Intra-annual density fluctuations of Pinus pinasterare a record of climatic changes in the westernMediterranean region

Joana Vieira, Filipe Campelo, and Cristina Nabais

Abstract: Climate projections for the Mediterranean area estimate a decline in total precipitation, warmer temperatures,and a higher frequency of extreme drought events. It is important to understand how trees respond to these climaticchanges and which wood anatomical structures best document the trees’ response to those changes. The present work in-vestigates the climatic signal of tree-ring width, latewood width, and the frequency of intra-annual density fluctuations(IADFs) during the last 100 years for Pinus pinaster Aiton growing in the western Mediterranean region. Based on mete-orological data, it was observed that since the 1950s, average annual temperature and autumn and winter precipitation in-creased. Tree-ring width and latewood width of P. pinaster were positively correlated with winter and summerprecipitation and negatively correlated with spring and summer temperatures. The frequency of latewood IADFs showed apositive and time-stable correlation with September and October precipitation. However, after the 1970s, the frequency ofIADFs also became correlated with climatic conditions later in the year, specifically with the temperatures of Novemberand December, probably because of the recent climate changes. IADFs chronologies, besides being very useful to recon-struct autumn precipitation, can add new climatic information to ring-width chronologies.

Resume : Les previsions climatiques pour la region mediterraneenne prevoient une diminution de la precipitation totale,des temperatures plus chaudes et une frequence plus elevee des periodes de secheresse extreme. Il est important de com-prendre comment les arbres reagissent a ces changements climatiques et quelles structures anatomiques du bois attestent lemieux de ces changements. Cette etude examine le signal climatique de la largeur des cernes annuels (LCA), de la largeurdu bois final (LBF) et de la frequence des fluctuations intra-annuelles de densite (FIADs) durant les derniers 100 ans chezPinus pinaster Aiton qui croıt dans la region occidentale de la Mediterranee. Selon les donnees meteorologiques, la tempe-rature annuelle moyenne ainsi que les precipitations automnales et hivernales ont augmente depuis les annees 1950. LaLCA et la LBF de P. pinaster etaient positivement correlees avec les precipitations hivernales et estivales et negativementcorrelees avec les temperatures printanieres et estivales. Il y avait une correlation positive et stable dans le temps entre lesFIADs dans le bois final et la precipitation durant les mois de septembre et octobre. Cependant, apres les annees 1970 lesFIADs sont aussi devenues correlees avec les conditions climatiques plus tard dans l’annee, particulierement avec la tem-perature durant les mois de novembre et decembre, probablement en lien avec les recents changements climatiques. Leschronologies des FIADs, en plus d’etre tres utiles pour reconstituer la precipitation automnale, peuvent ajouter une nou-velle information aux chronologies des cernes annuels.

[Traduit par la Redaction]

Introduction

During the second half of the 20th century, the Mediterra-nean area has experienced an increase in the mean annualtemperature, a decrease in the mean annual precipitation,and a higher frequency of intense drought periods (Martratet al. 2004; Xoplaki et al. 2004, 2006). In spite of the gen-eral decrease in total precipitation for the Mediterraneanarea, regional differences in the intra-annual precipitationpatterns and also in values of total precipitation have beendetected when comparing eastern and western Mediterraneanregions. Although a negative winter rainfall trend has been

observed since the 1960s in the eastern Mediterranean re-gion (Luterbacher and Xoplaki 2003; Xoplaki et al. 2004),winter precipitation in the western Mediterranean region hasincreased in the last decades (Maheras et al. 1999; Dunkelohand Jacobeit 2003). In spite of the regional differences, a de-crease in tree-ring width and a higher occurrence of narrowtree rings during the second half of the 20th century hasbeen observed in different Pinus species across the Mediter-ranean area (Andreu et al. 2007; Sarris et al. 2007). Varia-tions in the precipitation regime and the increasedfrequency of drought changed the availability of water dur-ing tree growth, affecting cambial activity and xylem devel-opment (Larson 1994). In fact, a reduction in the frequencyof cambial cell division and the radial diameter of tracheidswas observed in conifers in response to water deficit (Abe etal. 2003).

Tree rings integrate the prevailing environmental condi-tions during the growing season, making them a powerfulproxy to study climate variability with annual resolution(Briffa et al. 2004; Touchan et al. 2005; Nicault et al.

Received 11 November 2009. Accepted 20 April 2010.Published on the NRC Research Press Web site at cjfr.nrc.ca on24 July 2010.

J. Vieira,1 F. Campelo, and C. Nabais. Centre for FunctionalEcology, Department of Life Sciences, University of Coimbra,P.O. Box 3046, 3001-401 Coimbra, Portugal.

1Corresponding author (e-mail: joana.m.vieira@gmail.com).

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2008). In addition, intra-ring features, such as the width ofearlywood and latewood (Lebourgeois 2000), maximumlatewood density (Buntgen et al. 2006), intra-annual densityfluctuations (IADFs) or double rings (Wimmer et al. 2000;Masiokas and Villalba 2004; Campelo et al. 2007a), and lu-men area of vessels (Campelo et al. 2010; Fonti et al. 2010),are useful to reconstruct climatic conditions on a narrowertime scale. Latewood width has a half-year resolution and isstrongly correlated with climate during the summer(Lebourgeois 2000; Rigling et al. 2002). IADFs are varia-tions in wood density and are defined by the presence ofearlywood-like cells within latewood and (or) by the pres-ence of latewood-like cells within earlywood (Fritts 2001).The existence of these anatomical features reflects changesin the environmental conditions during the growing season(Campelo et al. 2007b; Vieira et al. 2009). Studies in Pinusnigra Arnold showed that earlywood IADFs were triggeredby dry periods during spring (Wimmer et al. 2000). In con-trast, latewood IADFs were triggered by precipitation duringlate summer and (or) early autumn, as observed in Pinuspinea L., Pinus halepensis Mill., and Pinus pinaster Aiton(Campelo et al. 2007b; de Luis et al. 2007; Vieira et al.2009). Therefore, the position and frequency of IADFs canbe used to improve the resolution of climatic reconstructionsduring the growing season.

Although temperature and precipitation have changedover the last 50 years, it is not clear yet how trees respondto these changes and which anatomical structures, if any,can be used to document tree response to climate change. Aprevious study using P. pinaster showed that the frequencyof IADFs varies with tree age and it is consistently corre-lated with autumn precipitation (Vieira et al. 2009). How-ever, these results were obtained for a time-window of65 years, from 1940 to 2005, when mean annual temperaturehad already started to increase. Longer chronologies areneeded to investigate the effect of temperature increase overthe last 100 years on tree growth and to determine if the re-

cent changes in temperature and precipitation can also bedetected by dendrochronological studies. To understandhow climate change is affecting tree growth, the presentwork investigates the stability of the climatic signal of tree-ring width (TRW), latewood width (LW), and the frequencyof IADFs during the last 100 years in P. pinaster treesgrowing in the western Mediterranean region.

Materials and methods

Study area and climate dataThe study site is located in Mata Nacional de Leiria

(–8.998E, 39.768N), a P. pinaster plantation on sand dunes(Fig. 1). Most of the Portuguese coastal forests are com-posed of P. pinaster and (or) P. pinea stands planted to pre-vent the advance of the sand dunes. The management ofthese stands consists of the seasonal clearing of corridorsand a 70-year cycle of tree cutting. Some stands are left un-cut to maintain seed production and natural regeneration.One of these stands was selected for the present study.

The climate is typically Mediterranean with oceanic influ-ence; the summer is dry, with the precipitation concentratedin the autumn and winter months. The monthly averagemean air temperature and total precipitation were obtainedfrom the nearest 0.58 � 0.58 grid point at http://climexp.knmi.nl/start.cgi?someone@somewhere (–8.758E; 39.758N),for 1901–2006. To analyse the time stability of the climaticdata, a 40-year moving average was computed and then sub-tracted by the whole-period average to highlight climaticchanges.

Tree-ring dataTwenty-two P. pinaster trees, older than 100 years, were

sampled in 2007. Two cores were taken per tree (in thenorth–south direction) at breast height to include the poten-tial variability in tree growth around the stem. Tree ringswere cross-dated using standard dendrochronological tech-

Fig. 1. Location of the study area (circle) and meteorological grid point (cross) and a climatic diagram for the grid point from 1901 to 2006.The climatic diagram consists of monthly precipitation (thin solid line) and mean temperature (thick solid line).

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niques (Stokes and Smiley 1996). LW and TRW were meas-ured to the nearest 0.01 mm using a linear table (LINTAB;Frank Rinn S.A., Heidelberg, Germany) and the programTSAP-Win, version 0.55 (Rinn 2003). The quality of thering-width series was checked using the programCOFECHA, version 6.06 (Holmes 1994).

Two residual chronologies were obtained, one for TRWand another for LW (Table 1), using a two-step procedure.Firstly, a negative exponential or a straight line was fittedto the series, followed by a cubic smoothing spline with a50% cut-off frequency and a response period of 60 years.Afterwards, an autoregressive model was fitted to the di-mensionless indices, and finally, to remove the effect of out-liers, a biweight estimate of the mean was applied.

IADFsThe correctly dated cores were visually examined for

IADFs using a stereomicroscope magnifying up to 25-fold.IADFs were easily distinguished from annual tree rings,since IADFs presented a nonsharp transition (Fig. 2). Be-cause of the great variability of IADFs across the stem,

IADFs were only considered if observed in both cores (Kuoand McGinnes 1973). In the present study, only IADFs lo-cated in latewood were considered, since earlywood IADFswere not frequent and their combination with latewoodIADFs could decrease the climatic signal.

The frequency of IADFs per year, F, was calculated asthe ratio

F ¼ N=n

where N is the number of trees that showed an IADF, and nis the total number of trees in that year. The changing of thenumber of trees, n, in time created a bias, which was ad-dressed by calculating the stabilized IADFs frequency, f,proposed by Osborn et al. (1997):

f ¼ Fn0:5

A negative exponential followed by a cubic spline with a50% cut-off frequency and a response period of 60 yearswere applied to the IADFs frequency chronology to removethe age trend.

Growth, IADFs, and climateThe influence of climatic variables (mean air temperature

and precipitation) on tree growth and IADFs formation wasinvestigated using Pearson’s correlation coefficient by boot-strap analyses for the period 1902–2006. The temporalstability of the climatic signal in TRW, LW, and IADFswas investigated by moving bootstrapped correlation coeffi-cients, with a time window of 40 years progressively slid by1 year.

The correlation coefficients were computed using 1000bootstrapped samples with replacement, and the percentilemethod was applied to test significance. Median correlationcoefficients were considered significant at an a level of 0.05if they exceed, in absolute value, half the difference betweenthe 97.5th and the 2.5th quantile of the 1000 estimates.

ResultsThe moving average analysis of the meteorological re-

cords showed that between 1910 and 1965 the total annual

Table 1. Descriptive statistics of tree-ring width (TRW) and la-tewood width (LW) residual chronologies.

TRW LWNo. of trees (no. of cores) 22 (42) 22 (42)Start year 1819 1819End year 2006 2006Length (years) 188 188Residual chronologies

No. of trees 22 22Mean sensitivity 0.361 0.477Standard deviation 0.435 0.462First-order autocorrelation 0.015 0.004

Common interval analysis (1900–2006)No. of trees 22 22Rbt* 0.314 0.310EPS* 0.935 0.935

*Mean correlation between trees (Rbt) and Expressed PopulationSignal (EPS) were used to evaluate the chronology quality.

Fig. 2. Anatomical structure and relative position of intra-annual density fluctuations (arrows) within tree rings of Pinus pinaster. The barrepresents 1 mm.

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Fig. 3. Moving average of the climatic data using a moving window of 40 years, for the period 1901–2006. For each month, the indiceswere calculated subtracting the 40-years running average value by the whole-period mean. The Py and Ty bars represent the annual averagefor the precipitation and temperature, respectively.

Fig. 4. (A) Raw tree-ring and latewood width chronologies of Pinus pinaster (black and grey lines, respectively) fitted with a 60-year and50% cut-off spline (smooth line). (B) Residual chronologies of tree-ring and latewood width and sample depth; in the upper left corner isthe correlation value (r) between both chronologies.

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precipitation was lower than the whole-period average, in-creasing afterwards (Fig. 3). Since the middle of the 20thcentury, March precipitation decreased almost 25 mm; Janu-ary, February, May, and October precipitation increased ap-proximately 20 mm; and April increased about 10 mm.From 1915 until 1980, the precipitation in October waslower than the average. Average air temperature increasedapproximately 0.8 8C during the last century.

TRW and LW raw chronologies showed wider rings inthe first decade, corresponding to the growth trend of young

trees, followed by a decrease until ca. 1940, an increase un-til 1980, and a decrease since then (Fig. 4A). Consideringthe period from 1902 to 2006, TRW and LW showed a pos-itive correlation with the precipitation of November and De-cember from the previous year and January, February,March, and July of the current year, and a negative correla-tion with the precipitation of November from the currentyear (Fig. 5). TRW chronology also presented a positivecorrelation with April precipitation, whereas LW chronologyshowed a positive correlation with October precipitation.

Fig. 5. Bootstrapped correlation analyses between tree-ring width (TRW) and latewood width (LW) residual chronologies of Pinus pinasterand climate for the period 1902–2006. The months represented with lowercase letters correspond to the previous year. An asterisk indicatesa significant correlation at P < 0.05.

Fig. 6. Bootstrapped moving correlation analyses between latewood width and monthly precipitation and temperature for the period 1902–2006, using a 40-year moving window. The months represented with lowercase letters correspond to the previous year.

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TRW chronology presented a negative correlation with thetemperature from April to June, while LW showed a posi-tive correlation with the temperature of December from theprevious year and a negative correlation with June and Julytemperature.

TRW and LW chronologies were highly correlated(Fig. 4B); therefore, the moving correlation analyses wereonly performed for the LW chronology, where most of theIADFs were found. The moving correlation analyses be-tween LW and climate showed a time-stable positive corre-lation with January, February, July, and Octoberprecipitation and with June and July temperature (Fig. 6).The positive correlation with the precipitation of Novemberfrom the previous year and March of the current year lostsignificance after the middle of the 20th century, while thecorrelation with the precipitation of December from the pre-vious year became significant.

All the analysed trees showed latewood IADFs. TheIADFs frequency was high from 1900 to 1940, decreasedfrom 1940 to 1970, and increased again after 1970 (Fig. 7).

The frequency of latewood IADFs showed a negative corre-lation with the precipitation of November and Decemberfrom the previous year and January, February, March, andJune of the current year, and a positive correlation with theprecipitation of September and October (Fig. 8). Tempera-ture of November presented a positive correlation with late-wood IADFs.

The frequency of IADFs showed a time-stable negativecorrelation with the precipitation of November and Decem-ber from the previous year and January and February of thecurrent year, and a positive correlation with September andOctober precipitation (Fig. 9). After the 1950s, the fre-quency of IADFs became positively correlated with the pre-cipitation and temperature of November and December andwith the temperature in June, while the temperature of Sep-tember became negatively correlated.

DiscussionIn the Mediterranean area during the second half of the

20th century, an overall increase of the mean annual temper-ature and a decrease of the annual precipitation has been ob-served (Martrat et al. 2004; Xoplaki et al. 2004, 2006). Inour study area, located in the western Mediterranean region,the mean annual temperature increased ca. 0.8 8C as did to-tal annual precipitation, especially in January, February,April, May, and October.

The effects of climate change on the growth of differentpine species have been reported for the Iberian Peninsula(Andreu et al. 2007; Bogino and Bravo 2008). In the lastdecades, the negative correlation between late summer toautumn temperature from the previous year and the growthof P. nigra, Pinus sylvestris L., and Pinus uncinata Ramondex. DC has become stronger (Andreu et al. 2007). Althoughmilder conditions during autumn can enable needle growthto be self-sustained (Maseyk et al. 2008), an extension ofplant metabolism can also reduce the carbon reserves thusaffecting radial growth in the following year (Zweifel et al.2006). In our study area, TRW and LW of P. pinaster werepositively correlated with winter and summer precipitationand negatively correlated with spring and summer tempera-tures. The moving correlation analysis of LW showed thatduring the study period, those climatic signals were essen-tially stable. In the last decades, the loss of significance be-tween March precipitation and LW could be related to theobserved reduction of precipitation during this month.

Fig. 7. Time distribution of stabilized frequencies of latewood intra-annual density fluctuations (IADFs) in Pinus pinaster. The solid line inthe graph is a cubic spline (60 years, 50% cut-off frequency) showing the tendency of IADFs formation.

Fig. 8. Bootstrapped correlation analyses between intra-annual den-sity fluctuations stabilized frequency and climate for the period 1902–2006. An asterisk indicates a significant correlation at P < 0.05.

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IADFs have a higher intra-annual resolution than do TRWand LW, and their frequency can detail the climatic condi-tions within the growing season (Wimmer et al. 2000;Campelo et al. 2007b; Vieira et al. 2009). The low fre-quency of earlywood IADFs observed in P. pinaster couldindicate that drought conditions during earlywood formationwere rare in our study area. Latewood IADFs of P. pinasterwere triggered by lower precipitation from the previous win-ter and early spring and by higher precipitation in autumn.During the growth process, cell division and expansion areaffected by the tree water status, with the cell expansionphase being more sensitive (Zweifel et al. 2006). Duringsummer drought, cell expansion decreases and small-diameter and thick-walled tracheids are formed in responseto low turgor (Domec and Gartner 2002; Abe et al. 2003).However, if after this dry period, water becomes available(autumn precipitation), cambial cells under differentiationcan rapidly recover the pressure necessary for their completeenlargement, and earlywood-like cells are produced (Abe etal. 2003; Rossi et al. 2009).

The frequency of latewood IADFs changed across thelife-span of P. pinaster. The high frequency of latewoodIADFs in P. pinaster during the first four decades of the20th century could be explained by the fact that IADFs aremore prone to occur in young tree rings (Villalba andVeblen 1994; Rigling et al. 2001; Vieira et al. 2009). Thereactivation of the cambium starts earlier in young trees, re-sulting in a longer growing season with a high number ofcells produced along a radial row (Rossi et al. 2008). There-fore, young trees have a longer time window to imprint cli-matic fluctuations during the growing season.

The moving correlation analysis showed that the climatic

signal of September and October precipitation in latewoodIADFs was stable throughout the 20th century. The stabilityof this correlation reinforces the importance of autumn pre-cipitation to trigger IADFs formation. The low frequency oflatewood IADFs observed between 1940 and 1970 could becaused by the low precipitation in October during that pe-riod. After the 1970s, the frequency of latewood IADFs ofP. pinaster increased. This could be related to an increaseof October precipitation during the last decades. Addition-ally, after the 1970s, latewood IADFs became correlatedwith climatic conditions latter in the year, especially withtemperatures of November and December. De Luis et al.(2007) found that in P. halepensis growing along the easterncoast of Spain, the process of differentiation of the last tra-cheids was still ongoing in December. Mild conditions fa-vour multiple flushing in conifers (Pardos et al. 2003),increasing the internal competition for carbohydrates, withshoot apices and leaves having priority as a sink for carbonmoreso than cambium (Minchin and Lacointe 2005). Thusxylem cells have less carbon available for the secondarywall formation of latewood cells, leading to the formationof earlywood-like cells within the latewood (Rossi et al.2009). From a functional point of view, earlywood-like cellsare more specialized for the transport of water, while late-wood cells provide mechanical stability (Domec and Gartner2002). Thus, the increasing frequency of earlywood cellswithin the latewood, observed in the last decades, couldplay an important role in the acclimatization of trees tochanging climatic conditions (Martinez-Meier et al. 2008).

In conclusion, the frequency of IADFs could be used todetect changes of climatic conditions within the growingseason. The climatic signals stored in TRW (or LW) were

Fig. 9. Bootstrapped moving correlation analyses between the latewood intra-annual density fluctuations stabilized frequency and themonthly precipitation and temperature, for the period 1902–2006, using a 40-year window.

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somehow opposite to those recorded by the frequency ofIADFs. While an increase of TRW and LW was associatedwith high precipitation in winter and summer, a high fre-quency of IADFs was associated with low precipitation inwinter and high precipitation in autumn. Also, after the1970s, the frequency of IADFs became correlated withmilder conditions in winter, a signal not detected by TRWand LW chronologies, and was probably linked to the recentclimate changes.

AcknowledgementsThanks to Susana Rodriguez Echeverria and two anony-

mous reviewers for their critical reading of and helpful com-ments on an earlier version of the manuscript. This workwas supported by the project POCI/CLI/58680/2004 fromthe Portuguese Foundation for Science and Technology andthe European Union (POCI 2010).

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