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Dendrochronologia 27 (2009) 173181 www.elsevier.de/dendro

Structure and stand development of secondary forests in Eastern Prealps (Italy)

Giorgio Albertia,, Alessandro Peressottia, Pietro Piussib, Giuseppe Zerbia
a b

Department of Agriculture and Environmental Sciences, University of Udine, Via delle Scienze 208, I-33100 Udine, Italy Department of Agriculture and Forest Sciences and Technologies, University of Firenze, Italy

Received 11 June 2007; accepted 19 February 2008

Abstract
The composition and temporal variations in species recruitment were examined by means of annual dendrochronological data, to determine the historical development and successional history of ash and sycamore mixed stands in ve secondary forests on the Eastern Prealps. The rst step of the investigation was to describe species composition and age structure. In accordance with data derived from land register and time series of orthophoto images, differences in time of colonization among the ve stands were detected. The second step was to describe spatial colonization patterns: only in one case a frontal pattern was found while in others the colonization started from some old alder or ash trees preserved by farmers in the meadows. & 2009 Elsevier GmbH. All rights reserved.
Keywords: Secondary succession; Dendroecology; Age; Structure; Ash

Introduction
Land use changes represent one of the most important components of global environmental change. In the mid-latitudes, the economic trends have promoted agriculture intensication, industrialization and migration of rural population from the rural areas. As a consequence, areas of marginal agriculture have been abandoned leading through secondary successions to the appearance of secondary forests. The wide range of studies on the topic of abandoned farmland underlines the many different elds of research covered by this subject (e.g., forest dynamic, carbon sequestration,
Corresponding author.

E-mail addresses: alberti@uniud.it (G. Alberti), peressotti@uniud.it (A. Peressotti), pietro.piussi@uni.it (P. Piussi), zerbi@uniud.it (G. Zerbi). 1125-7865/$ - see front matter & 2009 Elsevier GmbH. All rights reserved. doi:10.1016/j.dendro.2008.02.002

species composition) as well as its considerable geographical distribution (Harper, 1918; Raup and Carlson, 1941; Mather, 1992; Debussche et al., 1999; Piussi, 2000; Knops and Tilman, 2000). In general terms, secondary forests can be dened as forest regenerated largely through natural processes after signicant human or natural disturbance of the original forest vegetation (FAO, 2001). In Italy, according to the National Statistics Bureau (ISTAT), during the last 50 years, the total forest area increased by 14.9%, with natural forest recovery occurring mainly on the Alps and the Apennines (Piussi, 2002; Corona et al., 2005). In the Alps, the abandonment of agricultural land has become so widespread that the landscape has radically changed (Piussi and Pettenella, 1998). Thus, an appropriate management of these former agricultural areas requires a historical understanding of the chronology and of the mechanisms inuencing woody expansion to predict

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future vegetation pathways (Chauchard et al., 2007). However, although the process is quite widespread in Italy and data on species composition, structure and area interested by the colonization are reported in literature at regional and country scale (Piussi, 2002), few data about colonization patterns, inuence of previous land use and stands productivity (i.e. biomass and carbon sequestration) are available. In particular, as far as productivity and carbon sequestration is concerned, studies aimed at investigating these aspects usually adopted a chronosequence approach (Alberti et al., 2008). This technique, also called space-for-time substitution, assumes that spatial and temporal variation are equivalent, but, in the case of secondary successions, there are difculties in determining a precise stand age because woody encroachment usually takes place in several years. Furthermore, the correlations of species abundances and community attributes with stand age cannot be unambiguously attributed to successional processes if there are other confounding factors, including site status at the time of abandonment (Bakker et al., 1996). Therefore, the use of dendrochronology can help to assign an age to each stand for productivity and carbon sequestration calculations and the assessment of the history of the sites included in the chronosequence using interview and/or written sources can help to know pre-abandonment conditions (Piussi, 2002; Motta and Edouard, 2005). Dendrochronology has proven to be a particularly solid approach to reconstruct the origin and past dynamics of forest stand regimes, both in old-growth forests (e.g., Winter et al., 2002) and in those that have undergone heavy anthropogenic disturbances (Motta et al., 2002) by assessing age structure, which is the net budget between regeneration and mortality at the moment of the sampling. The aims of the present paper are: (a) to propose a methodology to assess age of secondary stands that may be used in studies about carbon stocks dynamics following forest colonization; (b) to describe age structure and temporal and spatial patterns of colonization, which caused a dramatic landscape transformation. The above mentioned aspects have been investigated using a chronosequence made up of secondary mixed ash (Fraxinus excelsior L.) and sycamore (Acer pseudoplatanus L.) stands in the Eastern Prealps.

Fig. 1. (A) Location of the study area and former land use in 1950. (B) Inhabitants dynamic and forest cover changes in the study area during the last century.

Methods
Study area
The study area is located in the Municipality of Taipana (Udine) on the Eastern Prealps of Friuli Venezia Giulia (Italy) (461120 N, 121200 E; Fig. 1A).

The elevation is about 600 m a.s.l., the mean annual temperature is 10 1C (mean winter temperature of about 0 1C) and an annual rainfall of more than 2500 mm. Soils can be classied as calcareous brown earths of low acidity. The topography is usually gentle; locally, slopes are steep but the greatest part of the land has been used as meadows (Salbitano, 1987). The ownership is mainly private, small-sized and fragmented (1.2 ha on average). Depopulation started at the turn of last century but accelerated dramatically since the 1960s: the inhabitants were 3700 at the beginning of the last century (Del Bene, 2002), while dropped to 715 in 2003 and the forest area increased from 27% to 80%, leaving large areas of the landscape unmanaged (Fig. 1B). The most important forest type is represented by hardwoods mixed stands dominated by ash (Fraxinus excelsior L.) and sycamore (Acer pseudoplatanus L.) with a cover area of 2800 ha (55% of the total forest area). Some small patches of pure beech forest (Fagus sylvatica L.) are also present on rocky soils that were not converted to meadows in the ancient times (Fig. 2).

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sprout) was registered, diameter at breast height (1.30 m; DBH) and total height were measured.

Age structure and secondary succession dynamic

One wood core was taken with a Pressler borer downslope from each tree (height 41.30 m) at a 2030 cm height. When stumps supported more than one stem, only the stem with the largest diameter was taken into consideration because it was supposed to be the oldest and to represent stump age. In plot T1, 53 trees were cut during thinning and basal wood sections were collected (Alberti et al., 2005). In total 374 samples were collected (53 basal sections and 23 cores from T1, 88 cores from T2, 56 from T3, 91 from T4 and 63 from T5) in order to calculate the age structure and to determine the growth pattern. In the eld, all the cores were xed to wooden supports and in the laboratory they were cleaned, using a razor blade, until annual rings could be clearly seen. In order to measure annual ring widths, a DENDROTAB 2003 table (& Walesch Electronic GmbH, CH) with a binocular microscope was used. To take into account the age determination errors due to missing or very narrow rings, the age structure was built according to age classes of 5 years (i.e. 15, 610, 1115, etc.). Data were collected and stored using T-Tools software (& Walesh Electronic GmbH, CH). In the case of basal sections, the ring measurements were taken along two directions and the average for each year was calculated so as to create an individual chronology. When a core did not reach the pith, the number of missing rings (n) was estimated using the following equation: n r rm Dn 1

Fig. 2. Five idealized stages in stand development can be recognized during a secondary succession. At initiation (I), seedlings are rarely affected by competition with other trees. At canopy closure, stem exclusion begins. As the over-story trees approach maximum height, the canopy opens and an under-story is re-initiated. Solid line represents number of trees sampled vs. year, dashed line represents annual increment in tree number.

Vegetation survey
Five stands (T1, T2, T3, T4 and T5) within a radius of 5 km and of presumably different ages were selected using a time series of orthophoto images (1954, 1976, 1998) according to the following criteria: evidence of historical use as meadow before 1957; overstoried vegetation dominated by ash and sycamore; recent anthropogenic disturbance absent or reduced; good accessibility. However, the time span among the aerial images was quite large (on average 20 years) so that the exact age determination was impossible; in any case through the aerial image the presence of scattered saplings cannot be detected. For this reason, the age structure of each stand was studied more precisely using a dendrochronological approach. All the stands had a relative regular and continuous canopy except stand T2 that was characterized by the presence of two clearly separated layers. Due to the reduced average extent of property, a 1000 m2 plot was subjectively set up to represent all the surrounding stand: live and dead standing trees, logs lying on the ground and stumps were identied, labelled and mapped, by referring to a XOY system. When humanmade structures were present (i.e. stone walls), they were included in the plot. The coordinates of the system origin were taken using a GPS. Stem origin (i.e. seed or

where r is the radius measured with calliper in the eld, rm is the sum of all the ring widths in the wood core and Dn is the numbers of rings in the last measured centimetre. The errors associated with estimating missing ring were obtained by core simulations. For this purpose, 36 basal sections with a diameter 412 cm from those collected at plot T1 were selected. Using each individual chronology, we simulated a missing radius from the pith in a range from 0.5 to 5 cm with an increment each time of 0.5 cm. Then, equation 1 was used to estimate missing rings at each simulation and age was determined. Absolute error in age was computed as absolute difference between estimated and true ages. The error increases with the length of the missing radius reaching a maximum of 15 years in the case of 5 cm missing radius, but, because more then 90% of the partial cores had a missing radius of less then 2 cm, the age estimation error was less than 10 years.

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As said above, we observed that succession generally takes place during several years so that it is impossible to establish a precise age. Therefore, using data from sample trees, a non-linear relationship between time and tree density was established for each plot. Nonlinear analysis was performed using the GaussNewton procedure in STATA 7 (& Stata Corporation, College Station, USA) and density was described using a modication of the Richards logistic function Density Bmax 1 Ceat 1 2

distribution maps by Ordinary Kriging analysis in SURFER version 5.02 (& Golden Software Inc.).

Results
Stand characteristics and size structure
The most important features of the ve plots studied are shown in Table 1. The number of living trees per hectare ranged from 970 trees for plot T5 to 1940 for plot T4. Many standing dead trees were found in plot T4 (400 trees ha1). Even if all these stands are included in the broad category of ash-maple woods (Del Favero et al., 1998), only in two plots (T1 and T2) the dominant species both in term of stem density and in term of basal area was ash (Fraxinus excelsior L.) while sycamore (Acer pseudoplatanus L.) was sporadic in all the plots. In plot T3 hornbeam (Ostrya carpinifolia Scop.) was the dominant species in term of density while alder (Alnus glutinosa L.), represented also in plots T2 and T5, had the highest basal area (29% of the total) (Table 2). In T4 and T5, whitebeam (Sorbus aria L.) and birch (Betula pendula Roth.) were the most numerous species in term of stems, although in T5 ash had the highest basal area (32% of the total). In the understory, hazel (Corylus avellana L.) was quite common. In all the plots with the exception of plot T1 and T4, alder was present. Standing wood volume ranged from 233 m3 ha1 of plot T5 to
Table 2. Species Ash% Birch% Black alder% Chestnut% Elm% Hornbeam% Sycamore maple% White beam% Others% Total tress (%) Total shrubs (%) Total (m2 ha1) Partition of basal area for species and plot. T1 71 T2 63 6 21 23 2 8 100 0 28.78 23 94 6 26.45 3 2 93 7 27.96 34 6 99 1 31.99 2 4 96 4 26.02 16 T3 8 19 29 9 T4 17 26 T5 32 24 34

where Bmax is the maximum tree number, a and C are coefcients controlling the rate and the inection point of the sinusoidal curve, respectively and t is age (years). Annual increment in tree number (n yr1) at each year was then calculated. Obviously, only trees surviving at the moment of the measurements were considered. Then ve stages in stand density were dened (Fig. 1): (1) pre-abandonment stage: the meadow was still mown but some isolated trees were growing possibly because they were grown as fruit or fodder trees, or for fertilisation purposes, or else; (2) initiation stage: abandonment took place and secondary succession began. The lower limit of this stage was determined as the 10th percentile of the annual tree number increment distribution; (3) maximum colonization: maximum annual tree number increment was reached; (4) stem exclusion stage: annual tree number increment gradually decreased presumably because of canopy closure. The upper limit of this stage was determined as the 90th percentile of the annual tree number increment distribution; (5) understoried re-initiation stage: gaps due to mortality or to wind-throw allow sunlight to penetrate to the forest oor and stimulate the re-initiation of under-story vegetation.

On this basis, each stand was assigned to a stage class: the lower limit of the initiation stage was conventionally assigned to each plot as the stand age. Finally, using age data recorded for each tree and their spatial position within the plot, the pattern of colonization was determined producing age spatial
Table 1. General features of the ve plots (1000 m2). Elevation T1 T2 T3 T4 T5 580 600 660 700 660 No. of living trees (n ha1) 1000 1320 1140 1940 970

No. of dead trees (n ha1) 160 100 200 400 200

Total (n ha1) 1160 1420 1340 2340 1170

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Fig. 3. Species and size-class distribution.

347 m3 ha1 of plot T1. Seedlings (height o1.30 m) were abundant in plot T2 while they were nearly absent in plot T1 (data not reported). All the stands showed an exponential negative trend (Fig. 3) with abundance of trees of small diameter and lack of large diameter trees resembling those of unevenaged stands.

Age structure and secondary succession dynamics

The age structure was similar among the ve plots (Fig. 4) but the beginning of the colonization was different. The woodland encroachment in the oldest plot (lower limit to the stand initiation stage, as specied before) started 75 years ago and 40 years ago in the youngest (Table 3). The colonization period lasted from 20 to 35 years and, generally, the colonisation was the most intense during a period of 1015 years. Furthermore, average species composition changed across the colonization period (Fig. 5): the number of births of elm and birch decreased across the stages and, usually, these trees were not in good health conditions

(data not reported); ash continued to establish until understoried re-initiation stage when gaps in the canopy were present; alder was present before the abandonment, but most of the colonization took place during the initiation stage. It is possible to distinguish two patterns of colonization by using trees position and age: (i) when humanmade structures were present (i.e. stone walls), the preexisting trees were usually located in the proximity of these structures and, after meadow abandonment, colonization followed a frontal pattern starting from the wall to the centre of the meadow (Fig. 6a); (ii) when human-made structures were not present, the preexisting trees were randomly distributed within the meadow and, after abandonment, the colonization followed a centrifugal pattern (Fig. 6b).

Discussion and conclusions

The rate at which a site is colonized depends on both the rate at which individual organisms arrive at the site

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Fig. 4. Age structure for cored trees. Arrow indicate the beginning of the initiation phase.

Table 3. Age assigned to each stand (lower limit of the stand initiation stage), limits and length of the all colonization periods, year when colonization is maximum. Plot Age Colonization Start T1 T2 T3 T4 T5 75 40 55 55 50 1929 1964 1949 1949 1954 End 1949 1994 1984 1969 1979 Length 20 30 35 20 25 Maximum colonization Year 1939 1979 1964 1959 1969

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Fig. 5. Average species mixture within the different colonization stages. All the values are averages of the ve stands. Bars indicate standard errors. Stage I=pre-abandonment phase; stage II=initiation phase; stage III=maximum colonization phase; stage IV=stem exclusion phase; stage V=understory re-initiation phase.

Fig. 6. (A) Example of frontal pattern of colonization (plot T2). Along the X axes a small stone wall was located. (B) Example of a nucleated pattern of colonization (plot T3). Colonization starts from some plants within the meadows.

and on their success at becoming established and surviving, that is the processes of migration and environmental selection (Gleason 1926; Kimmins, 1997). Thus, the presence of a seed source, on one hand, and the rate of competition and disturbance, on the other, are important in inuencing the type and the timing of the succession. The temporal encroachment

differs across tree species (Guidi and Piussi, 1993) and the composition in these secondary stands is still in evolution. In fact, while some species are present before the abandonment, others appear only in the following decades. Previous species such as alder are not in good health conditions and early phases species such as birch is being replaced by ash. However, after an initial

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colonization phase inuenced by previous land use, future dynamics will be more related to forest maturation (Chauchard et al., 2007). For example, late seral shade-tolerant species as beech, which, at the higher altitudes, is typical in the surrounding remnant old forests, is not yet present in these secondary stands; the same situation has been described by Colaone and Piussi (1975) in neighbouring areas. It is possible to expect that their recruitment will take place long after that of pioneer species; this lag could depend on seed dispersal mode and the absence of trees that are able to produce seeds. In fact, the remnant beech forests are too widespread in the study area and not connected one to the other. Colonization patterns and timing may be also strongly inuenced by human disturbances that are unforeseeable and irregular in space and time. In fact, previous land use and human management has a strong inuence on the initial oristic composition (Egler, 1954) and in creating sites favourable for colonization (safe site, Harper, 1977): the succession of plant species in abandoned agricultural elds depends mostly on the relative growth rates and shade tolerance of the assemblage of species in the elds at the time of abandonment or arriving shortly thereafter. Piussi (1998) reports that in this part of the Eastern Prealps farmers used to plant black alder in meadows in order to improve grass production; the Land Register of 1823 already mentions this plantations of alder and willow in the territory of Taipana. This agricultural technique is applied by farmers in other parts of the world (Austria, India, Costarica, Mexico, Philippines) using different alder species. It is possible to suppose that alder has modied soil conditions in such a way to interfere with regeneration, growth and competition of the other species. Furthermore, in Central Europe, so as in Northern Italy, common ash and other hardwood species, which were useful both for wood and fodder production, were also growing within the hedges or small woodlands. These trees could have represented the seed source for the encroachment of meadows after abandonment favouring a nucleated pattern of colonization. On the other hand, when particular man-made structures, like stone walls or stone heaps, were present, trees could have been settling on them before the abandonment, thanks to the lack of disturbance or competition; these were therefore safe sites for the young seedlings because they could not be reached by farmers when mowing the meadows. In this case the encroachment followed a frontal pattern, that is from an edge to the centre of the area. However, in both colonization patterns, the initiation phase has been quite short and canopy closure occurred in 1015 years probably because of a large seed availability due to the large crowns of pre-settled trees. The short colonization period is also due to the fact that

ash is quite plastic. In fact, this species spreads easily from the forest margins to clearings or adjacent meadows, thanks to the high samaras production (140.000 seeds or 10 kg per individual in adult trees Collin and Badot, 1997), the low post dispersal predation and the low competition by other species due to phytotoxic effects of ash litter (Grime, 2001). The initiation phase, due to abundant seedling establishment and rapid juvenile growth, is quite short: density creates unfavourable light conditions to the last seedling established so that these grow very slowly and nally cannot survive. This process can explain the stem diameter distribution we have observed.

Acknowledgement
This work was nancially supported by the European Commission through the Interreg-Cadses project CarbonPro, by the Italian government through the FIRB project Carboitaly and the PRIN project Methodologies for CO2 uptake accounting in agricultural and forest ecosystems. We would like to thank Diego Chiaba ` , Giacomo Blasone and Sara Berra for the help during eld campaigns and lab analysis.

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