Advertisement

Xylem anatomy of Robinia pseudoacacia L. and Quercus robur L. is differently affected by climate in a temperate alluvial forest

Abstract

Key message

Xylem hydraulic traits of native Quercus robur are more sensitive to previous-summer drought than those of alien Robinia pseudoacacia. The latter modulates vessel traits and ring porosity to cope with inter-annual climate variability, and is less affected by extreme events. This suggests that R. pseudoacacia might be more competitive under future drier conditions.

Context

Forest management strategies require knowledge on how co-occurring native and alien species respond to unprecedented climate conditions, which can severely affect xylem conductivity and tree performance.

Aims

We aimed at quantitatively comparing xylem anatomical traits of co-occurring native Quercus robur and alien Robinia pseudoacacia and assessing similarities and differences in their response to climate variability.

Methods

We analyzed tree-ring anatomy and built chronologies of several parameters related to vessel number, size, and theoretical conductivity. Mean chronologies for each parameter were correlated to monthly temperature and precipitation data for the period 1954–2005 and within 30-year moving windows. We also assessed responses to extreme conditions in 2003.

Results

Quercus robur showed typical ring-porous vessel distribution, while R. pseudoacacia modulated vessel size and number year by year, frequently showing semi-ring porous appearance. Previous rainy summers increased size of large vessels in Q. robur, and number of large vessels in R. pseudoacacia. In winter, R. pseudoacacia was sensitive to water excess. High temperature in March increased vessel size in Q. robur, but reduced it in R. pseudoacacia. The 2003 summer heatwave strongly reduced vessel size and number in the following year in Q. robur, but had much less effect on R. pseudoacacia.

Conclusion

Quercus robur xylem traits are more influenced by both inter-annual climate variability and extreme events than those of R. pseudoacacia. Lower performance under dry conditions might reduce competitiveness of Q. robur in the future, slowing down the natural replacement of the invasive pioneer R. pseudoacacia by later-stage Q. robur.

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

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Akhmetzyanov L, Buras A, Sass-Klaassen U, den Ouden J, Mohren F, Groenendijk P, García-González I (2019) Multi-variable approach pinpoints origin of oak wood with higher precision. J Biogeogr 2019:1–15

  2. Alla AQ, Camarero JJ (2012) Contrasting responses of radial growth and wood anatomy to climate in a Mediterranean ring-porous oak: implications for its future persistence or why the variance matters more than the mean. Eur J For Res 131:1537–1550

  3. Aloni R, Zimmermann MH (1983) The control of vessel size and density along the plant axis - a new hypothesis. Differentiation 24:203–208

  4. Aniol RW (1987) A new device for computer assisted measurement of tree-ring widths. Dendrochronologia 5:135–141

  5. Biondi F, Waikul K (2004) DENDROCLIM2002: a C++ program for statistical calibration of climate signals in tree-ring chronologies. Comput Geosci 30:303–311

  6. Bonan GB (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320:1444–1449

  7. Bréda N, Granier A (1996) Intra and interannual variations of transpiration, leaf area index and radial growth of a sessile oak stand (Quercus petraea). Ann For Sci 53:521–536

  8. Breda 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

  9. Bussotti F, Pollastrini M, Holland V, Brüggemann W (2015) Functional traits and adaptive capacity of European forests to climate change. Environ Exp Bot 111:91–113

  10. Carrer M, Nola P, Motta R, Urbinati R (2010) Contrasting tree-ring growth to climate responses of Abies alba toward the southern limit of its distribution area. Oikos 119:1515–1525

  11. Carrer M, von Arx G, Castagneri D, Petit G (2015) Distilling allometric and environmental information from time series of conduit size: the standardization issue and its relationship to tree hydraulic architecture. Tree Physiol 35:27–33

  12. Castagneri D, Garbarino M, Nola P (2013) Host preference and growth patterns of ivy (Hedera helix L.) in a temperate alluvial forest. Plant Ecol 214:1–9

  13. Castagneri D, Petit G, Carrer M (2015) Divergent climate response on hydraulic- related xylem anatomical traits of Picea abies along a 900-m altitudinal gradient. Tree Physiol 35:1378–1387

  14. Castagneri D, Regev L, Boaretto E, Carrer M (2017) Xylem anatomical traits reveal different strategies of two Mediterranean oaks to cope with drought and warming. Environ Exp Bot 133:128–138

  15. Cavalieri MA, Sack L (2010) Comparative water use of native and invasive plants at multiple scales: a global meta-analysis. Ecology 91(9):2705–2715

  16. Ciais P, Reichstein M, Viovy N, Granier A, Ogee J, Allard V, Aubinet M, Buchmann N, Bernhofer C, Carrara A, Chevallier F, De Noblet N, Friend AD, Friedlingstein P, Grünwald T, Heinesch B, Keronen P, Knohl A, Krinner G, Loustau D, Manca G, Matteucci G, Miglietta F, Ourcival JM, Papale D, Pilegaard K, Rambal S, Seufert G, Soussana JF, Sanz MJ, Schulze ED, Vesala T, Valentini R (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 473:529–533

  17. Cierjacks A, Kowarik I, Joshi J, Hempel S, Ristow M, von der Lippe M, Weber E (2013) Biological flora of the British Isles: Robinia pseudoacacia. J Ecol 101:1623–1640

  18. Cook ER, Krusic PJ (2005) Program Arstan, a tree-ring standardization program based on detrending and autoregressive time series modelling, with interactive graphics. Tree-ring Lab Lamont Doherty Earth Obs Columbia University

  19. Cook ER, Peters K (1981) The smoothing spline: a new approach to standardizing forest interior tree-ring width series for dendroclimatic studies. Tree-Ring Bull 41:45–53

  20. Cruiziat P, Cochard H, Ameglio T (2002) Hydraulic architecture of trees: main concepts and results. Ann For Sci 59:723–752

  21. De Micco V, Carrer M, Rathgerber CBK, Camarero JJ, Voltas J, Cherubini P, Battipaglia G (2019) From xylogenesis to tree rings: wood traits to investigate tree response to environmental changes. IAWA J 2019:2–29

  22. Dyderski MK, Paz S, Frelich LE, Jagodzinski AM (2018) How much does climate change threaten European forest tree species distributions? Glob Change Biol 24:1150–1163

  23. Fonti P, García-González I (2008) Earlywood vessel size of oak as a potential proxy for spring precipitation in Mesic sites. J Biogeogr 35(12):2249–2257

  24. Fonti P, Solomonoff N, García-González I (2007) Earlywood vessels of Castanea sativa record temperature before their formation. New Phytol 173:562–570

  25. Fonti P, Eilmann B, García-González I, von Arx G (2009) Expeditious building of ring-porous earlywood vessel chronologies without loosing signal information. Trees 23:665–671

  26. Fonti P, von Arx G, García-González I, Eilmann B, Saas-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

  27. Fritts HC (1976) Tree-rings and climate. Academic press, London

  28. García-González I, Eckstein D (2003) Climatic signals of earlywood vessels of oak on a maritime site. Tree Physiol 23:497–504

  29. García-González I, Fonti P (2008) Ensuring a representative sample of earlywood vessels for dendroecological studies: an example from two ring-porous species. Trees 22:237–244

  30. García-González I, Souto-Herrero M, Campelo F (2016) Ring-porosity and earlywood vessels: a review on extracting environmental information through time. IAWA J 37(2):295–314

  31. Gärtner H, Schweingruber FH (2013) Microscopic preparation techniques for plant stem analysis. Remagen Kessel Publishing House

  32. Gea-Izquierdo G, Fonti P, Cherubini P, Martin-Benito D, Chaar H, Canellas I (2012) Xylem hydraulic adjustment and growth response of Quercus canariensis Willd to climatic variability. Tree Physiol 32:401–413

  33. Giorgi F, Lionello P (2008) Climate change projections for the Mediterranean region. Glob Planet Change 63:90–104

  34. González-González BD, Rozas V, García-González I (2014) Earlywood vessels of the sub-Mediterranean oak Quercus pyrenaica have greater plasticity and sensitivity than those of the temperate Q. petraea at the Atlantic–Mediterranean boundary. Trees – Struct Funct 28:237–252

  35. González-González BD, Vázquez-Ruiz RA, García-González I (2015) Effects of climate on earlywood vessel formation of Quercus robur and Q. pyrenaica at a site in the northwestern Iberian Peninsula. Can Journal For Res 45(6):698–709

  36. Granier A, Reichstein M, Bréda N, Janssens IA, Falge E, Ciai P, Grunwald T, Aubinet M, Berbigier P, Bernhofer C, Buchmann N, Facini O, Grassi G, Heinesch B, Ilvesniemi H, Keronen P, Knohl A, Köstner B, Lagergren F, Lindroth A, Longdoz B, Loustau D, Mateus J, Montagnani L, Nys C, Moors E, Papale D, Peiffer M, Pilegaard K, Pita G, Pumpanen J, Rambal S, Rebmann C, Rodrigues A, Seufert G, Tenhunen J, Vesala T, Wang Q (2007) Evidence for soil water control on carbon and water dynamics in European forests during the extremely dry year: 2003. Agric For Meteorol 143:123–145

  37. Guada G, Vázquez-Ruiz RA, García-González I (2019) Response patterns of xylem and leaf phenology to temperature at the southwestern distribution boundary of Quercus robur: a multi-spatial study. Agric For Meteorol 269-270:46–56

  38. Hacke UG, Sperry JS (2001) Functional and ecological xylem anatomy. Perspect Plant Ecol Syst 4(2):97–115

  39. Hacke UG, Spicer R, Schreiber SG, Plavcová L (2017) An ecophysiological and developmental perspective on variation in vessel diameter. Plant Cell Env 40:831–845

  40. Hanewinkel M, Cullmann DA, Schelhaas MJ, Nabuurs GJ, Zimmermann NE (2013) Climate change may cause severe loss in the economic value of European forest land. Nat Clim Chang 3:203–207

  41. Harris I, Jones PD, Osborn TJ, Lister DH (2014) Updated high-resolution grids of monthly climatic observations – the CRU TS3.10 dataset. Int J Climatol 34:623–642

  42. Jackson DA (1993) Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74:2204–2214

  43. Kitin P, Funada R (2016) Earlywood vessels in ring-porous trees become functional for water transport after bud burst and before the maturation of the current-year leaves. IAWA J 37:315–331

  44. Kleinbauer I, Dullinger S, Peterseil J, Essl F (2010) Climate change might drive the invasive tree Robinia pseudacacia into nature reserves and endangered habitats. Biol Conserv 143:382–390

  45. Knüsel S, Conedera M, Rigling A, Fonti P, Wunder J (2015) A tree-ring perspective on the invasion of Ailanthus altissima in protection forests. For Ecol Manag 354:334–343

  46. Kutscha NP, Sachs IB (1962) Colour tests for differentiating heartwood and sapwood in certain softwood tree species. USDA, Forest Products Laboratory, University of Wisconsin, Report No. 2264

  47. Lebourgeois F, Mérian P, Courdier F, Ladier J, Dreyfus P (2012) Instability of climate signal in tree-ring width in Mediterranean mountains: a multi-species analysis. Trees 26:715–729

  48. Lévesque M, Saurer M, Siegwolf R, Eilmann B, Brang P, Bugmann H, Rigling A (2013) Drought response of five conifer species under contrasting water availability suggests high vulnerability of Norway spruce and European larch. Glob Chang Biol 19:3184–3199

  49. Lloret F, Keeling EG, Sala A (2011) Components of tree resilience: effects of successive low-growth episodes in old ponderosa pine forests. Oikos 120:1909–1920

  50. Mantovani D, Veste M, Freese D (2014) Black locust (Robinia pseudoacacia L.) ecophysiological and morphological adaptations to drought and their consequence on biomass production and water-use efficiency. New Zeal J For Sci 44:29

  51. Mantovani D, Veste M, Boldt-Burisch K, Fritsch S, Koning LA, Freese D (2015) Carbon allocation, nodulation, and biological nitrogen fixation of black locust (Robinia pseudoacacia L.) under soil water limitation. Ann For Res 58(2):259–274

  52. Martínez-Sancho E, Dorado-Liñán I, Heinrich I, Helle G, Menzel A (2017) Xylem adjustment of sessile oak at its southern distribution limits. Tree Physiol 37:903–914

  53. Michelot A, Simard S, Rathgeber C, Dufrêne 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

  54. Motta R, Nola P, Berretti R (2009) The rise and fall of the black locust (Robinia pseudoacacia L.) in the “Siro Negri” forest reserve (Lombardy, Italy): lessons learned and future uncertainties. Ann For Sci 66:410

  55. Nadal-Sala D, Sabaté S, Sánchez-Costa E, Poblador S, Sabater F, Gracia C (2017) Growth and water use performance of four co-occurring riparian tree species in a Mediterranean riparian forest. For Ecol Manag 396:132–142

  56. Nola P (1996) Climatic signal in earlywood and latewood of deciduous oaks from northern Italy. In: Dean JS, Meko DM, Swetnam TW (eds) Tree Rings. Environment and Humanity, Radiocarbon pp, pp 249–258

  57. Olson M, Soriano D, Rosell JA, Anfodillo T, Donoghue MJ, Edwards EJ, León-Gómez C, Dawson T, Camarero Martínez JJ, Castorena M, Echeverría A, Espinosa CI, Fajardo A, Gazol A, Isnard S, Lima RS, Marcati CR, Méndez-Alonzo R (2018) Plant height and hydraulic vulnerability to drought and cold. PNAS 115(29):7551–7556

  58. Pérez-De-Lis G, García-González I, Rozas V, Olano JM (2016a) Feedbacks between earlywood anatomy and non-structural carbohydrates affect spring phenology and wood production in ring-porous oaks. Biogeosciences 13(19):5499–5510

  59. Pérez-de-Lis G, Rossi S, Vázquez-Ruiz RA, Rozas V, García-González I (2016b) Do changes in spring phenology affect earlywood vessels? Perspective from the xylogenesis monitoring of two sympatric ring-porous oaks. New Phytol 209:521–530

  60. Pérez-de-Lis G, Olano JM, Rozas V, Rossi S, Vázquez-Ruiz RA, García-González I (2017) Environmental conditions and vascular cambium regulate carbon allocation to xylem growth in deciduous oaks. Funct Ecol 31(3):592–603

  61. Pérez-de-Lis G, Rozas V, Vázquez-Ruiz RA, García-González I (2018) Do ring-porous oaks prioritize earlywood vessel efficiency over safety? Environmental effects on vessel diameter and tyloses formation. Agric For Meteorol 248:205–214

  62. Sartori F (1984) Les forêts alluviales de la basse vallée du Tessin (Italie du nord). In: Cramer J (ed) Colloques phytosocologiques: la végétation des forêts alluviales, pp 201–216

  63. Schmitt U, Möller R, Eckstein D (2000) Seasonal wood formation dynamics of beech (Fagus sylvatica L.) and black locust (Robinia pseudoacacia L.) as determined by the “pinning” technique. J Appl Bot 74:10–16

  64. Schweingruber FH (1990) Anatomy of European woods. Paul Haupt, Bern

  65. Souto-Herrero M, Rozas V, García-González I (2017) A 481-year chronology of oak earlywood vessels as an age-independent climatic proxy in NW Iberia. Glob Planet Change 155:20–28

  66. Tessier L, Nola P, Serre-Bachet F (1994) Deciduous Quercus in the Mediterranean region: tree-ring/climate relationships. New Phytol 126:355–367

  67. Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap. Springer-Verlag, Berlin, Heidelberg, NewYork

  68. Vítková M, Müllerová J, Sádlo J, Pergl J, Pyšek P (2017) Black locust (Robinia pseudoacacia) beloved and despised: a story of an invasive tree in Central Europe. For Ecol Manag 384:287–302

  69. von Arx G, Carrer M (2014) ROXAS - a new tool to build centuries-long tracheid-lumen chronologies in conifers. Dendrochronologia 32:290–293

  70. 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

Download references

Author information

Correspondence to Paola Nola.

Ethics declarations

Data availability

The dataset generated during the current study is available from the corresponding author upon reasonable request.

Conflict of interest

The authors declare that they have no conflict of interest.

Statement on ethical approval

The field work and the sampling activities within “Siro Negri” State Natural Reserve were conducted under the explicit permission of the Director of the protected area.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributions of the co-authors PN designed the study. PN, FB and SA conducted field work. PN, GvA, and DC processed the samples and analyzed data. PN and DC wrote the first paper draft. All authors contributed to discussion of results and writing the manuscript.

This article is part of the topical collection on Wood formation and tree adaptation to climateRisk Analysis

Handling Editor: Cyrille B. K. Rathgeber

Annexes

Annexes

Fig. 8
figure8

Climate diagram from Pavia meteorological station

Fig. 9
figure9

Scree plot from PCA of tree-ring width and vessel parameters. The Y-axis represents the percentage of variance explained by each component (solid line). The dashed line represents the superimposed Broken-Stick Model

Fig. 10
figure10

Pearson’s correlations between tree-ring and vessel parameters and the first three principal components. Dotted lines indicate the level of significant correlation. Acronyms are explained in Table 2

Fig. 11
figure11

Pearson’s correlations between ring width and vessel chronologies for each species. Correlation values are coded according to the key at the bottom. Acronyms are explained in Table 2

Fig. 12
figure12

Inter-species correlations for each tree-ring width and vessel chronology. Dotted lines indicate the level of significant correlation and solid bars refer to significant values. Acronyms are explained in Table 2

Fig. 13
figure13

Moving correlation with a 30-year window between all the anatomical parameters and the most significant climatic variables. Months of the previous year are in lowercase letters. R values are coded according to the key at the bottom. Acronyms are explained in Table 2

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nola, P., Bracco, F., Assini, S. et al. Xylem anatomy of Robinia pseudoacacia L. and Quercus robur L. is differently affected by climate in a temperate alluvial forest. Annals of Forest Science 77, 8 (2020). https://doi.org/10.1007/s13595-019-0906-z

Download citation

Keywords

  • Alien species
  • Black locust
  • Climate response
  • Drought
  • Pedunculate oak
  • Tree-ring anatomy
  • Vessel