Declining hydraulic performances and low carbon investments in tree rings predate Scots pine drought-induced mortality

Trees - Structure and Function

Volumn 28, Issue 6, 2014, Pages 1737-1750

  Hereş, Ana Maria ^a,b   Camarero, Jesús Julio ^c   López, Bernat C ^a,b   Martínez Vilalta, Jordi ^a,b  

^a CREAF   (Spain)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c INSTITUTO PIRENAICO DE ECOLOGÍA   (Spain)

Author keywords

Drought; Mortality; Scots pine; Tracheid; Tree ring; Wood anatomy

Indexed keywords

CARBON; DETERIORATION; DROUGHT; DUCTS; RESINS; WOOD;

MORTALITY; SCOTS PINE; TRACHEID; TREE RINGS; WOOD ANATOMY;

FORESTRY;

DROUGHT; MORTALITY; PINUS SYLVESTRIS; WOOD STRUCTURE;

PINUS SYLVESTRIS;

EID: 84919915493     PISSN: 09311890     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00468-014-1081-3     Document Type: Article

References (79)

1. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD et al (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manage 259:660–684
2. Anderegg WRL, Berry JA, Field CB (2012) Linking definitions, mechanisms, and modelling of drought-induced tree death. Trends Plant Sci 17:693–700
3. Anderegg WRL, Plavcova L, Anderegg LDL, Hacke UG, Berry JA, Field CB (2013) Drought’s legacy: multiyear hydraulic deterioration underlies widespread aspen forest die-off and portends increased future risk. Global Ch Biol 19:1188–1196
4. Barbéro M, Loisel R, Quézel P, Richardson DM, Romane F (1998) Pines of the Mediterranean basin. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 153–170
5. Bigler C, Bräker OU, Bugmann H, Dobbertin M, Rigling A (2006) Drought as an inciting mortality factor in Scots pine stands of the Valais, Switzerland. Ecosystems 9:330–343
6. Bréda N, Huc R, Granier A, Dreyer E (2006) Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Ann For Sci 63:625–644
7. Brodribb TJ, Cochard H (2009) Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol 149:575–584
8. Camarero JJ, Guerrero-Campo J, Gutiérrez E (1998) Tree-ring growth and structure of Pinus uncinata and Pinus sylvestris in the Central Spanish Pyrenees. Arct Alp Res 30:1–10
9. Camarero JJ, Olano JM, Parras A (2010) Plastic bimodal xylogenesis in conifers from continental Mediterranean climates. New Phytol 185:471–480
10. Camarero JJ, Sangüesa Barreda G, Alla AQ, González de Andrés E, Maestro Martínez M, Vicente-Serrano SM (2012) Los precedentes y las respuestas de los árboles a sequías extremas revelan los procesos involucrados en el decaimiento de bosques mediterráneos de coníferas. Ecosistemas 21:22–30
11. Catalan Bachiller G, Gil Muñoz P, Galera Peral RM, Martin Albertos S, Agundez Leal D, Alia Miranda R (1991) Las regiones de procedencia de Pinus sylvestris L. y Pinus nigra Arn. subsp. salzmannii (Dunal) Franco de España. INIA-ICONA, Madrid
12. Cherubini P, Gartner BL, Tognetti R, Bräker OU, Schoch W, Innes JL (2003) Identification, measurement and interpretation of tree rings in woody species from Mediterranean climates. Biol Rev 78:119–148
13. Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ et al (2012) Global convergence in the vulnerability of forests to drought. Nature 491:752–755
14. Cochard H (1992) Vulnerability of several conifers to air embolism. Tree Physiol 11:73–83
15. Cochard H, Froux F, Mayr S, Coutand C (2004) Xylem wall collapse in water-stressed pine needles. Plant Physiol 134:401–408
16. Denne MP (1988) Definition of latewood according to Mork (1928). IAWA Bull 10:59–62
17. Denne MP, Dodd RS (1981) The environmental control of xylem differentiation. In: Barnett JR (ed) Xylem cell development. Castle House, Kent, pp 236–255
18. Eilmann B, Weber P, Rigling A, Eckstein D (2006) Growth reactions of Pinus sylvestris L. and Quercus pubescens Willd. to drought years at a xeric site in Valais Switzerland. Dendrochronologia 23:121–132
19. Eilmann B, Zweifel R, Buchmann N, Fonti P, Rigling A (2009) Drought-induced adaptation of the xylem in Scots pine and pubescent oak. Tree Physiol 29:1011–1020
20. Fonti P, von Arx G, García-González I, Eilmann B, Sass-Klaassen U, Gärtner H, Eckstein D (2010) Studying global change through investigation of the plastic responses of xylem anatomy in tree rings. New Phytol 185:42–53
21. Fritts HC (2001) Tree rings and climate. Blackburn Press, New Jersey
22. Galiano L, Martínez-Vilalta J, Lloret F (2010) Drought-induced multifactor decline of Scots pine in the Pyrenees and potential vegetation change by the expansion of co-occurring oak species. Ecosystems 13:978–991
23. Galiano L, Martínez-Vilalta J, Lloret F (2011) Carbon reserves and canopy defoliation determine the recovery of Scots pine 4 yr after a drought episode. New Phytol 190:750–759
24. Gaylord ML, Kolb TE, Pockman WT, Plaut JA, Yepez EA, Macalady AK, Pangle RE, McDowell NG (2013) Drought predisposes piñon-juniper woodlands to insect attack and mortality. New Phytol 198:567–578
25. Giorgi F, Lionello P (2008) Climate change projections for the Mediterranean region. Glob Planet Ch 63:90–104
26. Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA (2001) Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126:457–461
27. Hargreaves GH, Samani ZA (1982) Estimating potential evapotranspiration. J Irrig Drain Div ASCE 108:225–230
28. Hereş AM, Martínez-Vilalta J, Claramunt López B (2012) Growth patterns in relation to drought-induced mortality at two Scots pine (Pinus sylvestris L.) sites in NE Iberian Peninsula. Trees Str Funct 26:621–630
29. Hereter A, Sánchez JR (1999) Experimental areas of Prades and Montseny. In: Bellot J, Rodà F, Retana J, Gracia CA (eds) Ecology of Mediterranean evergreen Oak forests. Springer, Germany, pp 15–27
30. Hsiao TC, Acevedo E (1974) Plant responses to water deficits, water-use efficiency, and drought resistance. Agric Meteorol 14:59–84
31. IPCC (2013) Climate Change 2013: the Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge
32. Irvine J, Perks MP, Magnani F, Grace J (1998) The response of Pinus sylvestris to drought: stomatal control of transpiration and hydraulic conductance. Tree Physiol 18:393–402
33. Kane JM, Kolb TE (2010) Importance of resin ducts in reducing ponderosa pine mortality from bark beetle attack. Oecologia 164:601–609
34. Köppen W (1936) Das Geographische System der Klimate. In: Köppen W, Geiger R (eds) Handbuch der Klimatologie. Gebrüder Borntraeger, Berlin, pp 1–44
35. Levanič T, Čater M, McDowell NG (2011) Associations between growth, wood anatomy, carbon isotope discrimination and mortality in a Quercus robur forest. Tree Physiol 31:298–308
36. Martin-Benito D, Beeckman H, Cañellas I (2013) Influence of drought on tree rings and tracheid features of Pinus nigra and Pinus sylvestris in a mesic Mediterranean forest. Eur J For Res 132:33–45
37. Martínez-Vilalta J, Piñol J (2002) Drought-induced mortality and hydraulic architecture in pine populations of the NE Iberian Peninsula. For Ecol Manage 161:247–256
38. Martínez-Vilalta J, López BC, Adell N, Badiella L, Ninyerola M (2008) Twentieth century increase of Scots pine radial growth in NE Spain shows strong climate interactions. Glob Ch Biol 14:1–14
39. Martínez-Vilalta J, Cochard H, Mencuccini M, Sterck F, Herrero A, Korhonen JFJ, Llorens P, Nikinmaa E, Nolè A, Poyatos R, Ripullone F, Sass-Klaassen U, Zweifel R (2009) Hydraulic adjustments of Scots pine across Europe. New Phytol 184:353–364
40. Martínez-Vilalta J, Aguadé D, Banqué M, Barba J, Curiel Yuste J, Galiano L, Garcia N, Gómez M, Hereş AM, López BC, Lloret F, Poyatos R, Retana J, Sus O, Vayreda J, Vilà-Cabrera A (2012) Las poblaciones ibéricas de pino albar ante el cambio climático: con la muerte en los talones. Ecosistemas 21:15–21
41. Martίn JA, Esteban LG, de Palacios P, Garcίa Fernández F (2010) Variation in wood anatomical traits of Pinus sylvestris L. between Spanish regions of provenance. Trees Str Funct 24:1017–1028
42. Matías L, Jump AS (2012) Interactions between growth, demography and biotic interactions in determining species range limits in a warming world: the case of Pinus sylvestris. For Ecol Manage 282:10–22
43. Matlab (2010) Mathworks Company, Version 7.10 R2010a. Natick, Massachusetts
44. McCarroll D, Loader NJ (2004) Stable isotopes in tree rings. Quat Sci Rev 23:771–801
45. McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155:1051–1059
46. McDowell NG, Sevanto S (2010) The mechanisms of carbon starvation: how, when, or does it even occur at all? New Phytol 186:264–266
47. McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739
48. McDowell NG, Beerling DJ, Breshears DD, Fisher RA, Raffa KF, Stitt M (2011) The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol Evol 26:523–532
49. Nikolov N, Helmisaari H (1992) Silvics of the circumpolar boreal forest tree species. In: Shugart H, Leemans R, Bowan G (eds) A systems analysis of the global boreal forest. Cambridge University Press, Cambridge, pp 13–84
50. Ninyerola M, Pons X, Roure JM (2000) A methodological approach of climatological modeling of air temperature and precipitation through GIS techniques. Int J Climatol 20:1823–1841
51. Ninyerola M, Pons X, Roure JM (2007a) Monthly precipitation mapping of the Iberian Peninsula using spatial interpolation tools implemented in a geographic information system. Theor Appl Climatol 89:195–209
52. Ninyerola M, Pons X, Roure JM (2007b) Objective air temperature mapping for the Iberian Peninsula using spatial interpolation and GIS. Int J Climatol 27:1231–1242
53. Ogle K, Whitham TG, Cobb NS (2000) Tree-ring variation in pinyon predicts likelihood of death following severe drought. Ecology 81:3237–3243
54. Paine TD, Raffa KF, Harrington TC (1997) Interactions among scolytid bark beetles, their association fungi, and live host conifers. Ann Rev Entomol 42:179–206
55. Pasho E, Camarero JJ, de Luis M, Vicente-Serrano SM (2011) Impacts of drought at different time scales on forest growth across a wide climatic gradient in north-eastern Spain. Agric For Meteorol 151:1800–1811
56. Piñol J, Terradas J, Lloret F (1998) Climate warming, wildfire hazard, and wildfire occurrence in coastal Eastern Spain. Clim Ch 38:345–357
57. Pons X (1996) Estimación de la radiación solar a partir de modelos digitales de elevaciones. Propuesta metodológica. In: Juaristi J, Moro I (eds) VII Coloquio de Geografía Cuantitativa. Sistemas de Información Geográfica y Teledetección, Vitoria-Gasteiz, Spain, pp 87–97
58. Poyatos R, Aguadé D, Galiano L, Mencuccini M, Martínez-Vilalta J (2013) Drought-induced defoliation and long periods of near-zero gas exchange play a key role in accentuating metabolic decline of Scots pine. New Phytol 200:388–401
59. R (2013) R: A language and environment for statistical computing, Version 3.0. R foundation for statistical computing. Vienna, Austria
60. Rigling A, Brühlhart H, Bräker OU, Forster T, Schweingruber FH (2003) Effects of irrigation on diameter growth and vertical resin duct production in Pinus sylvestris L. on dry sites in the central Alps Switzerland. For Ecol Manage 175:285–296
61. Rigling A, Bigler C, Eilmann B, Feldmeyer-Christe E, Gimmi U, Ginzler C, Graf U, Mayer P, Vacchiano G, Weber P, Wohlgemuth T, Zweifel R, Dobbertin M (2013) Driving factors of a vegetation shift from Scots pine to pubescent oak in dry Alpine forests. Glob Ch Biol 19:229–240
62. Robertson A, Overpeck J, Rind D, Mosley-Thompson E, Zielinski G, Lean J, Koch D, Penner J, Tegen I, Healy R (2001) Hypothesized climate forcing time series for the last 500 years. J Geophys Res 106:14783–14803
63. Sala A, Piper F, Hoch G (2010) Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol 186:274–281
64. Sala A, Woodruff DR, Meinzer FC (2012) Carbon dynamics in trees: feast or famine? Tree Physiol 32:764–775
65. Seo J-W, Smiljanić M, Wilmking M (2014) Optimizing cell-anatomical chronologies of Scots pine by stepwise increasing the number of radial tracheid rows included—Case study based on three Scandinavian sites. Dendrochronologia 32:205–209
66. Sevanto S, McDowell NG, Dickman LT, Pangle R, Pockman WT (2014) How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant, Cell Environ 37:153–161
67. SPSS (2006) IBM Company, Version 15.0. Chicago, Illinois
68. Tyree MT, Zimmerman MH (2002) Xylem structure and the ascent of sap. Springer, New York
69. Vaganov EA (1990) The tracheidogram method in tree-ring analysis and its application. In: Cook ER, Kairiukstis LA (eds) Methods of dendrochronology: applications in the environmental sciences. Kluwer Academic Publishers, Dordrecht, pp 63–76
70. Vaganov EA, Hughes MK, Shashkin AV (2006) Growth dynamics of conifer tree rings: images of past and future environments. Springer, New York
71. Vicente-Serrano SM, Beguerίa S, López-Moreno JI (2010a) A multi-scalar drought index sensitive to global warming: the standardized precipitation evapotranspiration index. J Clim 23:1696–1718
72. Vicente-Serrano SM, Beguerίa S, López-Moreno JI, Angulo M, El Kenawy A (2010b) A new global 0.5° gridded dataset (1901–2006) of a multiscalar drought index: comparison with current drought index datasets based on the Palmer drought severity index. J Hydrometeorol 11:1033–1043
73. Vilà-Cabrera A, Martínez-Vilalta J, Galiano L, Retana J (2013) Patterns of forest decline and regeneration across Scots pine populations. Ecosystems 16:323–335
74. Vilà-Cabrera A, Martínez-Vilalta J, Retana J (2014) Variation in reproduction and growth in declining Scots pine populations. Persp Plant Ecol Evol Syst 16:111–120
75. von Wilpert K (1991) Intraannual variation of radial tracheid diameters as monitor of site specific water stress. Dendrochronologia 9:95–113
76. Vysotskaya LG, Vaganov EA (1989) Components of the variability of radial cell size in tree rings of conifers. IAWA Bull 10:417–428
77. Waring RH (1987) Characteristics of trees predisposed to die. Bioscience 37:569–574
78. Wimmer R (2002) Wood anatomical features in tree-rings as indicators of environmental change. Dendrochronologia 20:21–36
79. Zweifel R, Zimmermann L, Zeugin F, Newbery DM (2006) Intra-annual radial growth and water relations of trees: implications towards a growth mechanism. J Exp Bot 57:1445–1459