Sperry’s packing rule affects the spatial proximity but not clustering of xylem conduits: the case of Fagus sylvatica L.
In: IAWA JournalSearch for other papers by Angelo Rita in
Current site
Google Scholar
Search for other papers by Osvaldo Pericolo in
Current site
Google Scholar
Search for other papers by Antonio Saracino in
Current site
Google Scholar
Search for other papers by Marco Borghetti in
Current site
Google Scholar
Abstract
Sperry’s packing rule predicts the optimum packing of xylem conduits in woody plants, where the frequency of xylem conduits varies approximately inversely with the square of the conduit radius. However, it is well established that such anatomical disposition does not remain fixed but is subject to a suite of adaptations induced by physiological constraints driven by both ontogenetic development and environmental characteristics. Here we challenge the hypothesis that increasing frequency of xylem conduits, concomitant with the decrease in their lumen area along the xylem pathway, would affect the spatial distribution of vessels inside tree-rings and their aggregation. To this end, we measured the vessels’ anatomical characteristics inside each tree-ring along with a complete radial series taken at different stem heights of Fagus sylvatica L. trees. Point pattern analysis indicated a significant effect of the distance from the tree base and a weak effect of cambial age on the nearest neighbour distance among xylem vessels, suggesting that vessels were closer to each other near the apex, and became progressively more distant toward the base. The spatial pattern of xylem vessels violated the assumption of complete spatial randomness, vessel spatial arrangement followed a uniform distribution at different distances from the tree base. Although there was an increase in the intensity and proximity among vessels, we demonstrated that no patterns of aggregation between vessels were found in sampled F. sylvatica trees. Rather, point pattern profiles clearly highlighted a lack of aggregation of vessels in the face of a regular spatial distribution in the annual growth rings along the stems.
Purchase
Buy instant access (PDF download and unlimited online access):
Institutional Login
Log in with Open Athens, Shibboleth, or your institutional credentials
Personal login
Log in with your brill.com account
-
Anderegg WRL, Konings AG, Trugman AT, Yu K, Bowling DR, Gabbitas R, Karp DS, Pacala S, Sperry JS, Sulman BN, Zenes N. 2018. Hydraulic diversity of forests regulates ecosystem resilience during drought. Nature 561: 538–541. DOI: 10.1038/s41586-018-0539-7.
-
André JP, Catesson AM, Liberman M. 1999. Characters and origin of vessels with heterogenous structure in leaf and flower abscission zones. Can. J. Bot. 77: 253–261.
-
Anfodillo T, Carraro V, Carrer M, Fior C, Rossi S. 2006. Convergent tapering of xylem conduits in different woody species. New Phytol. 169: 279–290. DOI: 10.1111/j.1469-8137.2005.01587.x.
-
Arbellay E, Fonti P, Stoffel M. 2012. Duration and extension of anatomical changes in wood structure after cambial injury. J. Exp. Bot. 63: 3271–3277. DOI: 10.1093/jxb/ers050.
-
Baas P, Carlquist S. 1985. A comparison of the ecological wood anatomy of the floras of southern California and Israel. IAWA J. 6: 349–353. DOI: 10.1163/22941932-90000961.
-
Baddeley A. 2015. Spatial point patterns: methodology and applications with R. Chapman and Hall/CRC Press, Boca Raton, USA.
-
Bailey TC, Gatrell AC. 1995. Interactive spatial data analysis. Prentice-Hall, NJ, USA.
-
Barton K. 2020. MuMIn: Multi-Model Inference. R package version 1.43.17. https://CRAN.R-project.org/package=MuMIn.
-
Borghetti M, Gentilesca T, Leonardi S, van Noije T, Rita A. 2017. Long-term temporal relationships between environmental conditions and xylem functional traits: a meta-analysis across a range of woody species along climatic and nitrogen deposition gradients. Tree Physiol. 37: 4–17. DOI: 10.1093/treephys/tpw087.
-
Carlquist S. 1984. Vessel grouping in dicotyledon wood. Aliso 10: 505–525. DOI: 10.5642/aliso.19841004.03.
-
Carlquist S. 2001. Comparative wood anatomy. Springer Verlag, Berlin, Germany.
-
Carlquist S. 2009. Non-random vessel distribution in woods: patterns, modes, diversity, correlations. Aliso 27: 39–58. DOI: 10.5642/aliso.20092701.04.
-
Castagneri D, Carrer M, Regev L, Boaretto E. 2019. Precipitation variability differently affects radial growth, xylem traits and ring porosity of three Mediterranean oak species at xeric and mesic sites. The Science of the Total Environment 699: 134285. DOI: 10.1016/j.scitotenv.2019.134285.
-
Clark PJ, Evans FC. 1954. Distance to nearest neighbor as a measure of spatial relationships in populations. Ecology 35: 445–453. DOI: 10.2307/1931034.
-
Cressie N, Wikle CK. 2015. Statistics for spatio-temporal data. John Wiley & Sons, NJ, USA.
-
Diaconu D, Stangler DF, Kahle HP, Spiecker H. 2016. Vessel plasticity of European beech in response to thinning and aspect. Tree Physiol. 36(10): 1260–1271. DOI: 10.1093/treephys/tpw053.
-
Diggle PJ. 2013. Statistical analysis of spatial and spatio-temporal point patterns, 3rd Edn. CRC Press, Boca Raton, USA.
-
Diggle PJ, Cox TF. 1983. Some distance-based tests of independence for sparsely-sampled multivariate spatial point patterns. International Statistical Review/Revue Internationale de Statistique 51: 11.
-
Eilmann B, Sterck F, Wegner L, de Vries SMG, von Arx G, Mohren GMJ, den Ouden J, Sass-Klaassen U. 2014. Wood structural differences between northern and southern beech provenances growing at a moderate site. Tree Physiol. 34(8): 882–893. DOI: 10.1093/treephys/tpu069.
-
Fonti P, Von Arx G, García-González I, Eilmann B, Sass-Klaassen U, Gartner H, Eckstein D. 2010. Studying global change through investigation of the plastic responses of xylem anatomy in tree rings. New Phytol. 185: 42–53. DOI: 10.1111/j.14698137.2009.03030.x.
-
Gentilesca T, Rita A, Brunetti M, Giammarchi F, Leonardi S, Magnani F, van Noije T, Tonon G, Borghetti M. 2018. Nitrogen deposition outweighs climatic variability in driving annual growth rate of canopy beech trees: evidence from long-term growth reconstruction across a geographic gradient. Global Change Biol. 24: 2898–2912. DOI: 10.1111/gcb.14142.
-
González-Cásares M, Julio Camarero J, Colangelo M, Rita A, Pompa-García M. 2019. High responsiveness of wood anatomy to water availability and drought near the equatorial rear edge of Douglas-fir. Can. J. Forest Res. 49: 1114–1123. DOI: 10.1139/cjfr-2019-0120.
-
Haase P. 1995. Spatial pattern analysis in ecology based on Ripley’s K-function: introduction and methods of edge correction. J. Veg. Sci. 6: 575–582. DOI: 10.2307/3236356.
-
Hacke UG, Sperry JS. 2001. Functional and ecological xylem anatomy. Perspectives in Plant Ecology, Evolution and Systematics 4: 97–115. DOI: 10.1078/1433-8319-00017.
-
Holmes RL, Fritts HC. 1986. Tree-ring chronologies of western North America: California, eastern Oregon and northern great basin with procedures used in the chronology development work including user’s manuals for computer programs COFECHA and ARSTAN. https://repository.arizona.edu/handle/10150/304672.
-
Hölttä T, Vesala T, Perämäki M, Nikinmaa E. 2006. Refilling of embolised conduits as a consequence of “Münch water” circulation. Funct. Plant Biol. 33: 949. DOI: 10.1071/FP06108.
-
IAWA Committee. 1989. IAWA list of microscopic features for hardwood identification. IAWA Bull. 10: 219–332.
-
Jansen S, Gortan E, Lens F, Lo Gullo MA, Salleo S, Scholz A, Stein A, Trifilò P, Nardini A. 2011. Do quantitative vessel and pit characters account for ion-mediated changes in the hydraulic conductance of angiosperm xylem? New Phytol. 189: 218–228. DOI: 10.1111/j.1469-8137.2010.03448.x.
-
Kašpar J, Tumajer J, Treml V. 2019. IncrementR: analysing height growth of trees and shrubs in R. Dendrochronologia 53: 48–54. DOI: 10.1016/j.dendro.2018.11.001.
-
Lechthaler S, Turnbull TL, Gelmini Y, Pirotti F, Anfodillo T, Adams MA, Petit G. 2019. A standardization method to disentangle environmental information from axial trends of xylem anatomical traits. Tree Physiol. 39: 495–502. DOI: 10.1093/treephys/tpz068/5519844.
-
Lens F, Sperry JS, Christman MA, Choat B, Rabaey D, Jansen S. 2011. Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytol. 190: 709–723. DOI: 10.1111/j.1469-8137.2010.03518.x.
-
Lenth RV. 2016. Least-squares means: the R package lsmeans. J. Stat. Softw.: 69. DOI: 10.18637/jss.v069.i01.
-
Loepfe L, Martinez-Vilalta J, Piñol J, Mencuccini M. 2007. The relevance of xylem network structure for plant hydraulic efficiency and safety. J. Theor. Biol. 247: 788–803. DOI: 10.1016/j.jtbi.2007.03.036.
-
Martínez-Vilalta J, Mencuccini M, Alvarez X, Camacho J, Loepfe L, Piñol J. 2012. Spatial distribution and packing of xylem conduits. Am. J. Bot. 99: 1189–1196. DOI: 10.3732/ajb.1100384.
-
McCulloh K, Sperry JS, Lachenbruch B, Meinzer FC, Reich PB, Voelker S. 2010. Moving water well: comparing hydraulic efficiency in twigs and trunks of coniferous, ring-porous, and diffuse-porous saplings from temperate and tropical forests. New Phytol. 186: 439–450. DOI: 10.1111/j.1469-8137.2010.03181.x.
-
Mencuccini M, Manzoni S, Christoffersen B. 2019. Modelling water fluxes in plants: from tissues to biosphere. New Phytol. 222: 1207–1222. DOI: 10.1111/nph.15681.
-
Mencuccini M, Martinez-Vilalta J, Piñol J, Loepfe L, Burnat M, Alvarez X, Camacho J, Gil D. 2010. A quantitative and statistically robust method for the determination of xylem conduit spatial distribution. Am. J. Botany 97: 1247–1259. DOI: 10.3732/ajb.0900289.
-
Nakagawa S, Schielzeth H. 2013. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4: 133–142. DOI: 10.1111/j.2041-210x.2012.00261.x.
-
Nardini A, Dimasi F, Klepsch M, Jansen S. 2012. Ion-mediated enhancement of xylem hydraulic conductivity in four Acer species: relationships with ecological and anatomical features. Tree Physiol. 32: 1434–1441. DOI: 10.1093/treephys/tps107.
-
Nielsen SS, von Arx G, Damgaard CF, Abermann J, Buchwal A, Büntgen U, Treier UA, Barfod AS, Normand S. 2017. Xylem anatomical trait variability provides insight on the climate-growth relationship of Betula nana in western Greenland. Arct. Antarct. Alp. Res. 49: 359–371. DOI: 10.1657/AAAR0016-041.
-
Page GFM, Liu J, Grierson PF. 2011. Three-dimensional xylem networks and phyllode properties of co-occurring Acacia. Plant Cell Environ. 34: 2149–2158. DOI: 10.1111/j.1365-3040.2011.02411.x.
-
Petit G, Pfautsch S, Anfodillo T, Adams MA. 2010. The challenge of tree height in Eucalyptus regnans: when xylem tapering overcomes hydraulic resistance. New Phytol. 187: 1146–1153. DOI: 10.1111/j.1469-8137.2010.03304.x.
-
Ripley BD. 1988. Statistical inference for spatial processes. Cambridge University Press, UK.
-
Rita A, Cherubini P, Leonardi S, Todaro L, Borghetti M. 2015. Functional adjustments of xylem anatomy to climatic variability: insights from long-term Ilex aquifolium tree-ring series. Tree Physiol. 35: 817–828. DOI: 10.1093/treephys/tpv055.
-
Robert EMR, Koedam N, Beeckman H, Schmitz N. 2009. A safe hydraulic architecture as wood anatomical explanation for the difference in distribution of the mangroves Avicennia and Rhizophora. Funct. Ecol. 23: 649–657. DOI: 10.1111/j.1365-2435.2009.01551.x.
-
Ryan MG, Phillips N, Bond BJ. 2006. The hydraulic limitation hypothesis revisited. Plant Cell Environ. 29: 367–381. DOI: 10.1111/j.1365-3040.2005.01478.x.
-
Savage JA, Clearwater MJ, Haines DF, Tamir K, Mencuccini M, Sevanto S, Turgeon R, Zhang C. 2016. Allocation, stress tolerance and carbon transport in plants: how does phloem physiology affect plant ecology? Plant Cell Environ. 39: 709–725. DOI: 10.1111/pce.12602.
-
Savage VM, Bentley LP, Enquist BJ, Sperry JS, Smith DD, Reich PB, von Allmen EI. 2010. Hydraulic trade-offs and space-filling enable better predictions of vascular structure and function in plants. PNAS 107: 22722–22727. DOI: 10.1073/pnas.1012194108.
-
Scholz A, Klepsch M, Karimi Z, Jansen S. 2013. How to quantify conduits in wood? Front. Plant Sci. 4: 56. DOI: 10.3389/fpls.2013.00056.
-
Schuldt B, Knutzen F, Delzon S, Jansen S, Müller-Haubold H, Burlett R, Clough Y, Leuschner C. 2016. How adaptable is the hydraulic system of European beech in the face of climate change-related precipitation reduction? New Phytol. 210: 443–458. DOI: 10.1111/nph.13798.
-
Schweingruber FH. 2007. Wood structure and environment. Springer Verlag, Berlin, Germany.
-
Sperry JS, Meinzer FC, McCulloh KA. 2008. Safety and efficiency conflicts in hydraulic architecture: scaling from tissues to trees. Plant Cell Environ. 31: 632–645. DOI: 10.1111/j.1365-3040.2007.01765.x.
-
Trifilò P, Raimondo F, Lo Gullo MA, Barbera PM, Salleo S, Nardini A. 2014. Relax and refill: xylem rehydration prior to hydraulic measurements favors embolism repair in stems and generates artificially low PLC values. Plant Cell Environ. 37: 2491–2499. DOI: 10.1111/pce.12313.
-
Tyree MT, Davis SD, Cochard H. 1994. Biophysical perspectives of xylem evolution: is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction? IAWA J. 15(4): 335–360.
-
Tyree MT, Zimmermann MH. 2002. Xylem structure and the ascent of sap. Springer Verlag, Berlin, Germany.
-
von Arx G, Crivellaro A, Prendin AL, Čufar K, Carrer M. 2016. Quantitative wood anatomy — practical guidelines. Front. Plant Sci.: 7. DOI: 10.3389/fpls.2016.00781.
-
von Arx G, Kueffer C, Fonti P. 2013. Quantifying plasticity in vessel grouping — added value from the image analysis tool ROXAS. IAWA J. 34: 433–454. DOI: 10.1163/22941932-00000035.
-
West GB, Brown JH, Enquist BJ. 1999. A general model for the structure and allometry of plant vascular systems. Nature 400: 664–667. DOI: 10.1038/23251.
-
Wheeler JK, Sperry JS, Hacke UG, Hoang N. 2005. Inter-vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade-off in xylem transport. Plant Cell Environ. 28: 800–812. DOI: 10.1111/j.1365-3040.2005.01330.x.
-
Zimmermann MH, Jeje AA. 1981. Vessel-length distribution in stems of some American woody plants. Can. J. Bot. 59: 1882–1892.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 854 | 394 | 17 |
| Full Text Views | 34 | 11 | 1 |
| PDF Views & Downloads | 77 | 26 | 0 |
Sperry’s packing rule affects the spatial proximity but not clustering of xylem conduits: the case of Fagus sylvatica L.
In: IAWA JournalSearch for other papers by Angelo Rita in
Current site
Google Scholar
PubMed
Search for other papers by Osvaldo Pericolo in
Current site
Google Scholar
PubMed
Search for other papers by Antonio Saracino in
Current site
Google Scholar
PubMed
Search for other papers by Marco Borghetti in
Current site
Google Scholar
PubMed
Abstract
Sperry’s packing rule predicts the optimum packing of xylem conduits in woody plants, where the frequency of xylem conduits varies approximately inversely with the square of the conduit radius. However, it is well established that such anatomical disposition does not remain fixed but is subject to a suite of adaptations induced by physiological constraints driven by both ontogenetic development and environmental characteristics. Here we challenge the hypothesis that increasing frequency of xylem conduits, concomitant with the decrease in their lumen area along the xylem pathway, would affect the spatial distribution of vessels inside tree-rings and their aggregation. To this end, we measured the vessels’ anatomical characteristics inside each tree-ring along with a complete radial series taken at different stem heights of Fagus sylvatica L. trees. Point pattern analysis indicated a significant effect of the distance from the tree base and a weak effect of cambial age on the nearest neighbour distance among xylem vessels, suggesting that vessels were closer to each other near the apex, and became progressively more distant toward the base. The spatial pattern of xylem vessels violated the assumption of complete spatial randomness, vessel spatial arrangement followed a uniform distribution at different distances from the tree base. Although there was an increase in the intensity and proximity among vessels, we demonstrated that no patterns of aggregation between vessels were found in sampled F. sylvatica trees. Rather, point pattern profiles clearly highlighted a lack of aggregation of vessels in the face of a regular spatial distribution in the annual growth rings along the stems.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 854 | 394 | 17 |
| Full Text Views | 34 | 11 | 1 |
| PDF Views & Downloads | 77 | 26 | 0 |
