In: Pine Forests: Types, Threats and Management
Editor: Chris Thomas Frisiras
ISBN: 978-1-61324-493-7
©2011 Nova Science Publishers, Inc.
Chapter 11
PINUS NIGRA SUBSP. SALZMANNII FORESTS FROM
SOUTHEAST SPAIN: USING STRUCTURE AND
PROCESS INFORMATION TO GUIDE MANAGEMENT
Pedro Antonio Tiscar*1 and Juan Carlos Linares2
1
Centro de Capacitación y Experimentación Forestal, Cazorla, Spain
2Departamento de Sistemas Físicos, Químicos y Naturales,
Universidad Pablo de Olavide, Sevilla, Spain
SUMMARY
Forests of Pinus nigra subsp. salzmannii (Pinus nigra hereafter) cover about half a
million hectares of pure stands in Eastern Spain and Southern France. They have been felled
for timber during centuries, for example their stems were used in naval construction. Yet,
these forests are part of the European Union endangered habitats listing of natural habitats
requiring specific conservation measures, due to their biological values. As a consequence,
Pinus nigra forests represent a suitable area where implementing sustainable forestry.
How to manage forests in a sustainable way is a current topic in forestry research. In this
respect, most published papers deal with the link between ecosystem structure and function,
and management.
Mediterranean ecosystems have experienced major changes in ecological structure and
process because of long term human activities. Therefore, a clear reconstruction of their
evolutionary environment and reference conditions, as done for some North-American pine
forests (Pinus ponderosa for example), is not possible. Nevertheless, our aim in this study
was to define a preliminary reference conditions for Pinus nigra forests from Southeast Spain.
To do this, we used data from an old-growth stand and historical records to describe the
natural structure of the mentioned forests.
Results proved that Pinus nigra natural stand structure is more complex that the structure
found in current stands exploited for timber. Stands with a natural structure would be all-sized
*
Corresponding author:E-mail: [email protected]
2
Pedro Antonio Tiscar and Juan Carlos Linares
or uneven-aged and multistrata, including very large and old individual trees. They would
also include a better representation of Quercus species (Quercus ilex and Q. faginea), along
with other broadleaf species such as Sorbus aria and Acer opalus subsp. granatensis.
Nevertheless, Pinus nigra would be clearly the dominant species with over a 90% of the
overall standing biomass.
Since structure is the consequence of a demographic process, we confirmed the
consistency of the above results inferring the disturbances natural regimen from both
dendroecological records and information about the species natural history. Additionally, we
considered the recruitment dynamic of the species in the study area. Disturbances and
regeneration are two key processes of forest dynamic.
Fire is a principal disturbance in Mediterranean forests at present, because most of them
are human ignited. Present experience has proved that forests of Pinus nigra hardly
regenerates after wild fires, as also shown by palinological studies. It has been shown that
Pinus nigra and P. Sylvester’s populations sharply declined 6000 years ago as a consequence
of the extensive use of fire by humans. Compared to other Mediterranean-pine species more
exposed to fire-proned environments, such as Pinus halepensis and P. pinaster, P. nigra
presents poorer adaptations to survive crown fires and seems unlike that fire has been an
important condition in the evolutionary environment of this species. On the other hand, fire
turnover has been established in 229 years in the study area, so that more frequent and less
intensive disturbances than fire: heavy rain, snowfalls, insect outbreaks would be more
determinant in modeling the natural structure of Pinus nigra forests.
The life cycle of Pinus nigra was studied as a conjunction of consecutive stages (predispersed seed, dispersed seed, seedling and sapling) connected by processes with specific
transition probabilities. Thus, we could explore Pinus nigra recruitment dynamic analyzing
the relative contribution of the different potential limiting factors. The effects of masting,
ageing of mother plants, post-dispersal seed predation, litter, drought and light availability
were also explored. Results showed that the recruitment of new Pinus nigra individuals is
mainly limited by summer drought. This situation, along with the long species longevity and
irregular production of pine seeds, give rise to a slow rate of colonisation that generates
uneven-aged and multistrata stands.
1. INTRODUCTION
The science of forestry has long considered forests to be systems at equilibrium,
characterized by relative constancy in structural and compositional features and by a
predictable successional trend towards a climax state. Under this paradigm, forests could
easily be organized following the normal forest model, i.e. an idealized forest composed of
fully stocked stands with a balanced age-class distribution and preferably even-aged. This
point of view has changed over the last decades, after the realization that disturbances are an
inherent component of ecosystem development rather than events hindering it (Kuuluvainen,
2002). As a consequence, forests are now interpreted as complex ecosystems that show
multiscale heterogeneity and non-equilibrium dynamics, and traditional forestry as a practice
that reduces the structural and compositional diversity of natural forests or, in other words, a
practice that reduces forest biodiversity (Hunter, 1999).
Pinus Nigra Subsp. Salzmannii Forests from Southeast Spain: …
3
Biodiversity is one of the main topics in the new management strategies proposed under
the paradigm of sustainable forestry that arose following the 1992 Earth Summit held in Río
de Janeiro (Tíscar, 2006). Thus, foresters are currently challenged to produce wood and other
resources whilst maintaining forest biodiversity. This is a premise easy to endorse, but how
can foresters achieve this goal? The concepts of evolutionary environment and reference
conditions might provide the necessary background to do so.
Forest-dwelling species have evolved life-history strategies which make use of the
spatiotemporal distribution of habitats available in natural forests. This availability is
dependent on the characteristics of natural disturbances, so that the concept of evolutionary
environment assumes that forest-dwelling organisms will be better able to cope with logging
disturbances if they are designed to imitate natural disturbances (Seymour and Hunter, 1999).
The concept of reference conditions is closely related to the evolutionary environment
concept, and refers to the variability of composition, structure and function found in natural
forests (Moore et al., 1999; Kuuluvainen, 2002). We suggest that reference conditions might
be used as an alternative to the normal forest model and be used as a point of reference to
design sustainable forestry.
In this article, we review relevant literature and show new results about the structure and
process of Pinus nigra forests from southeast Spain in order to propose a set a preliminary
Reference Conditions for the area. We also address what could constitute the natural state and
process for this ecosystem (the evolutionary environment concept).
2. STUDY SPECIES AND SITE
European black pine (Pinus nigra Arnold) is a circum-Mediterranean pine species. Its
natural range extends from Spain and north Morocco to Austria, Turkey and Cyprus. Most
forests occur in mountainous areas between 1000 and 1500 m a.s.l. As a result, its populations
are fragmented and exhibit high morphological, physiological and ecological variability.
Numerous subspecies, varieties, and forms have been named following that diversity; five
subspecies are currently recognized: nigra, salzmannii, dalmatica, pallasiana and laricio
(Alejano and Martínez-Montes, 1996).
Pinus nigra subsp. salzmannii Dunal (Franco) (Pinus nigra or Black pine hereafter) is
native to the calcareous mountains of southeast France, eastern Spain and northern Morocco.
French and Moroccan populations cover no more than 4000 ha, but Pinus nigra is the
dominant tree species in 544.286 ha of Spanish forests (Alejano and Martínez-Montes, 1996;
Figure 1). Different historical documents prove that Black pine timber was already used for
building construction in Spain 1100 years ago. During the eighteenth century, the Spanish
Navy used the species for ship building, although trees had to be harvested hundreds of miles
away from the coast. Later on, these pineforests suffered pressure from railway companies
that used black pine timber to make sleepers. Nowadays, timber is still a valuable resource,
and trees are felled despite economic or environmental constraints. In this respect, it is worth
remembering that the price of Spanish timber has collapsed during the last two decades and
that 21% of the forests occupied by black pine are currently within nature reserves (100% in
southeast Spain). In fact, these pinewoods have been recognized as a priority habitat under the
European Union Habitats Directive, due to their biological values.
4
Pedro Antonio Tiscar and Juan Carlos Linares
Figure 1. (left) Geographical distribution of Pinus nigra subsp. salzmannii in Spain (dark areas).
Cazorla-Segura mountain range is located within the rectangle in the south east of the country. (right)
Detail of the distribution of Pinus nigra subsp. salzmannii in the area of Cazorla-Segura mountain
range. The area where most of the studies reported here were carried out appears within a rectangle.
In southeast Spain (our study area), Pinus nigra is found in ten separate mountain ranges
(Cazorla-Segura-Castril, Mágina, Sagra, Huétor, Baza, Nevada, Almijara, María, Lúcar and
Filabres) all of which are part of the Béticas Mountain Range (Figure 1). The ecology and
management of Pinus nigra forests from the Cazorla-Segura area (ca. 60.000 ha) have been
extensively studied during the last decade; all the studies and results we report here were
carried out in this mountain range, unless otherwise stated.
Cazorla-Segura mountain range has a Mediterranean type climate. Snowfalls and frost are
common during the winter, but summers are dry and hot. At the core of Cazorla-Segura
forests, the average rainfall is 1075 mm, of which 55 mm occur during the summer, and mean
monthly temperatures range from 5.1ºC in February to 22.3ºC in August.
Pinus pinaster, P. halepensis, Juniperus oxycedrus, Quercus ilex and Q. faginea are
possible companions of Black pine in those localities where it mixes with other tree species,
but Pinus nigra stands are mostly monospecific in the study area. Shrub species such as
Juniperus communis, Crataegus monogyna, Rosa sp., Amelanchier ovalis, Berberis hispanica
and Satureja montana are frequent across the natural distribution area of Pinus nigra in the
Béticas Mountain Range.
Most forests from Cazorla-Segura have been harvested following management plans
since the late 19th Century. At that time, Pinus nigra forests were put under the shelterwood
method, with a shelter-phase of 20 years and a rotation period of 120 years. This silvicultural
method changed to an uneven-aged system some decades later, due to the difficulties in
achieving successful natural regeneration. An ideal reverse-J diameter distribution was then
defined as the management target. The cutting cycle was established as 15 years and the
maximum residual diameter at breast height (DBH) as 50 cm. The ratio between the number
of trees in one diameter class to the number of trees in the next larger class (q) was set at 1.7
for 10 cm width diameter classes.
Pinus Nigra Subsp. Salzmannii Forests from Southeast Spain: …
5
Since 1986, Cazorla-Segura mountain range forms part of a Natural Park, well known for
its biological richness which includes an important number of endemic species.
3. EVOLUTIONARY ENVIRONMENT FOR SPANISH BLACK PINE
The term evolutionary environment refers to the environment in which a species evolved
(Moore et al., 1999). Although we are basically interested in the evolutionary environment of
the species Pinus nigra, it is important to realize that trees are main structural elements of
forest ecosystems and that they directly or indirectly modify, maintain and create habitats for
other organisms (Jones et al., 1994). Therefore, forests of Pinus nigra themselves constitute
an essential part of the evolutionary environment of the species dwelling in them. The loss of
natural habitats has been quoted as one of the greatest threats to biological diversity (Primack
and Ros, 2002). For these reasons, it seems essential to have some information about the
evolutionary environment of Pinus nigra to design silvicultural methods able to maintain the
biodiversity of these forests whilst producing resources that society needs and consumes.
Pinus nigra is one of the six pine species native to the Iberian peninsula. Native Spanish
pines exhibit different life-histories which may represent adaptations to fire types and
frequencies. Thus, Pinus nigra, Pinus sylvestris and Pinus uncinata thrive in mountainous
areas and they all share some evolutionary traits, such as late flowering and absence of
serotinous cones, which indicate that their natural forests did not evolve under an
environment of frequent crown fires (Tapias et al., 2004). Pinus nigra also shows other
evolutionary traits: height at maturity (up to 50 m), longevity (> 600 years), dispersal season
(late winter) and bark thickness (relatively thick), all of which can be interpreted as
adaptations to low-intensity surface fires.
Similarly, the populations of Maritime pine (Pinus pinaster) located close to Pinus nigra
forests within Cazorla-Segura mountain range are thought to have evolved under a lowintensity fire regime, because individuals are thick-barked with a low degree of serotiny
compared to other populations of this species (Tapias et al., 2004). Further evidence of the
absence or low frequency of stand replacement fires in the study area is the existence of an
old-growth patch with an abundance of trees over 600 years old (see section 4.1). Indeed, the
site has been extensively sampled to carry out different studies on dendroclimatology and no
fire scars have been identified in the cores extracted from the pinetrees (E. Gutiérrez,
personal communication). However, naturally ignited fires do occur in the area with an
estimated recurrence of 229 years (López-Soria and Castell, 1992). This frequency is low
enough to make minor disturbances (individual or small groups of black pines may be
uprooted by wind or heavy snowfalls, or killed by pathogens) prevail over major or standreplacing ones (Oliver and Larson, 1996). It is also known that post-fire regeneration of Pinus
nigra forests is almost nil after wildfires (Espelta et al., 2003; Rodrigo et al., 2004).
The continuous presence of Pinus nigra as the main tree species in the study area has
been confirmed by paleoecological indicators. Thus, Pinus nigra-type pollen predominates in
a stratigraphy elaborated from sediment cores that goes down to year 11500 BP.
Microcharcoal particles are also visible along the whole stratigraphy, indicating the
occurrence of fires over the mentioned period of time. The presence of microcharcoal
particles is more persistent during the last 5000 years, as climatic conditions have become
6
Pedro Antonio Tiscar and Juan Carlos Linares
drier and human activities have increased in the area. Nevertheless, there is no evidence
concerning intensification of agriculture and grazing before Roman times, 2000 years ago
(Carrión, 2002).
Forests from Iberian mountains tend to be dominated by one single species due to
ecological and paleobiogeographical reasons (Blanco et al., 1998), although other tree species
are present. For example, Pinus pinaster, Taxus bacata, Acer opalus and Sorbus aria in Pinus
nigra-dominated forests from the study area. Deciduous (Quercus faginea) and evergreen
oaks (Q. ilex) are also present in today’s forests, but, in this case, pallinological studies
confirm their presence and relative abundance for the last 7200 years (Carrión, 2002).
4. STRUCTURE OF PINUS NIGRA FORESTS
Rather than describe the current structure of Pinus nigra forests, we will focus on two
structural topics which are important for the establishment of Reference Conditions. Firstly,
we will describe the structure of a forest site relatively undisturbed by human activities.
Forests undisturbed by human activities provide an opportunity to obtain information about
their natural composition, structure and process, i.e. the three attributes that determine the
biodiversity of an area (Noss, 1993). This information can be used as a baseline to design
sustainable silvicultural systems.
Secondly, we will analyze the changes caused by selviculture in the structural diversity of
managed forests. Forest management normally implies the felling of trees in order to control
the establishment, growth and structure of forest stands. By cutting trees down, foresters
influence some ecosystem processes at various spatio-temporal scales (e.g. mortality rates of
tree species or the frequency of disturbances in given sites) and modify the structure of forest
stands (e.g. grouping harvesting operations in some stands). So, the monitoring of temporal
changes occurring in the structure of exploited forests seems a proper method for analyzing
the long-term influence of forestry practices on forest biodiversity.
4.1. Structure of an Old-Growth Pinus Nigra Forest
Old-growth forests can be used as templates to delineate nature-based forest management
with the aim of producing timber whilst maintaining forest biodiversity. Much of the existing
information about the composition, structure and processes of old-growth forests come from
boreal and wet-temperate regions, where relatively large old-growth forests still persist
(Foster et al., 1996). Studies from the circum-Mediterranean Regions are comparatively
scarce and normally refer to small patches located within larger human-disturbed forest areas
(Piovesan, 2005; Peterken, 1996). Obviously, this situation reflects the historical use of fire,
grazing and other forms of anthropogenic disturbances that have transformed Mediterranean
forests over several millennia of civilization, so that forests free of human activity are
virtually unknown in the region. Nevertheless, a forest does not need to be virgin in order to
be classified as old-growth (Peterken, 1996).
Definitions for old-growth forest include criteria relating to the degree of human
disturbance and to the age, size and successional status of the overstorey trees (Foster et al.,
Pinus Nigra Subsp. Salzmannii Forests from Southeast Spain: …
7
1996). In this article, we will consider as old-growth a patch of forest located in a remote site
from Cazorla-Segura mountain range. As said earlier, various pollen stratigraphys indicate
that the area has been continuously wooded by Pinus nigra forests since the beginning of the
Holocene. Two thousand years ago, under climatic conditions similar to present and
immediately before people became a significant ecological factor, Pinus nigra was the main
tree species in areas above 1200 m a.s.l. (Carrión, 2002). Accordingly, forests of Pinus nigra
are seen as the endpoint in the vegetation successional development of the oromediterranean
belt (Valle et al., 1989).
The study patch (ca. 60-ha) is located at 1800 m a.s.l. in a site that remained quite
inaccessible until 1955. This circumstance prevented the felling of trees until the early
1970’s. Then, one harvesting operation decreased the patch naturalness, although the previous
forest structure could be reconstructed, because the harvest was quantified and the data
recorded in management files, and many stumps are still visible in the area. No other trees
have been logged afterwards. Grazing by domestic livestock has not been allowed since 1893,
although wild ungulates are present. Among this guild of animals, there are two exotic species
introduced in the 1950’s: wild sheep (Ovis musimon) and fallow deer (Dama dama), that
exert a small amount of pressure on Pinus nigra saplings (Cuartas and García-González,
1992). The patch was discovered whilst carrying out a study on dedroclimatology, which led
to the identification of an unusually high number of very old trees and large snags (Creus,
1998).
In summary, the forest patch we describe here is composed of native species that
represent the late successional condition in the area. Trees regenerate naturally, all age-classes
are represented and many trees are very old and large. The site exhibits a small degree of
human disturbance and it is located within an area that has been continually wooded since
immemorial time. Despite obvious limitations, these characteristics make the population a
good template for the purpose of defining a set of Reference Conditions for Pinus nigra
forests in southeast Spain.
The current tree structure of the old-growth patch shows a mean density of 115.88 ind·ha1
for stems with DBH ≥ 10 cm, and a mean density of 324.65 ind·ha-1 with DBH < 10 cm.
Mean basal area is 25 m2·ha-1 and mean volume 176.44 m3·ha-1 (Table 1). These mean values
were calculated from data collected in nine circular plots placed at random in the site, each of
20 m radius. The two most widely separated plots were 800 m apart, and the two closest ones
50 m apart. Stumps from the harvest operation carried out in the early 1970’s were not found
within the plots.
The observed among-plots variability (expressed by the coefficient of variation, CV)
indicates that the site structure is highly heterogeneous, varying at relatively short distances.
Similarly, the range of diameters at breast height and the presence of regenerates in all the
plots would indicate an elevated degree of vertical complexity, since DBH and height were
positively correlated (RPEARSON= 0.82, n = 133, p-valor< 0.01; Table 1).
Pedro Antonio Tiscar and Juan Carlos Linares
8
Table 1. Structural variables of the nine plots sampled.
Ind·ha-1
(dbh<10cm)
1
191.08
2
79.62
3
31.85
4
71.66
5
1584.34
6
318.47
7
63.69
8
222.90
9
358.28
Mean 324.65
s.d.
162.19
C.V. 149.88%
Plot
Ind·ha-1
(dbh≥10cm)
79.62
302.50
79.62
47.77
71.62
167.19
167.19
71.65
55.73
115.88
27.61
71.49%
m2·ha-1
m3·ha-1
28.42
21.61
22.36
14.42
11.09
26.63
21.88
32.29
46.33
25.00
3.45
41.36%
206.30
112.43
139.08
99.47
71.29
161.45
141.75
265.39
390.80
176.44
33.05
56.20%
Range of
dbh≥10cm
46-109.5
10-99
24-91.5
10-10
12.5-58.5
15-82
10-89
30-125
11-190
160
140
120
Old-growth patch
Compartment A
Compartment B
ind.ha-1
100
80
60
40
20
0
0
50
100
150
200
Diameter class (cm)
Figure 2. Diameter distribution by DBH classes in an old-growth patch and in two comparments from
forests regularly harvested.
Diameter distribution in 10-cm DBH classes suggested a reverse J-shape distribution
typical of uneven-aged stands. This structure is frequent throughout the study area, because
Pinus nigra exhibits some degree of shade tolerance and regenerates in small gaps. However,
the slope of the reverse J-shape distribution from the old-growth patch is rather small
compared to that normally found in pinewoods that are regularly harvested. This means that
the q factor, i.e. the ratio of trees in a diameter size class to the number of trees in the next
Pinus Nigra Subsp. Salzmannii Forests from Southeast Spain: …
9
larger diameter class, is low in the old-growth study patch. On the other hand, the old-growth
patch contains a much higher density of old trees (some of the trees in the old-growth patch
are over 1000 years old (Creus, 1998), Figure 2).
Perhaps more than a fifth of the fauna of woodland depends on dead and decaying trees
(Fuller and Peterken, 1995). Current standing volume of dead trees (snags) is approximately
15 m3/ha, which represents an 8.5% of the overall standing volume.
4.2. Changes in Forest Structure Over 60 Years of Management
Most forests from Cazorla-Segura mountain range are divided in comparments to aid the
planning of tactical considerations, i.e. to answer the questions where and when silvicultural
treatments should be applied. In areas where Pinus nigra is the dominant tree species,
regularly harvested comparments usually exhibit the diameter distributions plotted in Figure
2. As can be observed, one effect of management is that large trees (DBH > 60 cm) are very
scarce in logged forests compared to those forests with minor human disturbances.
Data for Figure 2 came from 1996 forest inventory. Several forest inventories have been
carried out in the study area over the last century, as part of the planned management
implemented in Pinus nigra forests after 1893. Until the 1980’s, inventories were made
independently for each compartment by tallying all trees with a DBH equal to or bigger than
20 cm in classes of 10 cm.
Data from a sample of 12 compartments were used in a repeated-measurements analysis
of variance, in order to follow changes in forest structure between 1920 and 1979. Records
from earlier surveys were not considered, because they were thought to be insufficiently
accurate. Data from forest inventories carried out after 1979 were not considered either,
because they used sampling methods affected by an unknown error at the compartment level.
In the analysis, compartments were considered as sample units, because their boundaries have
never changed since they were first delineated.
Results from the analysis of variance, summarized in Table 2, indicate that the number of
trees up to 40 cm DBH increased steadily over the period considered, although a diminution
was recorded between 1967 and 1979. The density of thin (and young) trees increased,
probably due to the effective control of some grazing practices during the 20th century, which
favoured Pinus nigra regeneration. No significant changes were noted in the abundance of
trees of other sizes, although the density of large trees (DBH > 60 cm) was reduced by half
between 1920 and 1979.
Old black pines show a distinctive arquitecture that might provide biodiversity with
habitats different from those provided by younger trees, but little is known in this respect. As
far as we are aware, the only existing information refers to the importance of large black
pines as primary sources of deadwood, because the survival of some endangered saproxilic
beetles depends on the availability of large snags and logs (Molino, 1996). Therefore, the
observed reduction of large tree density might represent a decrease in biodiversity associated
with Pinus nigra forests, although this reduction was not significant in the repeatedmeasurements analysis of variance.
Similarly, large trees contribute to stand structural diversity, which can indicate overall
species diversity, as shown in studies concerning plant, avian and insect diversity (Jonsson
Pedro Antonio Tiscar and Juan Carlos Linares
10
and Jonsell, 1999; Tellería et al., 1992; González-Esteban et al., 1997; DeGraff et al., 1998;
Kirby, 1992).
Table 2. Diameter distribution of the mean number of trees per compartment and forest
inventory.
Year of forest inventory
Diameter class
(cm)
25
35
45
55
65
75
85
95
>100
> 40 cm
> 60 cm
TOTAL
1920
1944
1959
1967
1979
1619.92(a)
1070.92(a)
763.75
479.08
197.33
84.33
31.00
14.08
5.42
1574.99
332.16
4265.83
2126.00(b)
1298.25(a)
860.75
448.42
196.42
67.08
28.17
10.92
6.42
1618.18
309
5042.43
2304.83(b)
1374.25(a)
841.75
386.08
151.67
52.42
20.83
6.75
3.92
1463.42
235.59
5142.50
2885.25(c)
1501.67(b)
884.83
386.17
162.08
53.25
22.00
7.83
3.75
1519.91
248.91
5906.83
3154.17(c)
1544.58(b)
753.00
280.42
99.42
29.00
9.25
3.08
3.58
1177.75
144.33
5876.50
n = 12 comparments, with a mean surface of 48 ha. Different letters indicate significant differences in a
repeated-measurements ANOVA (p< 0.05).
Among the variety of indices available for expressing stand structural diversity, species
diversity indices have gained wide acceptance in forestry and, perhaps, Shannon’s index is
the most commonly used (Staudhammer and LeMay, 2001). It is defined as follows:
S
H ' = −∑ pi ln pi [1]
i =1
where pi is the proportion of individuals in the ith species, and S is the number of species.
Here, ‘species’ is a convenient term for the categories into which we place individuals, i.e.
either tree species or diameter classes can be thought of as ‘species’.
We computed equation [1] using the diameter distribution of the same 12 comparments
mentioned above. Diameter classes were considered as species. Results show that a
significant decrease occurred in the stand structural diversity over the period of time
considered (Kruskall-Wallis test; K = 10.67; p-value = 0.03; Figure 3). Little is known about
likely relationships between the existing biological diversity and the observed structural
diversity in any given site from the study area, but a positive relationship has been found in
other areas (Jonsson and Jonsell, 1999; Tellería et al., 1992; González-Esteban et al., 1997;
DeGraff et al., 1998; Kirby, 1992).
The sampling of relatively undisturbed sites and the remeasuring of permanent plots, or
comparments, may be suitable methods for establishing reference conditions (Moore et al.,
1999). As found in other studies on the impact of forestry in natural forests (Sendak et al.,
2003), the silvicultural removal of trees changed the size distribution in the sampled
compartments, and reduced their structural diversity (Linares et al., 2010). When these results
Pinus Nigra Subsp. Salzmannii Forests from Southeast Spain: …
11
are compared with the current structure of the old-growth patch, the most obvious effect of
forest management on Pinus nigra natural forests is a reduction of large tree density.
Year of forest inventory
1979
1967
1959
1944
1920
0.6
0.8
1.0
1.2
1.4
1.6
1.8
2.0
2.2
Shannon's indices
Figure 3. Changes in the values of Shannon’s index over 59 years of forest management. Error bars
represent the 5th/95th percentiles, boxes represent the standard errors, solid lines represent the mean
values and points are outliers. N = 12 comparments.
Forestry can affect species composition by the silvicultural removal of less desirable
species. Management plans from the study area have continuously considered Pinus nigra the
principal forest species. This explicitly justified the felling of Quercus species for charcoal
production with the ultimate aim of substituting oaks by pinetrees, at least during the first half
of the 20th century. Consequently, oaks only survived in specific sites which management
plans would eventually accommodate coppice stands.
5. THE REGENERATION PROCESS IN BLACK PINE FORESTS
The structure of a forest stand depends on the nature of the disturbances which occur, i.e.
their frequency, amount of overstory removed, size and shape of the area disturbed (Olive and
Larson, 1996), and on how new individuals and species appear after disturbance. Thus,
disturbance and regeneration patterns are essential in the development of nature-based forest
management.
The identification of factors that affect recruitment rates is important at both the
population and the community level (Harper, 1977; Clark et al., 1999). It is also a major goal
for foresters, who have long appreciated a quick stand regeneration following harvest
operations (Davis et al., 1987). Factors affecting forest regeneration might be biotic or
abiotic, and may act limiting seed production, seed dispersal, seed germination or seedling
12
Pedro Antonio Tiscar and Juan Carlos Linares
establishment (Tíscar, 2007). When recruitment is difficult because the number of seeds is
small, dispersal success is low or the number of seeds available for germination decreases
dramatically due to post-dispersal seed predation, plant recruitment is said to be seed-limited.
On the other hand, microsite-limitation occurs when recruitment is confined to a few
favorable micro-environments or patches (Eriksoson y Ehrlén, 1992; Rey et al., 2006).
The regeneration process of Pinus nigra has long concerned Spanish foresters. In this
section, we revise literature and present new results which are relevant for the regeneration of
this species in the Southeast mountain ranges. A number of factors that limit Pinus nigra
recruitment have been quoted over the last decades (Tíscar, 2005). They can be grouped as
seed-limiting factors: (i) the irregular production of pineseeds, (ii) the ageing of mother plants
and (iii) the predation of seeds, or microsite-limiting factors: (iv) the presence of litter, (v)
drought and (vi) the availability of light.
5.1. Masting as a Impediment for the Regeneration of Harvested
Pinus Nigra Stands
When the principles of forestry began to be applied in Spain at the end of the XIX
century, most Pinus nigra forests were intended to regenerate following prescriptions of the
uniform shelterwood method, with a shelter-phase of 20 years and a rotation period of 100 or
120 years. Pinus nigra stands often failed to regenerate under these prescriptions, so some
forests eventually adopted more flexible silvicultural methods, such as the selection method,
or extended the shelter-phase up to 40 years. Where the uniform shelterwood method has
maintained, pine-seeds might be added to the ground in order to increase the density of
seedlings.
Foresters resort to direct seeding because Pinus nigra shows considerable fluctuation in
the number of seeds produced from one year to another, there being years in which the
standing trees exhibit a very low crop-size. As a consequence, regeneration might be delayed
within the regeneration period fixed by silvicultural methods, and foresters tend to look at
crop-size variation as an impediment to establish new individuals after the realization of
harvest operations. However, from a biological point of view, Pinus nigra is a very long-lived
species, and can well pay the price of not reproducing during some years, if other benefits are
gained by doing so. This means that the irregular production of seeds may have evolutionary
implications that should be acknowledged, if more ecological-based silvicultural methods are
to be implemented.
The species producing intermittent crops of seeds are said to show “mast seeding” or
“masting”. More specifically, masting is “[the production of] seed crops synchronously at
irregular intervals but with an average periodicity characteristics of the species” (Silvertown
1980). Among Spanish foresters, Pinus nigra is considered as a species that shows masting,
because it produces large seed outputs every 3-4 years and small crops in between (Ruiz de la
Torre, 1979).
Nevertheless, long data sets are needed to make accurate calculations of intermast
intervals (Houle and Filion, 1993), and no such a long-term record exists for the most recent
years in the study area. However, there are records of annual crop-sizes from 1906 to 1925,
registered by Enrique Mackay, a forest engineer who worked in the area. He recorded
Pinus Nigra Subsp. Salzmannii Forests from Southeast Spain: …
13
annually the amount of pinecones according to an ordinal scale: abundant, medium, scarce
and nil, where an abundant outcrop was two-fold a medium one (Mackay, 1926).
Table 3 shows the mentioned records, besides available data of spring and September
rainfall. Mackay (1926) suggested that a lack of water during those moments of the year
would significantly reduce current crop size. The possibility that climate determines seed
output is the most parsimonious explanation for masting: seed production varies simply
because it mirrors variation in the environment. Indeed, all plants are expected to be affected
by environmental variability, but there may also be an adaptive value in masting so selective
forces may act to favour variation in crop-size.
Table 3. Crop sizes and meteorological variables over 20 years of observations.
Year
1906
1907
1908
1909
1910
1911
1912
1913
1914
1915
1916
1917
1918
1919
1920
1921
1922
1923
1924
1925
Crop size
Abundant
Nil
Nil
Abundant
Medium
Nil
Nil
Nil
Scarce
Scarce or Nil ¿?
Scarce or Nil ¿?
Scarce or Nil ¿?
Medium
Medium
Abundant
Medium
Abundant
Medium
Scarce or Nil ¿?
Scarce or Nil ¿?
Spring rainfall
402
241
285
465
193
371
337
226
342
171
342
September rainfall
77
118
0
0
104
31
109
38
35
0
13
¿? It was not possible to determine whether crop size was scarce or nil.
Kelly (1994) proposed different types of masting ranging from strict through normal to
putative masting, and ways to recognize them. For instance, normal masting can be confirmed
(i) by finding that annual seed output does not fluctuate around an average value, but exhibits
a marked trend toward bimodality, (ii) or by the presence of switching: in years of large
crops, resources are diverted from vegetative growth or reserves. Pinus species seem to
display normal masting.
Our personal observations are that most trees in a Pinus nigra population may produce no
cones at all during one or more consecutive years, although there are always some trees
producing either few or many pine cones. Table 3 exhibits this same pattern. In a study on
dendroclimatology, we also found a significant reduction in vegetative growth coinciding
with known high seed years (Linares and Tíscar, 2010). Additionally, we used data from a 4-
14
Pedro Antonio Tiscar and Juan Carlos Linares
year study to calculate a coefficient of variation for seed output, which resulted in a value of
1.57 (if CV>1.6, switching is highly likely to be present (Kelly, 1994)). Together, this
evidence indicates that Pinus nigra shows normal masting.
Studies on masting have concluded that mechanisms related to economy of scale (i.e. a
synchronization of the reproductive effort improves pollination efficiency and/or more seeds
survive seed predation) should favour the evolution of occasional large reproductive efforts
rather than regular smaller ones (Norton and Kelly, 1988; Kelly, 1994; Herrera et al., 1998).
In this respect, the wind pollination hypothesis states that wind-pollinated plants obtain
reproductive benefits by synchronizing large flowering efforts, because it increases the
probability of pollination (Smith et al., 1990). It is been observed that Pinus nigra produces
higher percentages of empty seeds (unpollinated) in low flowering years (Tíscar, 2007).
Similarly, the predator satiation hypothesis states that large seed crops are likely to satiate
seed predators, which thus destroy a lower percentage of crop (Kelly, 1994). Most Pinus
nigra dispersed-seeds are predated by rodents and birds in low seed years, while a higher
percentage survives predation in high seed years (Tíscar, 2003).
Whether masting has an adaptive value and even whether Pinus nigra actually shows
masting or not, might be of little interest for foresters aiming to regenerate Pinus nigra stands
in harvested forests. However, it might be convenient to admit that the irregular production of
pine-seeds is a natural phenomenon, when designing nature-based silvicultural methods.
5.2. Fertility of Senescent Trees of Pinus Nigra
Harper (1977, p.686) depicted an idealized life cycle according to which polycarpic
plants would increase their reproductive output over the years to a plateau and then gradually
decline during a phase of senescence. This variation in the lifetime fecundity of individual
plants is expected to influence patterns of recruitment dynamics, with important consequences
for the demographic structure and persistence of populations. This ecological fact has been
interpreted by Spanish foresters from a practical point of view: the presence of many old trees
is a seed-limiting factor that might prevent forest stand regeneration (Madrigal, 1994). Yet
new forestry strategies, developed under the paradigm of sustainability, recommend
maintaining old trees to favour biodiversity (Ferris and Pritchard, 2000). Thus, it is worth
recalling that most Pinus nigra forests from the study area are currently included in natural
parks, where management plans require foresters to consider both timber products and
biodiversity conservation.
The relationship between fertility and mother plant age has been studied to some extent
for the Pinus nigra populations from Cazorla-Segura mountain range. It has been found that
individuals over 200 years old show reduced fertility compared to that of younger trees,
fertility being defined as the capacity to produce sound seeds able to germinate (Tíscar,
2002). Two-hundred years must be seen as an arbitrary threshold to distinguish old trees; the
rotation age in the study forests is 120 years, so 200 years well represents the upper limit of
the time a black pine will remain in a managed stand.
Specifically, the quoted study found trees over 200 years old to have a fertility of about
81% (i.e. 19% of the sampled pine-seeds were empty or unable to germinate), 7.5 points less
than the fertility observed in mature trees with ages up to 120 years (Table 4). The possibility
that the overall seed output could be smaller in old trees was not tested, but that is not
Pinus Nigra Subsp. Salzmannii Forests from Southeast Spain: …
15
probably the case. Individual size is a surrogate for reproductive output and older pinetrees
normally have larger crowns (Dodd and Silvertown, 2000). Additionally, our personal
observations are that old trees, even up to 600 years old or more (and therefore far beyond the
200 years threshold), still produce abundant crops in masting years.
Table 4. Mean values ± standard errors of fertility and seedling performance estimates
for the three groups of age considered.
VARIABLE
Fertility
(%)
Age
<120 yr
89.21 ±1.04(a)
n= 66
121-200 yr 82.59 ±1.87(ab)
n= 54
>201 yr
81.74 ±1.25(b)
n= 78
Root length
(mm)
Stem length
(mm)
Above-ground Bellow-ground
biomass (mgr) biomass (mgr)
248.55 ±4.20(a)
n= 120
258.51 ±5.72(a)
n= 80
249.81 ±5.37(a)
n= 100
34.98 ±0.63(a)
n= 120
37.25 ±0.86(a)
n= 80
34.28 ±0.81(a)
n= 100
101.16 ±2.82(a)
n= 120
103.86 ±3.85(a)
n= 79
90.16 ±3.13(b)
n= 124
65.82 ±6.31(a)
n= 12
69.44 ±8.59(a)
n= 8
50.93 ±6.45(a)
n= 13
Different letters indicate significant differences (Scheffé pos hoc test, p<0.05).
The observed fertility in trees with an intermediate age (121-200 years) was around 83%.
This intermediate age-class includes trees that are currently under-represented in Pinus nigra
forests (but not as much as trees over 200 years), although their frequency would increase
gradually as rotation periods were extended in order to maintain biodiversity (Curtis, 1997).
Therefore, the implications for management of these findings about Pinus nigra fertility are
that rotation periods could be extended without risking the supply of fertile pine-seeds (there
was no significant difference in fertility between groups of intermediate age and old trees
(Table 4)). Moreover, Pinus nigra seedlings develop normally whatever the age of the mother
plant, as can be deduced from several seedling performance variables shown in Table 4.
Considering these observations, it seems Pinus nigra would conform to Harper’s cycle,
although the reproductive activity extends until very late in the life-span of this species. It is
been shown that even trees over 900 years old reproduce normally despite on their aspect of
senescence (Tíscar, 2002).
5.3. Impact of Post-Dispersal Seed Predation in the Regeneration of
Pinus Nigra Stands
Before new seedlings emerge, seeds of Pinus nigra need to escape post-dispersal
predation and find soil conditions suitable for germination. Predation of dispersed seeds may
have a considerable impact on plant populations (Hulme, 1998). For instance, pre- and postdispersal seed predation is a major limiting factor for Pinus sylvestris regeneration in the
Béticas Mountain Range (Castro et al., 1999). Some ants (for instance, Formica cunicularia,
Lasius niger, Messor structor, Pheidole pallidula) and birds (for instance, Fringilla coelebs,
Emberiza sp) consume pine-seeds once they have been dispersed onto the ground, but
woodmouse (Apodemus sylvaticus L.) is the main predator of dispersed seeds in the study
area (Tíscar, 2003).
16
Pedro Antonio Tiscar and Juan Carlos Linares
On the other hand, the accumulation of plant litter is another factor acknowledged by
foresters and ecologists for obstructing tree regeneration (Xiong and Nilsson, 1999). Thus, it
is generally accepted that Pinus nigra establishes better on soils disturbed by harvesting
operations (Tíscar et al., 2010).
Here, we report results from an experiment designed to account for both predation and
litter effects. In an area ca. 10 ha, we identified ten sites (gaps of similar size) where Pinus
nigra saplings had recently established, and randomly selected six of these sites (blocks). At
each site, we sowed 176 pineseeds distributed in 24 square plots (12.5-cm x 12.5-cm)
according to a three-factor design: predators (allowed versus excluded by wire cages), soil
disturbance (undisturbed versus disturbed by removing litter and vegetation until the ground
was bare), and density (three sowing densities: 4, 6 and 12 seeds per plot). Each treatment
combination was replicated twice within each site. 1056 pineseeds were sown for the whole
experiment. We examined the effects of predation and disturbance on seedling emergence
(percentage of seedlings emerged from the sown seeds) by a randomized block design, where
blocks were considered random, and predation and disturbance fixed factors.
A total of 169 seedlings emerged by the end of the experiment. Mean probability of
emergence per plot was 0.159 ± 0.021 seedlings emerged / seeds sown (range 0-1). 45 plots in
the predator-exclusion treatment contained at least one seedling by the end of the emergence
period, while only 8 did in the predator-allowed treatment (Table 5). Thus, the factor
predation explained satisfactorily the probability of emergence, i.e. the probability of finding
emerged seedlings in a plot (χ2 = 45.44; p-value < 0.001), and its interaction with the factor
disturbance (χ2 = 4.60; p-value < 0.05).
Table 5. Results of ANOVA on the probability of emergence (seedlings emerged / seeds
sown).
Source
Block
Predation
Density
Disturbance
Block x Predation
Block x Density
Predation x Density
Block x Disturbance
Predation x Disturbance
Density x Disturbance
Block x Predation x Density
Block x Predation x Disturbance
Block x Density x Disturbance
Predation x Density x Disturbance
Blo. x Pred. x Density x Perturbac.
Error
Angular transformed data.
d.f.
5
1
2
1
5
10
2
5
1
2
10
5
10
2
10
72
MS
442.40
13116.6
169.71
5306.21
121.78
276.25
341.28
75.47
5678.74
392.02
207.97
72.59
99.22
303.78
67.27
80.60
F
2.748
107.709
0.614
70.310
0.571
1.151
1.641
0.722
78.233
3.951
3.092
1.079
1.475
4.516
0.835
P
0.3581
0.0001
0.5602
0.0004
0.7217
0.4140
0.2419
0.6387
0.0003
0.0544
0.0447
0.4275
0.2751
0.0401
0.5971
Pinus Nigra Subsp. Salzmannii Forests from Southeast Spain: …
17
Woodmice consumed most of the pineseeds deposited on sowing plots. These rodents
usually search for food under the shelter of scrub, groups of saplings, or dense forest stands
(Alcántara et al., 1999), which happened to be the vegetation structure around the six study
sites in the sowing experiment we are reporting here. Accordingly, other studies have also
found that seeds of Pinus nigra are more intensively predated in the proximity of shrubs
(Tíscar, 2003, see section 5.7).
5.4. The Effect of Plant Litter on Pinus Nigra Recruitment
As with predation, plant litter also had a negative effect on seedling emergence. Litter
covering the ground of Pinus nigra stands is normally composed of forbs and pine-needles,
and its removal favours seedling emergence as shown by results from the sowing experiment
reported earlier (Table 5). However, another study found a positive correlation between
litterfall depth and density of seedlings in Pinus nigra stands from the study area (Alejano et
al., 1997). Since we have experimentally shown that emergence of new seedlings is higher in
disturbed soils, i.e. soils where litter has been completely removed (Table 5, see section 5.3),
results reported by Alejano et al. (1997) were likely to be reflecting a higher probability of
survival in sites with abundant litterfall, rather than higher emergence. Litter normally has a
stronger effect on plant germination than on establishment (Xiong and Nilsson, 1999). As a
consequence, there must be a balance between the negative and the positive interactions of
litter with Pinus nigra recruitment which eventually determines stand regeneration (see
section 5.6).
5.5. Drought as a Limiting Factor for Black Pine Regeneration
Summer drought is considered to be the main factor impeding the successful regeneration
of Pinus nigra stands in the study area. For instance, Tíscar (2007) observed less than 6% of
post-summer survival in a cohort of seedlings emerged in spring of that same year. Water
stress was reported as the major cause of mortality. This result and cause of mortality
coincide with other populations of Pinus nigra (Cerro et al., 2009), as well as with other plant
species in the area (Herrera et al., 1994; Rey and Alcántara, 2000; Gómez-Aparicio, 2008).
The irregular occurrence of late summer storms has consequently been quoted as a key event
for the regeneration of Pinus nigra stands (Mackay, 1926; Alejano et al., 1997). However,
temperature might be equally important, through its effect on water balance. Thus, most
saplings (height < 1.30 m) surveyed in a stand from the study area were found to have
established in years with an intensity of drought far below the observed mean value (684
mm), as shown in Figure 4. Drought intensity was estimated as the sum of monthly
differences between precipitation data and Thornthwaite potential evapotranspiration for
June, July, August and September. Correlation between drought intensity and establishment
of new trees might seem unclear in Figure 4, as some years with low drought intensity do not
recruit saplings, but it must be remembered that Pinus nigra produces intermittent crops of
pineseeds (see section 5.1).
Pedro Antonio Tiscar and Juan Carlos Linares
18
180
180
160
Drought intensity
Saplings
Drought intensity (mm)
140
140
120
120
100
100
80
80
60
60
40
40
20
20
0
1980
1985
1990
1995
No. of established saplings
160
0
2000
Regeneration year
Figure 4. Relationship between summer drought and establishment of new individuals of Pinus nigra.
The horizontal line represents the mean value for drought intensity from June to September.
Over the last 40 years, the mean June temperature has increased significantly in the study
area (0.92ºC/decade), while mean precipitation has decreased 6.41 mm/decade. On the
contrary, July, August and September do not show any significant trend in mean temperature
or precipitation values (Linares and Tíscar, 2010). This suggests that wet, cold weather in
early summer could be more important for Pinus nigra recruitment than the irregular
occurrence of storms later on. Unfortunately, Climatic Change projections and observational
data indicate that Pinus nigra recruitment may be very difficult in the future.
5.6. Light and Water Balance Interactions
Foresters manipulate canopy cover to allow light to reach the ground and trigger the
establishment of new tree individuals. Indeed, the manipulation of canopy cover is at the core
of silvicultural methods implemented to regenerate stands. Thus, the control of light appears
as a key aspect of a forester’s work. However, canopy cover also modulates soil water
balance (e.g. offering protection from excessive evapotranspiration, ameliorating extreme
temperatures, improving soil properties), which can be of more importance under
Mediterranean conditions (Gómez-Aparicio et al., 2009). Thus, different authors have
addressed the importance of facilitative interactions in which seedlings of Pinus nigra benefit
from the special abiotic conditions present beneath the overstory (Aunós et al., 2009; Trabaud
and Campant, 1991). Cover is normally expressed as a percentage, although stand basal area
measured in m2/ha is also used. Stand basal area is easy to measure and works as a surrogate
of cover, so foresters frequently use stand basal area as a control variable in silvicultural
Pinus Nigra Subsp. Salzmannii Forests from Southeast Spain: …
19
prescriptions. For Pinus nigra, recommendations are 18-30 m2/ha of stand basal area to
successfully regenerate the species (Cerro et al., 2009; Alejano et al., 1997).
That range of stand basal area supposes a canopy cover of 60-70%, which may represent
a compromise between light availability and facilitation benefits (improved water balance) in
Pinus nigra stands. Thus, there must be an upper limit of canopy cover above which Pinus
nigra regeneration is impeded, due to physiological constraints (Gómez-Aparicio et al.,
2006). On the other hand, despite the fact that Pinus nigra withstands high radiation, water
supply is the main limiting factor that controls regeneration in open spaces (see section 5.5),
so some cover below an upper limit is necessary to prevent excessive evapotranspiration and
improve water balance (Gómez-Aparicio et al., 2006 and 2009).
5.7. Recruitment Dynamics
So far, we have considered separately to the role of masting, mother plant age, postdispersal seed predation, soil conditions and summer drought in the recruitment dynamics of
Pinus nigra. However, those factors are just parts of a whole, i.e. recruitment is a multiphase
process involving several sequential life-history stages (i.e. seeds, seedling, saplings)
connected by transitional processes (i.e. dispersal, emergence, survival) which are affected by
factors, such as those already analyzed (Gómez-Aparicio, 2008; Jordano and Herrera, 1995;
Rey and Alcántara, 2000).
Figure 5 summarizes the stages (rectangles) that were considered in a previous study on
Pinus nigra recruitment dynamics (Tíscar, 2007). In the same figure, ovals represent
processes, i.e. any event that affects the probability of a propagule moving from one stage to
the next, and factors influencing processes appear on the right hand side.
Four stages are included in Figure 5: pre-dispersed seed, dispersed seed, seedling and
sapling. Pre-dispersed seed refers to seeds still contained in either closed or open cones. Some
insects (Pisodes sp.), birds (Loxia curvirostra, Sitta europaea, Parus sp.) and squirrels
(Sciurus vulgaris) are potential predators of pine-seed before they are removed by wind from
the open cones and dispersed onto the ground. Here, woodmouse and some ant and bird
species consume seeds as it was said earlier. If seeds survive post-dispersal predation and
overcome soil conditions preventing germination, they reach the stage of seedling. The
seedling needs to survive water stress, herbivory and other difficulties before it becomes a
sapling.
For every transitional process, there is an associated transition probability (TP) that
represents the probability of moving forward between consecutive stages. This probability is
measured as the number of propagules completing a stage divided by the number of
propagules entering the stage. Additionally, an overall probability of recruitment (OPR) can
be calculated as the product of every TP.
TPs and OPRs permit comparisons to be made of recruitment dynamics between
microhabitats. Thus, Table 6 shows the spatial dynamics of recruitment for the four
microhabitats most frequently found in Pinus nigra stands. They are: dense forest (cover >
80%), gap (openings in the canopy between 1000 and 1400 m2 in surface (Tíscar and Ruiz,
2005)), border (the dense forest-gap ecotone) and clear forest (cover < 50%). For a given
microhabitat, the probability of dispersal was defined as the ratio of mean seed density in this
microhabitat divided by the sum of mean seed densities in all the microhabitats. Therefore,
20
Pedro Antonio Tiscar and Juan Carlos Linares
probability of dispersion provides a measure of the relative likelihood of seeds being
deposited in each microhabitat. In the study we are reporting here, mean seed densities were
calculated from the number of seeds collected in seed traps (0.0744 m2 aluminium trays), that
had been place at 48 sampling locations per microhabitat.
Pre-dispersed seed
Escape from predispersal predation
Dispersal
Insects, birds and
squirrels
Wind
Dispersed seed
(sound + empty)
Escape from postdispersal predation
Germination
and emergence
Ants, birds and
woodmice
Litter and other
factors preventing
germination
Seedlings
Establishment
Physical damage,
herbivory,
Pests and diseases,
water stress
Saplings
Survival
As above
Pinus Nigra Subsp. Salzmannii Forests from Southeast Spain: …
21
Figure 5. diagram of recruitment to show stages (rectangles), proceses (ovals) and factor influencing
proceses (right hand side).
Probability of dispersion was rather similar between microhabitats (between 0.24 and
0.27, Table 6), i.e. all the microhabitats received a similar amount of pine-seeds which, on the
other hand, were equally viable (filled seeds able to germinate). However, the probability of a
pine-seed escaping seed predators was lower in clear forests, where the abundance of shrubs
(Juniperus communis, Berberis hispanica, Rosa sp.) favoured the presence of woodmice.
Once pineseeds had escaped mice and other seed predators, a seedling emerged from nearly
every sound seed deposited in the microhabitats border and clear forest (TPs ≈ 1), whilst the
probability of emergence decreased for seeds dispersed either to the gap or to the dense forest
microhabitats (TPs equaled 0.65 and 0.77 respectively). In any case, the main “bottleneck” in
the recruitment dynamics of Pinus nigra was survival to summer drought. Thus, OPRs ranged
from 0 to 0.0027, i.e. from none to 27 emerged seedlings out of 10000 were recruited after the
first hot and dry season in seedlings life.
On the contrary, survival expectations seem to be much higher for saplings, i.e. any tree
between 10 and 130 cm tall (Table 6).
Table 6. Spatial dynamics for Pinus nigra recruitment. Values shown are processspecific transition probabilities (TPs), with overall probabilities of recruitment (OPR)
given at the base of each column (shown in bold type).
Habitat
Stage
Process
clear forest
(1) Pre-dispersed
seed.......................... Reproduction
0.2366
(2) Dispersed seed Dispersal (sound
...............……………+ unviable seeds) 0.8738
Escape from
(3) Dispersed seed post-dispersal
0.6979
................................ predation
(4) Dispersed seed Germination and
..........................
emergence
~1
(5) Seedlings.......... Establishment 0.019
OPR
0.0027
(6) Sapling survival....................................... 0.9704
border
gap
dense forest
0.2651
0.2446
0.2537
0.9400
0.8858
0.9197
0.8437
0.9270
0.9271
~1
0.00
0.00
0.6533
0.00
0.00
0.7741
0.011
0.0018
6. REFERENCE CONDITIONS AND MANAGEMENT IMPLICATIONS
In theory, reference conditions for a particular type of ecosystem should consider all its
components, including organisms, structures, biogeochemical cycles, processes of natural
disturbances, etc. (Moore et al., 1999). In practice, many components are difficult to
understand or quantify. For example, the number of organisms present in any patch of forest
is enormous, so it is impossible to include all of them in management considerations.
Cazorla-Segura mountain range is well known for its biological diversity, yet new
invertebrate species, and possibly plants, are still to be discovered as the territory is better
explored (Alonso et al., 2004). Similarly, it is now that the diversity of micro-organisms and
22
Pedro Antonio Tiscar and Juan Carlos Linares
its role in ecosystem process are being devised (Herrera and Pozo, 2010). Considering such
known and unknown biological richness in forest management plans seems an overwhelming
task. However, management “shortcuts” are possible, because composition, structure and
function are intimately related (Noss, 1993). For instance, forest structure is the result of
processes, such as disturbance and regeneration, and both structure and process create habitats
for forest-dwelling species, i.e. forest composition.
Because of that intimate relationship between composition, structure and function, the
aim of sustainable forestry (producing resources whilst maintaining biodiversity) can be
achieved by the application of general management principles that refer to structure and
process in forests (Lindenmayer et al., 2006). The use of natural disturbance regimens to
guide human disturbance regimes (silvicultural systems) seems particularly important
(Seymour and Hunter, 1999). Other approaches simply emphasize creating structural diversity
at the stand level (O’Hara, 1996).
From the body of available information, we will present a set of preliminary reference
conditions which provide a baseline to: (i) determine the key structural variables of Pinus
nigra natural forests, and (ii) characterize the key natural disturbance regime operating within
them.
We infer that natural Pinus nigra forests were relatively open (canopy cover < 70%) and
multi-aged, with an important presence of large trees. Density of large trees constitutes our
first key structural variable. Based on a methodology explained in Emborg et al. (2000), we
elaborated a model of forest cycle in order to compare current structure with that expected in
a forest free of human intervention (Table 7). This model forest cycle offers a quantitative
estimation of the density of large trees in terms of occupied surface (up to 62.5%). Other
sources of data, such as the current structure of the old-growth study patch, offer information
on diameter distributions and patterns (Figure 2).
Table 7. Duration of each phase of the estimated forest cycle and the actual area covered
by each phase in two comparments from the study area.
Model duration
years
% surface
Innovation (Height < 2 m)
20
5
Early aggradation ( DBH < 50 cm)
130
32.5
50
Late aggradation (Heightmax = 27 m; 50 < DBH <200
80)
Biostatic (DBH ≥ 80 cm)
>50
12.5
Degradation
Variable
Phase of the forest cycle
Current value
% surface
3
84.9
12.1
0
0
The exact composition of natural Pinus nigra stands can not be inferred, although it
would be expected that this species accounted for more than 90% of the overall standing
biomass (Quercus, Acer, Fraxinus, Taxus, and Ulmus, among others, would account for the
remaining 10% (Carrión, 2002)). Considering the abiotic environment of the study area, the
life-history strategies of the species involved and the stochastic component of natural
disturbances, we will suggest that species tend to segregate themselves in the study area, and
would form mosaics with patches of single-species, although mixed-stands could also be
possible.
Pinus Nigra Subsp. Salzmannii Forests from Southeast Spain: …
23
On the other hand, we consider the natural disturbance regime operating within Pinus
nigra forests in the study area to be characterized by minor disturbances, which would clearly
prevail over stand-replacing ones. The death of individual or small groups of black pines,
either uprooted by wind or heavy snowfalls or killed by pathogens, breaks the canopy,
opening gaps in which Pinus nigra regenerates. As a result, natural structure would tend to
show both vertical complexity and horizontal heterogeneity. Such a structure can develop
under a surface fire regime (Moore et al., 1999).
In this article, we have suggested that reference conditions might be used as an
alternative to the normal forest model, and be used as a point of reference to design
sustainable forestry. We have also mentioned the convenience of using natural disturbance
regimens to guide silvicultural systems. Considering these and what has been said about the
evolutionary environment of Pinus nigra and about the structural attributes that one would
expect to find in Pinus nigra natural forests, we understand that close-to-nature management
may fit adequately within the aim of producing forest resources while maintaining
biodiversity in this type of pinewoods. Close-to-nature management is based on the treatment
of individual trees, taking into account the economic and ecological functions performed by
trees at the stand level (Martín-Fernández and García-Abril, 2005). In close-to-nature
management, harvest operations are restricted to trees of sufficient diameter that have already
attained their maximum economic value (timber of good quality) for the species and site.
Thus, a tree will remain in the stand, if it continues to increase its market price and/or it is
favouring the accumulation of value in other trees (productive function) or benefiting
biodiversity. Trees can develop productive functions on their own, or by the improvement of
adjacent trees (e.g. favouring natural pruning and shelf-thinning processes). Benefits for
biodiversity involve the conservation of rare tree species, and the maintenance of dead and
decaying trees, and of trees bearing holes for nesting birds, etc.
A remarkable aspect of close-to-nature management is that the felling of trees is not
affected by the desire to achieve a balance age-class distribution (a normal forest), rather trees
are felled according to their own vitality. This offers a better opportunity to resemble the
evolutionary environment of Pinus nigra forests while harvesting their resources.
7. REFERENCES
ALEJANO R., ALVAREZ L., MADRIGAL A., MARTINEZ E., 1997. Regeneración de
Pinus nigra ssp. salzmannii en las Sierras Béticas. II Congreso Forestal Español, Irati.
Mesa 4, pp. 15-20.
ALEJANO R., MARTINEZ E., 1996. Distribución de Pinus nigra Arn. subsp. salzmannii en
las sierras Béticas. Ecología 10, 231-241.
ALONSO C., GARRIDO J.L., HERRERA C.M., 2004. Investigaciones sobre plantas y
animales en las Sierras de Cazorla, Segura y Las Villas. 25 años de estudios por el CSIC.
Consejería de Medio Ambiente, Junta de Andalucía, Sevilla.
AUNÓS Á., RIBA A., BLANCO R., 2009. Caracterización selvícola de las masas
monoespecíficas de pino laricio en Cataluña. Inv. Agr. 18, 338-349
CARRIÓN J.S., 2002. Patterns and processes of late Quaternary environmental change in a
montane region of southwestern Europe. Quaternary Science Reviews 21, 2047-2066.
24
Pedro Antonio Tiscar and Juan Carlos Linares
CERRO A., LUCAS M.E., MARTÍNEZ E., LÓPEZ F.R., ANDRÉS M., GARCÍA F.A.,
NAVARRO R., 2009. Influence of stand density and soil treatment on the Spanish Black
Pine (Pinus nigra Arn. ssp. salzmannii) regeneration in Spain. Inv. Agr.: Sist. Recur. For.
18, 167-180.
CREUS J., 1998. A propósito de los árboles más viejos de la España peninsular: los Pinus
nigra Arn. ssp. salzmanii (Dunal) Franco de Puertollano-Cabañas sierra de Cazorla,
Jaén, Montes 54, 68-76.
CUARTAS, P., GARCIA-GONZALEZ, R., 1992. Quercus ilex utilization by Caprini in
Sierra de Cazorla and Segura (Spain). Vegetatio 99-100: 317-330.
CURTIS R.O., 1997. The role of extended rotations. En: Creating a forestry for the 21st
century: the science of ecosistem management, Franklin J.F., Kohm K.A. (Ed.), Island
Press, Washington, pp. 165-170.
DeGRAFF R.M., HESTBECK J.B., YAMASAKI M., 1998. Associations between breeding
bird abundance and stand structure in the White Mountains, New Hampshire and Maine,
USA. Forest Ecology and Management 1998, 217-233.
DODD M.E., SILVERTOWN J., 2000. Size-specific fecundity and the influence of lifetime
size variation upon effective population size in Abies balsamea. Heredity 85, 604-609.
EMBORG J., CHRISTENSEN M., HEILMANN-CLAUSEN J., 2000. The structural
dynamics of Suserup Skov, a near-natural temperate deciduous forest in Denmark. Forest
Ecology and Management 126, 173-189.
ESPELTA J.M., RETANA J., HABROUK A., 2003. An economic and ecological multicriteria evalutation of reforestation methods to recover burned Pinus nigra forests in NE
Spain. Forest Ecology and Managament 180, 185-198.
FERRIS R., PRITCHARD E.K., 2000. Risks associated with measures to enhance
biodiversity in European Scots pine forests. Investigación Agraria: Sistemas y Recursos
Forestales, Fuera de Serie nº 1, 255-272.
FOSTER D.R., ORWIG D.A., MCLACHLAN J.S., 1996. Ecological and conservation
insights from reconstructive studies of temperate old-growth forests. TREE 11, 419-429.
FULLER R.J., PETERKEN G.F., 1995. Woodland and scrub. In: Managing habitats for
conservation. W.F. Sutherland y D.A. Hill (eds). Cambridge University Press, pp. 327361.
GÓMEZ-APARICIO L., 2008. Spatial patterns of recruitment in Mediterranean plant species:
linking the fate of seeds, seedlings and saplings in heterogeneous landscapes at different
scales. Journal of Ecology 96, 1128-1140.
GÓMEZ-APARICIO L., VALLADARES F., ZAMORA R., 2006. Differential light
responses of Mediterranean tree saplings: linking ecophysiology with regeneration niche
in four co-occurring species. Tree Physiology 26, 947-958.
GÓMEZ-APARICIO L., ZAVALA M.A., BONET F.J., ZAMORA R., 2009. Are Pine
plantations valid tools for restoring Mediterranean forests? An assessment along abiotic
an biotic gradients. Ecological Applications 19, 2124-2141.
GONZALEZ-ESTEBAN J., IRIZAR I., CASTIEN E., VILLATE I., 1997. Relación entre las
características del hábitat y la diversidad de micromamíferos. La importancia del manejo
forestal. III Jornadas Españolas de Conservación y Estudio de Mamíferos, SECEM. Parc
Natural dels Aiguamolls de l´Empordà. Castelló d'Empúries. p. 47
HARPER J.L., 1977. Population Biology of Plants, Academic Press, London.
Pinus Nigra Subsp. Salzmannii Forests from Southeast Spain: …
25
HERRERA C.M., JORDANO P., GUITIAN J., TRAVESET A., 1998. Annual variability in
seed production by woody plants and the masting concept: reassessment of principles and
relationship to pollination and seed dispersal. The American Naturalist 152: 576-594.
HERRERA C.M., POZO M.I., 2010. Nectar yeasts warm the flowers of a winte-blooming
plant. Proceedings of the Royal Society B doi: 10-1098/rspb.2009.2252
HOULE G., FILION L., 1993. Interannual variations in the seed production of Pinus
banksiana at the limit of the species distribution in norhern Quèbec, Canada. Am. J. Bot
80 1242-1250
HUNTER M.L. Jr. (ed.), 1999. Maintaining biodiversity in forest ecosystems. Cambridge
University Press, pp. 3-21.
JONES C.G., LAWTON J.H., SHACHACK M., 1994. Organisms as ecosystem engeneers.
Oikos 69, 373-386.
JORDANO P., HERRERA C.M., 1995. Shuffling the offspring: Uncoupling and spatial
discordance of multiple stages in vertebrate seed dispersal. Ecoscience 2: 230-237.
KELLY D., 1994. The evolutionary ecology of mast seeding. Trends Ecol. Evol. 9, 465-470.
KUULUVAINEN T., 2002. Natural variability of forests as a reference for restoring and
managing biological diversity in boreal Fennoscandia. Silva Fennica 36, 97-125.
LINARES J.C., CARREIRA J.A., OCHOA V., 2010. Human impacts drive forest structure
and diversity. Insights from Mediterranean mountain forest dominated by Abies pinsapo.
European Journal of Forest Research. DOI 10.1007/s10342-010-0441-9.
LINARES J.C., TÍSCAR P.A., 2010. Climate change impacts and vulnerability of the
southern populations of Pinus nigra subsp. salzmannii. Tree Physiology 30 (7), 795-806.
LINDENMAYER D.B., FRANKLIN J.F., FISCHER J., 2006. General management
principles and a checklist of strategies to guide forest biodiversity conservation.
Biological Conservation 131, 433-445.
MACKAY E., 1926. El Pinus laricio Poir., y su aplicación a las repoblaciones forestales de la
región mediterránea. Congreso de Selvicultura de Roma.
MADRIGAL A., 1994. Ordenación de Montes Arbolados. MAPA-ICONA: Colección
MARTÍN-FERNÁNDEZ S., GARCÍA-ABRIL A., 2005. Optimisation of spatial allocation of
forestry activities within a forest stand. Computers and Electronics in Agriculture 49,
159-174.
MOLINO F., 1996. Los coleópteros saproxílicos de Andalucía. PhD dissertation. University
of Granada.
MOORE M.M., COVINGTON W.W., FULE P.Z., 1999. Reference conditions and ecological
restoration: a Southwestern Ponderosa pine perspective. Ecological Applications 9, 12661277.
NORTON D.A., KELLY D., 1988. Mast seeding over 33 years by Dacrydium cupressinum
Lamb. (rimu) (Podocarpaceae) in New Zealand: the importance of economies of scale.
Functional Ecology 2: 399-408.
NOSS, R.F., 1993. Sustainable Forestry or Sustainable Forests? En: Defining Sustainable
Forestry, Aplet G.H., Johnson N., Olson J.T., Sample V.A. (Eds.), Island Press,
Washington D.C. pp. 17-44 .
OLIVER C.D., LARSON B.C., 1996. Forest Stand Dynamics. John Wiley and Sons Inc., 520
pp.
PETERKEN G.F., 1996. Natural Woodland, ecology and conservation in northern temperate
regions. Cambridge University Press, 522 pp.
26
Pedro Antonio Tiscar and Juan Carlos Linares
PIOVESAN G., DI FILIPPO A., ALESSANDRINI A., BIONDI F., SHIRONE B., 2005.
Structure, dynamics and dendroecology of an old-growth Fagus forest in the Apennines.
Journal of Vegetation Science 16, 13-28.
PRIMACK R.B., ROS J., 2002. Introducción a la biología de la conservación. Ariel Ciencia.
Barcelona.
REY P.J., ALCANTARA J., 2000. Recruitment dynamics of a fleshy-fruited plant (Olea
europaea): connecting patterns of seed dispersal to seedling establishment. Journal of
Ecology 88: 622-633.
REY P.J., RAMÍREZ J.M., Sánchez-Lafuente A.M., 2006. Seed- vs. microsite-limited
recruitment in a myrmecochorous herb. Plant Ecology 184, 213-222.
RODRIGO A., RETANA J., PICÓ F.X., 2004. Direct regeneration is not the only response of
Mediterranean forests to large fires. Ecology 85, 716-729.
RUIZ DE LA TORRE J.,1979. Arboles y arbustos de la España peninsular. Escuela Técnica
Superior de Ingenieros de Montes, Sección de Publicaciones, 512 pp.
SENDAK P.E., BRISSETTE J.C., FRANK R.M., 2003. Silviculture affects composition,
growth, and yield in mixed northern conifers: 40-year results from the Penobscot
Experimental Forest. Can. J. For. Res. 33, 2116-2128.
SEYMUR R.S., HUNTER M.L. Jr.; (1999). Principles of ecological forestry: En:
Maintaining biodiversity in forest ecosystems. Cambridge University Press. Cambridge.
UK. pp. 22-61.
SILVERTOWN J.W., 1980. The evolutionary ecology of mast seeding in tress. Biological
Journal of the Linnean Society 14: 235-250.
SMITH C.C., HAMRICK J.L., KRAMER C.L., 1990. The advantage of mast years for wind
pollination. The American Naturalist 136, 154-166.
TAPIAS R., CLIMENT J., PARDOS J.A., GIL L., 2004. Life histories of Mediterranean
pines. Plant Ecology 171, 53-68.
TELLERIA J.L., SANTOS T., SANCHEZ A., GALARZA A., 1992. Habitat structure
predicts bird diversity distribution in Iberian forest better than climate. Bird Study 39, 6368.
TÍSCAR P.A. 2006. La gestión próxima a la naturaleza en el nuevo paradigma de la ciencia
forestal. In Tíscar P.A. (coord.): La Gestión Forestal Próxima a la Naturaleza. Prosilva,
pp. 15-39
TÍSCAR P.A., 2002. Capacidad reproductiva de Pinus nigra subsp. salzmannii en relación
con la edad de la planta madre. Invest Agrar: Sist Recur For 11, 357-371.
TÍSCAR P.A., 2003. Condicionantes y limitaciones de la regeneración natural en un pinar
oromediterráneo de Pinus nigra subsp. salzmannii. Invest. Agrar.: Sist. Recur. For. 12,
55-64.
TÍSCAR P.A., 2005. Situación actual del conocimiento sobre la regeneración del Pinus nigra
en la sierra de Cazorla y líneas de investigación futura. En: Los pinares de Pinus nigra
Arn. en España: ecología, uso y gestión. Fundación Conde del Valle de Salazar. pp. 535558.
TÍSCAR P.A., LUCAS M.E., TÍSCAR M.A., (2010). La alteración del suelo y la espesura
como factores de la regeneración de Pinus nigra subsp. salzmannii a lo largo de su área
de distribución. Revista Montes 103, 10-15.
Pinus Nigra Subsp. Salzmannii Forests from Southeast Spain: …
27
TÍSCAR P.A., RUIZ M.A., 2005. Relación entre la regeneración y la apertura del dosel
forestal en Pinus nigra Arn. ssp. salzmannii (Dunal) Franco. IV Congreso Forestal
Español, Zaragoza, 26-30 septiembre. Mesa temática 1.
TÍSCAR P.A.; 2007. Dinámica de regeneración de Pinus nigra subsp. salzmannii al sur de su
área de distribución: etapas, procesos y factores implicados. Inv. Agr.: Sist. Rec. For., 16:
124-135.
TRABAUD, L., CAMPANT, C., 1991. Difficulté de recolonisation naturelle du pin de
Salzmann Pinus nigra Arn. ssp. salzmannii (Dunal) Franco après incendie. Biological
Conservation 58:329-343.
VALLE F., GOMEZ F., MOTA J.F., DIAZ C., 1989. Guía botánico-ecológica del Parque
Natural de Cazorla, Seguras y Las Villas. Editorial Rueda, Madrid , 354 pp.
XIONG S., NILSSON C., 1999. The effects of plant litter on vegetation: a meta-analysis.
Journal of Ecology 87, 984-994.