Spring-Summer Drought Induces Extremely Low Radial Growth Reactions in North-Tyrrhenian Pinus pinea L.

Sergio Piraino Fidel Alejandro Roig About the authors

Abstract

Climate projections predict shifts in environmental conditions, with cascade effects on forest growth dynamics. As such, Pinus pinea L., an ecologically important low-elevation Mediterranean tree, can be threatened by drought events. The occurrence of negative stem growth anomalies (“negative pointer years”, or NPY) and its relation to climatic conditions were analyzed, as well as the influence of extreme dry spells upon the species growth. NPY were temporally independent among the analyzed forest stands, likely due to local factors. We observed that NPY depended on dry and hot conditions during the spring-summer period at both sites, while differences in the NPY-climate reflected the species medium term dendroclimatological signal. Extremely dry years directly reduced stem growth rates. Water stress differentially affected growth at each site, likely reflecting local adaptation to droughts. Because of the increasing drought trend expected for the Mediterranean basin, our findings must be considered regarding the conservation and management of these forests.

Keywords:
Mediterranean; pointer year analysis; ring width; umbrella pine; water stress

1. INTRODUCTION AND OBJECTIVES

During the last decades, climate change has been increasingly recognized as an influencing factor upon natural systems and human society (Walther et al., 2002Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC et al. Ecological responses to recent climate change. Nature 2002; 416: 389-395. 10.1038/416389a
https://doi.org/10.1038/416389a...
). In this sense, changing climatic conditions already triggered the growth, survival and distribution of tree species around the globe, inducing forest die-off and decline in tree productivity (Allen et al., 2015Allen CD, Breshears DD, McDowell NG. On underestimation of global vulnerability to tree mortality and forest die‐off from hotter drought in the Anthropocene. Ecosphere 2015; 6(8): 1-55. 10.1890/ES15-00203.1
https://doi.org/10.1890/ES15-00203.1...
; Walther et al., 2002).

The Mediterranean basin is considered a climate change hotspot, where shifts in climatic variability occurred recently (Diffenbaugh & Giorgi, 2012Diffenbaugh NS, Giorgi F. Climate change hotspots in the CMIP5 global climate model ensemble. Climatic change 2012; 114(3-4): 813-822. 10.1007/s10584-012-0570-x
https://doi.org/10.1007/s10584-012-0570-...
). Further changes in average conditions are predicted for this area, with consequent modification of the frequency, severity and nature of anomalous climatic episodes (e.g. heat waves, droughts) (IPCC, 2014Intergovernmental Panel on Climate Change - IPCC Summary for policymakers. In: IPCC. Climate Change 2014: Synthesis report. Geneva; 2014. p. 1-35.). As alterations in weather anomalies may have greater influence on the tree growth dynamics than gradual shifts in average conditions (Jentsch & Beierkuhnlein, 2008Jentsch A, Beierkuhnlein C. Research frontiers in climate change: effects of extreme meteorological events on ecosystems. Comptes Rendus Geoscience 2008; 340(9): 621-628. 10.1016/j.crte.2008.07.002
https://doi.org/10.1016/j.crte.2008.07.0...
), understanding the ecological impact of past anomalous episodes may contribute to improve forest conservation and management plans in an unstable environmental scenario.

Dendrochronology is a powerful tool in analyzing the relationship between environmental stress and plant growth (Speer, 2010Speer JH. Fundamentals of tree-ring research. Tucson: University of Arizona Press; 2010. 360 p.). Commonly, this method relies on continuous time series, for example matching annual radial increment with monthly or seasonal climate variables. On the other hand, tree-ring research allows the identification of anomalous growth events, either anatomically based or defined comparing extreme peaks in the width of tree rings in relation to their average development. False rings/intra-annual density fluctuations, for example, may reflect drought tolerance in trees (e.g. Campelo et al., 2006Campelo F, Nabais C, Freitas H, Gutierrez E. Climatic significance of tree-ring width and intra-annual density fluctuations in Pinus pinea from a dry Mediterranean area in Portugal. Annals of Forest Science 2006; 64(2): 229-238. 10.1051/forest:2006107
https://doi.org/10.1051/forest:2006107...
). Pointer years, expressed as particular widths of the total ring, in early or latewood portions, can be related to specific environmental conditions (Schweingruber et al., 1990Schweingruber FH, Eckstein D, Serre-Bachet F, Braker OU. Identification, presentation and interpretation of event years and pointer years in dendrochronology. Dendrochronologia 1990; 8: 9-38.). Extreme growth can thus reflect the occurrence of climatic anomalies, representing a relevant source of information concerning tree sensitivity to climate change (Ols et al., 2016Ols C, Hofgaard A, Bergeron Y, Drobyshev I. Previous growing season climate controls the occurrence of black spruce growth anomalies in boreal forests of Eastern Canada. Canadian Journal of Forest Research 2016; 46(5): 696-705. 10.1139/cjfr-2015-0404
https://doi.org/10.1139/cjfr-2015-0404...
).

Pinus pinea L. (umbrella pine) is one of the most characteristic trees of the low-elevation Mediterranean forests (Mutke et al., 2012Mutke S, Calama R, Gonzalez-Martines SC, Montero G, Javier-Gordo F, Bono D et al. Mediterranean stone pine: botany and horticulture. In: Janick J (ed.): Horticultural reviews. Hoboken: Wiley; 2012. p. 39153-39201. 10.1002/9781118100592.ch4
https://doi.org/10.1002/9781118100592.ch...
). Along the Tyrrhenian Italian coastline, umbrella pine has been planted since Roman times, performing important ecological, environmental and recreational functions up to this day (Teobaldelli et al., 2004Teobaldelli M, Mencuccini M, Piussi P. Water table salinity, rainfall and water use by umbrella pine trees (Pinus pinea L.). Plant Ecology 2004; 171(1-2): 23-33.). From a physiological point of view, P. pinea is considered a drought-tolerant species (Liphschitz et al., 1984Liphschitz N, Lev-Yadun S, Rosen E, Waisel Y. The annual rhythm of activity of the lateral meristems (cambium and phellogen) in Pinus halepensis Mill. and Pinus pinea L. IAWA Bulletin 1984; 5: 263-274. 10.1163/22941932-90000413
https://doi.org/10.1163/22941932-9000041...
; Teobaldelli et al., 2004). Nevertheless, drought-driven damage in the species canopy, along with declining stem growth rate related to decreasing precipitation trends, suggest the sensitivity of umbrella pine to extremely dry climatic conditions (Busotti et al., 1995Busotti F, Cenni E, Ferretti M, Cozzi A, Brogi L, Mecci A. Forest condition in Tuscany (Central Italy). Field surveys 1987-1991. Forestry 1995; 68(1): 11-24. 10.1093/forestry/68.1.11
https://doi.org/10.1093/forestry/68.1.11...
; Mazza & Manetti, 2013Mazza G, Manetti MC. Growth rate and climate responses of Pinus pinea L. in Italian coastal stands over the last century. Climate Change 2013; 121(4): 713-725. 10.1007/s10584-013-0933-y
https://doi.org/10.1007/s10584-013-0933-...
). This assumption is indirectly confirmed by the species natural distribution, where P. pinea grows in areas (east and west ends of the Mediterranean basin) characterized by relatively cooler and wetter summers than those of the classical Mediterranean climate (Richardson, 1996Richardson DM. Ecology and biogeography of Pinus. Cambridge: Cambridge University Press; 1996. 527 p.).

The climate-growth signal of P. pinea stands has been extensively addressed (e.g. De Luis et al., 2009De Luis M, Novak K, Čufar K, Raventós J. Size mediated climate-growth relationships in Pinus halepensis and Pinus pinea. Trees 2009; 23(5): 1065-1073. 10.1007/s00468-009-0349-5
https://doi.org/10.1007/s00468-009-0349-...
; Mazza & Manetti, 2013Mazza G, Manetti MC. Growth rate and climate responses of Pinus pinea L. in Italian coastal stands over the last century. Climate Change 2013; 121(4): 713-725. 10.1007/s10584-013-0933-y
https://doi.org/10.1007/s10584-013-0933-...
; Mazza et al., 2014Mazza G, Cutini A, Manetti MC. Site-specific growth responses to climate drivers of Pinus pinea L. tree rings in Italian coastal stands. Annals of Forest Science 2014; 71(8): 927-936. 10.1007/s13595-014-0391-3
https://doi.org/10.1007/s13595-014-0391-...
; Piraino & Roig-Juñent, 2014Piraino S, Roig-Juñent FA. North Atlantic Oscillation influences on radial growth of Pinus pinea on the Italian mid-Tyrrhenian coast. Plant Biosystems 2014; 148(2): 279-287. 10.1080/11263504.2013.770806
https://doi.org/10.1080/11263504.2013.77...
; Piraino et al., 2013). Nevertheless, the relation between umbrella pine radial growth anomalies and climatic factors is still poorly documented (Campelo et al., 2006Campelo F, Nabais C, Freitas H, Gutierrez E. Climatic significance of tree-ring width and intra-annual density fluctuations in Pinus pinea from a dry Mediterranean area in Portugal. Annals of Forest Science 2006; 64(2): 229-238. 10.1051/forest:2006107
https://doi.org/10.1051/forest:2006107...
; Nabais et al., 2014Nabais C, Campelo F, Vieira J, Cherubini P. Climatic signals of tree-ring width and intra-annual density fluctuations in Pinus pinaster and Pinus pinea along a latitudinal gradient in Portugal. Forestry 2014; 87(4): 598-605. 10.1093/forestry/cpu021
https://doi.org/10.1093/forestry/cpu021...
; Novak et al., 2011Novak K, De Luis M, Cufar K, Raventos J. Frequency and variability of missing tree rings along the stems of Pinus halepensis and Pinus pinea from a semiarid site in SE Spain. Journal of Arid Environments 2011; 75(5): 494-498. 10.1016/j.jaridenv.2010.12.005
https://doi.org/10.1016/j.jaridenv.2010....
; Toromani et al., 2015Toromani E, Pasho E, Alla AQ, Mine V, Collaku N. Radial growth responses of Pinus halepensis Mill. and Pinus pinea L. forests to climate variability in western Albania. Geochronometria 2015; 42(1): 91-99. 10.1515/geochr-2015-0012
https://doi.org/10.1515/geochr-2015-0012...
). To fill this gap, this research examined the radial growth of planted P. pinea woodlands located in the north-Tyrrhenian coasts of the Italian peninsula, aiming to answer the following questions: (i) are extremely narrow rings related to climatic factors? (ii) How are drought episodes expressed in the species stem growth?

2. MATERIALS AND METHODS

2.1. Sites description and sampling

Two populations, namely San Rossore and Cecina, were sampled during the autumn of 2003 along the western Italian coastline (Table 1 and Figure 1).

Table 1
Geographical and dendrometric settings of the sampled sites.

Figure 1
On the left: sampled sites (black dots) located on the Pinus pinea L. On the right: ombrothermic diagram of the analyzed forest stands for the period 1951-1994.

Both forest stands belong to the thermo-Mediterranean subhumid class, with one (San Rossore) and two (Cecina) months of summer drought, respectively (Figure 1). Both woodlands are pure and even age forest plantations, where trees grow on sandy-loamy (San Rossore) and sandy (Cecina) soils (Cambi et al., 2017Cambi M, Paffetti D, Vettori C, Picchio R, Venanzi R, Marchi E. Assessment of the impact of forest harvesting operations on the physical parameters and microbiological components on a Mediterranean sandy soil in an Italian stone pine stand. European journal of forest research 2017; 136(2): 205-215. 10.1007/s10342-016-1020-5
https://doi.org/10.1007/s10342-016-1020-...
; Raddi et al., 2009Raddi S, Cherubini P, Lauteri M, Magnani F. The impact of sea erosion on coastal Pinus pinea stands: a diachronic analysis combining tree-rings and ecological markers. Forest Ecology and Management 2009; 257(3): 773-781. 10.1016/j.foreco.2008.09.025
https://doi.org/10.1016/j.foreco.2008.09...
). Literature for the San Rossore and Cecina stands reports densities of respectively 200-565 and 200-377 trees/ha, and approximated ages of 100-120 and 80-100 years (Cambi et al. 2017; De Micco et al. 2007De Micco V, Saurer M, Aronne G, Tognetti R, Cherubini P. Variations of wood anatomy and δ13C within-tree rings of coastal Pinus pinaster showing intra-annual density fluctuations. IAWA Journal 2007; 28(1): 61-74. 10.1163/22941932-90001619
https://doi.org/10.1163/22941932-9000161...
; Maetzke & Travaglini, 2005Maetzke F, Travaglini D. Le pinete di pino domestico della costa toscana: ipotesi di gestione sistemica per la conservazione della biodiversità. L’Italia Forestale e Montana 2005; 60(4): 541-558.; Raddi et al., 2009).

Sampled sites were selected avoiding managed (e.g. thinned) areas, thus minimizing the possible effect of disturbance upon tree growth dynamics. Classical dendrochronological procedures were adopted (Speer, 2010Speer JH. Fundamentals of tree-ring research. Tucson: University of Arizona Press; 2010. 360 p.). As pinewood belonged to protected areas, at both sites only one sample per tree was extracted at breast height (about 1.3 m from the ground) from 13 dominant individuals with an increment borer. Samples were mounted on wooden supports and surfaced with a scalpel. Tree-rings were dated, then had their widths measured from bark to pith to the nearest 0.01 mm using the sliding stage micrometer CCTRMD and recorded through the CATRAS program (Aniol, 1983Aniol RW. Tree-ring analysis using CATRAS. Dendrochronologia 1983; 1: 45-53.).

2.2. Tree-ring chronology development and environmental-growth analyses

The tree-ring measurements were visually cross-dated and then checked through statistical control (COFECHA program) (Holmes, 1983Holmes RL. Computer-assisted quality control in tree-ring dating and measurement. Tree-Ring Bulletin 1983; 43: 69-78.). During the chronology building process, individual series showing correlation with master chronology rm2< 0.4 were discarded. Dendrochronological statistical indexes were considered: MS (Mean Sensitivity), which refers to the relative year-to-year change in tree-ring widths; EPS (Expressed Population Signal), an estimation of the reliability of a finite-sample chronology in representing the theoretical infinite-sample population; RBAR, a measure of the common variance between the single series in a chronology (Speer, 2010Speer JH. Fundamentals of tree-ring research. Tucson: University of Arizona Press; 2010. 360 p.; Wigley et al., 1984Wigley TML, Briffa KR, Jones PD. On the average value of correlated time series, with applications in dendroclimatology and hydrometeorology. Journal of Climate and Applied Meteorology 1984; 23(2): 201-213. 10.1175/1520-0450(1984)023<0201:otavoc>2.0.co;2
https://doi.org/10.1175/1520-0450(1984)0...
). EPS and RBAR were calculated for a 20-year window with a 19-year overlap. Statistical indices were obtained through the COFECHA and ARSTAN40c software (Cook & Krusic, 2006Cook ER, Krusic PJ. Program ARSTAN 40c. Palisades: Tree-ring Laboratory; 2006. 14 p.; Holmes, 1983).

A two-step process was adopted in analyzing the relation between anomalous radial growth patterns and environmental factors. Previous research showed that at the medium-term frequency the species’ ring development at both forest stands mainly depended on positive moisture balance of the current spring-summer season (Piraino et al., 2013Piraino S, Camiz S, Di Filippo A, Piovesan G, Spada F. A dendrochronological analysis of Pinus pinea L. on the Italian mid-Tyrrhenian coast. Geochronometria 2013; 40(1): 77-89. 10.2478/s13386-012-0019-z
https://doi.org/10.2478/s13386-012-0019-...
). Therefore, total precipitation, average temperature and drought index values for the March-August period of the current year were used as climatic variables. Drought conditions were evaluated through the self-calibrated Palmer Drought Severity Index (scPDSI) (van der Schrier et al., 2006Van der Schrier G, Briffa KR, Jones PD, Osborn TJ. Summer moisture variability across Europe. Journal of Climate 2006; 19: 2818-2834. 10.1175/JCLI3734.1
https://doi.org/10.1175/JCLI3734.1...
). Climate data was obtained from the database of KNMI Climate Explorer web page (http://climexp.knmi.nl/). Precipitation and temperature were downloaded from the E-OBS analyses v14.0 dataset (period 1950-2016), with a resolution of 0.25° × 0.25°. The scPDSI data was extracted from the CRU self-calibrating PDSI dataset (period 1901-2016) with a resolution of 0.5° × 0.5°.

Superposed Epoch Analysis (SEA) (Holmes & Swetnam, 1994Holmes RL, Swetnam T. Program EVENT users manual: superposed epoch analysis in fire history. Tucson: University of Arizona; 1994. 7 p.), a nonparametric technique, was performed to disentangle the origin of reduced P. pinea ring growth rates, as well as the influence of drought upon the species ring development. Two separate analyses were run, differing in the established background series. In the first SEA, total precipitation and mean temperature represented the background time series, and pointer years corresponded to notorious narrow rings. In the second SEA, drought episodes represented event years, while standardized (age-detrended) annual growth was considered as background series.

Concerning the first SEA, narrow rings were defined considering negative pointer years. Positive pointer years were not computed, since we aimed to reconstruct the temporal occurrence of anomalous growth rates related to water stress, which are most likely expressed as extremely narrow rather than wide ring widths. NPY were calculated upon raw ring data following the “normalization in a moving window” (Cropper, 1979Cropper JP. Tree-ring skeleton plotting by computer. Tree-Ring Bulletin 1979; 39: 47-60.). A 5-year-long timeframe was selected, and NPY were recorded when at least 75% of the analyzed trees exhibited a reduction in growth of at least 50%. The common period 1942-2003 was considered, excluding the years of juvenile radial growth and their possible influence upon NPY development. The WEISER software was run for the identification of NPY (Gonzalez, 2001Gonzalez IG. Weiser: a computer program to identify event and pointer years in dendrochronological series. Dendrochronologia 2001; 19(2): 239-244.). Regarding the second SEA, drought episodes were established following Drobyshev et al. (2013Drobyshev I, Gewehr S, Berninger F, Bergeron Y. Species specific growth responses of black spruce and trembling aspen may enhance resilience of boreal forest to climate change. Journal of Ecology 2013; 101(1): 231-242. 10.1111/1365-2745.12007
https://doi.org/10.1111/1365-2745.12007...
), thus selecting those years when annual drought index fell in the lowest 10% percentile of the historical series (1944, 1945, 1949, 1973 and 2000). In this analysis, the age effect upon raw ring widths was removed through standardization procedure with the aid of the ARSTAN40c program (Cook & Krusic, 2006Cook ER, Krusic PJ. Program ARSTAN 40c. Palisades: Tree-ring Laboratory; 2006. 14 p.). To this end, individual chronologies were built fitting a negative exponential function to the raw ring series. Then, annual measured ring widths were divided by the expected value. Finally, individual standardized series were averaged producing a mean chronology for each sampled population.

For both SEA, a 5-year window (2 years before and 2 years after the event) was established. This window was selected based on previous analyses showing the sensitivity of the species radial growth to climatic conditions up to two years before ring development (Mazza & Manetti, 2013Mazza G, Manetti MC. Growth rate and climate responses of Pinus pinea L. in Italian coastal stands over the last century. Climate Change 2013; 121(4): 713-725. 10.1007/s10584-013-0933-y
https://doi.org/10.1007/s10584-013-0933-...
; Raddi et al., 2009Raddi S, Cherubini P, Lauteri M, Magnani F. The impact of sea erosion on coastal Pinus pinea stands: a diachronic analysis combining tree-rings and ecological markers. Forest Ecology and Management 2009; 257(3): 773-781. 10.1016/j.foreco.2008.09.025
https://doi.org/10.1016/j.foreco.2008.09...
). For each event, windows were superimposed and averaged. The mean climatic and ring-width patterns for the selected event years were statistically examined for significance (95% bootstrap confidence intervals) through 1000 Monte Carlo random simulations (Mooney & Duval, 1993Mooney CZ, Duval RD. Bootstrapping: a nonparametric approach to statistical inference. Newbury Park: Sage; 1993. 80 p. 10.4135/9781412983532
https://doi.org/10.4135/9781412983532...
). SEA was performed through the EVENT software (Holmes & Swetnam, 1994Holmes RL, Swetnam T. Program EVENT users manual: superposed epoch analysis in fire history. Tucson: University of Arizona; 1994. 7 p.).

3. RESULTS

Twenty-two individual series contributed to the two tree-ring chronologies (Table 2 and Figure 2). Chronologies spanned similar periods, with San Rossore pinewood being slightly older than Cecina (Table 2). Mean annual ring width, mean correlation among series and mean sensitivity were higher at Cecina stand, whereas EPS and RBAR values were greater at San Rossore (Table 2).

Table 2
Characteristics of the tree-chronologies.

Figure 2
Site raw ring-width chronologies (top), residual tree-ring ch ronologies (middle), and sample depths (bottom) of the sampled umbrella pine populations.

Pointer year analysis showed the occurrence of six (San Rossore) and nine (Cecina) negative growth anomalies, respectively (Figure 3). At the San Rossore stand, NPY occurred during 1950, 1951, 1956, 1964, 1994, and 2000 (Figure 3a). At Cecina, narrow rings corresponded to 1945, 1949, 1957, 1970, 1973, 1987, 1990, 1997, and 1999 (Figure 3b). No temporal coincidence in NPY emerged among the two studied woodlands.

Figure 3
Raw ring-width series of the analyzed trees showing negative pointer years (vertical lines) at the examined forest stands for the common period 1942-2003.

Superposed Epoch Analysis, calculated selecting NPY as event years, showed a close relation among narrow ring formation and climatic factors. At the San Rossore forest stand, NPY are associated with dry conditions during the preceding year followed by high spring-summer temperatures during the current year (Figure 3a). On the other hand, negative growth anomalies at the Cecina population are related to March-August period of the current year characterized by low precipitation (Figure 4). Finally, SEA performed considering standardized ring widths as background time-series revealed that extreme drought translated into reduced species growth during the current year at both woodlands, and in the following year at the San Rossore stand (Figure 5).

Figure 4
Superposed epoch analysis (SEA) comparing spring-summer season precipitation and temperature departures during the growth event-years, corresponding to negative pointer years.

Figure 5
Superposed epoch analysis (SEA) comparing standardized ring growth departures during the event-years, corresponding to extremely drought years.

4. DISCUSSION

Regarding the statistical indices examined in this work, the relatively high values of MC for both chronologies are likely related to a common factor influencing the stem growth, possibly depending on local climate conditions (Speer, 2010Speer JH. Fundamentals of tree-ring research. Tucson: University of Arizona Press; 2010. 360 p.). Most important, the high EPS values, above the 0.85 critical threshold indicate that, despite the relatively low sample depth developed in this research, our findings could be extended to the whole woodlands where sampled trees grew (Wigley et al., 1984Wigley TML, Briffa KR, Jones PD. On the average value of correlated time series, with applications in dendroclimatology and hydrometeorology. Journal of Climate and Applied Meteorology 1984; 23(2): 201-213. 10.1175/1520-0450(1984)023<0201:otavoc>2.0.co;2
https://doi.org/10.1175/1520-0450(1984)0...
).

Interestingly, NPY emerged at the analyzed forests during different years, suggesting that narrow ring formation was unlikely driven by a regional environmental factor. Pointer years can either reflect large-scale climatic variability or more local environmental characteristics (Schweingruber, 1996Schweingruber FH. Tree rings and environment: dendroecology. Berne: Paul Haupt AG Bern; 1996.). Although not measured in this work, it is well known that insect outbreaks, masting events, stand factors, and local climatic conditions may be potential NPY drivers (Schweingruber, 1996). Further research should help to disentangle the origin of local NPY for the analyzed north-Tyrrhenian umbrella pine populations.

Superposed Epoch Analysis establishing NPY as event years revealed that extremely narrow ring development is climatically driven. Differences emerged among the selected stands, which seem to reflect the medium-term dendroclimatological signal at the studies sites (Piraino et al. 2013Piraino S, Camiz S, Di Filippo A, Piovesan G, Spada F. A dendrochronological analysis of Pinus pinea L. on the Italian mid-Tyrrhenian coast. Geochronometria 2013; 40(1): 77-89. 10.2478/s13386-012-0019-z
https://doi.org/10.2478/s13386-012-0019-...
). In this sense, previous research showed a strong relation between Cecina ring growth and spring-summer rainfall of current year, whereas at the San Rossore stand, radial growth reflected amount of precipitation of preceding years as well (Piraino et al., 2013).

Physiologically, the lagged response of radial growth to rainfall at the San Rossore stand may be related to the detrimental effect of reduced precipitation upon carbohydrate storage (Pallardy, 2010Pallardy SG. Physiology of woody plants. Burlington: Academic Press; 2010. 464 p.). On the other hand, high temperatures during spring-summer of current year (San Rossore) can enhance evapotranspiration processes, while low precipitations (Cecina) may reduce photosynthesis (Campelo et al., 2006Campelo F, Nabais C, Freitas H, Gutierrez E. Climatic significance of tree-ring width and intra-annual density fluctuations in Pinus pinea from a dry Mediterranean area in Portugal. Annals of Forest Science 2006; 64(2): 229-238. 10.1051/forest:2006107
https://doi.org/10.1051/forest:2006107...
; Oliveras et al., 2003Oliveras I, Martinez-Vilalta J, Jimenez-Ortiz T, Lledó MJ, Escarré A, Piñol J. Hydraulic properties of Pinus halepensis, Pinus pinea and Tetraclinis articulata in a dune ecosystem of Eastern Spain. Plant Ecology 2003; 169(1): 131. 10.1023/A:1026223516580
https://doi.org/131. 10.1023/A:102622351...
). Both climatic conditions can negatively affect carbohydrate production, thus promoting NPY occurrence (Liphschitz et al., 1984Liphschitz N, Lev-Yadun S, Rosen E, Waisel Y. The annual rhythm of activity of the lateral meristems (cambium and phellogen) in Pinus halepensis Mill. and Pinus pinea L. IAWA Bulletin 1984; 5: 263-274. 10.1163/22941932-90000413
https://doi.org/10.1163/22941932-9000041...
). The presented results agree with researches performed for P. pinea woodlands distributed in coastal Albania, showing that negative pointer years are tightly coupled to dry climatic conditions during the spring-through-autumn period (Toromani et al., 2015Toromani E, Pasho E, Alla AQ, Mine V, Collaku N. Radial growth responses of Pinus halepensis Mill. and Pinus pinea L. forests to climate variability in western Albania. Geochronometria 2015; 42(1): 91-99. 10.1515/geochr-2015-0012
https://doi.org/10.1515/geochr-2015-0012...
).

Further information is provided by SEA calculated considering extremely low scPDSI values. At the San Rossore and Cecina woodlands, tree-ring decreased in drought years, suggesting that although no common NPY occurred, stem growth at both stands is sensitive to extremely dry conditions during the year of ring formation. On the other hand, plasticity in the species response to drought emerged, expressed by the impact of the dry spell in the San Rossore pinewood. Variability in the species response to extreme drought could reflect either genetic variation in provenance or phenotypic plasticity. Although our research did not address this particular topic, the low genetic polymorphisms of umbrella pine suggested that this result is unlikely to be an expression of differences in genetic provenances (Fallour et al., 1997Fallour D, Fady B, Lefevre F. Study on isozyme variation in Pinus pinea L.: evidence for low polymorphism. Silvae Genetica 1997; 46(4): 201-206.). Therefore, local adaptation to climatic conditions possibly explains the different response of the analyzed forests to drought events. San Rossore could be considered, by a bio-climatological point of view, a transitional area located at the northern border of the Mediterranean bio-climate, characterized by the presence of Central European plant species lacking at southern latitudes along the Tyrrhenian coasts (Vagge & Biondi 1999Vagge I, Biondi E. La vegetazione delle coste sabbiose del Tirreno settentrionale italiano. Fitosociologia 1999; 36(2): 61-95.). In this sense, the San Rossore stand is under the influence of the orographic effect of the Apuan Alps, with consequent higher rainfall amounts than Cecina, where climate is modulated solely by the presence of the Tyrrhenian Sea (Rapetti, 1997Rapetti F. L’influenza del bosco mediterraneo sul clima I: la macchia di Migliarino (litorale pisano). Atti Societá Toscana di Scienze Naturali 1997; 104: 73-90.; 1999Rapetti F. L’influenza del bosco mediterraneo sul clima. 2-La Pineta di Marina di Cecina (Toscana centrale). Atti-Societá Toscana di Scienze Naturali 1999; 106: 17-31.). Additionally, hydroclimatic balance during dry years is more negative at Cecina than at San Rossore, suggesting more arid conditions at the former pinewood site (Rapetti 1997Rapetti F. L’influenza del bosco mediterraneo sul clima I: la macchia di Migliarino (litorale pisano). Atti Societá Toscana di Scienze Naturali 1997; 104: 73-90.; 1999Rapetti F. L’influenza del bosco mediterraneo sul clima. 2-La Pineta di Marina di Cecina (Toscana centrale). Atti-Societá Toscana di Scienze Naturali 1999; 106: 17-31.). The data presented in this research further supported these assumptions (Figure 1). Indeed, temperatures are similar between the sampled areas, whereas trees located at San Rossore grow under wetter regional climatic conditions than those of Cecina site at both annual and seasonal (spring-summer) timescales (Figure 1). Differences are more marked during the late-summer period, when pines growing at Cecina stand experienced a longer water deficit (Figure 1). For the abovementioned reasons, we could hypothesize that umbrella pines growing at San Rossore stand may experience a greater physiological stress during dry spell than those located at the Cecina site, where trees could probably be better adapted to water shortage episodes (De Luis et al., 2013De Luis M, Čufar K, Di Filippo A, Novak K, Papadopoulos A, Piovesan G et al. Plasticity in dendroclimatic response across the distribution range of Aleppo pine (Pinus halepensis). PLoS One 2013; 8(12): e83550. 10.1371/journal.pone.0083550
https://doi.org/10.1371/journal.pone.008...
).

Previous researches highlighted the effects of drought upon the species radial growth along the Mediterranean area. In the Iberian Peninsula, more arid conditions experienced by umbrella pine increased inter-annual variability in the species growth, suggesting an amplified sensitivity of ring development to water shortage (Natalini et al., 2015Natalini F, Correia AC, Vazquez-Pique J, Alejano R. Tree rings reflect growth adjustments and enhanced synchrony among sites in Iberian stone pine (Pinus pinea L.) under climate change. Annals of Forest Science 2015; 72(8): 1023-1033. 10.1007/s13595-015-0521-6
https://doi.org/1023-1033. 10.1007/s1359...
). Regarding P. pinea populations distributed in the Italian coastline, decreasing annual rainfall amount during the mid-1920s and the early 1970s induced significant downward trends in the species stem growth (Mazza & Manetti, 2013Mazza G, Manetti MC. Growth rate and climate responses of Pinus pinea L. in Italian coastal stands over the last century. Climate Change 2013; 121(4): 713-725. 10.1007/s10584-013-0933-y
https://doi.org/10.1007/s10584-013-0933-...
). On the other hand, the synergic action of reduced rainfall and expansion of tourism translated into less stored soil water, which likely deteriorated the growth conditions of mid-Tyrrhenian pinewoods (Mazza & Manetti, 2013Mazza G, Manetti MC. Growth rate and climate responses of Pinus pinea L. in Italian coastal stands over the last century. Climate Change 2013; 121(4): 713-725. 10.1007/s10584-013-0933-y
https://doi.org/10.1007/s10584-013-0933-...
).

5. CONCLUSION

This research explored the relationship between P. pinea radial growth anomalies and environmental conditions. Previous research concerning the analyzed pine stands dealt with the species dendroclimatological signal, but only at the medium-term frequency, thus not considering the occurrence of extreme radial growth (Piraino et al., 2013Piraino S, Camiz S, Di Filippo A, Piovesan G, Spada F. A dendrochronological analysis of Pinus pinea L. on the Italian mid-Tyrrhenian coast. Geochronometria 2013; 40(1): 77-89. 10.2478/s13386-012-0019-z
https://doi.org/10.2478/s13386-012-0019-...
). Furthermore, to our knowledge there are no studies that directly addressed the response of the species radial growth to drought events. Our findings highlighted the site-dependent stem growth response to dry spells, apparently modulated by local climatic conditions. In this sense, drought-related effect was more evident at the San Rossore woodland. This result is relevant considering that the San Rossore pinewood is among the most important productive plantations of P. pinea in Europe, characterized by long tradition in high-quality production of pine nuts exported globally (Peruzzi et al., 1998Peruzzi A, Cherubini P, Gorreri L, Cavalli S. Le pinete e la produzione dei pinoli dal passato ai giorni nostri, nel territorio del Parco di Migliarino, S. Rossore, Massaciuccoli. Pisa: Ente Parco Regionale Migliarino, San Rossore, Massaciuccoli. Litografia Felici; 1998. 134 p.). Our findings further demonstrated that the expected drying trend for the study area will be detrimental for the P. pinea growth dynamics, warning about the need to enact conservation and management policies in these forest resources.

ACKNOWLEDGEMENTS

Thanks to the DendrologyLab of the University of Viterbo “Tuscia”, particularly to Drs. Gianluca Piovesan and Alfredo Di Filippo for supervising the building of earlier version of the stone pine chronologies presented in this research, and to the latter for his fieldwork assistance at the Cecina forest stand. Thanks are due also to the Authorities of the National Parks that allowed sampling. Two anonymous reviewers are greatly acknowledged for their revisions that improved our manuscript.

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Publication Dates

  • Publication in this collection
    26 June 2020
  • Date of issue
    2020

History

  • Received
    20 June 2018
  • Accepted
    05 Nov 2018
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