Introduction
The biodiverse mountainous areas of the Mediterranean region (Cowling et al., Reference Cowling, Rundel, Lamont, Arroyo and Arianoutsou1996) were a refuge for certain conifer taxa (species of Abies, Cedrus, Cupressus, Juniperus and Pinus) during glacial periods (Bennett et al., Reference Bennett, Tzedakis and Willis1991). Some of these taxa have been widely used as sources of wood and food (Farjon et al., Reference Farjon, Page and Schellevis1993) and, as a result, many of these mountain conifers have been overexploited and are now of considerable conservation concern.
In the Taurus Mountains of Turkey, particularly around the ancient city of Sagalassos, the forests have been subjected to human use for thousands of years (Vanhaverbeke & Waelkens, Reference Vanhaverbeke and Waelkens2003, cited in Fontaine et al., Reference Fontaine, Aerts, Özkan, Mert, Gülsoy and Süel2007) and inappropriate silvicultural practices continue to threaten Abies cilicica (Fontaine et al., Reference Fontaine, Aerts, Özkan, Mert, Gülsoy and Süel2007). In Lebanon 10 conifer species are threatened to varying degrees by fragmentation and deterioration of their habitat (Talhouk et al., Reference Talhouk, Zurayk and Khuri2001). Elsewhere in the eastern Mediterranean Abies nordmanniana subsp. equi-trojani, Abies borisii-regis and some populations of Pinus heldreichii require management plans to guarantee their survival, as do the populations of Cedrus brevifolia in Cyprus (Quézel & Barbero, Reference Quézel and Barbero1990). Most of the conifer forests in the southern Mediterranean are threatened as a result of deforestation and overgrazing (Barbero et al., Reference Barbero, Bonin, Loisel and Quézel1990). In the Maghreb of Morocco there is particular concern for Abies numidica, Abies pinsapo var. tazaotana, Pinus nigra subsp. mauritanica, Cupressus atlantica, Cedrus atlantica, Tetraclinis articulata and Juniperus thurifera (Quézel & Barbero, Reference Quézel and Barbero1990; Quézel, Reference Quézel, Rejdali and Heywood1991).
In Spain human activity and climate change are affecting the regeneration of Juniperus communis in the south-east mountains (García et al., Reference García, Zamora, Hódar and Gómez1998). In northern Sicily Abies nebrodensis has been reduced to 29 individuals (Parducci et al., Reference Parducci, Szmidt, Madaghiele, Anzidei and Vendramin2001) and the species is categorized as Critically Endangered on the IUCN Red List (Farjon et al., Reference Farjon, Pasta and Troìa2006). A. numidica in Algeria and A. pinsapo var. tazaotana in Morocco are categorized as Vulnerable (Conifer Specialist Group, 1998). Although the other Mediterranean firs are categorized as Lower Risk (i.e. they have been assessed and found not to be in danger of extinction), they still face the threats common to all Mediterranean mountain conifer forests, i.e. the combination of felling (often illegal), livestock raising, farming and repeated fires.
From the time A. pinsapo was described by Boissier in 1837 (Barbey, Reference Barbey1931) until forests containing the species were protected by a variety of measures in the 1970s the species was subject to intense human pressure that fragmented and reduced its area of extent in both Spain and Morocco. The descriptions of the two Moroccan varieties were made in the early 20th century. Var. marocana was described by Ceballos & Martín-Bolaños (Reference Ceballos and Martín-Bolaños1928) and var. tazaotana by Sánchez-Cózar (Reference Sánchez-Cózar1946). It is likely that the isolation of these populations from human influence until the 19th century, due to difficulties of access, and the low mechanical properties of their wood in comparison with pine, are responsible for their survival.
However, the original area of A. pinsapo is now greatly reduced by timber harvesting, fire and overgrazing. Although felling for timber was not the principal cause of the reduction in extent of A. pinsapo forests, both single-species and mixed, there are records of timber occasionally being removed illegally, or without silvicultural criteria, and the natural structure of the forest has consequently been modified (Soto, Reference Soto2006). Greater damage was caused by overgrazing, which prevented natural regeneration, particularly in sites with poor soil or in full sun (Ceballos & Vicioso, Reference Ceballos and Vicioso1933). Fire has also destroyed A. pinsapo forests and caused a decline in their area of extent (Vega, Reference Vega and Araque1999).
Although A. pinsapo forests are now protected they are still threatened, particularly by fire and climate change. Although A. numidica and A. pinsapo may be more resistant to climate change than the other circum-Mediterranean firs, because they adapt better to dry periods (Aussenac, Reference Aussenac2002), the presence of pests associated with climate change could endanger their survival.
Here we review the current distribution of A. pinsapo, describe the effects of previous human influences on the species and the threats it now faces, and describe the conservation efforts so far undertaken and those still required.
Distribution and ecology
A. pinsapo has a very limited area of distribution. It is found in only five enclaves: three in the south of Spain and two in the north of Morocco.
Populations in Spain
A. pinsapo occurs in three areas in the high mountain ranges of the westernmost part of the Betic Cordillera, in Serranía de Ronda, spanning the provinces of Málaga and Cádiz (Fig. 1). The species occurs in shaded locations with a northerly or occasionally easterly or north-easterly exposure (Ceballos & Ruiz de la Torre, Reference Ceballos and Ruiz de la Torre1979).
Fig. 1 Distribution of Abies pinsapo forests (black shaded areas), which are restricted to southern Spain and northern Morocco: (a) Sierra de Grazalema (Cádiz), (b) Sierra de las Nieves (Málaga), (c) Los Reales de Sierra Bermeja (Málaga), (d) Tazaout and Talassemtane (Morocco).
In Málaga the species occurs at 1,000–1,800 m in the humid Mediterranean vegetation zone. The A. pinsapo forest in Los Reales de Sierra Bermeja (Fig. 1c), comprising 50 ha in 1933 (Ceballos & Vicioso, Reference Ceballos and Vicioso1933), is in the municipalities of Genalguacil, Estepona and Casares, at altitudes of 1,300–1,400 m on peridotites. In 2008 this A. pinsapo forest occupied an area of only c. 35 ha and was in regression because of major fires in the area, which have divided it into three groves. Sierra de las Nieves is the most extensive area of A. pinsapo in the province of Málaga (Fig. 1b, Plate 1a). It extends over the municipalities of Ronda, Tolox and Yunquera at altitudes of 1,000–1,800 m on limestone soils. There are also isolated groves in the ranges of Alcor, Caparaín, Real, Istán, Río Verde and Gialda (Ceballos & Vicioso, Reference Ceballos and Vicioso1933; Ceballos & Ruiz de la Torre, Reference Ceballos and Ruiz de la Torre1979). The A. pinsapo forest in Sierra de las Nieves expanded from 1,000 ha in 1933 to 2,871 ha in 2008.
Plate 1 Abies pinsapo forests. (a) Sierra de las Nieves (Spain). (b) Sierra de Grazalema (Spain). (c) Talassemtane National Park (Morocco). (d) Tazaout (Morocco): the stumps remained after the summer of 1946, from A. pinsapo felled for the building of a log hut as a base from which the Spanish Forest Service made an inventory of Mount Tazaout. (e) Sierra de las Nieves (Spain): a fire in 2004 affected trees in full sun that will not be able to regenerate. (f) Tazaout (Morocco): effects of the 2002 forest fire on the northern slope of Tazaout, in an area of 200 ha (photograph from 2004, showing almost no regeneration).
In the province of Cádiz A. pinsapo is found only in Sierra del Pinar, in the municipality of Grazalema (Fig. 1a, Plate 1b), where it grows on limestone at altitudes of 1,000–1,650 m. This forest expanded from 200 ha in 1933 to 418 ha in 2008. Groves and isolated stands are also found in the western part of Monte Prieto, the sides of El Montón and on the northern slopes of Zafalgar and Los Pinos (Ceballos & Martín-Bolaños, Reference Ceballos and Martín-Bolaños1930; Ceballos & Ruiz de la Torre, Reference Ceballos and Ruiz de la Torre1979).
A. pinsapo occurs in locations with average rainfall of > 1,000 mm but nevertheless copes well with drought, although total rainfall is > 100 mm during summer in all of its locations (Ceballos & Ruiz de la Torre, Reference Ceballos and Ruiz de la Torre1979). It grows in locations that have more hours of sunshine than areas where other Mediterranean firs grow and is capable of colonizing steep slopes, including eroded rocky ground. It occurs with drought tolerant oaks (Quercus faginea, Quercus alpestris, Quercus ilex and Quercus suber) and other conifers such as Pinus pinaster, and less commonly with Pinus halepensis, in this case in Sierra de la Yunquera (Ceballos & Ruiz de la Torre, Reference Ceballos and Ruiz de la Torre1979).
Populations in Morocco
A. pinsapo occurs in the western Rif in two enclaves (Fig. 1d). The northernmost is on Mount Tazaout (Plate 1d), also known as Yebel Tazaout, in the Beni Sey-yel region, where A. pinsapo var. tazaotana occupied an area of 493 ha at altitudes of 1,400–1,700 m in 2008. To the south A. pinsapo var. marocana spans the Chefchaouen mountains (Plate 1c), reaching as far as Ametráx, with a total area of 2,531 ha at altitudes of 1,400–2,100 m (Liu, Reference Liu1971). The soil on which A. pinsapo grows is limestone. At high altitudes near mountain peaks the trees show signs of limited growth because of the constant winds and shallow soil. The rainfall in the species’ area of occurrence averages > 1,000 mm (Charco, Reference Charco1999). Unlike the Spanish A. pinsapo forests, those in the Rif rarely form single-species forests but mix with Atlas cedars Cedrus atlantica. In some places the forests comprise firs, cedars and a conifer absent from the Andalusian A. pinsapo forests, Pinus nigra subsp. mauritanica, which is smaller than the P. nigra var. salzmannii found in the Betic Cordillera. In the lower, warmer and dryer areas A. pinsapo occurs with Tetraclinis articulata, Olea marocana and Quercus coccifera, and in the more humid, cooler areas it occurs with Quercus ilex. Of all the firs in the western Mediterranean, A. pinsapo var. tazaotana grows the tallest and has the greatest diameter.
Threats
Timber harvesting
Unlike other Mediterranean conifer species, such as Cedrus libani, which have been widely harvested throughout history (Speiser, Reference Speiser and Pritchard1955; Wilson, Reference Wilson and Pritchard1955), A. pinsapo has not been extensively felled for timber. This is probably because of the difficulty of access to the forests, the fact that the land occupied by the trees is unsuitable for farming because of the orography, and because A. pinsapo timber is no match in quality compared to pine or cedar.
Nevertheless, certain projects at various periods made use of A. pinsapo wood locally (Chapman & Buck, Reference Chapman and Buck1910). There are written records of A. pinsapo timber being used in the building of ships in the 16th century and for the Algeciras-Ronda-Boadilla railway in the early 20th century. A. pinsapo was also used for the seating at the bull ring in Ronda (Peraza, Reference Peraza1964; Prioton, Reference Prioton1964), in mining, and in ice pits (in which snow was stored during the winter in alternate layers separated by A. pinsapo branches so that the ice that was formed could be used in the summer; Rodríguez, Reference Rodríguez and Araque1999). Much of the timber of A. pinsapo forests was used as paper pulp (Ceballos & Ruiz de la Torre, Reference Ceballos and Ruiz de la Torre1979). Although as fuelwood and charcoal it is of poor quality, A. pinsapo was sometimes used for these purposes locally (Barbey, Reference Barbey1931).
In 1904 and 1905, without following any silvicultural criteria, forest owners in Sierra del Pinar, Grazalema, felled c. 15,000 A. pinsapo for the construction of the first section of the railway line between Ronda and Algeciras. Difficulties encountered in hauling and transporting the logs resulted in most of them being discarded in the forest. In 1906 there was a change of ownership and the refusal of the new owner to let local workers make charcoal with the wood resulted in an intentionally-lit fire that affected 20 ha. In the 1930s A. pinsapo trees were taken from the Berranga and Las Tablas estates, in Sierra de Las Nieves, for the second section of the Ronda-Boadilla railway line. In Villaluenga del Rosario, in the province of Cádiz, a 1 ha stand was destroyed for making charcoal in 1931 (Soto, Reference Soto2006).
Logging, in accordance with controlled logging plans, occurred in the A. pinsapo forests of the Rif in the first half of the 20th century, when Spain held the area as a Protectorate (Charco, Reference Charco1999). The protective measures that apply to the A. pinsapo forests in Spain and Morocco now prohibit logging, and felling is only permitted for the purpose of creating fire-breaks.
Fire
The earliest recorded loss of A. pinsapo forests due to fire is from 1570 (Hurtado de Mendoza, Reference Hurtado de Mendoza1842). In Sierra de Alcaparaín (municipality of Carratraca), Ceballos & Vicioso (Reference Ceballos and Vicioso1933) cite the disappearance in c. 1920 of the group of A. pinsapo trees listed by Laguna (Reference Laguna1884), as a result of repeated fires. A stand of c. 1 ha on the bank of the Guadaiza River in Sierra Palmitera disappeared as a result of fire in 1975. In 1991 fire destroyed 1,000 ha of maritime pine Pinus pinaster and scrub in Sierra Blanca and Sierra Real, in addition to all the A. pinsapo trees in Sierra Real, some of which were 360 years old.
In Sierra Bermeja forest fires have fragmented and degraded the enclave of A. pinsapo, reducing the area of 50 ha in 1933 (Ceballos & Vicioso, Reference Ceballos and Vicioso1933) to 35 ha in 2008. In the summer of 2004 fire destroyed an old stand with a south-east exposure in Sierra de las Nieves (Plate 1e) that cannot be restored because of the southerly exposure. A fire on the northern slope of Tazaout in 2002 affected an area of 200 ha. A visit to the area in 2004 confirmed that there was almost no regeneration because of the steep slope and competition from less demanding species (Plate 1f).
Although A. pinsapo lacks the resprouting ability characteristic of many Mediterranean plants (Keeley, Reference Keeley2006) it reacts to fire by adaptation. The species expands its cover and the diminished solar radiation hinders the build up of inflammable material (Vega, Reference Vega and Araque1999). A. pinsapo is, however, not particularly inflammable (Rodríguez, Reference Rodríguez and Araque1999).
Until the second half of the 20th century grazing and charcoal making were the two main causes of fire in the A. pinsapo forests. Fires now normally only occur as a result of carelessness or arson. Although some groves of A. pinsapo have been lost as a result of fire (Soto, Reference Soto2006) some, such as the Grazalema forest, have not been affected by fire for nearly 100 years (Arista, Reference Arista1995).
From 1968 to 2007 the total loss of A. pinsapo forests was 564.7 ha, whereas during 2004-2008 only 1 ha was lost (López Quintanilla, pers. comm.). The intervals of time between the fires in Sierra Bermeja, which occurred in 1840 and 1865, and between those of 1932, 1966 and 1973, resulted in a forest with trees of different ages that, in conjunction with the mature trees, gave great stability to the A. pinsapo forest (Vega, Reference Vega and Araque1999).
Fire destroys 700,000–1,000,000 ha of forest in the Mediterranean Basin every year (Vélez, Reference Vélez2000). Many of the areas recover through the adaptation mechanisms that many Mediterranean species have to fire (Pickett et al., Reference Pickett, Collins and Armesto1987). However, fire-damaged A. pinsapo forests regenerate poorly in shady exposures and are incapable of regenerating in full sun.
Agriculture and livestock
Agriculture and farming techniques have also contributed to the decrease in the area of A. pinsapo, as in the case of the forests in Lajares and Caina, which were affected by several fires in the 19th century as a result of management of land occupied by vineyards. Fire was also used as a way to renew or increase grazing areas for livestock and this was the reason for the 1928 fire in the A. pinsapo forest in Barranco de los Mármoles, intentionally lit to increase pasture land for goats (Rodríguez, Reference Rodríguez and Araque1999). Pasturing continues under strict control in the three areas of Spanish A. pinsapo forests in Grazalema and Sierra Bermeja but it does not represent the same degree of threat as it did prior to the 1950s (Arista et al., Reference Arista, Herrera and Talavera1997).
Pests
Drought affects the susceptibility of A. pinsapo to infestation by pests. The A. pinsapo in Sierra Bermeja have sometimes been infested with the basidiomycete Armillaria mellea, although the forest was never threatened and has fully recovered (Arista et al., Reference Arista, Herrera and Talavera1997). Infestation by the lepidopteran Dioryctria aulloi has also been recorded; its life cycle is strongly influenced by climate, as seen in the incidence of this pest during the drought of 1991–1995 (Arista et al., Reference Arista, Herrera and Talavera1997). However, the irregular annual seed production of A. pinsapo provides trees with a natural defence against establishment of this insect. During this drought a more serious attack by the coleopteran Cryphalus numidicus occurred, resulting in the death of some of the trees. In the Yunquera A. pinsapo forest this borer was accompanied by the appearance of the basidiomycete Heterobasidion annosum (Navarro et al., Reference Navarro, Calzado, Martínez, López and Trapero2003). The A. pinsapo forests are also affected by the homopterans Mindarus abietinus, Cinara pectinatae and Cinara confinis (Cobos et al., Reference Cobos, Cobos and Martínez1998). The damage caused by C. confinis can lead to the death of twigs and branches.
Other threats
The fragmentation of the original A. pinsapo forests has led to isolation in small stands and in some cases isolated individuals. The average seed viability of A. pinsapo at low densities is only 21% whereas in dense forests it can be 82% (Arista & Talavera, Reference Arista and Talavera1996). The formation of biogeographical islands (MacArthur & Wilson, Reference MacArthur and Wilson1967) causes progressive deterioration in the genetic variability of A. pinsapo, leading to endogamy (Arista & Talavera, Reference Arista and Talavera1996). Lower rainfall and higher evapotranspiration because of climate change are a potential threat. In the early 1990s several A. pinsapo died from a combination of water stress and the appearance, propitiated by climate, of pests (Génova, Reference Génova2007).
Discussion
The climate dynamics of the Strait of Gibraltar and the mountains on both sides of the Strait make the area a favourable enclave for A. pinsapo. The mist, high rainfall and altitudes up to 2,000 m give rise to unique bioclimatic conditions. Although the Spanish A. pinsapo are smaller than those of the Rif, in Sierra Bermeja they are more similar in shape to the firs of the Rif than to those of Grazalema or Sierra de las Nieves. The wood of the Moroccan varieties and the Sierra Bermeja A. pinsapo is also similar (Esteban et al., Reference Esteban, de Palacios, Guindeo and García Fernández2007). However, the trees in the Sierra Bermeja A. pinsapo forest are the least tall, and have the smallest diameters and a twisted form. The Yunquera A. pinsapo forest has regenerated well, with a sufficiently high tree density that it requires silvicultural treatment. The Grazalema A. pinsapo forest was threatened by felling and excessive stock raising in the early 20th century. It now consists of mostly even-aged trees of homogeneous form with high diameters but there is little regeneration.
The Moroccan A. pinsapo forests are in better condition than those in Spain, not only because they have been better preserved because of their isolation from populated areas and the consequently lower anthropogenic impacts, but also because they occur in an area with higher rainfall and a wider altitudinal range. In the event of any climate change the Moroccan A. pinsapo would therefore have a greater chance of persistence. Of all the A. pinsapo forests, Tazaout has the largest trees, attaining heights of up to 50 m and base diameters of 1.30 m. The vitality of this forest is evident in the intense regeneration and, although A. pinsapo is mixed with maples, cedars and maritime pine P. pinaster and European black pine Pinus nigra , it is dominant.
The poorer condition of the Spanish A. pinsapo forests leads not only to smaller-sized trees but also to greater vulnerability to pests. The drought of 1991–1995 caused a loss of trees growing in the least favourable conditions and if such droughts recur there are likely to be further such losses. While the exposures in the Betic Cordillera are always northerly, A. pinsapo in Morocco prospers in northerly, westerly and occasion southerly exposures, influenced by the position of the mountains in relation to the incoming direction of the damp Atlantic winds.
Attempts to reforest with this species have not been satisfactory and natural regeneration depends on intense seed dissemination followed by at least 2 years of high rainfall and short, mild summers. In general, however, the A. pinsapo forests are stabilized and recovering after years of intensive goat pasturing, forest fires and use for fuelwood and charcoal making. However, the risk of fire is ever-present and that of climate change is looming. Although Aussenac (Reference Aussenac2002) suggested that A. pinsapo and A. numidica will be affected less by climate change than other Mediterranean firs because they have adapted to a less favourable environment, if the recent droughts recur the altitude range will progressively decrease and there will be an increased risk of infestation by pests.
Although at the end of the 19th century the forest guards in the municipal forests of Ronda were given responsibility for one of the first initiatives to protect the A. pinsapo forests, conservation measures did not actually begin until 1945, when the three areas of the Ronda A. pinsapo forests were purchased by the Spanish state. This was followed by the 1972 purchase of the Grazalema A. pinsapo forest, which became a Natural Park in 1984. Sierra de las Nieves became a Natural Park in 1989, and the area of Los Reales de Sierra Bermeja was given the special protection level of Natural Site (Table 1).
Table 1 International and national regulations for the conservation of Abies pinsapo in Spain and Morocco.
1 UMMP, Use and Management Master Plan
2 NRMP, Natural Resources Management Plan
The Moroccan A. pinsapo forests are within Talassemtane National Park, where felling is prohibited. In addition, their remote location favours their conservation. The greatest threat besides fire comes from the crops of Indian hemp or hashish Cannabis sativa var. indica, which are increasingly being grown at mid-range altitudes.
All the A. pinsapo forests are now protected and safeguarded from the anthropogenic threats they have been subject to throughout history, with the exception of arson. Conservation efforts now focus on the development of fire prevention plans, including fire-break construction and constant surveillance, and pest control during severe drought. The possibility of undertaking silvicultural treatment is also being considered for some enclaves, to reduce competition among individual trees. In Spain, these initiatives are carried out through the Autonomous Community of Andalusia, Dirección General del Medio Natural, and in Morocco through the Haut Commissariat aux Eaux et Forêts et á La lutte contre la Désertification, Direction Régionale des Eaux et Forêts du Rif à Tetouan, Service Provincial des Eaux et Forêts du Chefchaouen.
Acknowledgements
We thank the Forestry Engineers Miguel A. Martín Casillas and José López Quintanilla for assistance during our visit to Sierra de las Nieves Natural Park and Sierra Bermeja Natural Site in the province of Málaga, and Sierra de Grazalema Natural Park in the province of Cádiz, Spain, and the Royaume du Maroc Haut Commissariat aux Eaux et Forêts et à la Lutte contre la Désertification, Direction Régionale des Eaux et Forêts du Rif à Tetouan, Service Provincial des Eaux et Forêts du Chefchaouen, in particular Amrani Mohamed, Ingénieur en Chef des Eaux et Forêts du Rif à Tetouan, and Assim El Houssain, Chef du District du Chefchaouen, who provided us with guided access to the forests in Talassemtane and Tazaout (Morocco).
Biographical sketches
Luis G. Esteban works in forestry engineering, including the study of the vegetation dynamics of the Spanish forests and human influences on them. Paloma de Palacios also works in forestry engineering. The two authors participated for 6 years as Director and Researcher, respectively, in the Spanish television documentary series El bosque protector (The Protective Forest), which aimed to make the public aware of the importance of the Spanish forests in the natural, social and economic history of Spain from remote times to the present, and to highlight the negative and serious impact of humans on the state of the forests (see http://www.elbosqueprotector.es). Both authors also conduct research on the anatomy, physics and mechanics of wood. Luis Rodríguez-Losada is currently studying the vegetation dynamics and management of the Spanish forests.
