Work Package 6
Ecological and physiological analysis of plant and epiphytic
vegetation answers to environmental modifications
Analisi ecologica e fisiologica delle risposte di piante
e vegetazione epifitica alle modificazioni ambientali
Studi Trent. Sci. Nat., Acta Biol., 81 (2004), Suppl. 1: 227-244
© Museo Tridentino di Scienze Naturali, Trento 2005
ISSN 0392-0542
Winter depression and spring recovering of photosynthetic function of five coniferous
species in the treeline zone of the Southern Alps (Trentino-South Tyrol)
Emanuele ECCEL1, Roberto ZORER2 & Massimo BERTAMINI2*
IASMA Research Center, Natural Resources Department, Via E. Mach 1, I-38010 San Michele all’Adige (TN), Italy
IASMA Research Center, Agricoltural Resources Department, Via E. Mach 1, I-38010 San Michele all’Adige (TN), Italy
Corresponding author e-mail: [email protected]
SUMMARY - Winter depression and spring recovering of photosynthetic function of five coniferous species in the
treeline zone of the Southern Alps (Trentino-South Tyrol) - Over a period of two years microclimate and physiological
features of five coniferous species (Spruce, Cembran pine, Larch, Mountain dwarf pine, Scots pine) growing at the
treeline on Mt. Weisshorn / Corno Bianco were monitored. Temperature profiles and plants light microclimate were
studied and chlorophyll fluorescence, chlorophyll and carotenoids concentrations and needle water content were
measured. An evident positive relationship between air temperature and quantum use efficiency of photosystem II
and a depression of photosynthetic pigments concentration during winter and spring were found. Excessive light
reduced quantum yield of PSII efficiency and, coupled with insufficient temperature, led to a permanent depression
of photosynthetic capacity at higher elevations or in more exposed sites. In some cases these damages induced winter
desiccations of needle and/or shoots. Sheltering effect of canopies positively influenced photosynthetic performances
and health of shoots, allowing higher growth and survival rates. In order to simulate the effects of temperature on
spring recovery of photochemical efficiency of PSII two models, based on thermal sums, have been calibrated and
tested for Norway spruce; nevertheless, simpler running mean models provided better results.
RIASSUNTO - Depressione invernale e recupero primaverile delle funzioni fotosintetiche in cinque specie di
conifere nella zona di limite del bosco nelle Alpi meridionali (Trentino-Alto Adige) - Nel corso di due anni sono
stati monitorati sia il microclima sia alcuni caratteri fisiologici di cinque specie di conifere (abete rosso, pino
cembro, larice, pino mugo, pino silvestre) che crescono al limite del bosco sul Monte Weisshorn / Corno Bianco.
Sono stati studiati i profili di temperatura e il microclima luminoso delle piante e sono stati misurati la fluorescenza
clorofilliana, la concentrazione di clorofilla e carotenoidi, e il contenuto d’acqua negli aghi. È stata trovata una
chiara relazione positiva tra la temperatura dell’aria e l’efficienza quantica del fotosistema II, ed evidenziato un calo
nella concentrazione dei pigmenti fotosintetici in inverno e primavera. La forte radiazione luminosa, in particolare
se combinata con una bassa temperatura, ha ridotto l’efficienza quantica del fotosistema II, comportando anche
una depressione permanente alle quote più elevate o nei siti più esposti. Questi danni, nei casi più gravi, hanno
provocato dei disseccamenti invernali di aghi e/o di interi getti. L’effetto di protezione (auto-ombreggiamento) delle
chiome influenza le prestazioni fotosintetiche e la salute dei getti fogliari, permettendo una più elevata crescita e
sopravvivenza delle piante. Per simulare gli effetti della temperatura sulla ripresa fotosintetica sono stati calibrati
e testati due diversi modelli, basati su sommatorie termiche e specifici per l’abete rosso; tuttavia, modelli di media
mobile hanno fornito risultati predittivi migliori.
Key words: treeline, chlorophyll content, chlorophyll fluorescence, PSII quantum yield, winter desiccation, spring
Parole chiave: limite del bosco, contenuto di clorofilla, fluorescenza clorofilliana, resa quantica PSII, disseccamenti
invernali, ripresa primaverile
Montagnani et al.
Alpine vegetation shows a clear ecotone in its upper limit. However, the interface between different biomes, such as forest and alpine grassland, has different
aspects due to the combination of physiological and environmental conditions of the site where plants live.
On the Apennines and on subtropical and southern
hemisphere mountains, the transition between the two
biomes is surprisingly sharp. In contrast, the Larch
forest shows a gradual reduction in tree density and
On the eastern Alps there is a fast decrease in tree
height and forest biomass moving from 2000 m a.s.l,
where a mixed coniferous forest exists, through to a
shrub-like mountain pine forest, where stunted trees
survive, to open alpine grassland growing at elevations higher than 2300 m.
This line of passage between biomes is called
treeline, and the knowledge of its features is necessary to understand the evolution of the alpine flora in
time and space.
Climate change can influence alpine species
growth and composition, in particular changing the
treeline altitude. While there is a common scientific
consensus about the limited direct influence of higher CO2 atmospheric concentration on mountain vegetation (Cooper 1986; Smith & Donahue 1991; Terashima et al. 1995), the increase of temperature and
the variations in precipitation regimes and snow cover can have a direct impact on constraints of alpine
plant growth (Hättenschwiler & Körner 1995; Vaganov et al. 1999).
Although the treeline has been the subject of a
privileged field for ecological research and scientific
theories for more than one century (Kerner 1869), up
to now there is no complete agreement about the determinants of this abrupt change between biomes.
Temperature is certainly a condition influencing
this vegetation change, however the small thermal
gradient, moving from the forest to alpine pastures,
can hardly be considered the single determinant for
this change.
Probably implicitly assuming a Liebig approach (Liebig 1840) to limiting factors, many researchers tried to
find a single limiting factor on tree vegetation.
Many factors and processes constraining tree
growth, survival and reproduction have been considered by different authors: worthy mention are decrease in seeds production (Fischer et al. 1959) and
their viability, winter desiccation (Tranquillini 1979),
carbon balance, loss of capacity to use assimilated
products (Körner 1998), xylem embolism (Feild &
Brodribb 2001).
Winter depression and spring recovering
Conifers are able to acquire deep frost hardiness
when exposed to short days and decreasing temperatures (see Levitt 1980 for review). This enables them
to survive extreme climatic conditions during winter,
although the metabolic activities may be strongly reduced (Havranek & Tranquillini 1995). As a result of
night frost, photosynthetic capacity gradually decreases during autumn (e.g., Troeng & Linder 1982; Strand
1995). In the boreal zone, photosynthesis is also curtailed during winter by low soil temperatures, and there
is no net carbon gain during periods when frozen soil
prevents water uptake (Troeng & Linder 1982).
This survey followed the ecophysiological approach used by Tranquillini (1957) nearly half a century ago in his memorable study on alpine plants. We
added the assessment of photochemical efficiency of
photosystem II (PSII) by the measurement of chlorophyll fluorescence, a tool widely used in the last 20
years to assess ecophysiological constraints on plant
growth (Öquist et al. 1987; Schreiber & Bilger 1987;
Greer et al. 1991; Ottander & Öquist 1991; Strand &
Lundmark 1995; Valentini et al. 1995; Koehn et al.
2003). We extended the period of study to two years,
including a winter without snow until February and
the warmest summer of the last century.
Modelling of spring photosynthetic recovery for
conifers has been investigated mainly for boreal conditions (Hänninen & Backman 1994; Hänninen 1996;
Linkosalo 2000; Hänninen & Hari 2002; Tanja et al.
2003). Indeed, the only common factor between climate at an elevation of 2000 m in the Alps and boreal
climate is low temperature. Radiative and temperature
range regimes are remarkably different: on boreal climate there is a large thermal amplitude and generally
lower radiation and precipitation. Models have to take
into consideration several aspects: dormancy break
mechanism; temperature effects on photosynthetic efficiency in general; efficiency recovery after low temperature episodes.
The study moved from the permanent site of Lavazè, where a meteorological and a monitoring station
exists since 1992, to the higher slopes of the mountain
where environmental conditions were harsher.
We studied the temperature and radiation effects
on photochemical efficiency of PSII for the coniferous species over two years, from February 2002 to
February 2004. Analyses of water content, chlorophyll, carotenoids and protein concentration in the dry
matter were performed on two of these species along
one year.
Effects of radiation on plant gas exchange potential were defined by studying the yearly amount of
available radiation on different positions within the
crowns chosen for the surveys.
Studi Trent. Sci. Nat., Acta Biol., 81 (2004), Suppl. 1: 227-244
In addition, the presence of different typologies
of damage to crowns was checked and recognised
during the investigation period, and environmental
conditions associated to such phenomena were defined.
The target of this work was to define limiting factors constraining growth and survival of five different conifers species at the treeline, in the Dolomitic­
2.1. Experimental site and plant materials
The study was carried out at Mt. Weisshorn / Corno Bianco, South Tyrol (46°21'N, 11°26'E), Italy. The
highest altitude range was considered, from 2000 m to
the top of the mountain, 2317 m a.s.l. At this elevation a mixed-conifer forest exists, growing on a thin
soil generated over a dolomite bedrock.
At lower elevations the forest, up to 15 m tall, is
composed of Cembran pine (Pinus cembra L.), Norway spruce (Picea abies (L.) Karsten) and Scots pine
(Pinus sylvestris L.) on the southern slopes. Some
larch (Larix decidua L.) and mountain pine (Pinus
mugo Turra) grow at the edge of the meadows.
At around 2100 m there is an abrupt change in the
vegetation height and species composition, that can
be assumed to be the treeline according to the indication of Körner (2003).
In the altitude range from 2100 m to 2300 m the
vegetation is dominated by the prostrate-ascending
mountain pine, with scattered emergent spruce and
larch, many of which bear a desiccated crown top.
The presence of stone pine is progressively lower
with height, however an abundant, dwarf population
is present near the top of the mountain (2317 m a.s.l.)
on the northern slope, where seeds are spread by a
community of ravens.
Two areas were selected for this study: the first
one was chosen on the western slope of the Mt. Weisshorn, around 2050 m a.s.l. Here five individuals for
each investigated species (Larix decidua, Pinus cembra, Picea abies, Pinus silvestris, Pinus mugo) were
selected, marked and geo-referred by a GPS system.
The selected plants grew isolated or in small groups
at the border of alpine meadows. The spruce sampling
individuals were collected along a gradient of forest
The second plot was placed on a Pinus cembra
population of saplings growing near the top of the
mountains, centred at 2300 m a.s.l., on north-facing
slope (Fig. 1).
2.2. Climate characterisation
Main meteorological features for the site were derived by the Lavazè Pass meteorological station located 3 km away, at 1780 m a.s.l. The station has been
operating since 1992.
The area of Lavazè Pass can be set in a climatic frame of the middle latitudes, but, because of its
elevated geographical location, climatic classifications usually adopted for cold climates better fit to its
features. According to Köppen (Hufty 1979) the area falls in a “Dfc” climatic zone, that is “Microthermal Climate”, which is humid all year round. The area displays some continentality features, particularly
if compared to most of territory in Trentino, which is
basically oceanic.
The experimental area represents well, from a thermal point of view, the typical climate of the mountain
belt at the elevation of the station itself; yearly average temperature is 3.9 °C.
The position of Lavazè Pass is favourably exposed to sun; in general, the horizon is open at the
pass, but the position, just at the bottom of mountain
peaks, makes the places prone to enhanced cloudiness, with respect to valley bottom locations, due
to a stronger convective activity, especially in summer months.
This feature is evident in the precipitation regime,
which is unimodal, displaying its maximum in July.
The area is not particularly rainy, considering the elevation: total average amount (period 1992-2003) is
946 mm. The relatively moderate rain height is, anyway, a general feature of the central-eastern alpine region, namely for E-W-oriented valleys. The area receives a reduced water contribution, both compared to
the pre-alpine area (south), and to the western Trentino valleys.
2.3. Microclimate characterisation
2.3.1.Temperature microclimate
Two air temperature profiles were set up in the selected plots at 2050 and 2300 m, with thin 0.08 mm
Copper-Constantane thermocouples placed at 6 levels (0.05 m, 0.15 m, 0.40 m, 1.09 m, 2.93 m, 8.07 m
above ground). Data were collected on a CR10 datalogger (Campbell Scientific, Lymington, UK). Longterm temperature measurements at the two selected
elevations and two different heights (0.1 m and 2.0
m above ground) were performed with four Tinytagultra data-logger, equipped with a shielded temperature probe.
Montagnani et al.
Winter depression and spring recovering
Fig. 1 - Aerial picture (ortophoto) of the investigated area: yellow stars represent positions of sampled trees, green lines
represent height level (Digital Orthophoto P.A.T. - S.I.A.T.).
Fig. 1 - Ortofoto dell’area oggetto di indagine: le stelle gialle rappre­sentano la posizione delle piante campionate, le linee
verdi le curve altimetriche (O.F.D. della P.A.T. - S.I.A.T.).
2.3.2.Sun light microclimate
The sun light microclimate above the sampled
shoots was computed taking hemispherical pictures
at the sample location to evaluate the shading effect
of the topography (slope, exposition) and of the canopy structure (north/south exposition, height of the
crown) on the light availability. Hemispherical pictures (lens: Fisheye Converter FC-E8 Nikon Corp.,
Tokyo, Japan; camera: Coolpix 995, Nikon Corp.,
Tokyo, Japan) were taken at the sampling sites where
shoots were periodically collected. Images were analysed with the software Gap Light Analyser version
2·0 (Frazer et al. 1999), in order to compute the canopy gap fraction at 10-degree zenith and azimuth reso-
lution and the monthly percentage of transmitted sun
Finally, monthly cumulated global radiation at
shoot level was estimated as the product of monthly percentage of transmitted light and corresponding
global radiation data obtained from the near Lavazè
Pass meteorological station (see also § 2.2. Climate
2.4. Collection of shoots and needles
In the first study area from February 2002 to
Februa­ry 2004, fully exposed, second-order shoots
from the lowest branches were collected early on the
morning once in three-four weeks. The samples were
Studi Trent. Sci. Nat., Acta Biol., 81 (2004), Suppl. 1: 227-244
collected from five individuals of each selected species: Larix decidua, Pinus cembra, Picea abies, Pinus silvestris, Pinus mugo. To study the influence of
light, exposed (south-facing) and moderately shaded
(north-facing) shoots from every different tree were
In the second plot, located in a Pinus cembra population growing at 2300 m a.s.l., from January 2003
to February 2004, needle samples were collected with
the same frequency from the basal and the top branches of these small, stunted plants (one meter high maximum).
After cutting, samples were immediately placed in
plastic vials and covered with aluminium foils. The
vials were kept in a cooling box during sampling and
then stored in a refrigerator at +4 °C. The shoots were
dark acclimated at 20 °C for at least 1 h before the fluorescence measurements.
2.5. Laboratory measurements and needles analysis
2.5.1.Chlorophyll fluorescence
Chlorophyll fluorescence was measured at room
temperature using a modulation fluorometer (PAM2000 Portable Chlorophyll Fluorometer Walz, Effeltrich, Germany). The shoots were fastened to a strip of
transparent tape and pressed against a bundle of ­optic
fibres; the angle and distance from the leaf surface to
the end of the optic fibre cable were kept constant during the experiments. Then the leaf sample was exposed
to a 0.1 s saturated flash of approximately ­6000 ­­μmol
-2 -1
m s to obtain the maximal fluorescence yield, Fm.
The ratio of variable to maximal fluorescence, Fv/Fm,
was calculated automatically according to measured
F0 and Fm. All measurements of F0 were performed
with the measuring beam set to a frequency of 600
Hz, whereas all measurements of Fm were performed
with saturating flash automatically switching to 20
kHz. The Fv/Fm ratio [Fv/Fm= (Fm - F0)/Fm] was used
as an index of maximum photochemical efficiency of
PS II function. Each chlorophyll fluorescence measu­
re was repeated three times on each sample.
2.5.2.Relative water content
Relative water content was determined with a double weighing. Fresh needles samples (1-2 g each)
were weighted on a analytical balance CP323S (Sartorius, Goettingen, Germany), with a resolution of 1
mg. Each sample was stored in an oven at 80 °C for
48 hours, in an aluminium foil. After the desiccation,
each sample was weighted again for the measure of
the dry weight.
2.5.3.Pigment determination
Photosynthetic pigments were determined in crude
acetone extracts. Needles were grinded to a fine powder in a mortar using liquid nitrogen and extracted
with 80% (v/v) acetone. Chlorophylls and carotenoids
were measured spectrophotometrically and their concentrations calculated on the basis of extinction coefficients given by Lichtenthaler & Buschmann (2001a,
2.6. Modelling approach to spring photosynthesis
We used the data concerning the Norway spruce
trees growing at 2000 m in order to set up a general photosynthesis recovery model following different
approaches: thermal sum (Bergh et al. 1998); “feedback” model (Pelkonen & Hari 1980); running mean.
In this analysis the mean of the two measurements
for every sample (north and south side) has been used,
better representing an average condition. The rough
ratio has been normalized aiming at a sounder defi­
nition of the value of full activity; the relative value of the ratio (Fv/Fm) has been obtained by dividing
any value by the maximum value measured in the two
years of survey:
(Fv/Fm)rel. = (Fv/Fm) / (Fv/Fm)max
All models have been calibrated using parameters
of photosynthetic efficiency measured on the field.
Most of the model parameters have been optimised by
a Generalized Reduced Gradient method (GRG2), letting them vary within a likely range and having as a target the minimum possible value for Root Mean Square
Error (RMSE), evaluated by differences between measured and modelled values. Such processing allowed to
improve model scores, getting better results than those
obtainable with a direct application of original formulations. Variable parameters include temperature damage thresholds, final thermal sum values, coefficients in
general, and, for the running mean model, the length of
the averaging period. Before discussing results, a short
overview is given on the implemented models; details
can be found in the originals.
Bergh et al. (1998)
developed a daily thermal sum
model, with no “base” temperature value for addends;
moderately low temperatures slow down the accumulation process, while severe frosts lower the thermal
sum attained until that moment; soil frost conditions
are explicitly taken into consideration.
Pelkonen & Hari (1980) worked on an hourly basis; the rate of development is a function of tempera-
Montagnani et al.
ture and of a critical value, corresponding to the fulfilment of the thermal requirements for the attainment
of full photosynthetic capacity. For the sake of homogeneity, a winter value equal to the surveyed minimum for (Fv/Fm)rel (0.14) has been set also in this formulation. This model, compared to the one by Bergh
et al. (1998), displays a quicker reaction to temperature fall, since the rate of development is less strongly
dependent on the integral value attained. A comparison of these two models is given in Hänninen & Hari
Finally, simple running average models have been
traditionally applied for smoothing effects of abrupt
temperature change; such algorithms proved to yield
results comparable to more sophisticated models
(Tanja et al. 2003); moreover, they have the advantage of avoiding any introduction of functional relationships whose functioning could be not fully explicable.
3.1. Temperature
In general, on the mountains larger temperature
variations are experienced by human beings than in
Winter depression and spring recovering
plain environments. However, if we perform air temperature measurements, we often find, on the contrary, a much more narrow fluctuation of daily temperature around the mean than we would perhaps expect
(Fig. 2).
In mountains climates, solar radiation is usually
able to induce a strong thermal gradient in a shallow
air layer. Its height and the extent of the temperature
gradient itself (usually negative during the day, positive during calm nights) is influenced by wind speed.
The effects of roughness of ground surface on wind
speed are generally expressed by a logarithmic equation (1), that becomes nearly linear within a forest
uh = (u*/k)ln((h-d)/h0)
where uh is the wind velocity at the height h above
ground, u* is the friction velocity, k is Von Karman
constant, d is the zero plane displacement, whose value is
generally around 2/3 of canopy height; h0 is the height
at which the wind speed would reach zero if it followed a logarithmic decrease near the ground, and not
a linear decrease, as in the case of vegetated surface
(Kaimal & Finnigan 1994).
Higher roughness is given by buildings, rocks
and, with particular effectiveness, by vegetation.
Fig. 2 - Temperature profiles measure during August, 2002, at the two plots (2050 and 2300 m a.s.l.) with thin (0.08 mm)
copper-constantane thermocouples, at six different heights (0.05 m, 0.10 m, 0.40 m, 1.09 m, 2.93 m, 8.07 m) above ground.
Continuous lines, circles: measures performed at 2050 m; dashed lines, squares: measures performed at 2300; black symbols:
night values (h 5:00 a.m.); open symbols: day values (h 3:00 p.m.).
Fig. 2 - Profili di temperatura misurati durante l’agosto 2002 nei due siti (2050 e 2300 m s.l.m.) con termocoppie fini di rame
costantana (0,08 mm) a sei differenti altezze (0,05 m, 0,10 m, 0,40 m, 1,09 m, 2,93 m, 8,07 m) sul livello del suolo. Linea
continua e circoli: misure raccolte a 2050 m; linee tratteggiata e quadrati: misure raccolte a 2300 m; simboli neri: valori
notturni (h 5:00); simboli aperti : valori diurni (h 15:00).
Studi Trent. Sci. Nat., Acta Biol., 81 (2004), Suppl. 1: 227-244
The profile of potential temperature follows closely that of wind speed (Sozzi et al. 2002). When­ever
temperature is a limiting factor, due to seasonal
and/or climatic conditions, plants can often exploit
just the short occurrence of temperatures higher
than a physiological­ threshold for their functioning. At the tree limit,­ the presence of vegetation not
only redu­ces wind speed, so reducing mechanical
damages to the vege­tation and evaporative demand
– evapotranspiration in stunted conifers is anyway
of little relevance – but, limiting wind speed, it al-
so enhances the occurrence of daily­ thermal ranges­
larger than in the case of clear soil. Hence, the time
period when the plants and their photosynthesising
organs can reach useful temperature values is increased.
On the other hand, trees act as obstacles to the solar radiation in its way to the ground, so the soil is
often cooler when it is covered by a thick canopy,
the shading effect exceeding in general that of reduction of long wave radiation loss at night. Soil temperature can hamper forest growth, particularly in
Fig. 3 - Hemispherical pictures, taken skyward at the shoots sampling sites, used to estimate the monthly cumulated global
radiation available at the shoot level, based on the incoming global radiation, measured at the Lavazé meteorological station,
and gap fraction distribution. A, B, C Pinus cembra located at 2300 m a.s.l.; D, E, F Pinus cembra at 2050 m; G, H, I Picea
abies at 2050 m.
Fig. 3 - Immagini emisferiche, ottenute mediante riprese verso il cielo al di sopra dei punti di raccolta dei getti, utilizzate
per stimare la radiazione globale cumulata mensilmente a livello dei getti campionati, basata sui dati della stazione
meteorologica di Lavazé e sulla distribuzione della gap fraction. A, B, C Pinus cembra posto a 2300 m s.l.m.; D, E, F Pinus
cembra posto a 2050 m, G, H, I Picea abies posto a 2050 m.
Montagnani et al.
circumpolar regions, where vegetation grows over a
permafrost layer. But, if soil temperature is not limi­
ting, the pre­sence of close woods is favourable for
tree growth.
3.2. Sun light microclimate
Hemispherical canopy photography is an indirect
optical technique that has been widely used in studies
of canopy structure and forest light transmission (Anderson 1964; Kull & Niinemetz 1998). Photographs
taken skyward with a 180° hemispherical (fisheye)
lens produce circular images that record size, shape,
and location of gaps in the forest overstory. These data can be subsequently combined to produce estimates
of growing-season light transmission, as well as ­other
measures more directly related to canopy structure,
such as openness, leaf area and sunflecks proportion
of incoming radiation.
The light regime experienced by shoots is influenced both by exposition and location in the crown.
The global radiation availability for the shoots collected in the upper part of the crown of small Pinus
cembra trees at 2300 meters, on a north-facing slope,
varied between 70 MJ m-2 (December 2003) and 620
MJ m-2 (July 2003) with a mean monthly value of 304
MJ m-2, about 72% of total available global radiation.
Lower shoots, in reason of orientation and reduced
habitus of the trees, showed a mean global radiation
availability of 200 MJ m-2, about 47% of the inco­ming
radiation and a range between 30 to 400 m-2 (Figs 3A,
3B, 3C).
At a lower elevation, 2050 m, west-facing slope,
the habitus of most of the trees is regular and the
crown reaches 3 m height. The crown shading effect
was in this case larger and the transmittance values at
the north and south face of the borderline trees were
different. The south facing shoots were exposed to
high values of global radiation (range of 80-480 MJ
m-2; mean value of 260 MJ m-2), 68% of the incoming
radiation (Figs 3D, 3E, 3F).
Over the north-face shoots, the canopy shading
was very effective and the global radiation showed
the lowest values during the year (24-180 MJ m-2).
Sampled spruces experienced different light regimes, according to position of the individual with
respect to other trees. Shoots were shaded by their
own crowns only or by the adjacent trees too. Mean
global radiation varied between 140 and 280 MJ m-2, respectively for north and south exposed shoots (Figs
3G, 3H, 3I). Isolated trees, that received the highest amount of global radiation, showed delayed recovery of greenness and severe damages during late
Winter depression and spring recovering
3.3. Needles water content
Needles water content in Cembran pine and spruce
was determined for the period January 2003 - Fe­bruary
2004. The summer of 2003 was extremely dry and
warm, so it could be suggested that even trees growing
near the timberline were subject to summer drought.
Water content, measured by a double weighing of
fresh and dry matter, showed conversely two main
peaks in winter 2003 and winter 2004, while the increase of dry matter percentage (and decrease of water
content) was little during the “heat wave” of 2003.
The more dehydration prone species was the spruce,
while the Cembran pine showed more drought-tolerant
Needles of spruce, and particularly sun-exposed
and wind exposed ones, had severe dehydration that,
in some case, led to needle death. The most acute and
easily recognisable effects of dehydration took place
in late winter 2003 (February, March) poor in snow,
while less effects had the previous winter without
snow until February.
Lethal levels of dehydration were reached in late
winter 2003, when water content in spruce leaves was
as low as 35% (Fig. 4).
During winter-drought period, sun-exposed needles had a severe photobleaching, indicating a synergy between action of drought and high light effects. Recovery from photochemical inhibition, after
restoration of favourable water relation, is very slow
(Bjorkman & Powles 1984).
3.4. Chlorophyll fluorescence
Plants have different ways to prevent photo­da­
mages. The easier is to shed the leaves, as lar­ches do;
a second way is to lose pigments, like Chlorophylls
and carotenoids, or to change the way of chloroplasts
stacking. Physiological adjustments involves xantho­
phyll cycle, with de-epoxidation of Violaxanthin in
Zeaxanthin and Antheraxanthin (Demmig-Adams &
Adams 1996), the fluorescence and the dissipation
of incoming short wave radiation as long wave, thermal radiation. Photoinhibition of photosystem II occurs when photosynthesis and protein turnover become inhibited by low temperatures and when nonphotochemical, heat dissipation mechanism are insufficient to deal with excess excitation (Anderson
& Osmond 1987; Öquist & Huner 2003).
The five studied coniferous species displayed similar trends in photochemical efficiency during the two
years of study.
The four evergreen species (spruce, Cembran pine,
Scots pine, mountain dwarf pine) had a minimum in
Studi Trent. Sci. Nat., Acta Biol., 81 (2004), Suppl. 1: 227-244
Da t e
C 80
Cembran pine needle dry matter (%)
Cembran pine needle dry matter (%)
20-07-2003 4528-10-2003
C 80
B 80
Higher crown
Lower crown
Da t e
Nort h
Sout h
Nort h
Sout h
B 80
Cembran pine needle dry matter (%)
A 80
Nort h
Sout h
Cembran pine needle dry matter (%)
Spruce needle dry matter (%)
Spruce needle dry matter (%)
A 80
20-07-2003 4528-10-2003 5-02-2004
Dat e
1-01-2003 11-04-2003 20-07-2003
Dat e
Higher crown
Lower crown
20-07-2003 4528-10-2003
Dat e
11-04-2003 20-07-2003 28-10-2003
Dat e
Fig. 4 - Trends of dry weight content percentage [(dry weight/fresh weight)*100] in spruce needles and in needles of
Cembran pines growing at different altitudes. Thick line: north facing or lower crown (2300 m plot) needles. Thin line: south
facing or higher crown needles. A: Spruce, growing at 2050 m a.s.l.; B: Cembran pine, growing at 2050 m a.s.l.; C: Cembran
pine growing at 2300 m a.s.l.
Fig. 4 - Andamento del peso secco percentuale [(peso secco/peso fresco)*100] negli aghi di abete rosso e pino cembro
vegetanti a diverse altitudini. Linea spessa: aghi appartenenti alla parte della chioma esposta a nord oppure alla parte
inferiore (sito a 2300 m). Linea fine: chioma a sud o parte superiore della chioma. A: abete rosso, vegetante a 2050 m s.l.m.;
B: pino cembro, vegetante a 2050 m s.l.m.; C: pino cembro, vegetante a 2300 m s.l.m.
winter, when the Fv/�
Fmvalue dropped to a very low value. It is known that under natural conditions, recovery is
slow and it may take several months before full photosynthetic capacity is achieved (Linder & Troeng 1980;
Linder & Lohammar 1981; Lundmark et al. 1988).
The timing of recovery showed some differences
among species, with the spruce slightly faster.
During year 2002 the higher values of Fv/�
approached at the beginning of the summer, but were
not kept for long time.
During the hot summer of 2003 all the plants
showed higher values of photochemical efficiency at
the beginning of July and at the end of the August,
but showed a clear depression of PSII efficiency in
mid July.
During the year 2003 the photochemical efficiency was measured also on Cembran pines located near
the top of Mt. Weisshorn. They showed a slower recovery and an anticipated loss of photochemical efficiency (Fig. 5).
During the spring and the beginning of summer
2003 an evident positive relation was found between
photochemical efficiency and needle development
during the previous year (Fig. 6). While at the lower
elevation the length of needles in saplings is similar,
or slightly higher in the higher parts of the crown, in
the group of Cembran pines growing above the actual timberline needles are shorter in the higher part of
the crown (Fig 7). Needle length is regular only on the
shaded shoots growing near the ground.
Also water content in needles was lower in the higher parts of the crown, suggesting a possible interaction
between water content, photochemical efficiency and
growth (Neuner et al. 1999).
Montagnani et al.
Winter depression and spring recovering
Fig. 5 - Trend of averaged value of photochemical efficiency of photosystem II, given by the parameter of fluorescence Fv/Fm along
two years. Period: February 2002-February 2004. Dotted lines: Cembran pines 2050m a.s.l.; dotted line Cembran pines 2300m
a.s.l.; thick black line: Larch; medium black line: Mountain dwarf pine; thick grey line: Spruce; light black line: Scots pine.
Fig. 5 - Andamento del valore medio, nel corso di due anni, dell’efficienza fotochimica del fotosistema II, rappresentata dal
parametro di fluorescenza Fv/�
Fm. Periodo: febbraio 2002 - febbraio 2004. Linee tratteggiata grossa: pino cembro 2050 m
s.l.m.; linea punteggiata: pino cembro 2300 m s.l.m; linea nera continua spessa: larice; linea nera continua media: pino
mugo; linea grigia, spessa: abete rosso; linea nera continua e sottile: pino silvestre.
Fig. 6 - Relation between needle length and quantum use
efficiency values, given by Fv/Fm. Needles collected in spring
2003 at 2300 m a.s.l. at different heights in the crown.
Fig. 6 - Relazione tra lunghezza degli aghi e i valori del­l’ef­
ficienza quantica (Fv/Fm). Aghi raccolti nella pri­-mavera
2003 a 2300 m di altitudine e a differenti altezze nella
Fig. 7 - Bar graph of the of needle length of secondary
shoots as a function of relative height in the crown. Grey
bars: needles at 2300 m.; black bars: needles at 2050 m.
Fig. 7 - Diagramma a barre della lungh ezza degli aghi
di getti secondari in funzione dell’altezza relativa nella
chioma. Barre grigie: aghi raccolti a 2300 m.; barre nere:
aghi raccolti a 2050 m.
3.5. Chlorophyll and carotenoids
al forest, Bowen ratio (sensible heat loss/evaporative
heat loss) is very high.
During spring there is a period of greening that, in
continental climates (central and eastern Europe and
Siberia), lasts few weeks, followed by the maximal
rate of CO2 uptake in late June or July (Röser et al.
2002; Tanja et al. 2003).
On the Alps, where climate is less continental, the
During winter, boreal evergreen forests lose part
of their leaf chlorophyll content. Although solar radiation is low, plants need to find a way to dissipate energy: since being the intracellular water frozen, they
cannot use solar energy to transform carbon dioxide
into organic compounds. During winter, over bore-
Studi Trent. Sci. Nat., Acta Biol., 81 (2004), Suppl. 1: 227-244
Total chlorophylls, a+b (mg g -1)
A 5
3.6. Relation between temperature and photosystem
Actual photosynthesis depends on temperature.
There are different processes involved in the adju­
stment of photosynthetic apparatus. Winter inhibition
of photosynthesis is well established for Scots pine
Total chlorophylls, a+b (mg g-1)
timing of this recovery is much slower. Chlorophylls
showed a minimum in late spring, at the moment of
the emission of new shoots, and a complete recovery
only in late summer.
Chlorophyll and carotenoids concentrations were
higher in the more shaded leaves and were significantly
lower at the higher elevation in Cembran pine (Fig. 8).
20-7-03 28-10-03
Carotenoids (mg g -1)
D 5
Carotenoids (mg g -1)
C 5
20-7-03 28-10-03
Higher crown
Lower crown
20-7-03 28-10-03
Higher crown
Lower crown
20-7-03 28-10-03
Fig. 8 - Trends of total Chlorophylls (Chl. a + Chl. b) and total carotenoids content (mg g d. m.-1) on dry matter, during the
period January 2003 - February 2004 on Cembran pines growing at different elevations. Light black lines, open symbols: sun
exposed shoots, south facing or growing in the higher crown; black thick lines: shaded shoots, north facing or growing in the
lower part of the crown. A: Total Chlorophyll content in needles of pines growing at 2050 m; B: Total Chlorophyll content in
needles of pines growing at 2300 m; C: Carotenoids content in needles of pines growing at 2050 m; D: Carotenoids content
in needles of pines growing at 2300 m.
Fig. 8 - Andamento della clorofilla totale (clorofilla a + clorofilla b) dei carotenoidi totali (mg g s. s. -1) riferiti alla sostanza
secca, durante il periodo gennaio 2003 - febbraio 2004 nei pini cembri che vegetano a diverse altezze. Linee nere sottili,
simboli aperti: getti esposti al sole, a sud o nella parte superiore della chioma; linee nere spesse: getti ombreggiati, esposti
a nord o nella parte inferiore della chioma. A: contenuto totale di clorofilla in aghi di pino che crescono a 2050 m; B:
contenuto totale di clorofilla in aghi di pino che crescono a 2300 m; C: contenuto totale di carotenoidi in aghi di pino che
crescono a 2050 m; D: contenuto totale di carotenoidi in aghi di pino che crescono a 2300 m.
Montagnani et al.
and Norway spruce (Linder & Troeng 1980; Leverenz
& Öquist 1987; Lundmark et al. 1988; Ottander &
Öquist 1991; Kull & Koppel 1992; Strand & Lundmark 1995) and seems to include both temperature
stress per se and low-temperature enhanced photoinhibition. Acclimation on temperature needs different time according to the process involved. So, the O2
evolution following the Rubisco activation has a direct (seconds) response to the temperature variation,
while the efficiency of Photosystem II and the energy
trapping by Chlorophyll a and b and by carotenoids
needs a longer period of adjustment.
Content of proteins involved in this process of adjustment, like D1 protein and Psbs protein (Li et al.
2000) depends by protein activation and turnover,
both temperature-related processes. Net loss of the reaction centre D1 protein occurs when the rate of D1
protein synthesis is lower than the rate of photodamages (Öquist & Huner 2003).
Plant photosynthesis is therefore influenced not only by actual temperature, but also by the temperatures
experienced in a recent past, days in the case of fluo­
rescence, months in the case of Chlorophylls.
The relation between temperature and measured
fluorescence found a best fit when, at the place of the
temperature measured at the moment of the sampling,
a moving average was used. In this case, the best fit
between temperature and Fv/Fm was found with an average of eight days. An enhancement of the fitting was
obtained using a modified moving average equation,
previously used to determine time delay in instrument
outputs (Sozzi et al. 2002). The equation used was
where Tmod is the temperature modelled with a delay function, Tact is the actual temperature measured
at the moment of the sampling, the term ∆t/t is the
parameter influencing time delay. In this study was
assumed a value of 0.1 for this term. As an input,
were used temperature values measured at 2 m above
ground at the two plots sited at 2050 m and 2300 m.
Spruces reached a higher level of photoinhibition in winter, displaying large differences between
sun exposed and shaded parts of the crown. The clear
secondary minimum of photochemical efficiency displayed at 10 °C, in summer, confirms the sensitivity of this physiological traits to dehydration (Fig. 9a,
9b). Relation between temperature and photochemical efficiency showed a small hysteresis loop: at a given temperature Fv/Fm values were lower in spring than
in late summer, indicating the relative importance of
thermal sums in order to attain the efficiency of the
photosynthetic apparatus.
Winter depression and spring recovering
Fluorescence measured on Cembran pines growing at 2050 m showed a clear relation of saturation
with temperature. Photochemical efficiency of photo­
sy­stem II increased with the moving average of air
temperature, saturating at extremely low values, 5-6
°C above zero. It was evident the extreme adaptation
of this plant to alpine climate and low temperatures
(Figs 9c, 9d).
Cembran pines growing at 2300 m a.s.l. suffered,
in the higher part of the crown, for higher radiation
and low temperatures. In the higher part of the crown
maximal values of photochemical efficiency were never attained, suggesting a permanent degree of inactivation of some physiological process (Fig. 9e, 9f).
It is known that, under natural conditions, recovery
is slow, and it may take several months before photosynthetic capacity is restored (Linder & Troeng 1980;
Linder & Lohammar 1981; Lundmark et al. 1988).
3.7. Modelling approach to spring photosynthesis
After calibration of models according to the three
approaches, some useful results can be drawn. The parameter used to quantify spring photosynthetic recovery in spruce is Fv/Fm. From our analyses, a maximum
value of 0.79 has been estimated for (Fv/Fm)max and a
minimum of 0.14, very close to that used in Bergh
model (0.15). Referring to normalized ratios, full value (1.0) represents the typical summer situation.
The application of the optimisation algorithm
modified the original parameters of both models developed by Bergh et al. (1998) and by Pelkonen &
Hari (1980) (with some unavoidable arbitrariness,
due to the shortness of the available experimental set
– two years), yet improving their performances. In table 1 a comparison of the original values is given with
those obtained by calibration for our data set. Parameters not reported were not modified.
It can be seen that in the first model all temperature thresholds have been considerably lowered,
but no value for T3 lower than T2 was found. T2 is
the threshold value below which a decrease in the
state of development takes place, causing a reversal of the photosynthetic activity recovery; the latter can be reversed again with positive temperatures.
T3 is the threshold below which the damage due to
frost is maximum, affecting recovery permanently.
It must be inferred that either no major frost event
has occurred during the observation period, or that
a mechanism strongly limiting photosynthetic activity, to be ascribed to very low temperatures, would
not take place, at least in the terms under which the
model itself has been proposed. In the second model
Studi Trent. Sci. Nat., Acta Biol., 81 (2004), Suppl. 1: 227-244
Temperature (moving average) °C
01-2003 04-2003
Fv Fm-1
01-2003 04-2003
Temperature (moving average)°C
07-2003 10-2003
Temperature (moving average)°C
07-2003 10-2003
Fv Fm-1
Fv Fm-1
Fv Fm-1
Fv Fm-1
Fv Fm-1
07-2003 10-2003
Fig. 9 - Relation between a moving average (Eq. 2) of air temperature and photochemical efficiency of photosystem II given
by the chlorophyll fluorescence parameter Fv/Fm (A, C, E) and trends of the same parameter (B, D, F). Fv/Fm averaged values
of 5 samples from different trees. A, B: Spruce, growing at 2050 m a.s.l.; C, D: Cembran pine, growing at 2050 m a.s.l.; E,
F: Cembran pine, growing at 2300 m a.s.l. Thick line: north facing or lower crown (2300 m plot) needles; dotted line, open
symbols: south facing or higher crown (2300 m plot) needles; arrows show the direction of the hysteresis loop between
temperature and Fv/Fm during the year (January 2003 - February 2004).
Fig. 9 - Relazione tra una media mobile (Eq. 2) della temperatura dell’aria e l’efficienza fotochimica del fotosistema II dato dal
parametro Fv/Fm (A, C, E) e gli andamenti dello stesso parametro (figure B, D, F). Valori medi di Fv/Fm di cinque campioni da alberi
diversi. A, B: abete rosso, a 2050 m s.l.m.; C, D: pino cembro, a 2050 m s.l.m.; E, F: pino cembro, a 2300 m s.l.m.
Linea spessa: aghi della parte esposta a nord o della parte inferiore della chioma (sito a 2300 m s.l.m.). Linea sottile, simboli
aperti: aghi campionati sul lato esposto a sud oppure nella parte superiore della chioma (sito posto a 2300 m). Le frecce
mostrano la direzione del ciclo di isteresi tra la temperatura e Fv/Fm durante l’anno (gennaio 2003 - febbraio 2004).
Montagnani et al.
Winter depression and spring recovering
Tab. 1 - Results of models calibration.
Tab. 1 - Risultati della calibrazione dei modelli.
Physical meaning
Bergh et al. (1998)
T1 [°C]
T1’ [°C]
T2 [°C]
T2’ [°C]
T3 [°C]
Scrit [°C day]
Recovery slowing-down threshold – minimum daily temperature
Recovery slowing down threshold – mean daily temperature
Recovery reversal threshold – minimum daily temperature
Recovery reversal threshold – mean daily temperature
Temperature damage threshold
Value for attainment of critical state of development
Pelkonen & Hari (1980)
Curve shape parameter for development rate
Curve shape parameter for development rate
Value for attainment of critical state of development
Value after
(*) original formulation expressed on an hourly basis
(Pelkonen & Hari 1980), both c and Scrit have undergone to a heavy change with respect to the proposed
values, but that was largely expected, since original
formulation envisaged hourly values, while our application made use of daily data. c is a parameter of
the exponential term of the model, while Scrit is the
critical “state of development” (i. e. the integral over
time of the rate of development), when the maximum
photosynthetic capacity is attained. The application
of both models was not satisfactory to represent the
photochemical efficiency process for Norway spruce
at Mt. Weisshorn. Particularly, results are poor in reproducing spring recovery (more evidently in 2002
than in 2003), while they seem to better reproduce
the drop in photosynthetic efficiency in autumn. Only for summer 2003 models fit experimental va­lues.
This is the expected result of a calibration carried out
with only two years measures, with substantially different summer regimes: 2003 will be remembered as
an exceptionally warm season (Rebetez et al. 2004)
and temperature must have promoted photosynthetic
activity, allowing highest efficiency for a long period. On the contrary, summer 2002 was wet and cool,
with low solar radiation. Anyway, experimental data do not display a summer plateau of full photosynthetic efficiency like both models do. A similar conclusion was reached by Tanja et al. (2003): temperature sums do not allow to represent rapid temperature rise and fall and are affected by too long “memory”.
Better results can be attained by an application of
running mean models to mean daily temperature. Attempts have been done by varying the length of the
ave­raging period, from 2 to 25 days. Best outcomes
have been obtained with temperatures averaged over
a period spanning from 8 to 15 days, according to the
side of the tree – north or south – where samples were
taken. For a 8-days moving window, R2 = 0.76 (p<
0.001). Results from the three model approaches are
given in Fig. 10.
When estimating the carbon balance of cold-temperate and boreal forests, the seasonal variation in
photosynthetic capacity and performance must be
considered, to avoid overestimating annual carbon
assimilation (Linder & Lohammar 1981; McMurtrie
et al. 1994; Bergh et al. 1998a). Bergh
������ et al. (1998),
­using the process-based simulation model BIOMASS (McMurtrie et al. 1990), estimated that the
combined effect of autumn decline of photosynthetic capacity, winter-damaged photosynthetic apparatus and frozen soils may reduce annual gross primary production in a boreal Norway spruce stand by
3.8. Shoot and needles damages
During the year 2003 a regular presence of suf­
fering needles was observed on all the Cembran pines
in the plot at 2300 m a.s.l. The needles on the upper branches were discolouring during the winter season, yellowing in spring and, in some cases, turned to
brown in summer. This kind of damage was not observed on lower branches of the same trees: here the
needles appeared always green (Fig. 11). Most of the
affected needles seemed not able to recover during the
growing season, maintaining the yellow appearance,
while the new vegetation showed the same symptoms
after the following winter.
Studi Trent. Sci. Nat., Acta Biol., 81 (2004), Suppl. 1: 227-244
Fig. 10 - Models comparison. Solid grey: application of the Bergh et al. (1998) model; dashed grey: Pelkonen & Hari, 1980
model; solid black: 8 days running mean model; black dots: relative photosynthetic capacity from analyses of Fv/Fm.
Fig. 10 - Confronto tra modelli. Linea grigia continua: modello di Bergh et al. (1998); grigio tratteggiato; modello di
Pelkonen & Hari (1980); linea nera continua: modello a media mobile di 8 giorni; punti neri: andamento della capacità
fotosintetica normalizzata proveniente dai dati osservati di Fv/Fm.
Phacidium infestans P. Karsten was detected on
the lower branches of some Pinus cembra at 2300
a.s.l. This snow-related parasite caused discoloration
of needles that turned to pale grey in summer. The
presence of the fungus was confirmed by the appearance of apothecia during August 2003. Incidence of
this disease was irregular and located on some patches
of trees. During the surveys the fungus was observed
only on lower branches.
The combination of pathologies and suffering status brought to a wide loss of branches and death of
saplings (about 30%) during the year 2003. Similar
losses were not found at 2050 m a.s.l.
In March 2003, a sudden damage on needles
was observed on the sampled trees in the 2050 m
plot (Fig. 12). Needles of 2002 season growing on
exposed branches became partially or completely white, starting from the tip; then, in the following months, all turned reddish-brown and finally fell
­during summer. This kind of damage was observed
all around the edge of the forest between 1800 and
2100 m a.s.l. Only exposed trees were affected,
while no effects were observed on plants inside the
wood. The more severe damages were present on the
side exposed to wind. All evergreen species studied
showed the same symptoms, but the spruce had more
severe damages (Fig. 13). In some cases, exposed
branches and the top of the crown were desiccated.
In the following year, the new vegetation was not affected by the same attack.
Fig. 11 - Small Pinus cembra L. tree at 2300 m a.s.l. Can be
seen the apical shoot desiccated in a previous year and the
yellowing top crown. ��������������������������������
Photograph taken in spring 2004.
Fig. 11 - Piccolo albero di Pinus cembra L. a 2300 m di
quota. È possibile notare gli apici terminali disseccati negli
anni precedenti e l’ingiallimento della parte alta della
chioma. Foto primavera 2004.
Montagnani et al.
Winter depression and spring recovering
Fig. 12 - A branch of an isolated group of young spruces during subsequent winters (2003, 2004). During winter 2003 (A)
the tree had severe de-hydration and chlorophyll bleaching on sun exposed shoots. In the following year (B), needles of year
2002 were fell down, but the new shoot was in good conditions.
Fig. 12 - Un ramo di un gruppo isolato di giovani abeti rossi durante inverni successivi (2003, 2004). Durante l’inverno
2003 (A) l’albero ha avuto una pesante disidratazione e una degradazione della clorofilla sui rami esposti al sole. Nell’anno
seguente (B) gli aghi del 2002 erano ormai caduti, mentre il nuovo getto era in buone condizioni.
Fig. 13 - Winter desiccation on Spruce and mountain dwarf
pine observed in the plot in April 2003. It is to notice the
different level of damages in the two species.
Fig. 13 - Danni da disseccamento invernale su abete rosso
e pino mugo osservati nell’area nell’aprile 2003. Si osservi
la differente intensità di danneggiamento fra le due specie.
The physiological character distinguishing the
plants growing above the timberline is the incomplete
recovery of the efficiency of the photosynthetical machinery in the higher part of the crown. This feature
is determined by a lower chlorophyll content and a
lower efficiency of photosystem II, and is coupled
with an incomplete growth of foliage and branchlets. This low-temperature-induced photoinhibition
of ­evergreen plant during winter, is well indicated by
low Fv/Fm ratio.
Damages also occurred during winter in photo-
synthetic or meristematical tissues, both above and
under the treeline, at the more exposed parts of the
canopy. This damage occurs at a side in the photosynthetic electron transport chain that can readily be
repaired (Ottander & Öquist 1991). The recovering
process is strongly temperature and light dependent
(Greer et al. 1986). Since replacement of damaged
tissues needs a high level of assimilating capacities
(Waring 1991), we suggest that the long lasting effects of photoinhibition on the more exposed parts
of the crown have a key role in treeline occurrence
on the Alps.
All limiting factors, such as low temperature, high
radiation (Strasser et al. 1996) and water or nutrients shortage (Sakai & Larcher 1987), that can induce
photoinhibition and photochemical damages or withstand D1 protein synthesis, can be ascribed as drivers
for the treeline formation.
Since trees growing in dense canopies are less triggered by limiting factors than isolated trees, we confirm by a physiological point of view the importance
of the sylvicultural practice of keeping a forest defense close to tree limit on the mountains.
The assistance for field work of Alberto Conter
and the GIS data elaboration of Ruggero Valentinotti
is kindly acknowledged.
This work was supported by a grant from Provincia Autonoma of Trento: project “EFOMI: Ecological
Studi Trent. Sci. Nat., Acta Biol., 81 (2004), Suppl. 1: 227-244
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Work Package 6