

ere

calc

ulat

edfo

rth

eth

ree

altit

udin

alsu

btra

nsec

tsat

each

plot

.The

high

est

mea

nan

dm

axim

umva

lues

for

each

site

are

inbo

ld

Per

iod

OT

EP

Mea

nS

ubtr

anse

cts

(%)

1850

–74

0.64

±0.

84(0

.82)

0.87

±1.

50(3

.99)

0.03

±0.

05(0

)1.

60±

2.11

50.0

0

1875

–99

0.22

±0.

39(0

)0.

39±

0.39

(0)

0.84

±1.

35(0

.05)

0.02

±0.

0366

.67

1900

–24

0.17

±0.

29(0

.50)

0.90

±1.

25(0

.36)

0.63

±0.

99(0

.80)

0.55

±0.

2255

.55

1925

–49

0.24

±0.

24(0

)0.

47±

0.40

(0.1

3)0.

97±

1.23

(0.6

2)0.

25±

0.33

77.7

8

1950

–74

0(0

)0.

27±

0.47

(0)

0.39

±0.

67(0

)0

±0

22.2

2

1975

–95

0(0

)0

(0)

0(0

)0

±0

0


Figure 5. Climatic influence on tree recruitment and treeline advance at P. uncinata treeline eco-tones. (A) Relationship between tree recruitment (absolute recruit number per hectare and year)and monthly mean minimum temperature (data from the Pic du Midi station, 1880–1980) at threetreeline ecotones (O, T, EP sites) in the Spanish Pyrenees. The correlation was obtained for 10-yrperiods (n = 10). (B) Relationship between monthly mean temperature reconstructed for a nearbyalpine lake (Estany Redo, 1781–1995) and maximum treeline-advance rate for 25-yr periods (sitesT and EP, n = 9; site O, n = 6). In both cases, the correlation (Spearman index, rs) calculatedfor all months and seasons (WIN, January–March; SPR, April–June; SUM, July–September; FAL,October–December). Significance level is indicated by the symbol over the bar (∗ = P ≤ 0.05;¶ = P ≤ 0.01).

(Kullman, 1979; Frey, 1983). In any case, most of them are affected directly orindirectly by air and soil temperatures.

The positive relationship between spring-summer temperature and tree recruit-ment at treeline has been observed both at altitudinal and latitudinal treelines(Kullman, 1983; Szeicz and MacDonald, 1995; Gutiérrez et al., 1998; Camareroand Gutiérrez, 1999). This relationship is related to temperature requirements,over a period of several summers, for successful seed production, germinationand seedling establishment (Zasada et al., 1992; Scott et al., 1997). Appropriatetemperatures are rarely attained at treeline environments, which causes the absenceof sexual regeneration (Arseneault and Payette, 1997). In addition, extremely coldepisodes have caused rapid treeline recession in the Swedish Scandes (Kullman,1996). The recent reduction in tree recruitment at the studied treeline ecotones, and


that observed at the turn of the twentieth century, could also be explained withinsuch context. If temperature interannual variability increased, the probability ofsuccessive favorable springs or summers would decrease. Therefore, tree recruit-ment would also decrease. This is shown in our data where ring-width is used asa proxy for climatic variability (Figure 4A–E). The hypothesis should be tested bycomparing forests with treeline ecotones, so as to quantify possible temporal lagsbetween tree recruitment peaks and warm episodes in such contrasting areas. Tem-poral lags up to 20–30 years have been found in boreal and subalpine forests (Scottet al., 1987; Gutiérrez et al., 1998; Suárez et al., 1999; Gervais and MacDonald,2000). These lags could be related to the greater importance for tree recruitment oftemperature at treelines vs. disturbances at forests (Zackrisson et al., 1995).

The advance of treeline was consistent and negatively related to high meanMarch and November temperatures (Figure 5B). Such negative correlation betweenmean March temperature and maximum treeline-advance rate for 25-yr was foundagain when comparing temperature data with the regional mean value (rs = −0.64;P = 0.06). However, this relationship was positive and weaker in the case ofspring temperature (April–June). The positive correlation between the regionaltreeline-advance rate and spring temperature was also significant (rs = 0.68;P ≤ 0.05). Paradoxically, November temperature of the year prior to growth isamongst the main climatic variables controlling positively the radial growth of P.uncinata during the year of growth (Camarero, 1999; Tardif et al., 2003). Thus,warm Novembers are related to high rates of radial growth in adults. However,higher November temperatures were associated with lower rates of treeline advanceat sites O and T (Figure 5B). In the Pyrenees, warm Novembers are associatedwith cyclonic conditions and high snow precipitation (Del Barrio et al., 1990),which may induce higher rates of mortality among established treeline individualsbecause of direct physical damage or snow avalanches (Furdada, 1996).

Overall, the responses of tree recruitment and treeline advance were rather sim-ilar at sites O and T as compared with site EP. It could be explained by four facts:(i) site EP is under the strongest Mediterranean influence, (ii) it is the farthestsite from the meteorological observation points used in both analyses, (iii) it isslightly disturbed, and (iv) this site’s spatial pattern is clumped, dominated by‘tree islands’. Such pattern can strongly buffer the responses of tree growth andtree recruitment to climate variability (Scott et al., 1993). The great increase in re-cruitment at site EP in 1950–74 could be related with the general decline in grazingsince the 1950s in the Spanish Pyrenees (Bas, 1993). Indeed, if recruitment at themost undisturbed sites (O, T) for this period is subtracted from recruitment at siteEP, a value of recruitment controlled by non-climatic factors might be established.

At the Ordesa site we found strong inverse correlations between the rate of tree-line invasion and summer temperature (Figure 5B). This finding might be explainedbecause of the Mediterranean influence at this site, which implies the presenceof frequent summer droughts. Warmer summers at site O could induce a greaterevaporative demand and increase the mortality rates of established P. uncinata


seedlings, which are very sensitive to soil water availability in July (Camarero andGutiérrez, 1999). A similar but less pronounced relationship is also observed atthe more mesic site T. Analogously, Jacoby and D’Arrigo (1995) found at Alaskatreelines evidences of moisture stress induced by recent climate warming, whichis limiting the radial-growth response of trees at those sites. The treeline-advancerates for site EP showed a different response to summer temperature, which couldbe due to its greater level of local disturbance, and its clumped spatial patterndescribed before. Interestingly, several authors have noted that drought has becomea main stress factor at boreal forests because of recent global warming in the latetwentieth century (D’Arrigo and Jacoby, 1993; Jacoby and D’Arrigo, 1995; Barberet al., 2000). This has caused radial-growth declines in response to warmer temper-atures, specially at the more xeric treelines (Lloyd and Fastie, 2002). This might bethe case of the Ordesa site, where there is a strong Mediterranean influence in spiteof its western location in the Pyrenees (Camarero and Gutiérrez, 1999). Therefore,drought might be the prevalent factor explaining the negative influence of summerand September temperatures on treeline advance at this site. Lloyd and Graumlich(1997) showed how severe multi-decadal droughts increased the mortality of theuppermost individuals causing treeline descent in the Sierra Nevada, U.S.A.

We found a negative relationship between mean treeline-advance rate andradial-growth variability for high-elevation chronologies (Figure 6A). In fact,the three longest periods with very few trees (0–15%) showing wide or narrowtree-rings, i.e., ‘stable’ periods for radial growth, were: 1744–64, 1861–77, and1905–52 (Figure 4A). These periods preceded or coincided with treeline-advanceepisodes, which were also characterised by low interannual variability in meantemperature (Figure 4E). Since ring-width is not an independent variable and maybe related with recruitment (circular argument), we analyzed the treeline-shift rateand standard deviation of mean monthly and seasonal temperatures reconstructedfor a nearby alpine lake. The only significant correlation was found between thetreeline-advance rate and standard deviation of mean March temperature (rs =−0.66; P ≤ 0.05; Figure 6B).

The synchrony between periods of high March-temperature variability and peri-ods of lower treeline-advance rate may be viewed within the recent climatic contextin the Central Pyrenees characterised by: (i) the rise of mean temperature (Bücherand Dessens, 1991), and (ii) the increase of interannual variability in mean tem-perature (Figure 4E; see also Tardif et al., 2003). A treeline ascent implies theoccurrence of several consecutive processes: production of viable seeds, disper-sal, availability of adequate regeneration sites, germination, successful seedlingestablishment, vertical growth up to ca. 2 m (treeline individual), and survival andpersistence until the individual is sampled. Climate variability affects all thesesequential stages, but its influence is probably different for each process (Earle,1993). For instance, the same climatic variable can enhance one of these processeswhile inhibiting another one.


Figure 6. Negative relationship between treeline-advance rate and radial-growth variability (A) orclimatic variability (B). The scatter diagrams represent the relationship between: (A) mean ‘regional’rate of treeline shift and standard deviation (SD) of mean residual chronology (average of sevenhigh-elevation P. uncinata chronologies); (B) this rate and SD of mean March temperature (recon-structed for the nearby alpine lake Estany Redo, 1781–1995). Values are means for 25-yr periods,except for those of 1781–99 and 1975–95. In both cases, the 1850–74 period value is an outlier(mean treeline-advance rate = 1.6 m · yr−1; see Table I). The exponential function was fitted in (A)excluding this outlier (r = −0.81, P = 0.015), and only to highlight the negative correlation.


Overall, warmer springs (April–June) are positively related with seedling estab-lishment, and treeline advance (Figure 5). This mode of treeline dynamics wouldcorrespond to a decrease in mortality rate of the uppermost trees, and an increase inrecruitment rate. Higher temperatures in March favor tree recruitment, but they arenegatively related with the rate of treeline-advance (Figure 5). In addition, a higherdispersion of March temperatures are also negatively related with the occurrence oftreeline ascents (Figure 6). This mode of treeline decline would correspond to an in-crease in the mortality rate of marginal upright treeline individuals, while seedlingestablishment remains high. The transition from winter to the spring (March) seemsto be critical for successful treeline ascent. Maximum snow thickness at the studiedsites may be reached in late winter-early spring but its interannual variability isvery high depending on temperature fluctuations (Furdada, 1996). Warmer Marchtemperatures could speed up the snowmelt, reduce the thickness of the protec-tive snow cover, enhance the negative effects of wind abrasion on upright treelineindividuals, and increase the mortality of these marginal trees (Tranquillini, 1979;Frey, 1983). This could explain the negative influence of March temperature and itsvariability on the rate of treeline advance. This is also supported by the negative re-lationship between winter temperature and the rate of treeline advance (Figure 5B).We suggest that the described relationships between recruitment, treeline shift andtemperatures should be applicable to similar treelines where spring temperaturesand the associated snow melt limit tree recruitment through temporal variability.

Little attention has been paid in the literature to the relationship between treelinedynamics and climatic variability. For instance, long-term reconstructions of tree-line dynamics in the Sierra Nevada (U.S.A.) during the Holocene concluded thatincrease in treeline elevation was favored by higher temperature and wet conditions(LaMarche, 1973; Lloyd and Graumlich, 1997). A similar long-term study in thePolar Ural treelines stated that the forming of an adult generation of Larix sibiricaat treeline required favorable conditions during at least 50 years (Shiyatov, 1993).This is one of the few studies emphasizing the importance of climatic stability inunderstanding treeline dynamics.

Some authors have reported an increase in tree density within treeline ecotonesbut minor treeline fluctuation in response to the recent climate warming (Kullman,1979; Payette and Filion, 1985; Scott et al., 1987; Szeicz and MacDonald, 1995;MacDonald et al., 1998). It would suggest that tree abundance might be a more sen-sitive monitor of climate change than treeline position (Slatyer and Noble, 1992). Infact, we found a more significant correlation between tree recruitment and temper-ature than between treeline-shift rate and temperature (Figure 5). Long periods oftreeline stasis punctuated by brief periods of change seem to be a common featureof treeline dynamics (Kullman, 1979, 1990; Slatyer and Noble, 1992; Shiyatov,1993; Lloyd and Graumlich, 1997). The described scenario would agree with a con-ceptual model based on non-linear treeline response to climatic thresholds (Slatyerand Noble, 1992; Arseneault and Payette, 1997). The treeline would remain staticor ascend gradually during long periods, but it could descend suddenly in response


to intense disturbance, including extreme climatic events (Kullman, 1990). Thedata we report show that the studied treelines were ascending until a period of highclimatic variability started (1950–95). Minor changes in treeline position duringthe last fifty years coincided with recent episodes of tree recruitment. Both ofthe variables responded contrastingly to apparently similar climatic signals. Pinusuncinata recruitment was favored by high March temperature whereas treelineascended in response to warm spring (Figure 5). Similar results were found forP. sylvestris regeneration at Swedish treelines (Kullman, 1990).

Treeline response usually lags behind climatic fluctuation and tree recruitmentpeaks (treeline inertia) because of the great longevity and phenotypic plasticityin tree species dominant at treeline ecotones (Kullman, 1979, 1990, 1996). Suchplasticity can explain why the response of treelines to climatic fluctuation is asym-metric. Some treeline individuals (e.g., krummholz) can persist for decades tocenturies during harsh climatic periods and respond with an accelerated verticalgrowth in reaction to improved climatic conditions. However, if the climatic thresh-old is surpassed due to an extreme climatic event (severe frost or drought, periodof scarce snow cover, intense warming) the treeline response can be fast (Scott etal., 1987; Kullman, 1990). A greater interannual variability in mean temperaturewould increase the probability of surpassing these climatic thresholds. This couldproduce unexpected treeline-shifts in response to climate fluctuations.

Local factors also modulate the relationship between climate and tree recruit-ment (Hobbie and Chapin, 1998). It has been pointed out in several studies atdifferent treeline ecotones (Payette and Filion, 1985; Szeicz and MacDonald, 1995;Lloyd, 1997; Camarero et al., 2000a), but never proved conclusively, that themodification of microenvironmental conditions by trees or krummholz within theecotone could enhance further tree establishment (nurse effect). It is clear thatkrummholz patches modify snow conditions in a different way than isolated uprighttrees do (Scott et al., 1993). If a positive-feedback switch, as the one proposedabove, is operating at a treeline under unfavorable climate conditions, abrupt limitshould appear (Wilson and Agnew, 1992). In fact, sharp boundaries have beendescribed at site O as a result of past tree-establishment episodes (Camarero etal., 2000b). The appearance of such abrupt limits could be regarded as a spatialindication of the existence of a positive feedback.

Our results suggest that the turn of the twentieth century marked a climatictransition, in the Spanish Pyrenees, between the end of the Little Ice Age and thecurrent period. The period of 1881–1895 in Spain is regarded as a very cold episodemarking the start of a warming trend at the beginning of the twentieth century(Font Tullot, 1988). The past century can be divided in the Spanish Pyrenees intotwo well defined climatic periods. During the first one (∼1900–49), the interannualtemperature variability was low and spring-summer temperatures were responsiblefor the observed warming. The following period (∼1950–99) was characterised bya greater interannual temperature variability and higher fall-winter temperatures(Bücher and Dessens, 1991; Agustí-Panareda et al., 2000). These factors allowed


the treeline to remain static while tree density increased within the ecotone. There-fore, higher temperature was not the only climatic factor stimulating an upwardshift in the studied altitudinal treelines. We predict that the recent global warmingis unlikely to cause an altitudinal ascent of the studied treelines, if it is accompaniedby an increase in temperature variability. Both the climatic and dendroecologicaldata we report confirm such recent increase for subalpine forests in the SpanishPyrenees (Tardif et al., 2003). Other findings suggest that it is a trend valid formost of the Iberian Peninsula (Manrique and Fernández-Cancio, 2000).

Acknowledgements

We sincerely thank many people for their help in the field (O. Bosch, X. Lluch,M. Manzanera, E. Muntán, M. Ribas, M. A. Rodríguez, J. A. Romero, R. Ro-mano, P. R. Sheppard, J. Tardif, and L. Viñolas). ‘Aigüestortes i Estany de SantMaurici’ and ‘Ordesa y Monte Perdido’ National Parks provided logistic help. Drs.A. Bücher, J. Dessens, J. Catalán, and R. Thompson provided climatic data. Wethank Mrs. G. Marsan (Musée Pyrénéen, Lourdes, France) and J. L. Acín Fanlofor providing permission to reproduce the 1909 and 1997 photographs at Punta Di-azas. This research was funded by the Spanish CICyT (AMB95–0160) and the EUproject FORMAT (ENV4-CT97–0641). We thank Daria Generowicz-Wasowiczand two anonymous reviewers for their helpful comments.

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(Received 30 May 2002; in revised form 11 April 2003)

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