An understanding of the interactions between climate change and forest structure on tree growth are needed for decision making in forest conservation and management. In this paper, we investigated the relative contribution of tree features and stand structure on Atlas cedar ( Cedrus atlantica) radial growth in forests that have experienced heavy grazing and logging in the past. Dendrochronological methods were applied to quantify patterns in basal-area increment and drought sensitivity of Atlas cedar in the Middle Atlas, northern Morocco. We estimated the tree-to-tree competition intensity and quantified the structure in Atlas cedar stands with contrasting tree density, age, and decline symptoms. The relative contribution of tree age and size and stand structure to Atlas cedar growth decline was estimated by variance partitioning using partial-redundancy analyses. Recurrent drought events and temperature increases have been identified from local climate records since the 1970s. We detected consistent growth declines and increased drought sensitivity in Atlas cedar across all sites since the early 1980s. Specifically, we determined that previous growth rates and tree age were the strongest tree features, while Quercus rotundifolia basal area was the strongest stand structure measure related to Atlas cedar decline. As a result, we suggest that Atlas cedar forests that have experienced severe drought in combination with grazing and logging may be in the process of shifting dominance toward more drought-tolerant species such as Q. rotundifolia.
References
[1]
Williamson, G.B.; Laurance, W.F.; Oliveira, A.A.; Delamonica, P.; Gascon, C.; Lovejoy, T.E.; Pohl, L. Amazonia tree mortality during the 1997 El Ni？o drought. Conserv. Biol. 2000, 14, 1538–1542.
[2]
Rice, K.J.; Matzner, S.L.; Byer, W.; Brown, J.R. Patterns of tree dieback in Queensland, Australia: The importance of drought stress and the role of resistance to cavitation. Oecologia 2004, 139, 190–198.
[3]
Dobbertin, M. Tree growth as indicator of tree vitality and of tree reaction to environmental stress: A review. Eur. J. Forest Res. 2005, 124, 319–333.
[4]
Van Mantgem, P.J.; Stephenson, N.L.; Byrne, J.C.; Daniels, L.D.; Franklin, J.F.; Fulé, P.Z.; Harmon, M.E.; Larson, A.J.; Smith, J.M.; Taylor, A.H.; et al. Widespread increase of tree mortality rates in the western United States. Science 2009, 323, 521–524.
[5]
Allen, C.D.; Macalady, A.K.; Chenchouni, H.; Bachelet, D.; McDowell, N.; Vennetier, M.; Kitzberger, T.; Rigling, A.; Breshears, D.D.; Hogg, E.H.; et al. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For. Ecol. Manag. 2010, 259, 660–684.
[6]
Pe？uelas, J.; Lloret, F.; Montoya, R. Severe drought effects on mediterranean woody flora in Spain. For. Sci. 2001, 47, 214–218.
[7]
Martínez-Vilalta, J.; Pi？ol, J. Drought-induced mortality and hydraulic architecture in pine populations of the NE Iberian Peninsula. For. Ecol. Manag. 2002, 161, 247–256.
[8]
Sarris, D.; Christodoulakis, D.; K？rner, C. Impact of recent climatic change on growth of low elevation eastern Mediterranean forest trees. Clim. Change 2010, 106, 203–223.
[9]
Linares, J.C.; Tíscar, P.A. Climate change impacts and vulnerability of the southern populations of Pinus nigra subsp. salzmannii. Tree Physiol. 2010, 30, 795–806.
[10]
Boisvenue, C.; Running, S.W. Impacts of climate change on natural forest productivity-evidence since the middle of the 20th century. Glob. Change Biol. 2006, 12, 1–12.
[11]
Thuiller, W.; Albert, C.; Araujo, M.B.; Berry, P.M.; Cabeza, M.; Guisan, A.; Hickler, T.; Midgley, G.F.; Paterson, J.; Schurr, F.M.; et al. Predicting global change impacts on plant species’ distributions: Future challenges. Perspect. Plant Ecol. Evol. Syst. 2008, 9, 137–152.
[12]
Gonzalez, P.; Neilson, R.P.; Drapek, R.J. Global patterns in the vulnerability of ecosystems to vegetation shifts due to climate change. Glob. Ecol. Biogeogr. 2010, 19, 755–768.
[13]
Bigler, C.J.; Gricar, J.; Bugmann, H.; Cufar, K. Growth patterns as indicators of impending tree death in silver fir. For. Ecol. Manag. 2004, 199, 183–190.
[14]
Bréda, N.; Huc, R.; Granier, A.; Dreyer, E. Temperate forest trees and stands under severe drought: A review of ecophysiological responses, adaptation processes and long-term consequences. Ann. For. Sci. 2006, 63, 625–644.
[15]
Wunder, J.; Reineking, B.; Bigler, C.J.; Bugmann, H. Predicting tree mortality from growth data: How virtual ecologists can help real ecologists. J. Ecol. 2008, 96, 174–187.
[16]
McDowell, N.; Allen, C.D.; Marshall, L. Growth, carbon isotope discrimination, and climate-induced mortality across a Pinus ponderosa elevation transect. Glob. Change Biol. 2010, 16, 399–415.
[17]
Allen, C.D.; Breshears, D.D. Drought-induced shift of a forest woodland ecotone: Rapid landscape response to climate variation. Proc. Natl. Acad. Sci. USA 1998, 95, 14839–14842.
[18]
Aitken, S.N.; Yearman, S.; Holliday, J.A.; Wang, T.; Curtis-McLane, S. Adaptation, migration or extirpation: Climate change outcomes for tree populations. Evol. Appl. 2008, 1, 95–111.
[19]
Galiano, L.; Martinez-Vilalta, J.; Lloret, F. Drought-induced multifactor decline of Scots pine in the Pyrenees and potential vegetation change by the expansion of co-occurring oak species. Ecosystems 2010, 13, 978–991.
[20]
Pautasso, M.; Dehnen-Schmutz, K.; Holdenrieder, O.; Pietravalle, S.; Salama, N.; Jeger, M.J.; Lange, E.; Hehl-Lange, S. Plant health and global change—Some implications for landscape management. Biol. Rev. 2010, 85, 729–755.
[21]
Bala, G.; Caldeira, K.; Wickett, M.; Phillips, T.J.; Lobell, D.B.; Delire, C.; Mirin, A. Combined climate and carbon-cycle effects of large-scale deforestation. Proc. Natl. Acad. Sci. USA 2007, 104, 6550–6555.
[22]
Bonan, G.B. Forests and climate change: Forcings, feedbacks, and the climate benefits of forests. Science 2008, 320, 1444–1449.
[23]
Rotenberg, E.; Yakir, D. Contribution of semi-arid forests to the climate system. Science 2010, 327, 451–454.
[24]
Aussenac, G. Interactions between forest stands and microclimate: Ecophysiological aspects and consequences for silviculture. Ann. For. Sci. 2000, 57, 287–301.
[25]
Stephenson, N.L. Climatic control of vegetation distribution: The role of water balance. Am. Nat. 1990, 135, 649–670.
[26]
Linares, J.C.; Camarero, J.J.; Carreira, J.A. Competition modulates the adaptation capacity of forests to climatic stress: Insights from recent growth decline and death in relict stands of the Mediterranean fir Abies pinsapo. J. Ecol. 2010, 98, 592–603.
[27]
Peet, R.K.; Christensen, N.L. Competition and tree death. BioScience 1987, 37, 586–594.
[28]
Kenkel, N.C. Pattern of self-thinning in jack pine: Testing the random mortality hypothesis. Ecology 1988, 69, 1017–1024.
[29]
Runkle, J.R. Canopy tree turnover in old-growth mesic forests of Eastern North America—Statistical data included. Ecology 2000, 79, 1768–1780.
[30]
Suarez, M.L.; Kitzberger, T. Recruitment patterns following a severe drought: Long-term compositional shifts in Patagonian forests. Can. J. For. Res. 2008, 38, 3002–3010.
[31]
Oliver, C.D.; Larson, B.C. Forest Stand Dynamics; McGraw-Hill: New York, NY, USA, 1990; p. 467.
[32]
Veblen, T.T. Regeneration dynamics. In Plant Succession: Theory and Prediction; Glenn-Lewin, D.C., Peet, R.K., Veblen, T.T., Eds.; Chapman and Hall: London, UK, 1992; pp. 152–187.
[33]
Abrams, M.D.; Orwig, D.A. A 300-year history of disturbance and canopy recruitment for co-occurring white pine and hemlock on the Allegheny Plateau, USA. J. Ecol. 1996, 84, 353–363.
[34]
Condit, R. Ecological implications of changes in drought patterns: Shifts in forest composition in Panama. Clim. Change 1998, 39, 413–427.
[35]
Benabid, A. Biogéographie phytosociologie et phytodynamique des cédraies de l'Atlas Cedrus atlantica (Manetti). Le cèdre de l'Atlas. Actes du séminaire international sur le cèdre de l'Atlas. Annal. Rech. For. Maroc 1994, 27, 62–76.
[36]
Cheddadi, R.; Fady, B.; Fran？is, L.; Hajar, L.; Suc, J.-P.; Huang, K.; Demateau, M.; Vendramin, G.; Ortu, E. Putative glacial refugia of Cedrus atlantica deduced from quaternary pollen records and modern genetic diversity. J. Biogeogr. 2009, 36, 1361–1371.
[37]
Et-tobi, M.; Mhirit, O.; Benzyane, M. Changements climatiques, dégradations et dépérissements: Arguments et nouveaux outils pour une reforme de la sylviculture des cédraies au Maroc. Ann. Rech. For. Maroc 2009, 41, 27–47.
[38]
Bentouati, A. La situation du cèdre de l'Atlas en Algérie. Forêt méditerr. 2008, 29, 203–208.
[39]
Mokrim, A. Dépérisement du cèdre de l'Atlas: Ambiance climatique et bilan de la croissance radiale. Ann. Rech. For. Maroc 2009, 41, 48–68.
[40]
Chenchouni, H.; Abdelkrim, S.B.; Athmane, B. The deterioration of the Atlas Cedar (Cedrus atlantica) in Algeria. Presented at the conference Adaptation of Forests and Forest Management to Changing Climate with Emphasis on Forest Health: A Review of Science, Policies, and Practices, Ume？, Sweden, 25–28 August 2008.
[41]
Barbero, M.; Bonin, G.; Loisel, R.; Quezel, P. Changes and disturbances of forest ecosystems caused by human activities in the western part of the mediterranean basin. Vegetatio 1990, 87, 151–173.
[42]
Camperio Ciani, A.; Martinoli, C.; Capiluppi, C.; Arahou, M.; Mouna, M. Effects of water availability and habitat quality on bark-stripping behavior in Barbary macaques. Conserv. Biol. 2001, 15, 259–265.
[43]
Ferris-Kaan, R.; Peace, A.J.; Humphrey, J.W. Assessing structural diversity in managed forests. In Assessment of Biodiversity for Improved Forest Planning; Bachmann, P., Kohl, M., Paivinen, R., Eds.; Kluwer Academic Publishers: Dordrecht, The Netherlands, 1998; pp. 331–342.
[44]
Slik, J.W.F. El Ni？o droughts and their effects on tree species composition and diversity in tropical rain forests. Oecologia 2004, 141, 114–120.
[45]
Kelly, A.E.; Goulden, M.L. Rapid shifts in plant distribution with recent climate change. Proc. Natl. Acad. Sci. USA 2008, 105, 11823–11826.
[46]
Mhirit, O. Le cèdre de l'Atlas (Cedrus atlantica Manetti). Présentation générale et état des connaissances à travers le reseau Silva Mediterranea ‘Le Cèdre'. Le cèdre de l'Atlas. Actes du seminaire international sur le cèdre de l'Atlas. Ann. Rech. For. Maroc 1994, 27, 4–21.
[47]
Hegyi, F. A Simulation Model for Managing Jack-Pine Stands. In Growth Models for Tree and Stand Simulation; Fries, J., Ed.; Royal College of Forestry: Stockholm, Sweden, 1974; pp. 74–90.
[48]
Zuur, A.F.; Ieno, E.N.; Smith, G.M. Analysing Ecological Data; Springer: New York, NY, USA, 2007; p. 680.
[49]
Holmes, R.L. Computer-assisted quality control in tree-ring dating and measurement. Tree-Ring Bull. 1983, 43, 68–78.
[50]
Esper, J.; Frank, D.C.; Büntgen, U.; Verstege, A.; Luterbacher, J.; Xoplaki, E. Long-term drought severity variations in Morocco. Geophys. Res. Lett. 2007, 34, L17702.
[51]
Till, C.; Guiot, J. Reconstruction of precipitation in Morocco since 1100 AD based on Cedrus atlantica tree-ring widths. Quat. Res. 1999, 33, 337–351.
[52]
Touchan, R.; Anchukaitis, K.J.; Meko, D.M.; Attalah, S.; Baisan, C.; Aloui, A. Long term context for recent drought in northwestern Africa. Geophys. Res. Lett. 2008, 35, L13705.
[53]
Luterbacher, J.; Dietrich, D.; Xoplaki, E.; Grosjean, M.; Wanner, H. European seasonal and annual temperature variability, trends and extremes since 1500. Science 2004, 303, 1499–1503.
[54]
Norrant, C.; Douguédroit, A. Monthly and daily precipitation trends in the Mediterranean (1950–2000). Theor. Appl. Climatol. 2006, 88, 89–106.
[55]
Luterbacher, J.; Xoplaki, E.; Casty, C.; Wanner, H.; Pauling, A.; Küttel, M.; Rutishauser, T.; Br？nnimann, S.; Fischer, E.; Fleitmann, D.; et al. Mediterranean climate variability over the last centuries: A review. In The Mediterranean Climate: An Overview of the Main Characteristics and Issues; Lionello, P., Malanotte-Rizzoli, P., Boscolo, R., Eds.; Elsevier: Amsterdam, The Netherlands, 2006; pp. 27–148.
[56]
Xoplaki, E.; González-Rouco, J.F.; Luterbacher, J.; Wanner, H. Wet season Mediterranean precipitation variability: Influence of large-scale dynamics and trends. Clim. Dyn. 2004, 23, 63–78.
[57]
Eilmann, B.; Weber, P.; Rigling, D.; Eckstein, D. Growth reactions of Pinus sylvestris L. and Quercus pubescens Willd. to drought years at a xeric site in Valais, Switzerland. Dendrochronologia 2006, 23, 121–132.
[58]
Martínez-Vilalta, J.; López, B.C.; Adell, N.; Badiella, L.; Ninyerola, M. Twentieth century increase of Scots pine radial growth in NE Spain shows strong climate interactions. Glob. Change Biol. 2008, 14, 2868–2881.
[59]
Camarero, J.J.; Padró, A.; Martin-Bernal, E.; Gil-Pelegrín, E. Aproximación dendroecológica al decaimiento del abeto (Abies alba Mill.) en el pirineo Aragonés. Montes 2002, 70, 26–33.
[60]
Macias, M.; Andreu, L.; Bosch, O.; Camarero, J.J.; Gutiérrez, E. Increasing aridity is enhancing silver fir Abies alba (Mill.) water stress in its south-western distribution limit. Clim. Change 2006, 79, 289–313.
[61]
Linares, J.C.; Camarero, J.J.; Carreira, J.A. Interacting effects of climate and forest-cover changes on mortality and growth of the southernmost European fir forests. Glob. Ecol. Biogeogr. 2009, 18, 485–497.
[62]
Camperio Ciani, A.; Mouna, M. Human and environmental causes of the rapid decline of the Barbary Macaque in the Middle Atlas of Morocco. In The Barbary Macaque: Biology; Hodges, J.K., Cortes, J., Eds.; Management & Conservation, Nottingham University Press: Nottingham, UK, 2007.
[63]
Mehlman, P. Comparative density, demography, and ranging behavior of Barbary macaques (Macaca sylvanus) in marginal and prime conifer habitats. Int. J. Primatol. 1989, 10, 269–292.
Breshears, D.D.; Allen, C.D. The importance of rapid, disturbance-induced losses in carbon management and sequestration. Glob. Ecol. Biogeogr. 2002, 11, 1–5.
[66]
Breda, N.; Granier, A.; Aussenac, G. Effects of thinning on soil water balance and tree water relations, transpiration and growth in oak forest (Quercus petraea (Matt) Liebl.). Tree Physiol. 1995, 15, 295–306.
[67]
Aussenac, G.; Finkelstein, D. Influence de la sécheresse sur la croissance et la photosyntheses du Cèdre. Ann. Sci. For. 1983, 40, 67–77.
[68]
Till, C. The summary response function of Cedrus atlantica (Endl.) Carriere in Morocco. Tree-Ring Bull. 1987, 47, 23–36.
