Skip to main content

Advertisement

SpringerLink
Log in

Xylogenesis of Pinus pinaster under a Mediterranean climate

  • Original Paper
  • Published:
Annals of Forest Science Aims and scope Submit manuscript

Abstract

Context

The knowledge on cambial activity in water-limited environments, such as the Mediterranean, is still fragmentary. Dendrochronological studies have determined that spring precipitation plays an important part in determining tree-ring width and the properties of tracheids. However, the complex relation between cambial phenology and climate is still far from understood.

Aims

We studied the influence of climate, especially water stress, on maritime pine wood formation with the aim of determining the influence of drought on cambial activity.

Methods

A plantation of maritime pine (Pinus pinaster) was selected in the west coast of Portugal, to monitor cambial activity and wood formation using anatomical observations and band dendrometers. The trees were monitored weekly over 2 years (2010 and 2011).

Results

Xylem differentiation started earlier when warmer late winter temperatures were observed. Water stress triggered an earlier stop of wood formation and also the formation of tracheids with smaller lumen area. In both years a bimodal pattern of stem radial increment was registered by band dendrometers with two periods of increment: one in spring and another in autumn. The xylem anatomy study suggests that the autumnal increment period corresponded mostly to stem rehydration, since the differentiation of new xylem cells by the cambium was not observed.

Conclusion

Maritime pine cambial activity appears to be under a double climatic control: temperature influences cambial onset and water availability growth cessation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abe H, Nakai T, Utsumi Y, Kagawa A (2003) Temporal water deficit and wood formation in Cryptomeria japonica. Tree Physiol 23:859–863

    Article  PubMed  Google Scholar 

  • Adams HD, Germino MJ, Breshears DD, Barron-Gafford GA, Guardiola-Claramonte M, Zou CB, Huxman TE (2013) Nonstructural leaf carbohydrate dynamics of Pinus edulis during drought-induced tree mortality reveal role for carbon metabolism in mortality mechanism. New Phytol 197:1142–1151. doi:10.1111/nph.12102

    Article  PubMed  CAS  Google Scholar 

  • Adams HD, Guardiola-Claramonte M, Barron-Gafford GA, Villegas JC, Breshears DD, Zou CB, Troch PA, Huxman TE (2009) Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought. Proc Natl Acad Sci U S A 106:7063–7066. doi:10.1073/pnas.0901438106

    Article  PubMed  CAS  Google Scholar 

  • Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim J-H, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684. doi:10.1016/j.foreco.2009.09.001

    Article  Google Scholar 

  • Begum S, Nakaba S, Bayramzadeh V, Oribe Y, Kubo T, Funada R (2008) Temperature responses of cambial reactivation and xylem differentiation in hybrid poplar (Populus sieboldii × P-grandidentata) under natural conditions. Tree Physiol 28:1813–1819

    Article  PubMed  Google Scholar 

  • Begum S, Nakaba S, Oribe Y, Kubo T, Funada R (2007) Induction of cambial reactivation by localized heating in a deciduous hardwood hybrid poplar (Populus sieboldii × P. randidentata). Ann Bot 100:439–447. doi:10.1093/Aob/Mcm130

    Article  PubMed  Google Scholar 

  • Belien E, Rossi S, Morin H, Deslauriers A (2012) Xylogenesis in black spruce subjected to rain exclusion in the field. Can J For Res-Revue Canadienne De Recherche Forestiere 42:1306–1315. doi:10.1139/x2012-095

    Article  Google Scholar 

  • Bogino SM, Bravo F (2008) Growth response of Pinus pinaster Ait. to climatic variables in central Spanish forests. Ann For Sci 65:506. doi:10.1051/forest:2008025

    Article  Google Scholar 

  • Camarero JJ, Olano JM, Parras A (2010) Plastic bimodal xylogenesis in conifers from continental Mediterranean climates. New Phytol 185:471–480. doi:10.1111/j.1469-8137.2009.03073.x

    Article  PubMed  Google Scholar 

  • Campelo F, Vieira J, Nabais C (2013) Tree-ring growth and intra-annual density fluctuations of Pinus pinaster responses to climate: does size matter? Trees - Struct Funct 27:763–772. doi:10.1007/s00468-012-0831-3

    Article  Google Scholar 

  • Carrer M, Urbinati C (2006) Long-term change in the sensitivity of tree-ring growth to climate forcing in Larix decidua. New Phytol 170:861–871

    Article  PubMed  Google Scholar 

  • Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CPP, Osorio ML, Carvalho I, Faria T, Pinheiro C (2002) How plants cope with water stress in the field. Photosynthesis and growth. Ann Bot 89:907–916. doi:10.1093/aob/mcf105

    Article  PubMed  CAS  Google Scholar 

  • Cherubini P, Gartner BL, Tognetti R, Braker OU, Schoch W, Innes JL (2003) Identification, measurement and interpretation of tree rings in woody species from Mediterranean climates. Biol Rev 78:119–148

    Article  PubMed  Google Scholar 

  • Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG, Jacobsen AL, Lens F, Maherali H, Martinez-Vilalta J, Mayr S, Mencuccini M, Mitchell PJ, Nardini A, Pittermann J, Pratt RB, Sperry JS, Westoby M, Wright IJ, Zanne AE (2012) Global convergence in the vulnerability of forests to drought. Nature 491:752–755. doi:10.1038/nature11688

    PubMed  CAS  Google Scholar 

  • CRU, Netherlands Royal Meteorological Institute, 2011. CRU TS 3.1. http://climexp.knmi.nl/

  • Dalla-Salda G, Martinez-Meier A, Cochard H, Rozenberg P (2009) Variation of wood density and hydraulic properties of Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco) clones related to a heat and drought wave in France. For Ecol Manag 257:182–189. doi:10.1016/j.foreco.2008.08.019

    Article  Google Scholar 

  • de Luis M, Gricar J, Cufar K, Raventos J (2007) Seasonal dynamics of wood formation in Pinus halepensis from dry and semi-arid ecosystems in Spain. Iawa J 28:389–404

    Google Scholar 

  • de Luis M, Novak K, Cufar K, Raventos J (2009) Size mediated climate-growth relationships in Pinus halepensis and Pinus pinea. Trees - Struct Funct 23:1065–1073. doi:10.1007/s00468-009-0349-5

    Article  Google Scholar 

  • Denne MP (1989) Definition of latewood according to Mork (1928). Iawa Bull 10:59–62

    Google Scholar 

  • Deslauriers A, Morin H (2005) Intra-annual tracheid production in balsam fir stems and the effect of meteorological variables. Trees-Struct Funct 19:402–408

    Article  Google Scholar 

  • Deslauriers A, Rossi S, Anfodillo T, Saracino A (2008) Cambial phenology, wood formation and temperature thresholds in two contrasting years at high altitude in southern Italy. Tree Physiol 28:863–871

    Article  PubMed  Google Scholar 

  • Domec JC, Gartner BL (2002) How do water transport and water storage differ in coniferous earlywood and latewood? J Exp Bot 53:2369–2379. doi:10.1093/jxb/erf100

    Article  PubMed  CAS  Google Scholar 

  • Eilmann B, Zweifel R, Buchmann N, Pannatier EG, Rigling A (2011) Drought alters timing, quantity, and quality of wood formation in Scots pine. J Exp Bot 62:2763–2771. doi:10.1093/jxb/erq443

    Article  PubMed  CAS  Google Scholar 

  • Ferreira O, Torrinha AM, Cardoso PM (2010) Plano de gestão florestal: Mata Nacional do Urso e Mata Nacional do Pedrogão

  • Fritts HC (1976) Tree rings and climate. Academic, London

    Google Scholar 

  • Gricar J, Cufar K, Oven P, Schmitt U (2005) Differentiation of terminal latewood tracheids in silver fir during autumn. Ann Bot 95:959–965. doi:10.1093/aob/mci112

    Article  PubMed  Google Scholar 

  • Gricar J, Krze L, Cufar K (2009) Number of cells in xylem, phloem and dormant cambium in silver fir (Abies alba), in trees of different vitality. Iawa J 30:121–133

    Article  Google Scholar 

  • Gricar J, Zupancic M, Cufar K, Koch G, Schmitt U, Oven P (2006) Effect of local heating and cooling on cambial activity and cell differentiation in the stem of Norway spruce (Picea abies). Ann Bot 97:943–951. doi:10.1093/aob/mc1050

    Article  PubMed  Google Scholar 

  • Hacke UG, Sperry JS (2001) Functional and ecological xylem anatomy. Perspect Plant Ecol Evol Syst 4:97–115. doi:10.1078/1433-8319-00017

    Article  Google Scholar 

  • Hsiao TC, Acevedo E, Fereres E, Henderson DW (1976) Stress metabolism: water stress, growth and osmotic adjustment. Phil Trans R Soc London Series B Biol Sci 273:479–500. doi:10.1098/rstb.1976.0026

    Article  Google Scholar 

  • IPCC (2007) Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge Univertisy Press, Crambridge

    Google Scholar 

  • Jyske T, Holtta T, Makinen H, Nojd P, Lumme I, Spiecker H (2010) The effect of artificially induced drought on radial increment and wood properties of Norway spruce. Tree Physiol 30:103–115. doi:10.1093/treephys/tpp099

    Article  PubMed  Google Scholar 

  • Korner C (1998) A re-assessment of high elevation treeline positions and their explanation. Oecologia 115:445–459. doi:10.1007/s004420050540

    Article  Google Scholar 

  • Lebourgeois F, Merian P, Courdier F, Ladier J, Dreyfus P (2012) Instability of climate signal in tree-ring width in Mediterranean mountains: a multi-species analysis. Trees-Struct Funct 26:715–729. doi:10.1007/s00468-011-0638-7

    Article  Google Scholar 

  • Linares JC, Camarero JJ, Carreira JA (2009) Plastic responses of Abies pinsapo xylogenesis to drought and competition. Tree Physiol 29:1525–1536. doi:10.1093/treephys/tpp084

    Article  PubMed  Google Scholar 

  • Linares JC, Camarero JJ, Carreira JA (2010) 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 98:592–603. doi:10.1111/j.1365-2745.2010.01645.x

    Article  Google Scholar 

  • Liphschitz N, Levyadun S (1986) Cambial activity of evergreen and seasonal dimorphics around the Mediterranean. Iawa Bull 7:145–153

    Google Scholar 

  • Lupi C, Morin H, Deslauriers A, Rossi S (2010) Xylem phenology and wood production: resolving the chicken-or-egg dilemma. Plant Cell Environ 33:1721–1730. doi:10.1111/j.1365-3040.2010.02176.x

    Article  PubMed  Google Scholar 

  • 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. doi:10.1111/j.1469-8137.2008.02436.x

    Article  PubMed  Google Scholar 

  • McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155:1051–1059. doi:10.1104/pp.110.170704

    Article  PubMed  CAS  Google Scholar 

  • Michelot A, Simard S, Rathgeber C, Dufrene E, Damesin C (2012) Comparing the intra-annual wood formation of three European species (Fagus sylvatica, Quercus petraea and Pinus sylvestris) as related to leaf phenology and non-structural carbohydrate dynamics. Tree Physiol 32:1033–1045

    Article  PubMed  Google Scholar 

  • Nizinski JJ, Saugier B (1988) A model of leaf budding and development for a mature Quercus forest. J Appl Ecol 25:643–652. doi:10.2307/2403851

    Article  Google Scholar 

  • Oberhuber W, Gruber A (2010) Climatic influences on intra-annual stem radial increment of Pinus sylvestris (L.) exposed to drought. Trees - Struct Funct 24:887–898. doi:10.1007/s00468-010-0458-1

    Article  Google Scholar 

  • Olano JM, Eugenio M, Garcia-Cervigon AI, Folch M, Rozas V (2012) Quantitative tracheid anatomy reveals a complex environmental control of wood structure in continental Mediterranean climate. Int J Plant Sci 173:137–149. doi:10.1086/663165

    Article  Google Scholar 

  • Oribe Y, Funada R, Kubo T (2003) Relationships between cambial activity, cell differentiation and the localization of starch in storage tissues around the cambium in locally heated stems of Abies sachalinensis (Schmidt) Masters. Trees-Struct Funct 17:185–192. doi:10.1007/s00468-002-0231-1

    Google Scholar 

  • Oribe Y, Funada R, Shibagaki M, Kubo T (2001) Cambial reactivation in locally heated stems of the evergreen conifer Abies sachalinensis (Schmidt) Masters. Planta 212:684–691

    Article  PubMed  CAS  Google Scholar 

  • Pasho E, Julio Camarero J, Vicente-Serrano SM (2012) Climatic impacts and drought control of radial growth and seasonal wood formation in Pinus halepensis. Trees-Struct Funct 26:1875–1886. doi:10.1007/s00468-012-0756-x

    Article  Google Scholar 

  • Pittermann J, Sperry JS, Wheeler JK, Hacke UG, Sikkema EH (2006) Mechanical reinforcement of tracheids compromises the hydraulic efficiency of conifer xylem. Plant Cell Environ 29:1618–1628. doi:10.1111/1365-3040.2006.01539.x

    Article  PubMed  Google Scholar 

  • Ripullone F, Guerrieri MR, Nole A, Magnani F, Borghetti M (2007) Stomatal conductance and leaf water potential responses to hydraulic conductance variation in Pinus pinaster seedlings. Trees-Struct Funct 21:371–378. doi:10.1007/s00468-007-0130-6

    Article  Google Scholar 

  • Rossi S, Anfodillo T, Menardi R (2006a) Trephor: a new tool for sampling microcores from tree stems. Iawa J 27:89–97

    Article  Google Scholar 

  • Rossi S, Deslauriers A, Anfodillo T, Carraro V (2007) Evidence of threshold temperatures for xylogenesis in conifers at high altitudes. Oecologia 152:1–12

    Article  PubMed  Google Scholar 

  • Rossi S, Deslauriers A, Anfodillo T, Morin H, Saracino A, Motta R, Borghetti M (2006b) Conifers in cold environments synchronize maximum growth rate of tree-ring formation with day length. New Phytol 170:301–310

    Article  PubMed  Google Scholar 

  • Rossi S, Deslauriers A, Gricar J, Seo JW, Rathgeber CBK, Anfodillo T, Morin H, Levanic T, Oven P, Jalkanen R (2008) Critical temperatures for xylogenesis in conifers of cold climates. Glob Ecol Biogeogr 17:696–707. doi:10.1111/j.1466-8238.2008.00417.x

    Article  Google Scholar 

  • Rozas V, Lamas S, Garcia-Gonzalez I (2009) Differential tree-growth responses to local and large-scale climatic variation in two Pinus and two Quercus species in northwest Spain. Ecoscience 16:299–310. doi:10.2980/16-3-3212

    Article  Google Scholar 

  • Sperry JS (2003) Evolution of water transport and xylem structure. Int J Plant Sci 164:S115–S127. doi:10.1086/368398

    Article  Google Scholar 

  • Sperry JS, Hacke UG, Pittermann J (2006) Size and function in conifer tracheids and angiosperm vessels. Am J Bot 93:1490–1500. doi:10.3732/ajb.93.10.1490

    Article  PubMed  Google Scholar 

  • Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap. Springer, Heidelberg

    Book  Google Scholar 

  • Vicente-Serrano SM, Begueria S, Lopez-Moreno JI (2010) A multiscalar drought index sensitive to global warming: the standardized precipitation evapotranspiration index. J Clim 23:1696–1718. doi:10.1175/2009jcli2909.1

    Article  Google Scholar 

  • Vieira J, Campelo F, Nabais C (2009) Age-dependent responses of tree-ring growth and intra-annual density fluctuations of Pinus pinaster to Mediterranean climate. Trees-Struct Funct 23:257–265. doi:10.1007/s00468-008-0273-0

    Article  Google Scholar 

  • Vieira J, Campelo F, Nabais C (2010) Intra-annual density fluctuations of Pinus pinaster are a record of climatic changes in the western Mediterranean region. Can J For Res-Revue Canadienne De Recherche Forestiere 40:1567–1575. doi:10.1139/X10-096

    Article  Google Scholar 

  • Vieira J, Rossi S, Campelo F, Nabais C (2013) Are neighboring trees in tune? Wood formation study in Pinus pinaster. Eur J For Res. doi:10.1007/s10342-013-0734-x

  • Vieira J, Rossi S, Campelo F, Freitas H, Nabais C (2013) Seasonal and daily cycles of stem radial variation of Pinus pinaster in a drought-prone environment. Agric For Meteorol 180:173–181. doi:10.1016/j.agrformet.2013.06.009

    Article  Google Scholar 

  • von Wilpert K (1991) Intraanual variation of radial tracheid diameters as monitor of site specific water stress. Dendrochronologia 9:95–113

    Google Scholar 

  • 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. doi:10.1093/jxb/erj125

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank A. Garside for checking the English. This study was supported by the Fundação para a Ciência e a Tecnologia, Ministério da Educação e Ciência (FCT) cofinanced by Compete, through the project PTDC/AAC-AMB/111675/2009. Joana Vieira was supported by a PhD grant (SFRH/BD/48089/2008) and Filipe Campelo by a postdoctoral research grant (SFRH/BPD/47822/2008); both of them received grants from FCT with funds from Portuguese Operational Human Potential Program (POPH) and QREN Portugal (Portuguese National Strategic Reference Framework).

Author information

Authors and Affiliations

  1. CFE – Centro de Ecologia Funcional, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade de Coimbra, Apartado 3046, 3001-401, Coimbra, Portugal

    Joana Vieira, Filipe Campelo, Helena Freitas & Cristina Nabais

  2. Départment des Sciences Foundamentales, Université du Québec à Chicoutimi, Chicoutimi, Canada

    Sergio Rossi

Authors
  1. Joana Vieira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sergio Rossi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Filipe Campelo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Helena Freitas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cristina Nabais
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joana Vieira.

Additional information

Handling Editor: Gilbert Aussenac

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vieira, J., Rossi, S., Campelo, F. et al. Xylogenesis of Pinus pinaster under a Mediterranean climate. Annals of Forest Science 71, 71–80 (2014). https://doi.org/10.1007/s13595-013-0341-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13595-013-0341-5

Keywords

Search

Navigation