[en] This study reconstructs and interprets the changing range of Atlas cedar in northern Morocco over the last 9,000 years. A synthesis of fossil pollen records indicated that Atlas cedars occupied a wider range at lower elevations during the mid-Holocene than today. The mid-Holocene geographical expansion reflected low winter temperatures and higher water availability over the whole range of the Rif Mountains relative to modern conditions. A trend of increasing aridity observed after 6,000 years BP progressively reduced the range of Atlas cedar and prompted its migration toward elevations above 1,400 masl. To assess the impact of climate change on cedar populations over the last decades, we performed a transient model simulation for the period between 1960 and 2010. Our simulation showed that the range of Atlas cedar decreased by about 75% over the last 50 years and that the eastern populations of the range in the Rif Mountains were even more threatened by the overall lack of water availability than the western ones. Today, Atlas cedar populations in the Rif Mountains are persisting in restricted and isolated areas (Jbel Kelti, Talassemtane, Jbel Tiziren, Oursane, Tidighine) that we consider to be modern microrefugia. Conservation of these isolated populations is essential for the future survival of the species, preserving polymorphisms and the potential for population recovery under different climatic conditions.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Cheddadi, Rachid
Henrot, Alexandra-Jane ; Université de Liège - ULiège > Département d'astrophys., géophysique et océanographie (AGO) > Modélisation du climat et des cycles biogéochimiques
François, Louis ; Université de Liège - ULiège > Département d'astrophys., géophysique et océanographie (AGO) > Modélisation du climat et des cycles biogéochimiques
Bush, Marc
Carré, Matthieu
Coissac, Eric
De Oliveira, Paulo E.
Ficetola, Francesco
Hambuckers, Alain ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale
Microrefugia, climate change, and conservation of Cedrus atlantica in the Rif Mountains, Morocco
Publication date :
2017
Journal title :
Frontiers in Ecology and Evolution
eISSN :
2296-701X
Publisher :
Frontiers Research Foundation, Lausanne, Switzerland
Volume :
5
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
Belmont Forum [UY] F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Funding text :
This work is a contribution to the Belmont Forum funded project VULPES (Project ID: ANR-15-MASC-0003). This research is also supported by the F.R.S.-FNRS under research grant FRS-FNRS X.3041.17—VULPES-ULg
Aitken, S. N., Yeaman, S., Holliday, J. A., Wang, T., and Curtis-McLane, S. (2008). Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol. Appl. 1, 95-111. doi: 10.1111/j.1752-4571.2007.00013.x
Ajbilou, R., Maranon, T., and Arroyo, J. (2006). Ecological and biogeographical analyses of Mediterranean forests of northern Morocco. Acta Oecolog. 29, 104-113. doi: 10.1016/j.actao.2005.08.006
Akima, H., and Gebhardt, A. (2016). Akima: Interpolation of Irregularly and Regularly Spaced Data. R Package Version 0.6-2.
Alba-Sánchez, F., López-Sáez, J. A., Nieto-Lugilde, D., and Svenning, J. C. (2015). Long-term climate forcings to assess vulnerability in North Africa dry argan woodlands. Appl. Veg. Sci. 18, 283-296. doi: 10.1111/avsc.12133
Ashcroft, M. B., Chisholm, L. A., and French, K. O. (2009). Climate change at the landscape scale: predicting fine-grained spatial heterogeneity in warming and potential refugia for vegetation. Glob. Chang. Biol. 15, 656-667. doi: 10.1111/j.1365-2486.2008.01762.x
Ashcroft, M. B., Gollan, J. R., Warton, D. I., and Ramp, D. (2012). A novel approach to quantify and locate potential microrefugia using topoclimate, climate stability, and isolation from the matrix. Glob. Chang. Biol. 18, 1866-1879. doi: 10.1111/j.1365-2486.2012.02661.x
Aussenac, G., and Finkelstein, D. (1983). Influence de la sécheresse sur la croissance et la photosynthèse du cèdre. Ann. Des Sci. Forest. 40, 67-77. doi: 10.1051/forest:19830103
Aussenac, G., and Valette, J. C. (1982). Comportement hydrique estival de Cedrus atlantica Manetti, Quercus ilex L. et Quercus pubescens Willd. et de divers pins dans le Mont Ventoux. Ann. Des Sci. Forest. 39, 4162. doi: 10.1051/forest:19820103
Bennett, K. D., and Provan, J. (2008). What do we mean by "refugia"? Quat. Sci. Rev. 27, 2449-2455. doi: 10.1016/j.quascirev.2008.08.019
Bennett, K. D., Tzedakis, P. C., and Willis, K. J. (1991). Quaternary refugia of north European trees. J. Biogeogr. 18, 103-115. doi: 10.2307/2845248
Biltekin, D., Popescu, S.-M., Suc, J.-P., Quézel, P., Jiménez-Moreno, G., Yavuz, N., et al. (2015). Anatolia: a long-time plant refuge area documented by pollen records over the last 23million years. Rev. Palaeobot. Palynol. 215, 1-22. doi: 10.1016/j.revpalbo.2014.12.004
Bou Dagher-Kharrat, M., Mariette, S., Lefèvre, F., Fady, B., Savouré, A., et al. (2007). Geographical diversity and genetic relationships among Cedrus species estimated by AFLP. Tree Genet. Genomes 3, 275-285. doi: 10.1007/s11295-006-0065-x
Cacho, I., Grimalt, J. O., Canals, M., Sbaffi, L., Shackleton, N. J., Schönfeld, J., et al. (2001). Variability of the western Mediterranean Sea surface temperature during the last 25,000 years and its connection with the Northern Hemisphere climatic changes. Paleoceanography 16, 40-52. doi: 10.1029/2000PA000502
Cheddadi, R. B., Fady, L., François, L., Hajar, J.-P., Suc, K., et al. (2009). Putative glacial refugia of Cedrus atlantica deduced from quaternary pollen records and modern genetic diversity. J. Biogeogr. 36, 1361-1371. doi: 10.1111/j.1365-2699.2008.02063.x
Cheddadi, R., Bouaissa, O., Rhoujjati, A., and Dezileau, L. (2016). Environmental changes in the moroccan western Rif Mountains over the last 9,000 years. Quaternaire 27, 15-25. doi: 10.4000/quaternaire.7517
Cheddadi, R., Guiot, J., and Jolly, D. (2001). The Mediterranean vegetation: what if the atmospheric CO2 increased? Landsc. Ecol. 16, 667-675. doi: 10.1023/A:1013149831734
Cheddadi, R., Lamb, H. F., Guiot, J., and van der Kaars, S. (1998). Holocene climatic change in Morocco: a quantitative reconstruction from pollen data. Clim. Dyn. 14, 883-890. doi: 10.1007/s003820050262
Cheddadi, R., Nourelbait, M., Bouaissa, O., Tabel, J., Rhoujjati, A., López-Sáez, J. A., et al. (2015). A history of human impact on Moroccan Mountain Landscapes. Afr. Archaeol. Rev. 32, 233-248. doi: 10.1007/s10437-015-9186-7
Davis, M. B., and Shaw, R. G. (2001). Range shifts and adaptive responses to quaternary climate change. Science 292, 673-679. doi: 10.1126/science.292.5517.673
DeMenocal, P., Ortiz, J., Guilderson, T., and Sarnthein, M. (2000). Coherent high- and low-latitude climate variability during the holocene warm period. Science 288, 2198-2202. doi: 10.1126/science.288.5474.2198
Dlugokencky, E. J., Lang, P. M., Masarie, K. A., Crotwell, A. M., and Crotwell, M. J. (2014). Atmospheric Carbon Dioxide Dry Air Mole Fractions from the NOAA ESRL Carbon Cycle Cooperative Global Air Sampling Network, 1968-2012. Version: 2013-08-28. Available online at: ftp://aftp.cmdl.noaa.gov/data/trace/symuscoregases/co2/flask/surface
Dobrowski, S. Z. (2011). A climatic basis for microrefugia: the influence of terrain on climate. Glob. Chang. Biol. 17, 1022-1035. doi: 10.1111/j.1365-2486.2010.02263.x
Dury, M., Hambuckers, A., Warnant, P., Henrot, A.-J., Favre, E., Ouberdous, M., et al. (2011). Response of the European forests to climate change: a modelling approach for the 21st century. iForest 4, 82-99. doi: 10.3832/ifor0572-004
Elias, S. A. (1997). The mutual climatic range method of palaeoclimate reconstruction based on insect fossils: new applications and interhemispheric comparisons. Quat. Sci. Rev. 16, 1217-1225. doi: 10.1016/S0277-3791(97)00029-2
Engler, R., Randin, C. F., Thuiller, W., Dullinger, S., Zimmermann, N. E., Araújo, M. B., et al. (2011). 21st century climate change threatens mountain flora unequally across Europe. Glob. Chang. Biol. 17, 2330-2341. doi: 10.1111/j.1365-2486.2010.02393.x
Epron, D. (1997). Effects of drought on photosynthesis and on the thermotolerance of photosystem II in seedlings of cedar [Cedrus atlantica and C. libani). J. Exp. Bot. 48, 1835-1841. doi: 10.1093/jxb/48.10.1835
Esper, J., Frank, D., Büntgen, U., Verstege, A., Luterbacher, J., and Xoplaki, E. (2007). Long-term drought severity variations in Morocco. Geophys. Res. Lett. 34, 1-5. doi: 10.1029/2007GL030844
Ezzahiri, M., and Belghazi, B. (2000). Synthèse de quelques résultats sur la régénération naturelle du cèdre de l'Atlas au Moyen Atlas (Maroc). Sci. Change. Planét. Sécheresse 11, 79-84.
Fady, B., Lefèvre, F., Reynaud, M., Vendramin, G. G., Dagher-Kharrat, M. B., Anzidei, M., et al. (2003). Gene flow among different taxonomic units: evidence from nuclear and cytoplasmic markers in Cedrus plantation forests. Theor. Appl. Genet. 107, 1132-1138. doi: 10.1007/s00122-003-1323-z
Feddi, N., Fauquette, S., and Suc, J. P. (2011). Histoire plio-pléistocène des écosystèmes végétaux de Méditerranée sud-occidentale: apport de l'analyse pollinique de deux sondages en mer d'Alboran. Geobios 44, 57-69. doi: 10.1016/j.geobios.2010.03.007
Fontaine, C., Dedoncker, N., De Vreese, R., Jacquemin, I., Marek, A., Van Herzele, A., et al. (2014). Towards participatory integrated valuation and modelling of ecosystem services under land-use change. J. Land. Use Sci. 9, 278-303. doi: 10.1080/1747423X.2013.786150
Gérard, J.-C., Nemry, B., Francois, L., and Warnant, P. (1999). The interannual change of atmospheric CO2: contribution of subtropical ecosystems? Geophys. Res. Lett. 26, 243-246. doi: 10.1029/1998GL900269
Graham, C. H., Carnaval, A. C., Cadena, C. D., Zamudio, K. R., Roberts, T. E., Parra, J. L., et al. (2014). The origin and maintenance of montane diversity: integrating evolutionary and ecological processes. Ecography 37, 711-719. doi: 10.1111/ecog.00578
Hajar, L., Khater, C., and Cheddadi, R. (2008). Vegetation changes during the late Pleistocene and Holocene in Lebanon: a pollen record from the Bekaa Valley. Holocene 18, 1089-1099. doi: 10.1177/0959683608095580
Hannah, L., Midgley, G., Andelman, S., Araújo, M., Hughes, G., Martinez-Meyer, E., et al. (2007). Protected area needs in a changing climate. Front. Ecol. Environ. 5, 131-138. doi: 10.1890/1540-9295(2007)5[131:PANIAC]2.0.CO;2
Hanski, I. (1991). Single-species metapopulation dynamics: concepts, models and observations. Biol. J. Linnean Soc. 42, 17-38. doi: 10.1111/j.1095-8312.1991.tb00549.x
Hanski, I. (1994). A practical model of metapopulation dynamics. J. Anim. Ecol. 63, 151-162. doi: 10.2307/5591
Hanski, I. (1998). Metapopulation dynamics. Nature 396, 41-49. doi: 10.1038/23876
Hanski, I. (2005). Landscape fragmentation, biodiversity loss and the societal response. Eur. Mol. Biol. Org. 6, 388-392. doi: 10.1038/sj.embor.7400398
Hanski, I., and Ovaskainen, O. (2003). Metapopulation theory for fragmented landscapes. Theor. Popul. Biol. 64, 119-127. doi: 10.1016/S0040-5809(03)00022-4
Harris, I., Jones, P. D., Osborn, T. J., and Lister, D. H. (2014). Updated high-resolution grids of monthly climatic observations-the CRU TS3.10 Dataset. Int. J. Climatol. 34, 623-642. doi: 10.1002/joc.3711
Hessl, A. E., and Baker, W. L. (1997). Spruce and fir regeneration and climate in the forest-tundra ecotone of rocky mountain national park, Colorado, U.S.A. Arct. Alp. Res. 29, 173-183. doi: 10.2307/1552044
Hewitt, G. M. (2000). The genetic legacy of the quaternary ice ages. Nature 405, 907-913. doi: 10.1038/35016000
Hewitt, G. M. (2004). Genetic consequences of climatic oscillations in the Quaternary. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 359, 183-195. doi: 10.1098/rstb.2003.1388
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., and Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965-1978. doi: 10.1002/joc.1276
Horne, D. J. (2007). A Mutual temperature range method for quaternary palaeoclimatic analysis using European nonmarine Ostracoda. Quat. Sci. Rev. 26, 1398-1415. doi: 10.1016/j.quascirev.2007.03.006
Hubert, B., Francois, L. M., Warnant, P., and Strivay, D. (1998). Stochastic generation of meteorological variables and effects on global models of water and carbon cycles in vegetation and soils. J. Hydrol. 212, 318-334. doi: 10.1016/S0022-1694(98)00214-5
Hughes, P. D., Fenton, C. R., and Gibbard, P. L. (2011). "Quaternary Glaciations of the Atlas Mountains, North Africa," in Developments in Quaternary Science, Vol. 15, eds J. Ehlers, P. L. Gibbard, and P.D. Hughes (Amsterdam: Elsevier), 1065-1074.
Hylander, K., Ehrlén, J., Luoto, M., and Meineri, E. (2015). Microrefugia: not for everyone. Ambio 44, 60-68. doi: 10.1007/s13280-014-0599-3
IPCC (2014). "Climate change 2014: synthesis report," in Contribution of Working Groups, I., II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, eds R. K. Pachauri, L. A. Meyer, and Core Writing Team (Geneva: IPCC), 151.
IUCN (2017). The IUCN Red List of Threatened Species. Version 2017-1. Available online at: http://www.iucnredlist.org.
Jalas, J., and Suominen, J. (1973). Atlas Florae Europaeae. Distribution of Vascular Plants in Europe. 2. Gymnospermae (Pinaceae to Ephedraceae). The Committee for Mapping the Flora of Europe and Societas Biologica Fennica, Helsinki.
Jalas, J., and Suominen, J. (1979). Atlas Florae Europaea. Distribution of Vascular Plants in Europe Vol 4. The Committee for Mapping the Flora of Europe and Societas Biologica Fennica, Helsinki.
Jalas, J., and Suominen, J. (1980). Atlas Florae Europaeae: Distribution of Vascular Plants in Europe. Vol 5. Chenopodaceae to Basellaceae. Committee for Mapping the Flora of Europe and Societas Biologica Fennica, Helsinki.
Keppel, G., Van Niel, K. P., Wardell-Johnson, G. W., Yates, C. J., Byrne, M., Mucina, L., et al. (2012). Refugia: identifying and understanding safe havens for biodiversity under climate change. Glob. Ecol. Biogeogr. 21, 393-404. doi: 10.1111/j.1466-8238.2011.00686.x
Körner, C. (2016). When it gets cold, plant size matters-a comment on tree line. J. Veg. Sci. 27, 6-7. doi: 10.1111/jvs.12366
Körner, C., and Paulsen, J. (2004). A world-wide study of high altitude treeline temperatures. J. Biogeogr. 31, 713-732. doi: 10.1111/j.1365-2699.2003.01043.x
Kühl, N., Gebhardt, C., Litt, T., and Hense, A. (2002). Probability density functions as botanical-climatological transfer functions for climate reconstruction. Quat. Res. 58, 381-392. doi: 10.1006/qres.2002.2380
Ladjal, M., Huc, R., and Ducrey, M. (2005). Drought effects on hydraulic conductivity and xylem vulnerability to embolism in diverse species and provenances of Mediterranean cedars. Tree Physiol. 25, 1109-1117. doi: 10.1093/treephys/25.9.1109
Lamb, H. F., and van der Kaars, S. (1995). Vegetational response to Holocene climatic change: pollen and palaeolimnological data from the Middle Atlas, Morocco. Holocene 5, 400-408. doi: 10.1177/095968369500500402
Lamb, H. F., Damblon, F., and Maxted, R. W. (1991). Human impact on the vegetation of the Middle Atlas, Morocco, during the last 5000 years. J. Biogeogr. 18, 519-532. doi: 10.2307/2845688
Lamb, H. F., Gasse, F., Benkaddour, A., El Hamouti, N., van der Kaars, S., Perkins, W. T., et al. (1995). Relation between century- scale Holocene arid intervals in tropical and temperate zones. Nature 373, 134-137. doi: 10.1038/373134a0
Lamb, H. F., Roberts, N., Leng, M., Barker, P., Benkaddour, A., and van der Kaars, S. (1999). Lake evolution in a semi-arid montane environment: responses to catchment change and hydroclimatic variation. J. Paleolimnol. 21, 325-343. doi: 10.1023/A:1008099602205
Laurent, J.-M., Francois, L., Bar-Hen, A., Bel, L., and Cheddadi, R. (2008). European bioclimatic affi- nity groups: data-model comparisons. Glob. Planet. Change 61, 28-40. doi: 10.1016/j.gloplacha.2007.08.017
Lenoir, J., Gégout, J. C., Marquet, P. A., de Ruffray, P., and Brisse, H. (2008). A significant upward shift in plant species optimum elevation during the 20th century. Science 320, 1768-1771. doi: 10.1126/science.1156831
Leonelli, G., Pelfini, M., di Cella, U. M., and Garavaglia, V. (2011). Climate warming and the recent treeline shift in the European Alps: the role of geomorphological factors in high-altitude sites. Ambio 40, 264-273. doi: 10.1007/s13280-010-0096-2
Linares, J. C., Taïqui, L., and Camarero, J. J. (2011). Increasing drought sensitivity and decline of Atlas Cedar (Cedrus atlantica) in the Moroccan Middle Atlas Forests. Forests 2, 777-796. doi: 10.3390/f2030777
Linstädter, J., Kehl, M., Broich, M., and López-Sáez, J. A. (2016). Chronostratigraphy, site formation processes and pollen record of Ifri n'Etsedda, NE Morocco. Quat. Int. 410, 6-29. doi: 10.1016/j.quaint.2015.11.017
Magri, D. (2012). Quaternary history of Cedrus in southern Europe. Ann. Di Bot. 2, 57-66. doi: 10.4462/annbotrm-10022
Magri, D., and Parra, I. (2002). Late quaternary western Mediterranean pollen records and African winds. Earth Planet. Sci. Lett. 200, 401-408. doi: 10.1016/S0012-821X(02)00619-2
Malcolm, J. R., Liu, C., Neilson, R. P., Hansen, L., and Hannah, L. (2006). Global warming and extinctions of endemic species from biodiversity hotspots. Conserv. Biol. 20, 538-548. doi: 10.1111/j.1523-1739.2006.00364.x
McGregor, H. V., Dima, M., Fischer, H. W., and Mulitza, S. (2007). Rapid 20th-century increase in coastal upwelling off northwest Africa. Science 315, 637-639. doi: 10.1126/science.1134839
Medail, F., and Quezel, P. (1997). Hot-spots analysis for conservation of plant biodiversity in the mediterranean basin. Ann. Missouri Bot. Gard. 84, 112-127. doi: 10.2307/2399957
Meinshausen, M., Smith, S. J., Calvin, K., Daniel, J. S., Kainuma, M. L., Lamarque, J.-F., et al. (2011). The RCP greenhouse gas concentrations and their extensions from 1765 to 2300. Clim. Change 109, 213. doi: 10.1007/s10584-011-0156-z
Mercuri, A. M., Sadori, L., and Uzquiano Ollero, P. (2011). Mediterranean and north-African cultural adaptations to mid-Holocene environmental and climatic changes. Holocene 21, 189-206. doi: 10.1177/0959683610377532
Moine, O., Rousseau, D.-D., Jolly, D., and Vianey-Liaud, M. (2002). Paleoclimatic reconstruction using mutual climatic range on terrestrial mollusks. Quat. Res. 57, 162-172. doi: 10.1006/qres.2001.2286
Moritz, C., and Agudo, R. (2013). The future of species under climate change: resilience or decline? Science 341, 504-508. doi: 10.1126/science.1237190
Mosblech, N. A. S., Bush, M., and van Woesik, R. (2011). On metapopulations and microrefugia: palaeoecological insights. J. Biogeogr. 38, 419-429. doi: 10.1111/j.1365-2699.2010.02436.x
Mosbrugger, V., and Utescher, T. (1997). The coexistence approach-a method for quantitative reconstructions of tertiary terrestrial palaeoclimate data using plant fossils. Palaeogeogr. Palaeoclimatol. Palaeoecol. 134, 61-86. doi: 10.1016/S0031-0182(96)00154-X
Navarro-Cerrillo, R. M., Manzanedo, R. D., Bohorque, J., Sanchez, R., Sanchez, J., Miguel, S., et al. (2013). Structure and spatio-temporal dynamics of cedar forests along a management gradient in the Middle Atlas, Morocco. For. Ecol. Manage. 289, 341-353. doi: 10.1016/j.foreco.2012.10.011
Nour El Bait, M., Rhoujjati, A., Eynaud, F., Benkaddour, A., Dezileau, L., Wainer, K., et al. (2014). An 18 000-year pollen and sedimentary record from the cedar forests of the Middle Atlas, Morocco. J. Quat. Sci. 29, 423-432. doi: 10.1002/jqs.2708
Ooms, J., James, D., DebRoy, S., Wickham, H., and Horner, J. (2016). RMySQL: Database Interface and 'MySQL' Driver for R. R Package Version 0.10.9. Available online at: https://CRAN.R-project.org/package=RMySQL.
Ouborg, N. J., and Eriksson, O. (2004). "Toward a metapopulation concept for plants," in Ecology, Genetics, and Evolution of Metapopulations, eds I. Hanski and O. E. Gaggiotti (San Diego, CA: Elsevier), 447-469.
Pautasso, M. (2009). Geographical genetics and the conservation of forest trees. Perspect. Plant Ecol. Evol. Syst. 11, 157-189. doi: 10.1016/j.ppees.2009.01.003
Petit, R. J., El Mousadik, A., and Pons, O. (1998). Identifying populations for consevation on basis of genetic markers. Conserv. Biol. 12, 844-855. doi: 10.1046/j.1523-1739.1998.96489.x
Pross, J., Klotz, S., and Mosbrugger, V. (2000). Reconstructing paleotemperatures for the early and middle pleistocene using the mutual climatic range method based on plant fossil. Quat. Sci. Rev. 19, 1785-1799. doi: 10.1016/S0277-3791(00)00089-5
Qiao, C.-Y., Ran, J.-H., Li, Y., and Wang, X.-Q. (2007). Phylogeny and biogeography of Cedrus (Pinaceae) inferred from sequences of seven paternal chloroplast and maternal mitochondrial DNA regions. Ann. Bot. 100, 573-580. doi: 10.1093/aob/mcm134
Raghunathan, N., François, L., Huynen, M.-C., Oliveira, L., and Hambuckers, A. (2015). Modelling the distribution of key tree species used by lion tamarins in the Brazilian Atlantic forest under a scenario of future climate change. Reg. Environ. Change 15, 683-693. doi: 10.1007/s10113-014-0625-9
R Core Team (2014). R: A Language and Environment for Statistical Computing. Vienna: Foundation for Statistical Computing. Available online at: URL http://www.R-project.org/
Rehfeldt, G. E., and Jaquish, B. C. (2010). Ecological impacts and management strategies for western larch in the face of climate-change. Mitig. Adapt. Strateg. Glob. Change 15, 283-306. doi: 10.1007/s11027-010-9217-2
Reille, M. (1976). Analyse pollinique de sédiments postglaciaires dans le Moyen Atlas et le Haut Atlas marocains: premiers résultats. Ecol. Mediterr. 2, 155-170.
Reille, M. (1977). Contribution pollenanalytique a l'histoire holocène de la végétation des montagnes du rif (Maroc septentrional). Bull. AFEQ 50, 53-76.
Reimer, P. J., Bard, E., Bayliss, A., Warren Beck, J., Blackwell, P. G., Bronk, C., et al. (2013). IntCal13 and Marine13 Radiocarbon Age Calibration Curves 0-50,000 Years cal BP. Radiocarbon 55, 1869-1887. doi: 10.2458/azu_js_rc.55.16947
Renau-Morata, B., Nebauer, S. G., Sales, E., Allainguillaume, J., Caligari, P., and Segura, J. (2005). Genetic diversity and structure of natural and managed populations of Cedrus atlantica (Pinaceae) assessed using random amplified polymorphic DNA. Am. J. Bot. 92, 875-884. doi: 10.3732/ajb.92.5.875
Rhanem, M. (2011). Aridification du climat régional et remontée de la limite inférieure du cèdre de l'Atlas (Cedrus atlantica Manetti) aux confins de la plaine de Midelt (Maroc). Physiol. Géo. 5, 143-165. doi: 10.4000/physio-geo.1983
Rull, V. (2009). Microrefugia. J. Biogeogr. 36, 481-484. doi: 10.1111/j.1365-2699.2008.02023.x
Rull, V. (2011). Neotropical biodiversity: timing and potential drivers. Trends Ecol. Evol. 26, 508-513. doi: 10.1016/j.tree.2011.05.011
Sarmiento, F. O. (2011). "Sustainability and the biosphere reserve: a compromise between biodiversity, conservation and farmscape transformation," in An Austrian Contribution to the 40th Anniversary of UNESCO's MAB Biosphere Reserves in the Mountains of the World. Excellence in the Clouds? (Vienna: Austrian Academy of Sciences Press), 19-23.
Schenk, H. J., and Jackson, R. B. (2002). The global biogeography of roots. Ecol. Monogr. 72, 311-328. doi: 10.1890/0012-9615(2002)072[0311:TGBOR]2.0.CO;2
Schepaschenko, D., Shvidenko, A., Usoltsev, V., Lakyda, P., Luo, Y., Vasylyshyn, R., et al. (2017). A dataset of forest biomass structure for Eurasia. Sci. Data 4, 170070. doi: 10.1038/sdata.2017.70
Soliani, C., Gallo, L., and Marchelli, P. (2012). Phylogeography of two hybridizing southern beeches (Nothofagus spp.) with different adaptive abilities. Tree Genet. Genomes 8, 659-673. doi: 10.1007/s11295-011-0452-9
Stuiver, M., Reimer, P. J., and Reimer, R. (2013). Radiocarbon Calibration Program Revision 7.0. Copyright 1986-2013. Available online at: http://calib.qub.ac.uk/calib/calib.htm.
Tabel, J., Khater, C., Rhoujjati, A., Dezileau, L., Bouimetarhan, I., Carre, M., et al. (2016). Environmental changes over the past 25000 years in the southern Middle Atlas, Morocco. J. Quat. Sci. 31, 93-102. doi: 10.1002/jqs.2841
Taberlet, P., and Cheddadi, R. (2002). Quaternary refugia and persistence of biodiversity. Science 297, 2009-2010. doi: 10.1126/science.297.5589.2009
Takos, I., and Merou, T. (2001). Effect of storage conditions and seed treatment on germination of Cedrus deodora Loud. and C. libani A. Rich. Silvae Genet. 50, 205-208.
Terrab, A., Paun, O., Talavera, S., Tremetsberger, K., Arista, M., and Stuessy, T. F. (2006). Genetic diversity and population structure in natural populations of Moroccan Atlas Cedar (Cedrus atlantica; Pinaceae) determined with CPSSR markers. Am. J. Bot. 93, 1274-1280. doi: 10.3732/ajb.93.9.1274
Thuiller, W., Lavorel, S., Araújo, M. B., Sykes, M. T., and Prentice, I. C. (2005). Climate change threats to plant diversity in Europe. Proc. Natl. Acad. Sci. U.S.A. 102, 8245-8250. doi: 10.1073/pnas.0409902102
Tierney, J. E., Pausata, F. S. R., and deMenocal, P. (2017). Rainfall regimes of the Green Sahara. Sci. Adv. 3, 1-9. doi: 10.1126/sciadv.1601503
Till, C., and Guiot, J. (1990). Reconstruction of precipitation in Morocco Since 1100 A.D. Based on Cedrus atlantica tree-ring widths. Quat. Res. 33, 337-351. doi: 10.1016/0033-5894(90)90060-X
Tucker, C. J., Dregne, H. E., and Newcomb, W. W. (1991). Expansion and contraction of he Sahara desert from 1980 to 1990. Science 253, 299-301. doi: 10.1126/science.253.5017.299
Tzedakis, P. C., Lawson, I. T., Frogley, M. R., Hewitt, G. M., and Preece, R. C. (2002). Buffered tree population changes in a quaternary refugium: evolutionary implications. Science 297, 2044-2047. doi: 10.1126/science.1073083
Willis, K. J., and Bhagwat, S. A. (2010). Questions of importance to the conservation of biological diversity: answers from the past. Clim. Past 6, 759-769. doi: 10.5194/cp-6-759-2010
Willis, K. J., and Birks, H. J. B. (2006). What is natural? The need for a long-term perspective in biodiversity conservation. Science 314, 1261-1265. doi: 10.1126/science.1122667
Willis, K. J., Araújo, M. B., Bennett, K. D., Figueroa-Rangel, B., Froyd, C. A., et al. (2007). How can a knowledge of the past help to conserve the future? Biodiversity conservation and the relevance of long-term ecological studies. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 362, 175-186. doi: 10.1098/rstb.2006.1977
Wolf, D. E., Takebayashi, N., and Rieseberg, L. H. (2001). Predicting the risk of extinction through hybridization. Conserv. Biol. 15, 1039-1053. doi: 10.1046/j.1523-1739.2001.0150041039.x
Wright, J. (1952). "Pollen dispersion of some forest trees," in Station Paper 46, United States Department of Agriculture, Forest Service, Northeastern Forest Experiment Station (Upper Darby, PA).
Zapata, L., Lopez-Saez, J. A., Ruiz-Alonso, M., Linstadter, J., Perez-Jorda, G., Morales, J., et al. (2013). Holocene environmental change and human impact in NE Morocco: palaeobotanical evidence from Ifri Oudadane. Holocene 23, 1286-1296. doi: 10.1177/0959683613486944
Zielhofer, C., Fletcher, W. J., Mischke, S., De Batist, M., Campbell, J. F. E., Joannin, S., et al. (2017). Atlantic forcing of Western Mediterranean winter rain minima during the last 12,000 years. Quat. Sci. Rev. 157, 29-51. doi: 10.1016/j.quascirev.2016.11.037