- Email: [email protected]
On the pyrophytism in the Mediterranean area
Journal of Arid Environments 120 (2015) 1e3
Contents lists available at ScienceDirect
Journal of Arid Environments journal homepage: www.elsevier.com/locate/jaridenv
Think note
On the pyrophytism in the Mediterranean area Angelo Troia a, *, Emilio Laguna b degli Studi di Palermo, via Archirafi 38, I-90123, Palermo, Italy Dipartimento STEBICEF, sezione di Botanica ed Ecologia Vegetale, Universita , 114, n y Experimentacio n Forestal, Servicio de Vida Silvestre e Generalitat Valenciana, Avda. Comarques del País Valencia Centro para la Investigacio E-46930, Quart de Poblet, Valencia, Spain a
b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 6 January 2015 Received in revised form 25 March 2015 Accepted 7 April 2015 Available online 11 April 2015
Authors briefly present some observations and reflections on the “seeding strategy” of some plant species (Cistus spp., Cistaceae, in particular) in the Mediterranean area in relation to fire: they conclude it does not seem a specific adaptation to wildfires (as suggested in a relevant part of the recent literature), but a generalistic adaptation to open, high energy and variable habitats with aleatory fluctuations. The difference is important both for theoretical and applied aspects, e.g. for the correct management of Cistus species and of other Mediterranean species and habitats. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Fire ecology Adaptation Evolution Habitat management Opportunistic strategy High energy habitats Cistus
Fire is undoubtedly a major ecological factor in the Mediterranean area. Many botanists have postulated the relevant role of fire in the evolution of Mediterranean vegetation and flora, beginning with the milestone papers of Le Houerou (1973) and Naveh (1975) and up to the most recent works (e.g. Keeley et al., 2011; Pausas and Schwilk, 2012). Consequently, pyrophytism (or adaptation of plants to wildfires) in Mediterranean vegetation and flora has been the subject of many studies and papers, with many consequences also on the management strategies of habitats and species. According to Trabaud (2002), KuhnholtzeLordat in 1938 was the first to define the term “pyrophytes”, distinguishing plant species with passive resistance (e.g. thick bark in Quercus suber), species with the capability to resprout after destruction of the aboveground organs, and species that regenerate by seed (e.g., Cistus spp.). In this note we want to express e in a concise way, considering the complexity of the topic e our point of view, different from the prevailing (though not only) one, according to which too often Mediterranean species and communities are defined “pyrophytic”. As a general premise, we think that in the Mediterranean region
* Corresponding author. E-mail addresses: [email protected] (E. Laguna).
(A.
http://dx.doi.org/10.1016/j.jaridenv.2015.04.003 0140-1963/© 2015 Elsevier Ltd. All rights reserved.
Troia),
[email protected]
it is not easy to describe “pyrophytic” adaptation of species, if we consider that in this region current wildland fires are e as a rule e of anthropogenic origin (Caldararo, 2002; FAO, 2006; Türkmen and Dunzenli, 2011). In detail, our note focuses on the seeding strategy mentioned above. According to some recent literature (e.g. Moreira and Pausas, 2012; Pausas and Schwilk, 2012), the obligatory seeding Cistus species in the Mediterranean are considered to be “adapted to fire”. To support this hypothesis, authors usually mention the post-fire explosion of seedlings, related to a mechanical rupture of dormancy of the hard-coated seeds caused by high temperatures, but also to the effects of smoke coming from burnt vegetation on water-permeable seeds. Indeed, the post-fire explosions of Cistus species are well known and it is easy to relate the massive germination of the seeds to their thermal scarification. But these facts can also be related to a general opportunistic strategy (Thanos and Georghiou, 1988), including the production of heterogeneous seeds (as far as coatedness and size are concerned). In this case, temperatures occurring during fires can induce germination of a certain percentage of seeds but e also e cause the death of another fraction of the soil seed-bank. It should be noted that this seed heterogeneity, well known in the genus, has already been interpreted as an adaptation to an environment with aleatory fluctuations (Vuillemin and Bulard, 1981)
2
A. Troia, E. Laguna / Journal of Arid Environments 120 (2015) 1e3
and not specifically to fire. We think that Cistus species are not adapted mainly and specifically to wildfires, but to open, high energy and variable habitats (such as rocky territories, garrigues and lithosols in Mediterranean areas), in which the mechanical effects on the coats of seeds are achieved not in a few minutes (as during wildfires), but during the whole hot summer season, and even during several years in the soil seed-bank. In normal conditions seeds, produced and released on the soil at the end of spring and beginning of summer, will be progressively scarified by the high temperatures occurring for several hours during the summer on the soil surface (up to 68 C at 1 cm depth in Valencian Community, Spain, Santana et al., 2013). Seeds will also lose their impermeability during the hot dry season, becoming able to germinate only at the end of that season, i.e. when regular (and not occasional) rains and lower temperatures will guarantee the survival of plantlets. To this regard, see the recent papers by Santana et al. (2013) and Bradshaw et al. (2011a), for general references, and also the papers by Moretti et al. (2006) and Luna et al. (2007) for Cistus. Rereading previous papers on the influence of heat on germi, 1992; Tilki, nation (e.g. Thanos and Georghiou, 1988; Roy and Sonie 2008), we can see that thermal pre-germination treatments of ca. 100 C for 1e30 min caused the highest germination rates: this fact was used as an evidence of the role of wildfires in germination. Indeed, the same germination rates were achieved also with exposure to lower temperatures, for a longer time (e.g. 50 C for 1 h in Tilki, 2008), i.e. with the temperatures usually experienced by seeds on the lithosols in the mid-day hours of summer days. Note that in several cases, pre-treatments at 100 C for 5 (Herrero et al., 2007) or 10 min (Tilki, 2008) already cause lower germination rates, and that higher lethal temperatures usually occur in natural wildfires. Finally, note that Moreira and Pausas (2012), in their experimental plan to test the influence of summer temperatures on germination, used a “summer treatment” with only 4 h at just 43 C: in our opinion, a better simulation of summer conditions would include, for example, higher temperatures (50e60 C). On the basis of these observations, we hypothesize that the primary habitats of Cistus species are garrigues on lithosols and similar habitats, where the species live and maintain stable populations in the absence or unpredictable presence of wildfires, and that the general strategy of this genus (and of other Mediterranean hard-coated seed species as well) is not connected specifically with wildfires as the main evolutive force, but with open habitats in Mediterranean-type seasonal climate, or, using the words of Troumbis and Trabaud (1986), with the “spectrum of unpredictable disturbances and stresses (man made disturbances, climate variability, etc.) characterizing the Mediterranean landscape” (in this sense, see the “extreme case” described by Bartoli et al., 2014). The wildfires are one of these unpredictable stresses but the same adaptations could be obtained as an answer to other co-incident causes. As suggested by Buhk et al. (2007: 12), maybe it is better to avoid the term “pyrophytic plant”, especially if it is not demonstrated that a specific trait is a response to fire or to another disturbance or effect. We consider it important to stress this view for its ecological and evolutionary implications, first of all for a better management of the species and the habitats where they occur (in this sense we nshare the concerns expressed by Bradshaw et al., 2011b; Garzo Machado et al., 2012). In fact, if Mediterranean plants are considered “adapted” to wildfires, surely wildfires will be seen as welcome and natural events, making the fight against them harder; remember that e as a rule e Mediterranean wildfires originate directly or indirectly from human activities and constitute a serious problem for biodiversity, additionally causing soil loss and erosive
processes. Regarding the hypothesis of Pausas et al. (2006), according to which the seeding strategy evolved later than the resprouter strategy, i.e. during the Quaternary period and concomitantly with the Mediterranean climate and frequent fires, it does not seem definitely proven since the presence of nonanthropic fire in the Mediterranean is irregular and local (e.g. connected with volcanism or with “dry storms” usually limited to restricted territories). In addition, according to some data (e.g. Conedera et al., 2002; Sadori et al., 2008; Bisculm et al., 2012), wildfires seem to be sometimes massive only in very recent times, i.e. in the last 10,000 years, when they appear related to human action; but we have to consider that missing evidence for older times could be due to the difficulty of finding such kind of evidences. Finally, some cases (e.g. Pinus canariensis, the unique European resprouter pine species, living in the volcanic archipelago of the Canary Islands) seems to be in contrast with the above mentioned hypothesis. Additional research focused on the role of summer and fire temperatures in the regulation of seed dormancy release in Mediterranean plant species (such as Cistus sp. pl.) is needed and welcome, both to improve our understanding of theoretical aspects e such as the evolution and diversification of the species, or the adaptation of the plants to the environment- and of applied aspects e such as, for example, the role and the management of fire in Mediterranean ecosystems, also considering climate changes and carbon balance. Acknowledgements Thanks to Elisabetta Oddo (Dip. STEBICEF, Universit a di Palermo) for linguistic corrections. References , C., 2014. Plant adaptation Bartoli, G., Bottega, S., Forino, L.M.C., Ciccarelli, D., Spano to extreme environments: the example of Cistus salviifolius of an active geothermal alteration field. C. R. Biol. 337, 101e110. Bisculm, M., Colombaroli, D., Vescovi, E., van Leeuwen, J.F.N., Henne, P.D., Rothen, J., Procacci, G., Pasta, S., La Mantia, T., Tinner, W., 2012. Holocene vegetation and fire dynamics in the supra-mediterranean belt of the Nebrodi Mountains (Sicily, Italy). J. Quat. Sci. 27, 687e698. Bradshaw, D.S., Dixon, K.W., Hopper, S.D., Lambers, H., Turner, S.R., 2011a. Little evidence for fire-adapted plant traits in Mediterranean climate regions. Trends Plant Sci. 16 (2), 69e76. Bradshaw, D.S., Dixon, K.W., Hopper, S.D., Lambers, H., Turner, S.R., 2011b. Response to Keeley et al.: fire as an evolutionary pressure shaping plant traits. Trends Plant Sci. 16 (8), 405. Buhk, C., Meyn, A., Jentsch, A., 2007. The challenge of plant regeneration after fire in the Mediterranean Basin: scientific gaps in our knowledge on plant strategies and evolution of traits. Plant Ecol. 192, 1e19. Caldararo, N., 2002. Human ecological intervention and the role of forest fires in human ecology. Sci. Total Environ. 292, 141e165. Conedera, M., Moretti, M., Tinner, W., 2002. Storia ed ecologia degli incendi boschivi al sud delle Alpi della Svizzera. In: Anfodillo, T., Carraro, V. (Eds.), Il fuoco in foresta: ecologia e controllo. Forest fires: ecology and control, Proceedings of degli Studi di Padova, the XXXIX Corso di Cultura in Ecologia. Universita pp. 15e30. FAO, 2006. Global Forest Resources Assessment 2005 e Report on Fires in the Mediterranean Region. In: Fire Management Working Paper 8. http://www.fao. org/docrep/009/j7564e/j7564e00.htm. Accessed 1 July 2014. n-Machado, V., del Arco Aguilar, M.J., Valde s Gonza lez, F., Pe rez-de-Paz, P.L., Garzo 2012. Fire as a threatening factor for endemic plants of the Canary Islands. Biodivers. Conserv. 21, 2621e2632. Herrero, C., San Martin, R., Bravo, F., 2007. Effect of heat and ash treatments on germination of Pinus pinaster and Cistus laurifolius. J. Arid Environ. 70, 540e548. Keeley, J.E., Pausas, J.G., Rundel, P.W., Bond, W.J., Bradstock, R.A., 2011. Fire as an evolutionary pressure shaping plant traits. Trends Plant Sci. 16, 406e411. Le Houerou, H.N., 1973. Fire and vegetation in the Mediterranean basin. In: Proc. 13th Annual Tall Timbers Fire Ecology Conference Tallahassee, Florida, pp. 237e277. lez, F., 2007. Heat-shock and seed Luna, B., Moreno, J.M., Cruz, A., Fern andez-Gonza germination of a group of Mediterranean plant species growing in a burned area: an approach based on plant functional types. Environ. Exp. Bot. 60, 324e333.
A. Troia, E. Laguna / Journal of Arid Environments 120 (2015) 1e3 Moreira, B., Pausas, J.G., 2012. Tanned or burned: the role of fire in shaping physical seed dormancy. PLoS One 7 (12), e51523. http://dx.doi.org/10.1371/ journal.pone.0051523. Moretti, M., Conedera, M., Moresi, R., Guisan, A., 2006. Modelling the influence of change in fire regime on the local distribution of a Mediterranean pyrophytic plant species (Cistus salviifolius) at its northern range limit. J. Biogeogr. 33, 1492e1502. Naveh, Z., 1975. The evolutionary significance of fire in the Mediterranean region. Vegetatio 29, 199e208. Pausas, J.G., Schwilk, D., 2012. Fire and plant evolution. New Phytol. 193, 301e303. Pausas, J.G., Keeley, J.E., Verdú, M., 2006. Inferring differential evolutionary processes of plant persistence traits in Northern Hemisphere Mediterranean fireprone ecosystems. J. Ecol. 94, 31e39. , L., 1992. Germination and population dynamics of Cistus species in Roy, J., Sonie relation to fire. J. Appl. Ecol. 29, 647e655. Sadori, L., Zanchetta, G., Giardini, M., 2008. Last glacial to holocene palaeoenvironmental evolution at Lago di Pergusa (Sicily, Southern Italy) as inferred by pollen, microcharcoal, and stable isotopes. Quat. Int. 181, 4e14. Santana, V.M., Baeza, M.J., Blanes, M.C., 2013. Clarifying the role of fire heat and
3
daily temperature fluctuations as germination cues for Mediterranean Basin obligate seeders. Ann. Bot. Lond. 111, 127e134. Thanos, C.A., Georghiou, K., 1988. Ecophysiology of fire-stimulated seed germination in Cistus incanus ssp. creticus (L.) Heywood and C. salvifolius L. Plant Cell Environ. 11, 841e849. Tilki, F., 2008. Seed germination of Cistus creticus L. and Cistus laurifolius L. as influenced by dry-heat, soaking in distilled water and gibberellic acid. J. Environ. Biol. 29 (2), 193e195. Trabaud, L., 2002. Effects of fire on mediterranean plants and ecosystems. In: Anfodillo, T., Carraro, V. (Eds.), Il fuoco in foresta: ecologia e controllo. Forest fires: ecology and control, Proceedings of the XXXIX Corso di Cultura in Eco degli Studi di Padova, pp. 49e60. logia. Universita Troumbis, A., Trabaud, L., 1986. Comparison of reproductive biological attributes of two Cistus species. Acta Oecol. Oec. Plant. 7, 235e250. Türkmen, N., Duzenli, A., 2011. Early post-fire changes in Pinus brutia forests (Amanos Mountains, Turkey). Acta Bot. Croat. 70, 9e21. Vuillemin, J., Bulard, C., 1981. Ecophysiologie de la germination de Cistus albidus L. et Cistus monspeliensis L. Naturalia Monspel. Ser. Bot. 46, 1e11.
Contents lists available at ScienceDirect
Journal of Arid Environments journal homepage: www.elsevier.com/locate/jaridenv
Think note
On the pyrophytism in the Mediterranean area Angelo Troia a, *, Emilio Laguna b degli Studi di Palermo, via Archirafi 38, I-90123, Palermo, Italy Dipartimento STEBICEF, sezione di Botanica ed Ecologia Vegetale, Universita , 114, n y Experimentacio n Forestal, Servicio de Vida Silvestre e Generalitat Valenciana, Avda. Comarques del País Valencia Centro para la Investigacio E-46930, Quart de Poblet, Valencia, Spain a
b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 6 January 2015 Received in revised form 25 March 2015 Accepted 7 April 2015 Available online 11 April 2015
Authors briefly present some observations and reflections on the “seeding strategy” of some plant species (Cistus spp., Cistaceae, in particular) in the Mediterranean area in relation to fire: they conclude it does not seem a specific adaptation to wildfires (as suggested in a relevant part of the recent literature), but a generalistic adaptation to open, high energy and variable habitats with aleatory fluctuations. The difference is important both for theoretical and applied aspects, e.g. for the correct management of Cistus species and of other Mediterranean species and habitats. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Fire ecology Adaptation Evolution Habitat management Opportunistic strategy High energy habitats Cistus
Fire is undoubtedly a major ecological factor in the Mediterranean area. Many botanists have postulated the relevant role of fire in the evolution of Mediterranean vegetation and flora, beginning with the milestone papers of Le Houerou (1973) and Naveh (1975) and up to the most recent works (e.g. Keeley et al., 2011; Pausas and Schwilk, 2012). Consequently, pyrophytism (or adaptation of plants to wildfires) in Mediterranean vegetation and flora has been the subject of many studies and papers, with many consequences also on the management strategies of habitats and species. According to Trabaud (2002), KuhnholtzeLordat in 1938 was the first to define the term “pyrophytes”, distinguishing plant species with passive resistance (e.g. thick bark in Quercus suber), species with the capability to resprout after destruction of the aboveground organs, and species that regenerate by seed (e.g., Cistus spp.). In this note we want to express e in a concise way, considering the complexity of the topic e our point of view, different from the prevailing (though not only) one, according to which too often Mediterranean species and communities are defined “pyrophytic”. As a general premise, we think that in the Mediterranean region
* Corresponding author. E-mail addresses: [email protected] (E. Laguna).
(A.
http://dx.doi.org/10.1016/j.jaridenv.2015.04.003 0140-1963/© 2015 Elsevier Ltd. All rights reserved.
Troia),
[email protected]
it is not easy to describe “pyrophytic” adaptation of species, if we consider that in this region current wildland fires are e as a rule e of anthropogenic origin (Caldararo, 2002; FAO, 2006; Türkmen and Dunzenli, 2011). In detail, our note focuses on the seeding strategy mentioned above. According to some recent literature (e.g. Moreira and Pausas, 2012; Pausas and Schwilk, 2012), the obligatory seeding Cistus species in the Mediterranean are considered to be “adapted to fire”. To support this hypothesis, authors usually mention the post-fire explosion of seedlings, related to a mechanical rupture of dormancy of the hard-coated seeds caused by high temperatures, but also to the effects of smoke coming from burnt vegetation on water-permeable seeds. Indeed, the post-fire explosions of Cistus species are well known and it is easy to relate the massive germination of the seeds to their thermal scarification. But these facts can also be related to a general opportunistic strategy (Thanos and Georghiou, 1988), including the production of heterogeneous seeds (as far as coatedness and size are concerned). In this case, temperatures occurring during fires can induce germination of a certain percentage of seeds but e also e cause the death of another fraction of the soil seed-bank. It should be noted that this seed heterogeneity, well known in the genus, has already been interpreted as an adaptation to an environment with aleatory fluctuations (Vuillemin and Bulard, 1981)
2
A. Troia, E. Laguna / Journal of Arid Environments 120 (2015) 1e3
and not specifically to fire. We think that Cistus species are not adapted mainly and specifically to wildfires, but to open, high energy and variable habitats (such as rocky territories, garrigues and lithosols in Mediterranean areas), in which the mechanical effects on the coats of seeds are achieved not in a few minutes (as during wildfires), but during the whole hot summer season, and even during several years in the soil seed-bank. In normal conditions seeds, produced and released on the soil at the end of spring and beginning of summer, will be progressively scarified by the high temperatures occurring for several hours during the summer on the soil surface (up to 68 C at 1 cm depth in Valencian Community, Spain, Santana et al., 2013). Seeds will also lose their impermeability during the hot dry season, becoming able to germinate only at the end of that season, i.e. when regular (and not occasional) rains and lower temperatures will guarantee the survival of plantlets. To this regard, see the recent papers by Santana et al. (2013) and Bradshaw et al. (2011a), for general references, and also the papers by Moretti et al. (2006) and Luna et al. (2007) for Cistus. Rereading previous papers on the influence of heat on germi, 1992; Tilki, nation (e.g. Thanos and Georghiou, 1988; Roy and Sonie 2008), we can see that thermal pre-germination treatments of ca. 100 C for 1e30 min caused the highest germination rates: this fact was used as an evidence of the role of wildfires in germination. Indeed, the same germination rates were achieved also with exposure to lower temperatures, for a longer time (e.g. 50 C for 1 h in Tilki, 2008), i.e. with the temperatures usually experienced by seeds on the lithosols in the mid-day hours of summer days. Note that in several cases, pre-treatments at 100 C for 5 (Herrero et al., 2007) or 10 min (Tilki, 2008) already cause lower germination rates, and that higher lethal temperatures usually occur in natural wildfires. Finally, note that Moreira and Pausas (2012), in their experimental plan to test the influence of summer temperatures on germination, used a “summer treatment” with only 4 h at just 43 C: in our opinion, a better simulation of summer conditions would include, for example, higher temperatures (50e60 C). On the basis of these observations, we hypothesize that the primary habitats of Cistus species are garrigues on lithosols and similar habitats, where the species live and maintain stable populations in the absence or unpredictable presence of wildfires, and that the general strategy of this genus (and of other Mediterranean hard-coated seed species as well) is not connected specifically with wildfires as the main evolutive force, but with open habitats in Mediterranean-type seasonal climate, or, using the words of Troumbis and Trabaud (1986), with the “spectrum of unpredictable disturbances and stresses (man made disturbances, climate variability, etc.) characterizing the Mediterranean landscape” (in this sense, see the “extreme case” described by Bartoli et al., 2014). The wildfires are one of these unpredictable stresses but the same adaptations could be obtained as an answer to other co-incident causes. As suggested by Buhk et al. (2007: 12), maybe it is better to avoid the term “pyrophytic plant”, especially if it is not demonstrated that a specific trait is a response to fire or to another disturbance or effect. We consider it important to stress this view for its ecological and evolutionary implications, first of all for a better management of the species and the habitats where they occur (in this sense we nshare the concerns expressed by Bradshaw et al., 2011b; Garzo Machado et al., 2012). In fact, if Mediterranean plants are considered “adapted” to wildfires, surely wildfires will be seen as welcome and natural events, making the fight against them harder; remember that e as a rule e Mediterranean wildfires originate directly or indirectly from human activities and constitute a serious problem for biodiversity, additionally causing soil loss and erosive
processes. Regarding the hypothesis of Pausas et al. (2006), according to which the seeding strategy evolved later than the resprouter strategy, i.e. during the Quaternary period and concomitantly with the Mediterranean climate and frequent fires, it does not seem definitely proven since the presence of nonanthropic fire in the Mediterranean is irregular and local (e.g. connected with volcanism or with “dry storms” usually limited to restricted territories). In addition, according to some data (e.g. Conedera et al., 2002; Sadori et al., 2008; Bisculm et al., 2012), wildfires seem to be sometimes massive only in very recent times, i.e. in the last 10,000 years, when they appear related to human action; but we have to consider that missing evidence for older times could be due to the difficulty of finding such kind of evidences. Finally, some cases (e.g. Pinus canariensis, the unique European resprouter pine species, living in the volcanic archipelago of the Canary Islands) seems to be in contrast with the above mentioned hypothesis. Additional research focused on the role of summer and fire temperatures in the regulation of seed dormancy release in Mediterranean plant species (such as Cistus sp. pl.) is needed and welcome, both to improve our understanding of theoretical aspects e such as the evolution and diversification of the species, or the adaptation of the plants to the environment- and of applied aspects e such as, for example, the role and the management of fire in Mediterranean ecosystems, also considering climate changes and carbon balance. Acknowledgements Thanks to Elisabetta Oddo (Dip. STEBICEF, Universit a di Palermo) for linguistic corrections. References , C., 2014. Plant adaptation Bartoli, G., Bottega, S., Forino, L.M.C., Ciccarelli, D., Spano to extreme environments: the example of Cistus salviifolius of an active geothermal alteration field. C. R. Biol. 337, 101e110. Bisculm, M., Colombaroli, D., Vescovi, E., van Leeuwen, J.F.N., Henne, P.D., Rothen, J., Procacci, G., Pasta, S., La Mantia, T., Tinner, W., 2012. Holocene vegetation and fire dynamics in the supra-mediterranean belt of the Nebrodi Mountains (Sicily, Italy). J. Quat. Sci. 27, 687e698. Bradshaw, D.S., Dixon, K.W., Hopper, S.D., Lambers, H., Turner, S.R., 2011a. Little evidence for fire-adapted plant traits in Mediterranean climate regions. Trends Plant Sci. 16 (2), 69e76. Bradshaw, D.S., Dixon, K.W., Hopper, S.D., Lambers, H., Turner, S.R., 2011b. Response to Keeley et al.: fire as an evolutionary pressure shaping plant traits. Trends Plant Sci. 16 (8), 405. Buhk, C., Meyn, A., Jentsch, A., 2007. The challenge of plant regeneration after fire in the Mediterranean Basin: scientific gaps in our knowledge on plant strategies and evolution of traits. Plant Ecol. 192, 1e19. Caldararo, N., 2002. Human ecological intervention and the role of forest fires in human ecology. Sci. Total Environ. 292, 141e165. Conedera, M., Moretti, M., Tinner, W., 2002. Storia ed ecologia degli incendi boschivi al sud delle Alpi della Svizzera. In: Anfodillo, T., Carraro, V. (Eds.), Il fuoco in foresta: ecologia e controllo. Forest fires: ecology and control, Proceedings of degli Studi di Padova, the XXXIX Corso di Cultura in Ecologia. Universita pp. 15e30. FAO, 2006. Global Forest Resources Assessment 2005 e Report on Fires in the Mediterranean Region. In: Fire Management Working Paper 8. http://www.fao. org/docrep/009/j7564e/j7564e00.htm. Accessed 1 July 2014. n-Machado, V., del Arco Aguilar, M.J., Valde s Gonza lez, F., Pe rez-de-Paz, P.L., Garzo 2012. Fire as a threatening factor for endemic plants of the Canary Islands. Biodivers. Conserv. 21, 2621e2632. Herrero, C., San Martin, R., Bravo, F., 2007. Effect of heat and ash treatments on germination of Pinus pinaster and Cistus laurifolius. J. Arid Environ. 70, 540e548. Keeley, J.E., Pausas, J.G., Rundel, P.W., Bond, W.J., Bradstock, R.A., 2011. Fire as an evolutionary pressure shaping plant traits. Trends Plant Sci. 16, 406e411. Le Houerou, H.N., 1973. Fire and vegetation in the Mediterranean basin. In: Proc. 13th Annual Tall Timbers Fire Ecology Conference Tallahassee, Florida, pp. 237e277. lez, F., 2007. Heat-shock and seed Luna, B., Moreno, J.M., Cruz, A., Fern andez-Gonza germination of a group of Mediterranean plant species growing in a burned area: an approach based on plant functional types. Environ. Exp. Bot. 60, 324e333.
A. Troia, E. Laguna / Journal of Arid Environments 120 (2015) 1e3 Moreira, B., Pausas, J.G., 2012. Tanned or burned: the role of fire in shaping physical seed dormancy. PLoS One 7 (12), e51523. http://dx.doi.org/10.1371/ journal.pone.0051523. Moretti, M., Conedera, M., Moresi, R., Guisan, A., 2006. Modelling the influence of change in fire regime on the local distribution of a Mediterranean pyrophytic plant species (Cistus salviifolius) at its northern range limit. J. Biogeogr. 33, 1492e1502. Naveh, Z., 1975. The evolutionary significance of fire in the Mediterranean region. Vegetatio 29, 199e208. Pausas, J.G., Schwilk, D., 2012. Fire and plant evolution. New Phytol. 193, 301e303. Pausas, J.G., Keeley, J.E., Verdú, M., 2006. Inferring differential evolutionary processes of plant persistence traits in Northern Hemisphere Mediterranean fireprone ecosystems. J. Ecol. 94, 31e39. , L., 1992. Germination and population dynamics of Cistus species in Roy, J., Sonie relation to fire. J. Appl. Ecol. 29, 647e655. Sadori, L., Zanchetta, G., Giardini, M., 2008. Last glacial to holocene palaeoenvironmental evolution at Lago di Pergusa (Sicily, Southern Italy) as inferred by pollen, microcharcoal, and stable isotopes. Quat. Int. 181, 4e14. Santana, V.M., Baeza, M.J., Blanes, M.C., 2013. Clarifying the role of fire heat and
3
daily temperature fluctuations as germination cues for Mediterranean Basin obligate seeders. Ann. Bot. Lond. 111, 127e134. Thanos, C.A., Georghiou, K., 1988. Ecophysiology of fire-stimulated seed germination in Cistus incanus ssp. creticus (L.) Heywood and C. salvifolius L. Plant Cell Environ. 11, 841e849. Tilki, F., 2008. Seed germination of Cistus creticus L. and Cistus laurifolius L. as influenced by dry-heat, soaking in distilled water and gibberellic acid. J. Environ. Biol. 29 (2), 193e195. Trabaud, L., 2002. Effects of fire on mediterranean plants and ecosystems. In: Anfodillo, T., Carraro, V. (Eds.), Il fuoco in foresta: ecologia e controllo. Forest fires: ecology and control, Proceedings of the XXXIX Corso di Cultura in Eco degli Studi di Padova, pp. 49e60. logia. Universita Troumbis, A., Trabaud, L., 1986. Comparison of reproductive biological attributes of two Cistus species. Acta Oecol. Oec. Plant. 7, 235e250. Türkmen, N., Duzenli, A., 2011. Early post-fire changes in Pinus brutia forests (Amanos Mountains, Turkey). Acta Bot. Croat. 70, 9e21. Vuillemin, J., Bulard, C., 1981. Ecophysiologie de la germination de Cistus albidus L. et Cistus monspeliensis L. Naturalia Monspel. Ser. Bot. 46, 1e11.