Under pressure: How a Mediterranean high-mountain forb coordinates growth and hydraulic xylem anatomy in response to temperature and water constraints

Functional Ecology

Volumn 27, Issue 6, 2013, Pages 1295-1303

  Olano, Jose Miguel ^a   Almería, Iván ^a   Eugenio, Màrcia ^a   von Arx, Georg ^b  

^a UNIVERSITY OF VALLADOLID   (Spain)

^b SWISS FEDERAL RESEARCH INSTITUTE WSL   (Switzerland)

Author keywords

Altitudinal gradient; Annual root rings; Climatic change; Climatic double stress; Functional xylem anatomy; Herb chronology; Mediterranean high mountains

Indexed keywords

ANATOMY; CLIMATE CHANGE; DROUGHT; DROUGHT STRESS; GROWTH RATE; REPRODUCTION; ROOT ARCHITECTURE; SUMMER; XYLEM;

CILIOPHORA; SILENE;

EID: 84887823052     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12144     Document Type: Article

References (77)

1. Alla, A.Q. & Camarero, J.J. (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. European Journal of Forest Research, 131, 1537-1550.
2. Aloni, R. & Zimmermann, M.H. (1983) The control of vessel size and density along the plant axis: A new hypothesis. Differentiation, 24, 203-208.
3. Aloni, R., Aloni, E., Langhans, M. & Ullrich, C.I. (2006) Role of cytokinin and auxin in shaping root architecture: Regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Annals of Botany, 97, 883-893.
4. Anfodillo, T., Carraro, V., Carrer, M., Fior, C. & Rossi, S. (2006) Convergent tapering of xylem conduits in different woody species. New Phytologist, 169, 279-290.
5. von Arx, G., Archer, S.R. & Hughes, M.K. (2012) Long-term functional plasticity in plant hydraulic architecture in response to supplemental moisture. Annals of Botany, 109, 1091-1100.
6. von Arx, G. & Dietz, H. (2005) Automated image analysis of annual rings in the roots of perennial forbs. International Journal of Plant Sciences, 166, 723-732.
7. von Arx, G. & Dietz, H. (2006) Growth rings in the roots of temperate forbs are robust annual markers. Plant Biology, 8, 224-233.
8. von Arx, G., Edwards, P.J. & Dietz, H. (2006) Evidence for increased longevity and changes in growth patterns in high-altitude populations of three perennial forbs. Ecology, 87, 665-674.
9. Bär, A., Pape, R., Bräuning, A. & Löffler, J. (2008) Growth-ring variations of dwarf shrubs reflect regional climate signals in alpine environments rather than topoclimatic differences. Journal of Biogeography, 35, 625-636.
10. Benito, B., Lorite, J. & Penas, J. (2011) Simulating potential effects of climatic warming on altitudinal patterns of key species in Mediterranean-alpine ecosystems. Climatic Change, 109, 471-483.
11. Burnham, K.P. & Anderson, D.R. (2002) Model selection and Multimodel Inference: A Practical Information Theoretic Approach. Springer-Verlag, Heidelberg, Germany.
12. Camarero, J.J., Olano, J.M. & Parras, A. (2010) Plastic bimodal xylogenesis in conifers from continental Mediterranean climates. New Phytologist, 185, 471-480.
13. Camarero, J.J., Palacio, S. & Montserrat-Martí, G. (2013) Contrasting seasonal overlaps between primary and secondary growth are linked to wood anatomy in Mediterranean sub-shrubs. Plant Biology doi:10.1111/j.1438-8677.2012.00702.x.
14. Camarero, J.J., Olano, J.M., Arroyo Alfaro, S.J., Fernández-Marín, B., Becerril, J.M. & García-Plazaola, J.I. (2012) Photoprotection mechanisms in Quercus ilex under contrasting climatic conditions. Flora - Morphology, Distribution, Functional Ecology of Plants, 207, 557-564.
15. Cao, K.-F., Yang, S.-J., Zhang, Y.-J. & Brodribb, T.J. (2012) The maximum height of grasses is determined by roots. Ecology Letters, 15, 666-672.
16. Chen, I.C., Hill, J.K., Ohlemuller, R., Roy, D.B. & Thomas, C.D. (2011) Rapid range shifts of species associated with high levels of climate warming. Science, 333, 1024-1026.
17. Crimmins, S.M., Dobrowski, S.Z., Greenberg, J.A., Abatzoglou, J.T. & Mynsberge, A.R. (2011) Changes in climatic water balance drive downhill shifts in plant species' optimum elevations. Science, 331, 324-327.
18. 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 Physiology, 28, 863-871.
19. DeSoto, L., Camarero, J.J., Olano, J.M. & Rozas, V. (2012) Geographically structured and temporally unstable growth responses of Juniperus thurifera to recent climate variability in the Iberian Peninsula. European Journal of Forest Research, 131, 905-917.
20. Dietz, H. & von Arx, G. (2005) Climatic fluctuation causes large-scale synchronous variation in radial increments of the main roots of northern hemisphere forbs. Ecology, 86, 327-333.
21. Doak, D.F. & Morris, W.F. (2010) Demographic compensation and tipping points in climate-induced range shifts. Nature, 467, 959-962.
22. Engler, R., Randin, C.F., Thuiller, W., Dullinger, S., Zimmermann, N.E., Araujo, M.B. et al. (2011) 21st century climate change threatens mountain flora unequally across Europe. Global Change Biology, 17, 2330-2341.
23. Fonti, P., Solomonoff, N. & García-González, I. (2007) Earlywood vessels of Castanea sativa record temperature before their formation. New Phytologist, 173, 562-570.
24. Fonti, P., von Arx, G., García-González, I., Eilmann, B., Sass-Klaassen, U., Gärtner, H. et al. (2010) Studying global change through investigation of the plastic responses of xylem anatomy in tree rings. New Phytologist, 185, 42-53.
25. Franklin, R.S. (2012) Growth response of the alpine shrub, Linanthus pungens, to snowpack and temperature at a rockglacier in the eastern Sierra Nevada, California. Quaternary International. doi:10.1016/j.quaint.2012.07.018.
26. García-Camacho, R., Albert, M.J. & Escudero, A. (2012) Small-scale demographic compensation in a high-mountain endemic: the low edge stands still. Plant Ecology & Diversity, 5, 37-44.
27. García-Cervigón, A.I., Olano, J.M., Eugenio, M. & Camarero, J.J. (2012) Arboreal and prostrate conifers coexisting in Mediterranean high mountains differ in their climatic responses. Dendrochronologia, 30, 279-286.
28. García-Fernández, A., Iriondo, J.M., Vallés, J., Orellana, J. & Escudero, A. (2012) Ploidy level and genome size of locally adapted populations of Silene ciliata across an altitudinal gradient. Plant Systematics and Evolution, 298, 139-146.
29. García-Fernández, A., Iriondo, J.M., Bartels, D. & Escudero, A. (2013) Response to artificial drying until drought-induced death in different elevation populations of a high-mountain plant. Plant Biology, 1, 93-100.
30. García-González, I. & Fonti, P. (2006) Selecting earlywood vessels to maximize their environmental signal. Tree Physiology, 26, 1289-1296.
31. 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.
32. Giménez-Benavides, L., Escudero, A. & Iriondo, J.M. (2007a) Local adaptation enhances seedling recruitment at the southernmost limit of a high mountain Mediterranean plant. Annals of Botany, 99, 723-734.
33. Giménez-Benavides, L., Escudero, A. & Iriondo, J.M. (2007b) Reproductive limits of a late-flowering high-mountain Mediterranean plant along an elevational climate gradient. New Phytologist, 173, 367-382.
34. Giménez-Benavides, L., Albert, M.J., Iriondo, J.M. & Escudero, A. (2011a) Demographic processes of upward range contraction in a long-lived Mediterranean high mountain plant. Ecography, 34, 85-93.
35. Giménez-Benavides, L., García-Camacho, R., Iriondo, J.M. & Escudero, A. (2011b) Selection on flowering time in Mediterranean high-mountain plants under global warming. Evolutionary Ecology, 25, 777-794.
36. Gottfried, M., Harald, P., Futschik, A., Akhalkatsi, M., Barančok, P., Benito Alonso, J.L. et al. (2012) Continent-wide response of mountain vegetation to climate change. Nature Climate Change, 2, 111-115.
37. Graae, B.J., De Frenne, P., Kolb, A., Brunet, J., Chabrerie, O., Verheyen, K. et al. (2012) On the use of weather data in ecological studies along altitudinal and latitudinal gradients. Oikos, 121, 3-19.
38. Grabherr, G., Gottfried, M. & Pauli, H. (1994) Climate effects on mountain plants. Nature, 369, 448.
39. Grace, J.B., Anderson, T.M., Olff, H. & Scheiner, S.M. (2010) On the specification of structural equation models for ecological systems. Ecological Monographs, 80, 67-87.
40. Gray, W.M., Östin, A., Sandberg, G., Romano, C.P. & Estelle, M. (1998) High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proceedings of the National Academy of Sciences, 95, 7197-7202.
41. Hacke, U.G., Jacobsen, A.L. & Pratt, R.B. (2009) Xylem function of arid-land shrubs from California, USA: an ecological and evolutionary analysis. Plant, Cell & Environment, 32, 1324-1333.
42. Hacke, U.G. & Sperry, J.S. (2001) Functional and ecological xylem anatomy. Perspectives in Plant Ecology, Evolution and Systematics, 4, 97-115.
43. Hastie, T. & Tibshirani, R. (1986) Generalized Additive Models. Statistical Science, 1, 297-318.
44. Iriondo, J.M., Albert, M.J. & Escudero, A. (2003) Structural equation models: An alternative for assesing causal relationships in threatened plant populations. Biological Conservation, 113, 367-377.
45. Körner, C. (2003) Alpine Plant Life: Functional Plant Ecology of High Mountain Ecosystems, 2nd edn. Springer-Verlag, Berlin.
46. Körner, C. (1998) A re-assessment of high elevation treeline position and their explanation. Oecologia, 115, 445-459.
47. Liu, Y.B. & Zhang, Q.B. (2010) Effect of climate on the growth of annual rings in the main roots of perennial forbs in an Inner Mongolian semi-arid grassland, China. Journal of Vegetation Science, 21, 899-907.
48. de Luis, M., Gričar, J., Čufar, K. & Raventós, J. (2007) Seasonal dynamics of wood formation in Pinus halepensis from dry and semi-arid ecosystems in Spain. IAWA Journal, 28, 389-404.
49. Martín, J.A., Esteban, L.G., de Palacios, P. & Fernández, F.G. (2010) Variation in wood anatomical traits of Pinus sylvestris L. between Spanish regions of provenance. Trees, 24, 1017-1028.
50. Matesanz, S., Gianoli, E. & Valladares, F. (2010) Global change and the evolution of phenotypic plasticity in plants. Annals of the New York Academy of Sciences, 1206, 35-55.
51. McCullagh, P. & Nelder, J.A. (1989) Generalized Linear Models. Chapman and Hall/CRC, Boca Raton, Florida, USA.
52. Mitrakos, K.A. (1980) A theory for Mediterranean plant life. Acta Oecologica, 1, 245-252.
53. Moser, L., Fonti, P., Buntgen, U., Esper, J., Luterbacher, J., Franzen, J. et al. (2010) Timing and duration of European larch growing season along altitudinal gradients in the Swiss Alps. Tree Physiology, 30, 225-233.
54. Nogues-Bravo, D.N., Araujo, M.B., Lasanta, T. & Moreno, J.I.L. (2008) Climate change in Mediterranean mountains during the 21st century. Ambio, 37, 280-285.
55. Olano, J.M., Eugenio, M. & Escudero, A. (2011) Site effect is stronger than species identity in driving demographic responses of Helianthemum (Cistaceae) shrubs in gypsum environments. American Journal of Botany, 98, 1016-1023.
56. Palacios, D., de Andrés, N. & Luengo, E. (2003) Distribution and effectiveness of nivation in Mediterranean mountain: Peñalara, Spain. Geomorphology, 54, 157-178.
57. Parmesan, C. & Yohe, G. (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421, 37-42.
58. Pauli, H., Gottfried, M., Dullinger, S., Abdaladze, O., Akhalkatsi, M., Benito Alonso, J.L. et al. (2012) Recent plant diversity changes on Europe's mountain summits. Science, 336, 353-355.
59. R Development Core Team (2011) R: A language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
60. Randin, C.F., Engler, R., Normand, S., Zappa, M., Zimmermann, N.E., Pearman, P.B. et al. (2009) Climate change and plant distribution: local models predict high-elevation persistence. Global Change Biology, 15, 1557-1569.
61. Rivas-Martínez, S. & Loidi, J. (1997) Bioclimatology of the Iberian Peninsula. Itinera Geobotánica, 13, 41-47.
62. Rossi, S., Deslauriers, A., Gricar, J., Seo, J.W., Rathgeber, C.B.K., Anfodillo, T. et al. (2008) Critical temperatures for xylogenesis in conifers of cold climates. Global Ecology and Biogeography, 17, 696-707.
63. Sanz-Elorza, M., Dana, E.D., González, A. & Sobrino, E. (2003) Changes in high-mountain vegetation of the central Iberian Peninsula as a probable sign of global warming. Annals of Botany, 92, 273-280.
64. Secchi, F. & Zwieniecki, M.A. (2011) Sensing embolism in xylem vessels: the role of sucrose as a trigger for refilling. Plant, Cell & Environment, 34, 514-524.
65. Sperry, J.S., Smith, D.D., Savage, V.M., Enquist, B.J., McCulloh, K.A., Reich, P.B. et al. (2012) A species-level model for metabolic scaling in trees I. Exploring boundaries to scaling space within and across species. Functional Ecology, 26, 1054-1065.
66. Tanaka, J.S. (1987) How big is enough?: sample size and goodness of fit in structural equation models with latent variables. Child Development, 58, 134-146.
67. Thomas, C.D., Franco, A.M.A. & Hill, J.K. (2006) Range retractions and extinction in the face of climate warming. Trends in Ecology and Evolution, 21, 415-416.
68. Trujillo, E., Molotch, N.P., Goulden, M.L., Kelly, A.E. & Bales, R.C. (2012) Elevation-dependent influence of snow accumulation on forest greening. Nature Geoscience, 5, 705-709.
69. Tulik, M., Marciszewska, K. & Adamczyk, J. (2010) Diminished vessel diameter as a possible factor in the decline of European ash (Fraxinus excelsior L.). Annals of Forest Science, 67, 103.
70. Tyree, M.T. (2003) Hydraulic limits on tree performance: transpiration, carbon gain and growth of trees. Trees, 17, 95-100.
71. Tyree, M.T. & Zimmermann, M.H. (2002) Xylem Structure and the Ascent of Sap. Springer, New York, USA.
72. Väre, H., Lampinen, C., Humphries, C. & Williams, P. (2003) Taxonomic diversity of vascular plants in the European alpine areas. Alpine biodiversity in Europe (eds L. Nagy, G. Grabherr, C. Körner & D.B.C. Thompson ), pp. 133-148. Springer, Berlin.
73. Villar-Salvador, P., Castro-Díez, P., Pérez-Rontomé, C. & Montserrat-Martí, G. (1997) Stem xylem features in three Quercus (Fagaceae) species along a climatic gradient in NE Spain. Trees-Structure and Function, 12, 90-96.
74. Walker, M.D. & Webber, P.J. (1994) Effects of interannual climate variation on aboveground phytomass in alpine vegetation. Ecology, 75, 393-408.
75. Wilson, R.J., Gutiérrez, D., Gutiérrez, J. & Monserrat, V.J. (2007) An elevational shift in butterfly species richness and composition accompanying recent climate change. Global Change Biology, 13, 1873-1887.
76. Ze-Xin, F., Shi-Bao, Z., Guang-You, H., Slik, J.W.F. & Cao, K.-F. (2012) Hydraulic conductivity traits predict growth rates and adult stature of 40 Asian tropical tree species better than wood density. Journal of Ecology, 100, 732-741.
77. Zuur, A.F., Leon, E.N., Walker, N., Saveliev, A.A. & Smith, G.M. (2009) Mixed effects models and extensions in ecology with R. Springer, New York, USA.