Tree Physiology 34, 426–437
doi:10.1093/treephys/tpu022
Tree Physiology review
Ecophysiological variables influencing Aleppo pine seed and
cone production: a review
Abdelaziz Ayari1 and Mohamed Larbi Khouja
Institut National de Recherches en Génie Rural, Eaux et Forêts, BP 10, Rue Hedi Karray, Ariana 2080, Tunisie; 1Corresponding author ([email protected])
Received November 12, 2013; accepted February 18, 2014; published online April 8, 2014; handling Editor Jörg-Peter Schnitzler
The most interesting factors associated with seed and cone production of Aleppo pine were largely reviewed to identify
broad patterns and potential effectiveness of reforestation efforts and planning. Aleppo pine cone production and seed
yields are relatively variable, with differences between spatial and temporal influences. These differences are considered,
mainly between (i) year, (ii) stand characteristics and (iii) individual tree measurements. Annual variability among populations
was recorded for cone production per tree, based on influencing factors such as genetic characteristics, wetness, nutrient availability, insect pests and disease. In addition, some factors may affect Aleppo pine tree growth directly but may be
affecting seed and cone production indirectly. Therefore, reduced stand density results in less competition among Aleppo
pine trees and accompanying understory flora, which subsequently increases the stem diameter and other tree dimensions,
including seed production. This review suggests that reforestation planning, particularly thinning, will result in improved tree
morphology that will increase Aleppo pine seed and cone crops. Wildfire intensity and stand conditions such as light and soil
nutrient status are also examined.
Keywords: cone crops, forest productivity, fruit development, physiological responses, regulation factors, seed yields.
Introduction
Aleppo pine (Pinus halepensis Mill.) is a native Mediterranean
and North African indigenous species (Krugman and Jenkinson
1974). This species constitutes the natural widespread Pinus
forests in the Mediterranean region (Quezel 2000, Nathan
and Ne’eman 2004). During the last few decades, an historical
Mediterranean reforestation effort of Aleppo pine has shown
a wide and important rise in its forest densities (Matziris
1997, Bladé and Vallejo 2008, Rigolot et al. 2012). This has
resulted in an emphasis towards restoration of P. halepensis
forests to avoid wildfires, to re-establish stands and to promote associated wildlife (Sirois 2000, Bladé and Vallejo 2008,
Moya et al. 2008). The Aleppo pine is the most abundant
Pinus species in eastern Spain, northern Algeria and Tunisia,
but is dominated by other coniferous species in other areas
of the Mediterranean region (Nahal 1962, Quezel 2000). This
species (P. halepensis) is of interest in Tunisia because its
cones provide the only appropriate seed source used for many
human and forestry purposes (Sghaier et al. 1997, Nasri et al.
2004, Khouja et al. 2006, Sghaier and Ammari 2012).
Recent research has indicated that large-diameter trees of
P. halepensis are more seed and cone productive than trees
with smaller diameter (Ayari et al. 2012a). Reforestation efforts
in Mediterranean countries have focused on several coniferous species, of which Aleppo pine is the main species used for
recent plantations. Pinus halepensis does not occur in the North
African arid zone, but small reforestation efforts by plantations
were started in the last 50 years, which have required considerable investment. The main objectives of such efforts were to
limit desertification and to re-establish the native flora and fauna
(Middleton and Thomas 1997, Goberna et al. 2007). In Tunisia,
many research teams have promoted and initiated restoration
of P. halepensis forests (DGF 1995, 2010) and have started
© The Author 2014. Published by Oxford University Press. All rights reserved. For Permissions, please email: [email protected]
Factors influencing Aleppo pine seed and cone production 427
documenting the effects of restoration on the innovative status
of the forest ecosystem (Touchan et al. 2008, Jeddi et al. 2009).
Because of the minimal benefits of current plantation efforts
for food-seed producing species, such as P. halepensis (Ayari
et al. 2012c), Pinus pinaster and Pinus pinea, this review focuses
on what is known about cone production in P. halepensis in
order to determine possible innovations to promote improved
seed production.
Study species
Species world distribution
Natural discontinuous bands and large geographical distributions of Aleppo pine were recorded in the Mediterranean
region (Figure 1), covering ~3.5 million hectares (Quezel
1986). Aleppo pine forests range from southern France (45°N)
to northeastern Palestine (31°30′N) and from the southwest
high Atlas region of Morocco (9°E) to Lebanon, Syria and
Jordan in the east (36°E). In the Mediterranean basin, natural Aleppo forests grow at elevations ranging from sea level
to 2600 m above sea level, as confirmed in Morocco (Khouja
et al. 2000, Boulli et al. 2001, Ayari et al. 2012b). During the
19th century, P. halepensis was also introduced to the USA,
Australia, Venezuela and South Africa (Hall et al. 1997, Gibbs
et al. 1999, Spencer 2001, Hokche et al. 2008). The Aleppo
pine habitat is broadly characterized by warm and cold winters,
in addition to dry summers with periods of prolonged drought.
Annual precipitation of the Aleppo pine forest zone within the
Mediterranean region ranges from 200 to 1500 mm with an
optimal species spreading range from 350 to 750 mm (Quezel
1986).
Reproductive cycle
In its natural habitat and at an early growth stage from 4 to
18 years, seeds and cones of P. halepensis trees in the
Mediterranean region are initiated in mid- to late summer and
differentiate in September to October (Krugman and Jenkinson
1974, Owens and Blake 1985). Pollination occurs from April
to June the following year (Floret and Pontanier 1982, Khouja
1997), which is when pollen tube and ovule expansion starts
and proceeds until mid-summer (Gorenflot 1992, Roland et al.
1997). Reproductive expansion proceeds the following spring
when fertilization occurs under favourable conditions (Mugnozza
1986, Climent et al. 2008). This lengthy reproductive cycle
(~3 years) from embryo initiation to seed maturity (shown in
Figure 2) requires a complex range of interacting factors that
influence the quantity and quality of cones and seeds produced
by mature P. halepensis trees (Aussenac et al. 1982, Owens and
Blake 1985). However, Aleppo pine physiological performance
differences are not apparent in the published literature relating
vegetative growth and reproduction traits to physiological tree
status, mainly among ecological regions and provenances.
Seed and cone production variability
Aleppo seed cone production is variable, with three factors
that contribute to the variability: (i) years with or without abundant fructification (Moya et al. 2008); (ii) stand characteristics;
and (iii) individual tree dimensions (Goubitz et al. 2004, Moya
et al. 2008, Ayari et al. 2011a, 2012a). Several years of reports
have documented years with abundant seed and cone production and others years with insignificant production (Tapias
et al. 2001, Moya et al. 2008). Across its Mediterranean range,
abundant Aleppo pine seed and cone crops take place about
every 3–5 years (Climent et al. 2008, Paula et al. 2009, DGF
2010, Espelta et al. 2011). Variability in seed and cone production (Table 1) within an Aleppo pine forest has been frequently
reported (Ne’eman and Izhaki 1999, Goubitz et al. 2004, Ayari
et al. 2011b). Within the same Aleppo pine forest stand, seed
and cone production variability among individual trees can
also be significant, with specific trees being noted as massive
Figure 1. ​Aleppo pine forest distribution in the Mediterranean region (Quezel 2000).
Tree Physiology Online at http://www.treephys.oxfordjournals.org
428 Ayari and Khouja
Figure 2. ​Aleppo pine reproductive cycle, including seed and cone maturation (Khouja 1997).
Table 1. ​Cone characteristics, and seed and cone production (number and mass) in Aleppo pine Mediterranean forests.
Variable
Measurement results (country and experimental design)
Sources
Cone weight (g)
Wet weight 12.9–16 (Tunisia1), dry weight 21.0 (Tunisia1),
wet 30–77.2 g (Greece2), dry 27.2–70.2 g (Greece2)
66–116 (Greece1), 66.6 (Tunisia2), 73.7–87.4 (Algeria3),
90 (Spain4), 31.28–37.62 (Morocco5)
32–46 (Greece1), 45.1–56.2 (Algeria2), 30.5 (Tunisia3),
63.50–90.13 (Morocco4)
168 (at age 9 years), 155 (at age 10 years) (Greece1),
242 (Israel2), 113 (Tunisia3)
Control: 6202 (10 years)—27,175 (22 years), thinning:
475 (10 years)—10,892 (18 years) (Spain)
19.0 (Spain1), 15.7 (Tunisia2), 20.07–36.60 (Morocco3)
Nasri et al. (2004),1 Ayari et al. (2011a),1 Matziris
(1998)2
Matziris (1998),1 Ayari et al. (2011a),2 Harfouche et al.
(2003),3 Tapias et al. (2001),4 Boulli et al. (2001)5
Matziris (1998),1 Harfouche (2003),2 Ayari et al.
(2011a)3
Matziris (1997),1 Nathan et al. (1999),2 Ayari et al.
(2011a)3
Verkaik and Espelta (2006)
Cone length (mm)
Cone width (mm)
Cone no./tree
Cone no./tree
(cone per ha)
Seed weight (mg)
Weight 1000 seeds (g)
Weight 100 seeds (g)
Seed no./tree
Seed no./cone
1–3Corresponding
17.6–40.8 (Greece1), 21.47–35.54 (Morocco2)
15.8–22.6 g (Algeria)
10,290/tree/year (Israel)
72 (Israel1), 25 (3–62) (Greece2), 58 in Calaspara,
79 in Yest (Spain3)
country, study and research authors.
Tree Physiology Volume 34, 2014
Tapias et al. (2001),1 Ayari et al. (2011a),2 Boulli et al.
(2001)3
Matziris (1998),1 Boulli et al. (2001)2
Harfouche et al. (2003)
Nathan et al. (1999)
Nathan et al. (1999),1 Matziris (1998),2 Moya et al.
(2008)3
Factors influencing Aleppo pine seed and cone production 429
producers (Climent et al. 2008, Ayari et al. 2012b). Across its
natural Mediterranean distribution range, Climent et al. (2008)
observed that Aleppo pine trees have an increasing reproductive allocation from east (Greece) to west (Spain), with a
smaller increase from north to south (Tunisia).
Regulation of seed and cone production
The 3 year development of a mature Aleppo pine cone provides numerous opportunities for a major maternal role in seed
and cone production through interactions between the ovule
and pollen to produce the diploid embryo, which is sometimes
aborted (Gorenflot 1992). However, Aleppo pine cone production can be decreased by pests, such as insects or other vectors (Goubitz et al. 2002, Climent et al. 2008), where previous
research showed that the cone abortion rate for the species
ranges from 40 to 60% (Girard et al. 2012). The volume of the
mature cones depends on environmental conditions and pine
tree size (Ayari et al. 2012a), where larger cone sizes and a
higher number of sound cones correlate with higher seed quality (Nathan et al. 1999, Moya et al. 2008). Years with abundant cone production are also excellent years for sound and
filled seed yields (Goubitz et al. 2004, Climent et al. 2008).
Conversely, Aleppo pine under stressed environmental conditions, such as limited nutrient resources (Climent et al. 2008),
severe drought (Ayari et al. 2011a, 2011c) or cold winters
(Vennetier et al. 2011), produce low seed yields. In fact, the
extremely low seed yields are due to high cone abortion rates
(Ne’eman et al. 2011) at early stages of cone growth, and later
to low cone survival rates (Girard et al. 2012). Tree morphology is also important for successful fruiting, because the most
abundant cones were observed at the top and next in the middle of the tree crown (Ayari et al. 2012a, Girard et al. 2012).
Under poor weather conditions, high cone abortion rates have
been reported in the top and middle crown positions due to a
direct influence on flowering or pre-initiated cone buds (Girard
et al. 2012). An adaptive shift of vegetative growth or reproductive bud initiation can be employed during times of physiological stress, which further explains these trends. Similarly,
Aleppo pine embryo abortions rates reflect several interacting
factors associated with pollination, such as climate stress and
stand density added to tree health (Owens and Blake 1985,
Karlsson and Orlander 2002).
Factors affecting cone crops
Climate-related factors
Annual rainfall and forest wetness Little information was
found on the influences of annual rainfall and moisture on seed
and cone production of Aleppo pine, as well as for other coniferous species (Owens and Blake 1985, Pardos et al. 2003).
Recent research work showed a positive correlation with the
average precipitation recorded during the 3 years of Aleppo
pine cone development (Ayari et al. 2011c). Subsequent
research reported positive effects of the average 3-year rainfall
on seed number and seed mass per cone (Ayari et al. 2012b).
Furthermore, previous physiological findings (El-Aouni 1980,
Climent et al. 2008) showed that Aleppo pine vegetative growth
and reproductive features depend on ecophysiological patterns and resource allocation. Thus, abundant fructification in
Tunisia was observed in wet years, whereas a reduced rate was
recorded in dry years, such as in 1993 (Khouja 1997). Similarly,
poor resources favour an early reproduction while abundant
resources enhance vegetative growth (Climent et al. 2008).
During times of water stress, nutrients and water are often preferentially diverted to cone bud initiation, whereas formation of
new roots, bark, needles and wood is limited due to the lack of
nutrients and water (Forest Products Laboratory 1987). Similar
patterns of seed and cone production were noted with other
Pinus species by comparing the effects of temperature, rainfall
and sunlight days on cone bud initiation under conditions of limited soil resources (Dewers and Moehring 1970, Owens and
Blake 1985, Pardos et al. 2003).
Temperature influences Annual cone and seed crops are associated with temperature during the Aleppo pine fruiting cycle
(Pardos et al. 2003, Girard et al. 2012), as long as other environmental conditions are favourable and nutrients are available
(Thanos and Daskalakou 2000, Climent et al. 2008, Saunders
et al. 2012). Aleppo pine trees in Mediterranean countries have
maintained normal growth and other physiological processes
despite warming and drying across the whole region (Brochiero
et al. 1999, Maseyk et al. 2007, Rotenberg and Yakir 2011).
Previous physiological research in Tunisia estimated an Aleppo
pine growth period of ~167 days per year, which is relatively
longer in comparison with other Mediterranean pines such as
P. pinea, P. pinaster and P. radiata (Khouja 1997). During the
growing period, the species allocates a great proportion of the
photosynthetic assimilate to growth (El-Aouni 1980). Indeed,
the Aleppo pine exhibits the most rapid growth mainly in spring,
then slow growth in summer, and remains latent during autumn
and winter (Aramini et al. 2007, Del Campo et al. 2011, Monnier
et al. 2012). Over the last 20 years in Tunisia, total average temperatures for April and May have been >17 °C, and larger cone
crops were recorded (Jalel 2004). Recent research demonstrated the absence of any temperature effects in Aleppo pine
cone production (Ayari et al. 2012b). Seasonal temperature
fluctuations, such as hot and dry winters, cold winter temperatures, or in late spring variations, might negate seed and cone
crops in coniferous species by killing the second-year conelets
(Sorensen and Miles 1974, Owens and Blake 1985). Indeed,
decreasing photosynthesis in forest trees can be explained by
several climate change stresses, such as water deficits, extreme
temperature fluctuations and nutrient deficiencies (Méthy et al.
Tree Physiology Online at http://www.treephys.oxfordjournals.org
430 Ayari and Khouja
1994). This result is amplified by the negative effects of longterm exposure to elevated ozone (O3) levels, which reduces forest tree growth and reproductive rates (Matyssek et al. 2007).
Stand-related factors
Stand density Aleppo pine seed and cone production is negatively influenced by increasing stand density, whereas the basal
area of the forest site has the opposite influence (Table 2).
Several previous studies showed a positive influence on seed
and cone production after any management effort leading to
decreased stand density of Aleppo pine forests (Goubitz et al.
2004, Espelta and Verkaik 2007, Moya et al. 2008, 2009,
Ayari et al. 2012a). In Tunisia, the assessment of 79 Aleppo
pine forests showed that seed/cone number (rseed < −0.418,
rcone < −0.471 (P < 0.001)) and seed/cone mass production
(rseed < −0.451, rcone < −0.482 (P < 0.001)) were negatively
correlated to stand density (Ayari et al. 2011c). Therefore, a
flexible role of the stand density may influence the species
flowering rate by its subsequent effect on resource availability
and pollen quantity, which differ between years and individual
trees (Goubitz et al. 2002). Aleppo pine is a monoecious and
wind-pollinated coniferous tree (Krugman and Jenkinson 1974)
showing a link between seed production and resource availability, which characterizes several wind-pollinated tree species
(Allen and Platt 1990, Sork et al. 1993, Knapp et al. 2001).
Forest thinning efforts have many benefits, such as reducing
wildfire and enhancing biodiversity, as well as improving the
growth and productivity of the main species within the stand
(Gorte and Bracmort 2007, Turner et al. 2007, MacDonald et al.
2010). In Pinus forests, density reductions can also increase
soil moisture availability (Sucoff and Hong 1974, Teskey et al.
1987, Powers et al. 2010), and subsequently tree physiological responses, such as photosynthetic carbon assimilation
rates and stomatal conductance (McDowell et al. 2006, Bladon
et al. 2007). Likewise, after thinning treatments, the tree stem
diameter, total height and crown development of Pinus species
within the forest are improved (Latham and Tappeiner 2002,
López-Serrano et al. 2005, Prévosto et al. 2011, Adamopoulos
et al. 2012, Ruano et al. 2013). Furthermore, Aleppo pine tree
morphology (e.g., trunk diameter, height and crown size) is
always significantly coupled with cone production (Ayari et al.
2012a), and its annual increment is improved once thinning is
applied within a forest stand. In Tunisia, native Aleppo pine forests at low density grew faster in diameter and height than
those at high density (Sghaier and Ammari 2012). Aleppo
pine trees of larger trunk diameter produce massive cones
(Ayari et al. 2011c), therefore increased seed and cone production may be the greatest advantage of thinning treatments
(Ayari et al. 2012c). Analogous thinning advantages were also
reported for other coniferous species (Mencuccini et al. 1995,
Arista and Talavera 1996, Gilmore 2003, Ordonez et al. 2005,
Blanco et al. 2009, Horner et al. 2010).
Similarly, once Aleppo pine forest stands are thinned, there
are increases in light, which increases photosynthesis per tree
(Spiecker 2000, Climent et al. 2008). Thus, competition for
light in Pinus forests is a key limiting factor to productivity.
Later, the consequence of increased light penetration after
stands are thinned increases the forest productivity (Saunders
et al. 2012, Ruiz-Mirazo and Gonzalez-Rebollar 2013). In fact,
previous work showed that after thinning Aleppo pine or other
forest species (i.e. Picea abies (L.)), increases in light reaching the trees led to increases in nutrient storage (Hasenauer
and Sterba 2000, Spiecker 2000). Furthermore, the scientific
forest literature suggests that the ecophysiological status of
Pinus species, including Aleppo pine, is commonly dependent
on light as well as on water and nutrient availability (Naumburg
and DeWald 1999, Darabant et al. 2001, Ruano et al. 2009,
Zhang et al. 2012). Both photosynthetic activities and stomatal conductance vary among forest coniferous tree species (Delzon and Loustau 2005, Chavez et al. 2011), based
on the amount of light being received, site quality, individual
tree age, CO2, vapour pressure deficits between needles and
atmosphere, O3 levels and hormones that adjust the aperture
of stomata (Maier 2001, Matsumoto et al. 2005). Moreover,
in some Pinus thinned forests (e.g., P. sylvestris), the upper
crown location had twice the cone production in comparison to
cone number being produced on the lower crown position with
lower light availability (Karlsson and Orlander 2002), but this
Table 2. ​Influence of the site geo-position, site density and basal area on Aleppo pine seed and cone production.
Variable
Results (country and experimental design)
Sources
Stand geography
Positive correlation between longitude and weight of 100 seeds
(0.43, Algeria1), weight of 1000 seeds (0.776, Morocco2), weight of
1000 seeds (0.71, Tunisia3)
Negative correlation between latitude and weight of 1000 seeds
(−0.820, Morocco1), weight of 1000 seeds (−0.500, Tunisia2)
Positive correlation between altitude and weight of 1000 seeds
(0.630, Morocco1), weight of 1000 seeds (0.730, Tunisia2)
Negative correlation between density and seed yield or cone crop
(Tunisia1). Basal area had a positive influence on seed cone production
(Tunisia,1 Italy,2 Spain3)
Harfouche et al. (2003),1 Boulli et al.
(2001),2 Khouja and Sghaier (2000),3
Nasri et al. (2004)3
Boulli et al. (2001),1 Khouja and Sghaier
(2000),2 Nasri et al. (2004)2
Boulli et al. (2001),1 Khouja and Sghaier
(2000),2 Nasri et al. (2004)2
Ayari et al. (2011a, 2012a)1, Mencuccini
et al. (1995),2 Arista and Talavera (1996)3
Stand density and
basal area
1–3Corresponding
country, study and research authors.
Tree Physiology Volume 34, 2014
Factors influencing Aleppo pine seed and cone production 431
was not always the case in Aleppo pine stands (Girard et al.
2012). Nutrients and light maintain appropriate physiological
responses for isolated individual trees in open forest stands,
which positively influence growth rates and successful reproduction processes (Bladon et al. 2007, Roberts and Harrington
2008).
Nutrient availability and fertilizers Tree growth and biomass
production depend on the availability of nutrients in the soil
(Gallardo et al. 2003, Moya et al. 2007). Nutrient recruitment
varies by species, age, and nutritional and physiological status
of the individual trees. Previous findings showed that nitrogen,
calcium, potassium, phosphorus and magnesium are most often
measured and identified throughout Pinus tree organs (Del
Campo et al. 2011). The lack of any elements can negatively
affect tree growth and physiological activities (Kramer and
Kozlowski 1979, Gallardo et al. 2003). Therefore, a nitrogen
deficiency leads to needle chlorosis, explained by disturbed
metabolism of chlorophyll and cytochrome (Grebner et al.
2013). Likewise, needle chlorosis is often due to a magnesium
deficit, while any deficiencies of phosphorus and potassium can
hinder the tree growth and affect photosynthesis, respectively
(Kramer and Kozlowski 1979). Furthermore, a lack of calcium
has negative influences on cell wall and root tip growth. Similar
disturbances on physiological tree responses are also observed
with deficiencies of other micronutrients, such as boron, iron,
manganese, zinc, copper and molybdenum (Kramer and
Kozlowski 1979, Lehto et al. 2010).
Plant communities require resources (e.g., water and nutrients) to maintain their growth and reproduction, mainly in the
juvenile phase (Cuesta et al. 2010a, 2010b). Therefore, the
trade-off in nutrients stored for remobilization between plant
organs increases during establishment of severe environmental
circumstances (Obeso 2002). Furthermore, in plant development, the influence of increased nutrients has positive effects
on organ function (Goubitz et al. 2002, Karlsson and Orlander
2002, Moya et al. 2007). Moreover, once nutrients and water
are available there is improved seed and cone production in
Pinus stands (Owens and Blake 1985, Way 2006, Roberts and
Harrington 2008, Zhang et al. 2012). Previous reports from
the northern USA have shown that nutrient availability plays a
major role in the growth of Pinus species, but it remained less
significant than light effects (Lieffers and Stadt 1994, Finzi
and Canham 2000), which is due to the competition between
species and understory vegetation (Darabant et al. 2001).
Similarly, in the USA, the number of Pinus trees bearing cones
was always higher in stands with high fertilizer levels than in
unfertilized forest sites (Heidmann 1983).
Fire effects Recent Mediterranean reports have documented
increases in fire frequency affecting Aleppo pine forests during the last few decades, mainly in Spain, Italy and Greece
(Saracino et al. 1997, Andriopoulos and Arianoustou 2004, De
Marco et al. 2004, De las Heras et al. 2007, Moya et al. 2008).
However, within the forest stands, frequently plant regeneration
for either Aleppo pine or the understory vegetation is related
to their physiological traits and also influenced to fire regime
(Andriopoulos and Arianoustou 2004, Iglesias 2010). Aleppo
pine is a fire-resilient species, characterized by its high rate of
production of serotinous cones with a significant proportion
of filled seeds, if there are no adverse weather conditions and
there is availability of viable pollen (Nathan et al. 1999, Thanos
2000, Thanos and Daskalakou 2000). Individual trees with a
greater canopy seed bank have shown high post-fire seedling
production due to the stored seeds in cones after maturation
(Nathan et al. 1999, Ne’eman and Izhaki 1999). Thus, species
regeneration may depend on the availability of viable seeds
within the burned area where seeds come from serotinous
mature cones but are not killed by fire, or from the soil seed
bank (Thanos and Daskalakou 2000, Moya et al. 2008). Postfire forest rehabilitation showed increases in Aleppo pine stem
density, whereas from recent published work it is obvious that
thinning enhances early species regeneration (De las Heras
et al. 2007) and later its seed and cone production (Moya
et al. 2008). The effect of wildfire on Aleppo pine ecosystems
is complex and may be advantageous or not, while depending
on nutrient status of the stands, timing and rigorousness of
the burn (Nathan et al. 1999, Thanos 2000, Andriopoulos and
Arianoustou 2004).
Fire influences on cone and seed production may also be
evaluated by its effects on tree development since larger
trunk diameter trees have higher rates of cone production
and seed yields (González-Ochoa et al. 2004, Verkaik and
Espelta 2006, Haymes and Fox 2012). However, earlier
research showed a markedly reduced crown fire risk when fire
occurred in thinned young and dense stands with previously
constructed fire-breaks (Agee et al. 2000, Ruiz-Mirazo and
Gonzalez-Rebollar 2013). Likewise, after fires, pine species
have a life strategy of producing serotinous cones which facilitate recolonization (Moya et al. 2008). However, the relevant
regeneration rate in pine stands is associated with increased
resistance to pests (Petrakis et al. 2004), which may afterwards influence growth and seed yields via climatic conditions
(Climent et al. 2008). Nonetheless, for Aleppo pine, the effect
of fire on nutrient availability will be quickly evident on its seed
and cone production (Espelta and Verkaik 2007). Therefore,
when fire eliminates the understory flora, not only does the
ash contain micro- and macronutrients, but the reduction
in competition increases resource availability (Bladé and
Vallejo 2008).
Individual tree characteristics
Tree morphology In pine trees, including Aleppo pine, heavy
yearly seed and cone crops are produced by the trees with the
Tree Physiology Online at http://www.treephys.oxfordjournals.org
432 Ayari and Khouja
largest trunk diameters (Karlsson and Orlander 2002, Climent
et al. 2008, Ayari et al. 2012a). Likewise, recent research on
Aleppo pine trees growing in different climatic zones of Tunisia
showed that trunk diameter and crown height were better
parameters to predict seed and cone production within the
forest stands, while other significant correlations were also
detected with crown diameter, tree total height and age (Ayari
et al. 2012a). Consequently, we counted 250 cones per average Aleppo pine tree containing ~400 g of seeds in forests
having a trunk diameter > 35 cm, and a crown dimension of
at least 8 m in height and 4 m in diameter (Ayari et al. 2011c).
Seeds from Aleppo pine forests are estimated to annually earn
about 3 million US dollars (Ayari et al. 2012c). At an early
growth stage of Aleppo pine in Greece, there are no significant
relationships between cone production and either tree height
or crown measurements (Matziris 1997). Likewise, in southern
France, the frequency of cone crops is related to tree crown
position (Girard et al. 2012), and larger cones often contain
more and larger seeds (Bladé and Vallejo 2008, Ayari et al.
2011a). In the Mediterranean regions, Tunisian Aleppo pine
trees produced more cones and seeds compared with other
forest tree species (Climent et al. 2008). Recent research
showed that Aleppo pine seed and cone production in Tunisia
increased linearly with diameter, height (Table 3) and crown
volume (Goubitz et al. 2004, Ayari et al. 2012a). Similarly, the
species seed and cone production increased with age up to
14 years, but the rate of increase was smaller among older trees
(Ayari et al. 2012a). Likewise, within the forest stands, dominant trees with the biggest crowns tend to be more productive
than trees with co-dominant or lower canopy cover (Ayari et al.
2011b). In fact, all tree morphology parameters have significant
effects on Aleppo seed and cone crops (Ordonez et al. 2005),
but additional research will lead to a better understanding of
their influence and their interactions with other variables that
affect the species production rate.
Tree competition The largest Aleppo pine seeds and cones
produced are recorded within open stands and isolated trees
that are not competing for nutrition, water or solar radiation
(Goubitz et al. 2004, Espelta and Verkaik 2007, Ayari et al.
2012a). Several studies have documented the negative effects
of competition on reproduction and vegetative growth due to
scarce resource availability and the interference among tree
crowns (Thanos and Daskalakou 2000). Therefore, decreasing stand densities may encourage fruit production earlier by
better wind pollination and reducing competition for resource
availability (Grayson et al. 2004, Bladé and Vallejo 2008).
Earlier studies showed that some conifers, such as species
of Pinus or Picea, tend to develop male cones or femaleness
according to stand density, where low densities tend to encourage fructification (Arista and Talavera 1997). Later, Ayari et al.
(2012b) demonstrated that Tunisian Aleppo pines should be
twice as productive in seeds and cones when stand density is
decreased from 1000 to 250 trees ha−1. However, Aleppo pine
seedlings of unthinned or high stand densities have higher survival ability (Climent et al. 2008, Cuesta et al. 2011, Osem et al.
2013). Additionally, a reduced growth rate was explained by
greater insect damage (De las Heras et al. 2012, Tamir 2013).
Moreover, Aleppo pine growth and reproduction may also be
affected by competition with the understory shrub layer for
resources other than light. However, only a few studies have
been undertaken in this respect for Aleppo pine forests.
Genetics attitude Coniferous tree characteristics are determined by genetics, environmental conditions and the interaction
between the two (Khouja 1997, Harfouche et al. 2003, Louzada
2003, Tsukaya 2005). For Pinus species, the prevalent research
worldwide has been carried out in planted forest sites or seed
orchards from a forestry perspective rather than a multidisciplinary natural science approach (Goubitz et al. 2002, Aguiar
et al. 2003, Mason and Conolly 2013). Aleppo pine genetic differences were assumed in Greek forests when it was deduced
that flowering and cone production are under strong genetic
control (Matziris 1997). Within the same stand, a few Aleppo
pine trees produced abundant cone crops and they were genetically distinct from those that did not (Matziris 1998, Climent
et al. 2008). Aleppo pine genetic clone plantations in Greece
showed that seed cone production has a strong genetic component (Matziris 1993). Similarly, within the studied Aleppo pines
in Algerian forests, Harfouche et al. (2003) showed that stands
Table 3. ​Influences of tree size and crown measurements on Aleppo pine cone seed production.
Variables
Results (country and experimental design)
Sources
Tree size
Seed and cone production increased with an increase in tree height,
DBH and age (Tunisia1)
The level of cone serotiny decreased with an increase in tree height
(Israel,2 Spain3)
Seed and cone production increased with an increase in tree crown
height and tree crown diameter (Tunisia,1 France2)
Coniferous trees canopy and forest structure can have an influence
on coning with the majority of cones borne on dominant or opengrown trees (Scotland3)
Ayari et al. (2011c),1 Goubitz et al. 2004,2 Moya
et al. (2008),3 Verkaik and Espelta (2006)3
Tree crown
dimensions
1–3Corresponding
country, study and authors. DBH, diameter at breast height.
Tree Physiology Volume 34, 2014
Ayari et al. (2012a),1 Girard et al. (2012)2
Malcolm et al. (2001)3
Factors influencing Aleppo pine seed and cone production 433
were not greatly differentiated from each other. However, the
latter research team confirmed the possibility of gene migration
by pollen or seeds and common pools of genotype would be
shared if the distance between stands were small.
Insects and pests as factors affecting seed
and cone loss
Native pine forests worldwide host many insect species (Graf
and Mzibri 1994) and Mediterranean Aleppo pine trees host a
large proportion of them (Ben Jamaâ 2007). Several tools have
been used to discover and capture damaging insects (insect
pests) within pine species (Khous and Gachi 1996, Chatenet
2000). Recent studies have described >50 insect species on
Aleppo pine forests in Tunisia and Algeria (Chakali 1996, Ben
Jamaa et al. 2000, Chatenet 2000). Coleopteran insects are
present in forests of both countries, with >30 species having
different diets (Chakali 2006). Roques (1983) established an
extensive list of insect pests of seeds and cones in France.
However, within Mediterranean pine forests, numerous insects
are associated with buds, pollen, seeds, cones, bark and tree
needles (Chatenet 2000). Ben Jamaa et al. (2000) and Chakali
(2005) have highlighted serious insect pests of Aleppo pine
trees in semi-arid areas, such as Tomicus destruens. Similarly, the
cited studies showed that Coleoptera and Lepidoptera are the
most important insects discovered within these forests. Insect
pests seem to have the largest impact in Mediterranean forests (Ben Jamaâ 2007, Jactel et al. 2011), and can cause either
extensive damage to tree needles and bark or destroy high proportions of seed and cone crops (Jactel et al. 2009, FBD 2012).
As with insects, numerous diseases of pine forests can
decrease seed cone production directly or indirectly by damaging tree health (CABI 2002, Sturrock et al. 2011). Many
fungal diseases are widespread in Aleppo pine trees such as
Coleosporium inulae, which can seriously damage the foliage in
young Aleppo pine plantations (Magnani 1974), and Sirococcus
strobilinus, which causes bud death (Munoz-Lopez 1997).
Among forest trees, the parasite impairs growth and usually
decreases seed yields and viability (CABI 2002). Pine processionary moth (Thaumetopoea pityocampa) is the most serious
foliage disease in Aleppo pines and may slow down the growth
of mature trees and occasionally kill them (Ciesla 2004, Ben
Jamaâ 2007, Vallejo et al. 2012). Similarly, animals such as
squirrels destroy cone crops and consume large quantities of
seeds (Parchman et al. 2006, Smith and Benkman 2007).
Conclusion
Climate change and reforestation efforts in natural stands
influence Aleppo pine forest structure and dynamics, regeneration rate and resilience to fire, in addition to cone and seed
production. Following fire in Aleppo pine forest stands, the
germination rate is regularly high, which is influenced by the
availability of viable seeds either in the soil seed bank or in the
serotinous mature cones on trees. Significant soil seed banks
could be related to loss of factors, such as seed consumption
by predators (e.g., squirrels, reptiles, mice and ants). Similarly,
high viable seed contents in serotinous mature cones on the
tree can be explained by low cone damage rates by fire, pests
and insects. Previous research on Aleppo pine and other Pinus
species suggests that thinning enhances growth and seed
and cone production through reduced disease and pests, in
addition to better resource availability including light, nutrients and water. Within limited environmental conditions and
resource availability, several physiological disturbances are
manifest throughout the growth and reproduction periods.
Likewise, under stressed conditions, thinning treatments show
larger rates of ovule abortion. These have been shown to be
strongly related to seed and cone crop production. Wildfire
effects combined with thinning treatments lead to improved
tree health, growth, and better seed and cone production in
Aleppo pine forests. Therefore, climate and genetics may influence the seed and cone production in natural Aleppo pine
stands. However, seed yield is increased in larger trees with
larger crown size.
Acknowledgments
The authors thank all the Mediterranean forestry research colleagues for their cooperation, comments and help. Two anonymous reviewers, in addition to Dr Ram Oren and Dr Jörg-Peter
Schnitzler, are acknowledged for their useful suggestions on
the first draft. Special thanks to Prof. Scott O. Rogers (from
Bowling Green State University, OH, USA) for a review of the
manuscript and language editing.
Conflict of interest
None declared.
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