182 J. JULIO CAMARERO AND EMILIA GUTIÉRREZ
temperature, inﬂuences recruitment and treeline-shift at altitudinal forest-tundra
ecotones. Our main objective was to quantify the treeline-climate relationship at
a 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 relatively
undisturbed treeline ecotones in the Spanish Pyrenees. A similar response at all the
studied 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 more
sensitive to climate variability than tree mortality was (Payette and Filion, 1985;
Lloyd, 1997). We suggest that a greater variability in air temperature may be the
ultimate climate factor favoring an upward shift of alpine mesic treelines.
Like most Eurasian mountains, the Pyrenees provide a unique opportunity
to study the effect of two global-change components, i.e., climate warming and
land-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 grazing
pressure in a village in the Catalan Pyrenees paralleled by a shift from nomadic
to stabling ﬂocks of sheep. These combined processes have caused pronounced
changes 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 the
geographical variability in the Pyrenean treeline ecotone marked by the W-E cli-
mate gradient across the range (W – Atlantic inﬂuence; Central area – continental
inﬂuence; E – Mediterranean inﬂuence). The studied ecotones are dominated by
Pinus uncinata Ram., a shade-intolerant and long-lived (700 yrs.) conifer, which
forms most treelines in the Pyrenees (Ceballos and Ruiz de la Torre, 1979; Bosch
et 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 livestock
estimates ranged 2–24 sheep month ha−1 according to Aldezábal et al. (1992) and
Bas et al. (1994). According to historical documentation, site T has not been in-
tensively disturbed since the eighteenth century (Bringue, 1995). Site EP could be
regarded as slightly disturbed by grazing (estimated present livestock is ca. 25–50
sheep 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 the
studied treelines (O, T, EP). The black rectangles at each site correspond to the approximate location
of 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 annual
precipitation 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 reached
in winter-spring and ranges from 0.5 (O, EP) to 3 m (T). Snow cover differences
are reﬂected in the understory vegetation. At site T, we found a community typical
of longer and deeper snow-cover sites dominated by Rhododendron ferrugineum
and Vaccinium myrtillus. At sites O and EP, more xeric species were found such as
Juniperus 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 marked
out at each site in topographically uniform parts of the treeline ecotone. The plot
had its longer side parallel to maximum slope and included current treeline and
timberline. The following variables were recorded in the ﬁeld for every P. uncinata
184 J. JULIO CAMARERO AND EMILIA GUTIÉRREZ
individual within the plot: location in the plot (x and y coordinates); size (diameter
at breast height, height); and growth form (arborescent, ﬂagged-krummholz, and
krummholz). Individuals whose height was equal or less than 0.5 m were regarded
as 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’s
main 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 were
mounted, sanded, and crossdated using standard dendrochronological methodol-
ogy (Stokes and Smiley, 1968). Inner-ring dates were corrected for (i) years to
core 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 ﬁtting
of a circle template to the ring curvature so as to estimate the distance of the core
to the center. At sites T and EP, we estimated nondestructively the ages of those
individuals with height ≤0.5 m by counting the number of branch whorls and bud
scars on the main stem. This age estimation was validated comparing it with the
age obtained counting the tree-rings in basal disks taken from a subsample of trees
located outside but near the plot. This procedure was not carried out at site O
because of the multistemmed character of most of the individuals (Camarero and
Gutiérrez, 1999). A static age structure of live trees is the expression of change
in the rate of tree recruitment and mortality over time (Harcombe, 1987). In order
to interpret changes in tree density as a result of tree recruitment dynamics, we
assumed that mortality was nearly constant for all cohorts.
To analyze tree recruitment dynamics as related to radial growth, seven residual
chronologies 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 site
T, and they are a reliable sample of the variability in P. uncinata radial growth
in the Spanish Pyrenees (Gutiérrez et al., 1998). Trees were sampled following
standard 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 width
was measured using a semiautomatic system (Aniol-CATRAS) with a resolution
up to 0.01 mm. Each ring-width series was standardized using a spline function
with a 50% frequency response of 32 years (Cook and Peters, 1981). Autoregres-
sive modeling was then performed to remove temporal autocorrelation, which was
mostly of ﬁrst order. Standardization involved transforming the ring-width value
into a dimensionless index by dividing the observed values by the expected values
given by the spline function (Fritts, 1976). Then the indexed residual series were
averaged. Following this procedure, long-term (low frequency) trend was removed
from the tree-ring series. To standardize the tree-ring series we used the program
ARSTAN (Cook, 1985). Calculation details and chronology statistics can be found
elsewhere (Gutiérrez et al., 1998).
TREELINE DYNAMICS IN THE PYRENEES 185
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 altitudinal
subtransects (10-m wide), so as to take the treeline spatial heterogeneity into ac-
count. We calculated mean maximum elevation of the treeline and its standard
deviation for 25-yr intervals, using data from the three subtransects per site. Since
results 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 addition
was more related to our interest in the effect of temperature on tree recruitment
within the treeline ecotone. The treeline-shift rate (m · yr−1 ) was calculated by
dividing the change in treeline elevation, between successive intervals, by the time
elapsed. 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 treeline
advanced (rate >0) or remained stable (rate = 0) during all the considered periods
at the studied sites.
In order to study the effect of climate on tree recruitment, the number of pine
recruits within every ten year interval for the 1880–1980 period was calculated.
These data were related to monthly mean minimum temperatures (from the Pic du
Midi station) averaged for the same 10-yr intervals. Temperature was the most re-
liable climatic variable for this station (Bücher and Dessens, 1991). No signiﬁcant
temporal autocorrelation was detected for recruitment data. In order to quantify the
climatic inﬂuence of temperature on treeline dynamics, we used a reconstruction
of 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 climate
records (Agustí-Panareda et al., 2000). The temperatures were averaged for 25-
yr intervals and related to maximum treeline-advance rate estimated for the same
time 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 instead
of dendroclimatic reconstruction. In all the cases, Spearman’s rank correlation co-
efﬁcient (rs ) was used. If in any paired comparison one or two variables showed
a signiﬁcant (P ≤ 0.05) temporal trend their correlation value was not taken into
3. Results and Discussion
The main changes suggested by repeated historical photographs taken along the
twentieth century (Figure 2) were: (i) increase in tree size and density within
the 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 suggest
a common regional cause such as climate. The data in Figure 3 show this tendency
186 J. JULIO CAMARERO AND EMILIA GUTIÉRREZ
Figure 2. Structural changes at a treeline ecotone in the Spanish Pyrenees during the twentieth
century. The most prominent change is the increase in tree size and density across the treeline
ecotone. Maximum treeline elevation has not increased (white line). These two photographs were
taken in 1909 (Lucien Briet, Mus´ e Pyr´ n´ en, Lourdes) and 1997 (J. L. Ac´n Fanlo) at Punta Diazas
e e e ı
(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 density
within the ecotone, specially during the period of 1900–49. Secondly, the treeline
ascended greatly during the last half of the nineteenth century, reached maxi-
mum elevation at the beginning of the twentieth century and then remained stable
throughout the rest of that century. Mean treeline elevation followed a parallel
trend and remained approximately stable during the past century. Maximum spatial
TREELINE DYNAMICS IN THE PYRENEES 187
Figure 3. Spatiotemporal variability in tree density and treeline position (maximum elevation of
live individuals with stems at least 2 m high) within the alpine forest-tundra ecotone at site T. The
ﬁgure shows the same plot (30 m · 140 m; the y axis follows the altitudinal gradient upslope – the
arrow points upslope) during different time periods (1750–1849, . . . , 1950–97). Various limits are
shown: 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 only
by individuals established during each 25-yr interval) and its standard deviation (±SD – black thin
line). 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 represent
trees established during periods previous to the one indicated above. Different symbols represent
tree-establishment periods (e.g., circles = 1750–1849). Current timberline is at y = 40 m.
188 J. JULIO CAMARERO AND EMILIA GUTIÉRREZ
heterogeneity (standard deviation) of mean treeline elevation increased during the
period of 1850–99 and decreased during that of 1950–97. That pattern might be
the result of the high tree-recruitment rate during that period as well as during the
previous decades. Overall, these changes agree with those observed in repeated
historical photographs, i.e., increase of tree density within the ecotone but minor
or null treeline shifts (Figure 2). During the ﬁrst half of the twentieth century, the
spatial clustering of pine recruits was greater at short distance (less than 9 m) than
during the second half (Camarero et al., 2000a). These patterns developed at a time
characterised by very warm springs and summers and low temperature variability
during the ﬁrst half of the twentieth century, but warm fall-winter seasons and
high 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 variability
in radial growth (Tardif et al., 2003). High-elevation subalpine P. uncinata stands in
the Central Pyrenees showed two contrasting patterns of radial growth during the
twentieth century (Figures 4A–C). The ﬁrst half of that century was characterised
by: (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 and
during the nineteenth century. Pine recruitment at treeline was very high during the
periods 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 and
it reached maximum values at the end of the nineteenth century (1850–74, sites
O 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 reached
its highest values during the periods of 1850–74 and 1900–24. If these data were
analyzed subdividing each plot into three 10-m wide transects running along the
slope (n = 9 transects per site), the results varied slightly. During the period of
1900–49, 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 did
not 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 of
warm spring and fall could be related to the increase in seedling mortality due to
frost during those seasons. However, such relationships may be more complex. For
instance, high temperature in spring could speed up snowmelt, and lead to more
drying of soils in summer. This would intensify the negative effect of summer
drought on seedling survival (Puig, 1982; Lloyd, 1997). Other climatic factors,
such as winter-spring snow cover, could improve reproductive success at treeline
TREELINE DYNAMICS IN THE PYRENEES 189
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 Central
Pyrenees. (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 residual
chronologies 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 treeline
ecotones (O, T, EP sites). (E) Maximum treeline-advance rate at these sites (bars) and estimate of the
variability of mean annual temperature (line; CV, coefﬁcient of variation for each period based on
temperature reconstructed for the nearby ‘Estany Red´ ’ 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 and
last ones. Treeline-advance rate at site T during the period of 1850–74 was 4 m · yr−1 . The colors of
bars correspond to the different treeline sites in (D) and (E).
Mean, standard deviation (±SD) and maximum treeline-advance rate (m · yr−1 , in parentheses) at three altitudinal
treeline ecotones in the Central Pyrenees (O, T, and EP sites) during the last 150 years. The ﬁfth column shows
mean maximum rate (±SD) of treeline advance averaging the values for the three sites (‘regional’ mean). The
last column shows relative frequency (%) of substransects (n = 9) showing altitudinal ascent during each period.
Mean value and standard deviation were calculated for the three altitudinal subtransects at each plot. The highest
mean and maximum values for each site are in bold
Period O T EP Mean Subtransects (%)
1850–74 0.64 ± 0.84 (0.82) 0.87 ± 1.50 (3.99) 0.03 ± 0.05 (0) 1.60 ± 2.11 50.00
1875–99 0.22 ± 0.39 (0) 0.39 ± 0.39 (0) 0.84 ± 1.35 (0.05) 0.02 ± 0.03 66.67
1900–24 0.17 ± 0.29 (0.50) 0.90 ± 1.25 (0.36) 0.63 ± 0.99 (0.80) 0.55 ± 0.22 55.55
1925–49 0.24 ± 0.24 (0) 0.47 ± 0.40 (0.13) 0.97 ± 1.23 (0.62) 0.25 ± 0.33 77.78
1950–74 0 (0) 0.27 ± 0.47 (0) 0.39 ± 0.67 (0) 0±0 22.22
J. JULIO CAMARERO AND EMILIA GUTIÉRREZ
1975–95 0 (0) 0 (0) 0 (0) 0±0 0
TREELINE DYNAMICS IN THE PYRENEES 191
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 three
treeline ecotones (O, T, EP sites) in the Spanish Pyrenees. The correlation was obtained for 10-yr
periods (n = 10). (B) Relationship between monthly mean temperature reconstructed for a nearby
alpine lake (Estany Red´ , 1781–1995) and maximum treeline-advance rate for 25-yr periods (sites
T and EP, n = 9; site O, n = 6). In both cases, the correlation (Spearman index, rs ) calculated
for 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 or
indirectly 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; Camarero
and Gutiérrez, 1999). This relationship is related to temperature requirements,
over a period of several summers, for successful seed production, germination
and seedling establishment (Zasada et al., 1992; Scott et al., 1997). Appropriate
temperatures are rarely attained at treeline environments, which causes the absence
of sexual regeneration (Arseneault and Payette, 1997). In addition, extremely cold
episodes have caused rapid treeline recession in the Swedish Scandes (Kullman,
1996). The recent reduction in tree recruitment at the studied treeline ecotones, and
192 J. JULIO CAMARERO AND EMILIA GUTIÉRREZ
that observed at the turn of the twentieth century, could also be explained within
such context. If temperature interannual variability increased, the probability of
successive favorable springs or summers would decrease. Therefore, tree recruit-
ment would also decrease. This is shown in our data where ring-width is used as
a proxy for climatic variability (Figure 4A–E). The hypothesis should be tested by
comparing forests with treeline ecotones, so as to quantify possible temporal lags
between 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 (Scott
et 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 of
temperature at treelines vs. disturbances at forests (Zackrisson et al., 1995).
The advance of treeline was consistent and negatively related to high mean
March and November temperatures (Figure 5B). Such negative correlation between
mean March temperature and maximum treeline-advance rate for 25-yr was found
again 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 of
spring temperature (April–June). The positive correlation between the regional
treeline-advance rate and spring temperature was also signiﬁcant (rs = 0.68;
P ≤ 0.05). Paradoxically, November temperature of the year prior to growth is
amongst 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 advance
at sites O and T (Figure 5B). In the Pyrenees, warm Novembers are associated
with cyclonic conditions and high snow precipitation (Del Barrio et al., 1990),
which may induce higher rates of mortality among established treeline individuals
because 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 farthest
site from the meteorological observation points used in both analyses, (iii) it is
slightly disturbed, and (iv) this site’s spatial pattern is clumped, dominated by
‘tree islands’. Such pattern can strongly buffer the responses of tree growth and
tree 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 grazing
since the 1950s in the Spanish Pyrenees (Bas, 1993). Indeed, if recruitment at the
most undisturbed sites (O, T) for this period is subtracted from recruitment at site
EP, 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 explained
because of the Mediterranean inﬂuence at this site, which implies the presence
of frequent summer droughts. Warmer summers at site O could induce a greater
evaporative demand and increase the mortality rates of established P. uncinata
TREELINE DYNAMICS IN THE PYRENEES 193
seedlings, which are very sensitive to soil water availability in July (Camarero and
Gutiérrez, 1999). A similar but less pronounced relationship is also observed at
the more mesic site T. Analogously, Jacoby and D’Arrigo (1995) found at Alaska
treelines evidences of moisture stress induced by recent climate warming, which
is limiting the radial-growth response of trees at those sites. The treeline-advance
rates for site EP showed a different response to summer temperature, which could
be due to its greater level of local disturbance, and its clumped spatial pattern
described before. Interestingly, several authors have noted that drought has become
a main stress factor at boreal forests because of recent global warming in the late
twentieth century (D’Arrigo and Jacoby, 1993; Jacoby and D’Arrigo, 1995; Barber
et 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 be
the case of the Ordesa site, where there is a strong Mediterranean inﬂuence in spite
of its western location in the Pyrenees (Camarero and Gutiérrez, 1999). Therefore,
drought might be the prevalent factor explaining the negative inﬂuence of summer
and September temperatures on treeline advance at this site. Lloyd and Graumlich
(1997) showed how severe multi-decadal droughts increased the mortality of the
uppermost individuals causing treeline descent in the Sierra Nevada, U.S.A.
We found a negative relationship between mean treeline-advance rate and
radial-growth variability for high-elevation chronologies (Figure 6A). In fact,
the three longest periods with very few trees (0–15%) showing wide or narrow
tree-rings, i.e., ‘stable’ periods for radial growth, were: 1744–64, 1861–77, and
1905–52 (Figure 4A). These periods preceded or coincided with treeline-advance
episodes, which were also characterised by low interannual variability in mean
temperature (Figure 4E). Since ring-width is not an independent variable and may
be related with recruitment (circular argument), we analyzed the treeline-shift rate
and standard deviation of mean monthly and seasonal temperatures reconstructed
for a nearby alpine lake. The only signiﬁcant correlation was found between the
treeline-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 context
in the Central Pyrenees characterised by: (i) the rise of mean temperature (Bücher
and 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 the
occurrence of several consecutive processes: production of viable seeds, disper-
sal, availability of adequate regeneration sites, germination, successful seedling
establishment, vertical growth up to ca. 2 m (treeline individual), and survival and
persistence until the individual is sampled. Climate variability affects all these
sequential stages, but its inﬂuence is probably different for each process (Earle,
1993). For instance, the same climatic variable can enhance one of these processes
while inhibiting another one.
194 J. JULIO CAMARERO AND EMILIA GUTIÉRREZ
Figure 6. Negative relationship between treeline-advance rate and radial-growth variability (A) or
climatic 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 seven
high-elevation P. uncinata chronologies); (B) this rate and SD of mean March temperature (recon-
structed for the nearby alpine lake Estany Red´ , 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.
TREELINE DYNAMICS IN THE PYRENEES 195
Overall, warmer springs (April–June) are positively related with seedling estab-
lishment, and treeline advance (Figure 5). This mode of treeline dynamics would
correspond to a decrease in mortality rate of the uppermost trees, and an increase in
recruitment rate. Higher temperatures in March favor tree recruitment, but they are
negatively related with the rate of treeline-advance (Figure 5). In addition, a higher
dispersion of March temperatures are also negatively related with the occurrence of
treeline ascents (Figure 6). This mode of treeline decline would correspond to an in-
crease in the mortality rate of marginal upright treeline individuals, while seedling
establishment remains high. The transition from winter to the spring (March) seems
to be critical for successful treeline ascent. Maximum snow thickness at the studied
sites may be reached in late winter-early spring but its interannual variability is
very high depending on temperature ﬂuctuations (Furdada, 1996). Warmer March
temperatures could speed up the snowmelt, reduce the thickness of the protec-
tive snow cover, enhance the negative effects of wind abrasion on upright treeline
individuals, and increase the mortality of these marginal trees (Tranquillini, 1979;
Frey, 1983). This could explain the negative inﬂuence of March temperature and its
variability 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 and
temperatures should be applicable to similar treelines where spring temperatures
and the associated snow melt limit tree recruitment through temporal variability.
Little attention has been paid in the literature to the relationship between treeline
dynamics and climatic variability. For instance, long-term reconstructions of tree-
line dynamics in the Sierra Nevada (U.S.A.) during the Holocene concluded that
increase in treeline elevation was favored by higher temperature and wet conditions
(LaMarche, 1973; Lloyd and Graumlich, 1997). A similar long-term study in the
Polar Ural treelines stated that the forming of an adult generation of Larix sibirica
at treeline required favorable conditions during at least 50 years (Shiyatov, 1993).
This is one of the few studies emphasizing the importance of climatic stability in
understanding treeline dynamics.
Some authors have reported an increase in tree density within treeline ecotones
but 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). In
fact, we found a more signiﬁcant correlation between tree recruitment and temper-
ature than between treeline-shift rate and temperature (Figure 5). Long periods of
treeline stasis punctuated by brief periods of change seem to be a common feature
of 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 (Slatyer
and Noble, 1992; Arseneault and Payette, 1997). The treeline would remain static
or ascend gradually during long periods, but it could descend suddenly in response
196 J. JULIO CAMARERO AND EMILIA GUTIÉRREZ
to intense disturbance, including extreme climatic events (Kullman, 1990). The
data we report show that the studied treelines were ascending until a period of high
climatic variability started (1950–95). Minor changes in treeline position during
the last ﬁfty years coincided with recent episodes of tree recruitment. Both of
the variables responded contrastingly to apparently similar climatic signals. Pinus
uncinata recruitment was favored by high March temperature whereas treeline
ascended in response to warm spring (Figure 5). Similar results were found for
P. sylvestris regeneration at Swedish treelines (Kullman, 1990).
Treeline response usually lags behind climatic ﬂuctuation and tree recruitment
peaks (treeline inertia) because of the great longevity and phenotypic plasticity
in tree species dominant at treeline ecotones (Kullman, 1979, 1990, 1996). Such
plasticity can explain why the response of treelines to climatic ﬂuctuation is asym-
metric. Some treeline individuals (e.g., krummholz) can persist for decades to
centuries during harsh climatic periods and respond with an accelerated vertical
growth in reaction to improved climatic conditions. However, if the climatic thresh-
old is surpassed due to an extreme climatic event (severe frost or drought, period
of scarce snow cover, intense warming) the treeline response can be fast (Scott et
al., 1987; Kullman, 1990). A greater interannual variability in mean temperature
would increase the probability of surpassing these climatic thresholds. This could
produce 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 at
different treeline ecotones (Payette and Filion, 1985; Szeicz and MacDonald, 1995;
Lloyd, 1997; Camarero et al., 2000a), but never proved conclusively, that the
modiﬁcation of microenvironmental conditions by trees or krummholz within the
ecotone could enhance further tree establishment (nurse effect). It is clear that
krummholz patches modify snow conditions in a different way than isolated upright
trees do (Scott et al., 1993). If a positive-feedback switch, as the one proposed
above, is operating at a treeline under unfavorable climate conditions, abrupt limit
should appear (Wilson and Agnew, 1992). In fact, sharp boundaries have been
described at site O as a result of past tree-establishment episodes (Camarero et
al., 2000b). The appearance of such abrupt limits could be regarded as a spatial
indication of the existence of a positive feedback.
Our results suggest that the turn of the twentieth century marked a climatic
transition, in the Spanish Pyrenees, between the end of the Little Ice Age and the
current period. The period of 1881–1895 in Spain is regarded as a very cold episode
marking 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 into
two well deﬁned climatic periods. During the ﬁrst one (∼1900–49), the interannual
temperature variability was low and spring-summer temperatures were responsible
for the observed warming. The following period (∼1950–99) was characterised by
a greater interannual temperature variability and higher fall-winter temperatures
(Bücher and Dessens, 1991; Agustí-Panareda et al., 2000). These factors allowed
TREELINE DYNAMICS IN THE PYRENEES 197
the treeline to remain static while tree density increased within the ecotone. There-
fore, higher temperature was not the only climatic factor stimulating an upward
shift in the studied altitudinal treelines. We predict that the recent global warming
is unlikely to cause an altitudinal ascent of the studied treelines, if it is accompanied
by an increase in temperature variability. Both the climatic and dendroecological
data we report conﬁrm such recent increase for subalpine forests in the Spanish
Pyrenees (Tardif et al., 2003). Other ﬁndings suggest that it is a trend valid for
most of the Iberian Peninsula (Manrique and Fernández-Cancio, 2000).
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 Sant
Maurici’ and ‘Ordesa y Monte Perdido’ National Parks provided logistic help. Drs.
A. Bücher, J. Dessens, J. Catalán, and R. Thompson provided climatic data. We
thank Mrs. G. Marsan (Musée Pyrénéen, Lourdes, France) and J. L. Acín Fanlo
for 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 EU
project FORMAT (ENV4-CT97–0641). We thank Daria Generowicz-Wasowicz
and two anonymous reviewers for their helpful comments.
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