Introduction 

Aleppo pine (Pinus halepensis Mill.) is a widespread tree species whose natural range is limited to the Mediterranean basin ([65] - Fig. 1). In total, it covers an area of approximately 3.5 million hectares of natural and reforested stands ([63], [53]). Aleppo pine is well represented in the mountainous massifs of the Maghreb countries, where it spreads over 65,000 ha in Morocco (in the Rif, and the Middle and High Atlas) and 370,000 ha in Tunisia ([24] - Fig. 2). In Algeria, the species covers 35% of the wooded areas in the north, that is, approximately 800,000 ha ([8]). Aleppo pine is mainly found as natural stands in the eastern and central regions of the country, mainly in the Tellian and Saharan Atlas Mountains. The main forests are distributed on the ridges of the Saharan Atlas at altitudes between 1000 and 1500 m a.s.l. ([38]).

Fig. 1 - Natural range of P. halepensis ([16]).

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Fig. 2 - Aleppo pine tree.

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In Europe, the largest area covered by Aleppo pine forests is on the Mediterranean coast of Spain, where it forms pure stands of 1.046.978 ha and covers 497.709 ha in mixed stands with other species ([50]). In France, P. halepensis is found on the limestone hills of the coastal zone from Nice to the Italian border, with a surface area of 202,000 ha ([19]). In Italy, Aleppo pine is not very abundant (~20,000 ha), but it may be found in large populations in Southern Apulia and in a few localities in Sardinia and Sicily.

Aleppo pine is one of the most common species in the Mediterranean region, where it forms stands generally found at low altitudes (< 500 m a.s.l.) and along the coasts ([27]) in dry and warm environments ([53]). In Aleppo pine forests, nutrient cycling is influenced by litterfall and silvicultural practices ([79]). The species is characterized by a high production of seeds with a great capacity of natural dispersion, thus favoring the regeneration and expansion in suitable habitats. In Northern Africa, management practices seek to improve the seed and wood productivity of Aleppo pine trees ([37]). Indeed, Aleppo pine seeds are widely consumed in North Africa ([37]) and are used in the preparation of creams and cakes in many Arab countries. In addition, juice made from fermented seeds is used to prepare a traditional pudding ([49]). Therefore, the production of Aleppo pine seeds represents an important issue for the sustainable development and improvement of living standards of the people relying on these resources. Further, through the marketing of its seeds, Aleppo pine contributes to the livelihoods, food security, and improvement of the economy of the local population in rural areas of North Africa. It also provides an important economic safety net for the local population over a long period of the year ([85]). Hence, Aleppo pine has a high socio-economic value in such regions, where seed collection and timber harvest also provide employment for local workers. For all the above reasons, the reforestation of degraded areas in less developed countries should focus on Aleppo pine ([36]). The protection of Aleppo pine forests is essential for combating desertification and providing local communities with essential services ([35]).

The Aleppo pine forests in the Mediterranean zone are increasing in terms of area and biomass, and represent an important source of bioenergy as they offer an opportunity to mobilize woody matter, thereby contributing to the prevention and reduction of forest fires in the context of climate change and energy transition ([43]).

The relationship between Aleppo pine and climatic factors is modulated by local conditions, especially the soil. Stable stands are mostly located on sandstone substrates ([76]). Tree-ring analysis has shown that exposure, altitude, and topographic position are determinants of pine growth ([32]). The wood of Aleppo pine has high dimensional stability and high compressive strength ([27]). For centuries, Aleppo pine forests have been subjected to strong human pressures (clearings, illegal cuttings, fires, and grazing), causing the regression of the vegetation cover. The maintenance of Aleppo pine stands subjected to continuous degradation for several decades is currently a major ecological issue ([32]).

In addition, in recent years, the Aleppo pine has been the main reforestation species used in degraded areas in several countries, owing to its plasticity and resistance to drought conditions; it is even able to colonize degraded and dry limestone soils. In adult stands with regular fruiting, the natural regeneration of Aleppo pine after wildfire passage is fairly common ([11], [80]). Indeed, it has been noticed that after fire, Aleppo pine forests often undergo a massive regeneration, sometimes extending over large areas with a density of several tens of thousands of seedlings per hectare ([10], [84], [75]). This phenomenon has been the subject of numerous studies in various regions of the Mediterranean Basin ([1], [46]), which highlighted the rapid recolonization of burnt areas because of the great natural regeneration ability of pine. It also appears that natural regeneration is ensured by a large number of fertile seeds released from old (4 years and older), indehiscent cones known as “serotinous cones”, which are ejected by the thermal shock caused by fire ([1]).

The objective of this work was to review the production of Aleppo pine with regard to biomass, growth, and capacity for regeneration. Finally, we reviewed recent findings on the use of P. halepensis as rootstock in grafting operations and discuss its main advantages.

  Materials and methods 

Paper published between 1970 and 2021 were collected from Clarivate Web of Science®, Scopus®, and Science Direct®. The keywords used were “Aleppo pine stand”, “biomass”, “radial growth”, “regeneration”, “grafting”, and “arid land”. In addition, some doctoral thesis reports were consulted. The search results were refined based on the title and abstract of papers. After combining the relevant articles and all abstracts were scrutinized, the final database included 93 studies. The selected papers fulfilled the following criteria: (i) the study was published in English language; (ii) the scope of the study was biomass production in Aleppo pine stands.

  Aboveground biomass of Aleppo pine forests 

Smiris et al. ([83]) showed that the determination of the biomass distribution in Aleppo pine stands is important for their effective management, and for planning conservation strategies and ecosystem valorisation as well. Allometric models help estimate biomass or volumes based on the dendrometric parameters of sample trees ([44], [74]). In a study on P. halepensis biomass production in Mediterranean countries, Alfaro-Sánchez et al. ([3]) reported that biomass production varies depending on local climate, stand age, and density of forest stands. Tree crowns represent the largest amount of biomass in Aleppo pine stands, followed by the root system and the stem biomass. Tab. 1 summarizes the biomass models used in Greece and Spain for Aleppo pine. According to Smiris et al. ([83]), young (23-year-old) Aleppo pine stands have a productivity of 17.55 t ha^-1 of biomass, which becomes 764.86 t ha^-1 at the age of 48 years, 1192.24 t ha^-1 at the age of 70 years, and finally 1406.21 t ha^-1 at the age of 100 years. In this context, López-Serrano et al. ([44]) showed that biomass production varies significantly with age and environmental conditions. The average residual biomass of a P. halepensis forest is 33.55 t ha^-1, but the standard deviation between plots has been estimated at 134.23 t ha^-1 ([25]). Furthermore, Alfaro-Sánchez et al. ([3]) stated that climatic conditions are the main limiting factor for biomass production in Aleppo pine forests, showing that thinning practices play an important role in improving the biomass production of the stands. These evidences can help managers of forest ecosystems to assess the biomass, and determine the climatic and environmental factors influencing biomass production.

  Radial growth of Aleppo pine 

In recent decades, pine stands have been significantly affected by climate change worldwide ([4], [41], [45]), showing dieback, tree mortality, and a decrease in growth owing to long, severe, and repeated droughts ([13]). Camarero et al. ([14]) studied the effects of climate change on 32 P. halepensis forests using a dendroclimatological approach and found that the growth of Aleppo pine significantly increased in the more humid sites. Notably, Aleppo pine exploits the water available in the soil during cool seasons, especially in winter and autumn, in the absence of other limiting environmental factors ([28]). These authors indicated that in the adult stage, Aleppo pine is very resistant and plastic in its response to adverse environmental conditions, and it is able to modulate the physiological activity according to environmental and seasonal conditions. Indeed, active growth has been recorded during spring and autumn, which are suitable seasons for growth of this species in the presence of favorable temperature and soil water availability ([28]). This behavior is more noticeable in coastal ecosystems than in continental ecosystems ([60]). On the other hand, Aleppo pine is resistant to drought and unfavorable environmental conditions, and it is able to recover from the effects of drought when environmental conditions improve. For example, Gazol et al. ([29]) showed that Aleppo pine is able to uptake water from the soil during rainy seasons, thus presenting good growth performance in autumn and winter. This strategy allows Aleppo pine to successfully colonize nutrient-poor, abandoned, and dry lands ([17]). These authors concluded that Aleppo pine can form stands resilient to drought while adding ecological value to the forest in terms of production and protection.

Novak et al. ([55]) studied intra-annual density fluctuations (IADF) in the rings of P. halepensis, finding that IADF formation occurs under favorable conditions in autumn, and it is not related to stressful summer conditions. Novak et al. ([54]) suggested that IADF formation reflects the plasticity of Aleppo pine and its ability to resume cambial activity after summer drought. Sarmoum et al. ([76]) recorded a high variation in tree ring width among years even within the same stand. De Luis et al. ([21]) noted that in the young stage, Aleppo pine show great plasticity in wood formation under the effect of drought. Additionally, Olivar et al. ([57]) found that the radial growth of Aleppo pine was mainly influenced by rainfall. Similar results have been reported by Sarmoum et al. ([76]). Camarero et al. ([14]) studied the effect of environmental factors on the growth of P. halepensis stands and noted that their radial growth is related to the availability of water in the soil during previous wet seasons, namely previous spring and winter ([87], [18]). This result is similar to that of Olivar et al. ([57]), who reported that the growth of P. halepensis is controlled by soil water availability throughout the year. In light of the above studies, Aleppo pine is a promising species to be used in reforestation in the Mediterranean areas which are characterized by a high variability in annual rainfall, and shows many advantages thanks to its plasticity and response to climatic conditions ([33]). Guit & Nedjimi ([32]) showed that the physical environmental parameters have a significant effect on the growth of Aleppo pine, and the radial growth is an indicator of the performance of trees that are resistant to climate change. These positive relationships are explained by the high water requirement during the formation of tree rings ([61]). Olivar et al. ([57]) showed that precipitation during spring and summer has a positive effect on the radial growth of Aleppo pine. These results corroborate those of Raventós et al. ([67]) who found that, in the semi-arid climate of the Mediterranean zone, rainfall amount is the main factor that positively influences pine tree growth. Similarly, Bouachir et al. ([9]) found that the amount of precipitation in winter and spring influenced the radial growth of Aleppo pine trees in Northern Africa. Other studies on tree-ring growth in Mediterranean regions have confirmed these results ([67], [26], [15], [66], [47]). Contrastingly, Battipaglia et al. ([6]) reported that radial growth is significantly related to summer rainfall. Touchan et al. ([87]) reported that the amount of precipitation in winter and spring have positive effects on the growth of the Aleppo pine. According to De Luis et al. ([20]), the response functions of P. halepensis in the Mediterranean region revealed that temperature has a positive correlation with the tree-ring growth of Aleppo pine towards the northern limit of its geographical site and a negative correlation towards the southern limit. The results of Meko et al. ([48]) were similar to those of Touchan et al. ([87]) on the growth of Aleppo pine in the Mediterranean area, which showed that winter, spring, and summer precipitation positively influence the growth of the species, whereas species growth and summer temperature had a negative relationship ([87]). The most significant radial growth for Aleppo pine was recorded in early spring ([18]), though it is not always present ([60]). Finally, Camarero et al. ([14]) showed that radial growth in Aleppo pine is more pronounced at continental sites than at coastal sites.

  Regeneration capacity of Aleppo pine 

Aleppo pine is well known for the high seed productivity and the relevant regeneration ability ([52], [51]), which is positively affected by humidity and temperature. Owing to its great regenerative ability, the Aleppo pine can colonize new sites over long distances ([40], [42], [12]). Seed spread of Aleppo pine is largely favoured by wildlife in forests ([23], [22]). The colonization of Aleppo pine causes changes in the colonized ecosystem such as an increase in biomass and changes in the physicochemical characteristics of the soil ([71]). In North Africa, Aleppo pine has become an invasive species ([39]). For example, in Algeria the frequent wildfires and the changing climate have favored the expansion of Aleppo pine into the oak ecosystem ([77]), where it can influence the physiological performance of the cork oak ([30]).

As already mentioned, the natural range of Aleppo pine extends to southern Europe, northern Africa, and some areas of the eastern Mediterranean ([5], [64]), though the species is expanding in the Mediterranean area ([64]) and in several regions of its range Aleppo pine is considered an invasive species thanks to its ability to colonize different ecosystems ([51], [70]). Currently, Aleppo pine is rapidly colonizing oak ecosystems in many Mediterranean countries ([81]). Osem et al. ([59]) suggested that the expansion of Aleppo pine in Mediterranean areas could be favored by grazing, and Nuñez et al. ([56]) showed that wild boars and deer are active dispersers of pine mycorrhizal symbionts. In France, the growth in the height of Aleppo pine notably accelerated between 1960 and 2000 ([88]). Bello-Rodríguez et al. ([7]) reported that the expansion of Aleppo pine is very important to the island of La Gomera (Spain) and has increased since approximately 50 years, due to environmental conditions suitable to the species.

Several authors have confirmed the Aleppo pine expansion in many sites around the world where it has been introduced, including Australia, Brazil, Chile, Israel, New Zealand, South Africa, Uruguay, Venezuela, and the United States ([71], [72], [82]). Therefore, Pinus halepensis has become among the most important invasive pine species worldwide ([68], [69], [73], [86]), due to its great adaptability to different substrates and climates ([70], [58], [31], [89]). Lavi et al. ([40]) reported that the invasion of Aleppo pine severely affect the local ecosystems by creating pine “islands” within the natural vegetation.

  Use of Aleppo pine as rootstock for grafting 

Grafting of pine trees for pine nut production allows to anticipate the start of production. This makes the investment more profitable and partially solves the problem of labor scarcity for the harvesting of cones, thanks to the lower height of grafted trees. Grafting stone pine onto Aleppo pine rootstocks broadens the range of use of the former species, thus promoting pine nut production in marginal areas ([78]). Grafting stone pine grafts on Aleppo pine rootstocks has provided commendable results, especially because P. halepensis can adapt to degraded, dry, and nutrient-poor areas and grow on calcareous soils ([62]). Indeed, plantations of Pinus pinea grafts on Aleppo pine rootstocks led to significant and earlier production of cones and nuts. These results can be exploited for the restoration and rehabilitation of rural areas to improve the standard of living of the local population while simultaneously improving the soil. Aletà & Vilanova ([2]) showed that that using Aleppo pine as rootstock gave superior results compared to using stone pine rootstocks. The authors reported that using Aleppo pine rootstocks, the grafted plants were almost twice the height of trees grafted with stone pine rootstocks. Moreover, cone and seed production significantly improved, yielding 1.2 cones m^-2 of canopy and 290 kg ha^-1 using stone pine, compared with 4.8 cones m^-2 and 376 kg ha^-1 using Aleppo pine as rootstock. Grafted stone pine plantations in Spain and Tunisia showed high survival and promising growth rates, both with stone pine and Aleppo pine rootstocks, on many sites. Establishing stone pine fruit plantations requires grafting ([34]) with scions taken from selected subjects. This system is widely used in Spain, Portugal, and recently in Tunisia ([62]) where stone pine has been grafted onto Aleppo pine. Grafting is usually carried out when rootstocks are 2-4 years old, with grafts taken from individuals selected for their cone production performances ([78]). In Spain (Murcia and Castellon provinces), grafting was carried out on Aleppo pine rootstock, which is better adapted to on clay, marl, or gypsum soils than other pines. In the province of Castellon, more than 10.000 grafts of stone pine on Aleppo pine rootstocks have already been carried out; the oldest pines are now approximately 20-year-old ([78]).

  Conclusions 

P. halepensis is an important tree of the Mediterranean region, characterised by high biomass productivity, and high plasticity with respect to climate and drought. Its radial growth varies with the environmental characteristics. The regeneration capacity of this species is notable and it is now considered an invasive species in different areas of the world. Moreover, the use of Aleppo pine as rootstock for stone pine nut production seems promising based on preliminary evidences. In light of this, Aleppo pine can be exploited as a promoter species in marginalized and degraded areas. This review can help forest managers developing optimal management strategies for Aleppo pine stands.

  Conflicts of Interest 

The authors declare no conflict of interest.

  Acknowledgements 

This project is carried out under the MOBIDOC scheme funded by the Ministry of Higher Education and Scientific Research of Tunisia through the PromESsE project and managed by the ANPR.

  References