Convergent Vessel Diameter–Stem Diameter Scaling across Five Clades of New and Old World Eudicots from Desert to Rain Forest

Premise of research. Variation in average xylem vessel diameter across species has important functional consequences, but the causes of this variation remain unclear. Average vessel diameter is known to scale with stem size within and across species. Vessel diameter also seems to differ between clades and across environments, with dryland plants having narrower, more cavitation-resistant vessels. As a result, it is not clear to what extent phylogenetic affinity and environment are associated with differences in the vessel diameter–stem size relationship. Methodology. With linear models and correlations, we explored the influence of environment and phylogeny on the vessel diameter–stem diameter relationship in a molecular phylogenetic context across 83 species in four families spanning desert to rain forest in the Americas, Africa, Asia, and Madagascar. Pivotal results. Mean species vessel diameter was strongly predicted by trunk diameter (slope ∼0.33), and this slope was not affected by either phylogenetic affinity or environment. Clades differed only slightly in mean vessel diameter when controlling for stem size, and there was no tendency for plants of moist environments to have wider vessels. Of four climate indexes, only the temperature index contributed to explaining vessel diameter, although very weakly. Conclusions. Our results are congruent with models suggesting that natural selection should maximize vessel conductivity while minimizing cavitation risk via vessel taper in the context of conductive path length. Because neither environment nor phylogeny contributed to explaining vessel diameter–stem diameter scaling across species, our results appear congruent with the notion that selection favoring cavitation resistance via narrow vessels should lead to shorter statures independently of ancestry or habitat. The repeated finding of narrow vessels in dryland plants might therefore reflect the smaller average stem size of plants in drylands rather than the plants having vessels that are narrow for their stem diameters.

[1]  Julieta A. Rosell,et al.  Vessel diameter-stem diameter scaling across woody angiosperms and the ecological causes of xylem vessel diameter variation. , 2013, The New phytologist.

[2]  M. Westoby,et al.  Stem xylem conductivity is key to plant water balance across Australian angiosperm species , 2012 .

[3]  M. Suchard,et al.  Bayesian Phylogenetics with BEAUti and the BEAST 1.7 , 2012, Molecular biology and evolution.

[4]  T. Anfodillo,et al.  Testing the equi-resistance principle of the xylem transport system in a small ash tree: empirical support from anatomical analyses. , 2012, Tree physiology.

[5]  J. Montero,et al.  Insights into the historical construction of species-rich Mesoamerican seasonally dry tropical forests: the diversification of Bursera (Burseraceae, Sapindales). , 2012, The New phytologist.

[6]  P. Hanáček,et al.  Age and diversity in Old World succulent species of Euphorbia (Euphorbiaceae). , 2011 .

[7]  E. Nikinmaa,et al.  A carbon cost-gain model explains the observed patterns of xylem safety and efficiency. , 2011, Plant, cell & environment.

[8]  R. Malpassi,et al.  Comparative root anatomy of papilionoid Legumes , 2011 .

[9]  T. Terrazas,et al.  Stem and wood allometric relationships in Cacteae (Cactaceae) , 2011, Trees.

[10]  T. Anfodillo,et al.  Comment on “The blind men and the elephant: the impact of context and scale in evaluating conflicts between plant hydraulic safety and efficiency” by Meinzer et al. (2010) , 2011, Oecologia.

[11]  Mark A. Miller,et al.  Creating the CIPRES Science Gateway for inference of large phylogenetic trees , 2010, 2010 Gateway Computing Environments Workshop (GCE).

[12]  D D Smith,et al.  Hydraulic trade-offs and space filling enable better predictions of vascular structure and function in plants , 2010, Proceedings of the National Academy of Sciences.

[13]  Liam J. Revell,et al.  Phylogenetic signal and linear regression on species data , 2010 .

[14]  M. Clements,et al.  Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana , 2010, Proceedings of the National Academy of Sciences.

[15]  M. Adams,et al.  The challenge of tree height in Eucalyptus regnans: when xylem tapering overcomes hydraulic resistance. , 2010, The New phytologist.

[16]  Daniel M. Johnson,et al.  The blind men and the elephant: the impact of context and scale in evaluating conflicts between plant hydraulic safety and efficiency , 2010, Oecologia.

[17]  M. Tyree,et al.  A computational algorithm addressing how vessel length might depend on vessel diameter. , 2010, Plant, cell & environment.

[18]  M. Tyree,et al.  The impact of vessel size on vulnerability curves: data and models for within-species variability in saplings of aspen, Populus tremuloides Michx. , 2010, Plant, cell & environment.

[19]  Campbell O. Webb,et al.  Picante: R tools for integrating phylogenies and ecology , 2010, Bioinform..

[20]  D. Baum,et al.  Are spurred cyathia a key innovation? Molecular systematics and trait evolution in the slipper spurges (Pedilanthus clade: Euphorbia, Euphorbiaceae). , 2010, American journal of botany.

[21]  Daniel S Falster,et al.  Angiosperm wood structure: Global patterns in vessel anatomy and their relation to wood density and potential conductivity. , 2010, American journal of botany.

[22]  L. Flanagan,et al.  Warmer and drier conditions stimulate respiration more than photosynthesis in a boreal peatland ecosystem: analysis of automatic chambers and eddy covariance measurements. , 2009, Plant, cell & environment.

[23]  P. Soffiatti,et al.  Ecological Wood Anatomy of Miconia Sellowiana (Melastomataceae) in three vegetation types of paraná state, Brazil , 2010 .

[24]  C. Leuschner,et al.  Vessel diameter and xylem hydraulic conductivity increase with tree height in tropical rainforest trees in Sulawesi, Indonesia , 2010 .

[25]  S. Haag,et al.  ANDEAN SPECIATION AND VICARIANCE IN NEOTROPICAL MACROCARPAEA (GENTIANACEAE–HELIEAE)1 , 2009 .

[26]  Shawn W. Laffan,et al.  Global patterns in plant height , 2009 .

[27]  E. Smets,et al.  Woodiness within the Spermacoceae-Knoxieae alliance (Rubiaceae): retention of the basal woody condition in Rubiaceae or recent innovation? , 2009, Annals of botany.

[28]  David C. Tank,et al.  An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: , 2009 .

[29]  P. Becker,et al.  Axial and Radial Variations in Xylem Anatomy of Angiosperm and Conifer Trees in Yunnan, China , 2009 .

[30]  S. Magallón,et al.  Angiosperm diversification through time. , 2009, American journal of botany.

[31]  Broome,et al.  Literature cited , 1924, A Guide to the Carnivores of Central America.

[32]  Campbell O. Webb,et al.  Bioinformatics Applications Note Phylocom: Software for the Analysis of Phylogenetic Community Structure and Trait Evolution , 2022 .

[33]  S. Razafimandimbison,et al.  Ambilobea, a new genus from Madagascar, the position of Aucoumea, and comments on the tribal classification of the frankincense and myrrh family (Burseraceae) , 2008 .

[34]  D. Posada.  jModelTest: phylogenetic model averaging. , 2008, Molecular biology and evolution.

[35]  Frederick C Meinzer,et al.  Safety and efficiency conflicts in hydraulic architecture: scaling from tissues to trees. , 2008, Plant, cell & environment.

[36]  A. R. Ennos,et al.  Are radial changes in vascular anatomy mechanically induced or an ageing process? Evidence from observations on buttressed tree root systems , 2008, Trees.

[37]  Maurizio Mencuccini,et al.  Tapering of xylem conduits and hydraulic limitations in sycamore (Acer pseudoplatanus) trees. , 2008, The New phytologist.

[38]  J. Grant,et al.  Wood anatomy of Gentianaceae, tribe Helieae, in relation to ecology, habit, systematics, and sample diameter , 2005, Brittonia.

[39]  T. Terrazas,et al.  Wood anatomy and its relation to plant size and latitude in Buddleja L. (Buddlejaceae) , 2008 .

[40]  S. Pallardy,et al.  Applying a universal scaling model to vascular allometry in a single-stemmed, monopodially branching deciduous tree (Attim's model). , 2008, Tree physiology.

[41]  Rodrigo Lopez,et al.  Clustal W and Clustal X version 2.0 , 2007, Bioinform..

[42]  Federico Magnani,et al.  Sanio's laws revisited. Size-dependent changes in the xylem architecture of trees. , 2007, Ecology letters.

[43]  M. Olson.  Wood ontogeny as a model for studying heterochrony, with an example of paedomorphosis in Moringa (Moringaceae) , 2007 .

[44]  J. Fisher,et al.  Wood vessel diameter is related to elevation and genotype in the Hawaiian tree Metrosideros polymorpha (Myrtaceae). , 2007, American journal of botany.

[45]  Joey Shaw,et al.  Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. , 2007, American journal of botany.

[46]  S. Carlquist,et al.  WOOD ANATOMY OF TASMANNIA; SUMMARY OF WOOD ANATOMY OF WINTERACEAE , 2007 .

[47]  P. Baas,et al.  Variations In Dieot Wood Anatomy: A Global Analysis Based on the Insidewood Database , 2007 .

[48]  B. Simpson,et al.  Molecular phylogenetic analysis of Commiphora (Burseraceae) yields insight on the evolution and historical biogeography of an "impossible" genus. , 2007, Molecular phylogenetics and evolution.

[49]  D. Coomes,et al.  Scaling of tree vascular transport systems along gradients of nutrient supply and altitude , 2007, Biology Letters.

[50]  J. Sperry,et al.  Size and function in conifer tracheids and angiosperm vessels. , 2006, American journal of botany.

[51]  Ulrike Groemping,et al.  Relative Importance for Linear Regression in R: The Package relaimpo , 2006 .

[52]  J. Sperry,et al.  Scaling of angiosperm xylem structure with safety and efficiency. , 2006, Tree physiology.

[53]  Julieta A. Rosell,et al.  USING HETEROCHRONY TO DETECT MODULARITY IN THE EVOLUTION OF STEM DIVERSITY IN THE PLANT FAMILY MORINGACEAE , 2006, Evolution; international journal of organic evolution.

[54]  Joshua S. Weitz,et al.  Ontogenetically stable hydraulic design in woody plants , 2006 .

[55]  Tommaso Anfodillo,et al.  Convergent tapering of xylem conduits in different woody species. , 2006, The New phytologist.

[56]  Xu Yu-bo,et al.  Reachability Checking of Finite Precision Timed Automata , 2006 .

[57]  K. Niklas,et al.  A comparison between the record height-to-stem diameter allometries of Pachycaulis and Leptocaulis species. , 2006, Annals of botany.

[58]  J. L. Parra,et al.  Very high resolution interpolated climate surfaces for global land areas , 2005 .

[59]  S. Jansen,et al.  Relationships within balsaminoid Ericales: a wood anatomical approach. , 2005, American journal of botany.

[60]  S. Zaehle.  Effect Of Height On Tree Hydraulic Conductance Incompletely Compensated By Xylem Tapering , 2005 .

[61]  J. Sperry,et al.  Patterns in hydraulic architecture and their implications for transport efficiency. , 2005, Tree physiology.

[62]  Hanns-Christof Spatz,et al.  Growth and hydraulic (not mechanical) constraints govern the scaling of tree height and mass. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[63]  J. Fisher,et al.  Hydraulic conductivity and embolism in the mangrove tree Laguncularia racemosa. , 2004, Tree physiology.

[64]  J. Fisher,et al.  A survey of vessel dimensions in stems of tropical lianas and other growth forms , 1990, Oecologia.

[65]  C. Lundgren.  Cell Wall Thickness and Tangential and Radial Cell Diameter of Fertilized and Irrigated Norway Spruce , 2004 .

[66]  S. Jansen,et al.  Ecological trends in the wood anatomy of Vaccinioideae (Ericaceae s.l.) , 2004 .

[67]  M. Möller,et al.  Monophyly and relationships of the tribe Exaceae (Gentianaceae) inferred from nuclear ribosomal and chloroplast DNA sequences. , 2003, Molecular phylogenetics and evolution.

[68]  M. Olson.  Stem and leaf anatomy of the arborescent Cucurbitaceae Dendrosicyos socotrana with comments on the evolution of pachycauls from lianas , 2003, Plant Systematics and Evolution.

[69]  T. Garland,et al.  TESTING FOR PHYLOGENETIC SIGNAL IN COMPARATIVE DATA: BEHAVIORAL TRAITS ARE MORE LABILE , 2003, Evolution; international journal of organic evolution.

[70]  J. Sperry,et al.  Water transport in plants obeys Murray's law , 2003, Nature.

[71]  B. Enquist.  Cope's Rule and the evolution of long‐distance transport in vascular plants: allometric scaling, biomass partitioning and optimization , 2003 .

[72]  M. Olson.  Combining Data from DNA Sequences and Morphology for a Phylogeny of Moringaceae (Brassicales) , 2009 .

[73]  B. Enquist.  Universal scaling in tree and vascular plant allometry: toward a general quantitative theory linking plant form and function from cells to ecosystems. , 2002, Tree physiology.

[74]  Maurizio Mencuccini.  Hydraulic constraints in the functional scaling of trees. , 2002, Tree physiology.

[75]  G. Quinn,et al.  Experimental Design and Data Analysis for Biologists , 2002 .

[76]  P. Campanello,et al.  Axial and radial water transport and internal water storage in tropical forest canopy trees , 2002, Oecologia.

[77]  Mark W. Chase,et al.  Evolution of the angiosperms: calibrating the family tree , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[78]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[79]  P. Becker,et al.  Estimation of conduit taper for the hydraulic resistance model of West et al. , 2001, Tree physiology.

[80]  M. Olson,et al.  Stem and root anatomical correlations with life form diversity, ecology, and systematics in Moringa (Moringaceae) , 2001 .

[81]  N. Holbrook,et al.  Hydraulic properties of individual xylem vessels of Fraxinus americana. , 2001, Journal of experimental botany.

[82]  P. Becker,et al.  Tapered conduits can buffer hydraulic conductance from path-length effects. , 2000, Tree physiology.

[83]  P. Herendeen,et al.  Utility of wood anatomical characters in cladistic analyses , 2000 .

[84]  E. S. Alves,et al.  ECOLOGICAL TRENDS IN THE WOOD ANATOMY OF SOME BRAZILIAN SPECIES. 1. GROWTH RINGS AND VESSELS , 2000 .

[85]  James H. Brown,et al.  A general model for the structure and allometry of plant vascular systems , 1999, Nature.

[86]  Steven E. Ruzin,et al.  Plant Microtechnique and Microscopy , 1999 .

[87]  T. F. Hansen,et al.  TRANSLATING BETWEEN MICROEVOLUTIONARY PROCESS AND MACROEVOLUTIONARY PATTERNS: THE CORRELATION STRUCTURE OF INTERSPECIFIC DATA , 1996, Evolution; international journal of organic evolution.

[88]  S. Carlquist.  Wood Anatomy of Compositae: A Summary, With Comments on Factors Controlling Wood Evolution , 1996 .

[89]  R. Bosker.  Boekbespreking van "A.S. Bryk & S.W. Raudenbusch - Hierarchical linear models: Applications and data analysis methods" : Sage Publications, Newbury Parki, London/New Delhi 1992 , 1995 .

[90]  K. Niklas.  The allometry of safety‐factors for plant height , 1994 .

[91]  H. Lindorf.  Eco-Anatomical Wood Features of Species from a Very Dry Tropical Forest , 1994 .

[92]  S. Davis,et al.  Biophysical Perspectives of Xylem Evolution: is there a Tradeoff of Hydraulic Efficiency for Vulnerability to Dysfunction? , 1994 .

[93]  R. Crook,et al.  Radial variation in wood specific gravity, fibre length and vessel area for two Central American hardwoods: Hyeronima alchorneoides and Vochysia guatemalensis: natural and plantation-grown trees. , 1993 .

[94]  Anthony S. Bryk,et al.  Hierarchical Linear Models: Applications and Data Analysis Methods , 1992 .

[95]  F. Ewers,et al.  The hydraulic architecture of trees and other woody plants , 1991 .

[96]  J. Fisher,et al.  VARIATION IN VESSEL LENGTH AND DIAMETER IN STEMS OF SIX TROPICAL AND SUBTROPICAL LIANAS , 1989 .

[97]  Peter Gasson,et al.  IAWA List of Microscopic Features for Hardwood Identification by an IAWA Committee , 1989 .

[98]  S. Carlquist.  Wood Anatomy of Tasmannia , 1989 .

[99]  A. Tyree,et al.  Vulnerability of Xylem to Cavitation and Embolism , 1989 .

[100]  P. M. Esser,et al.  Wood Anatomy of the Oleaceae , 1988 .

[101]  H. Goldstein.  Multilevel Statistical Models , 2006 .

[102]  J. Felsenstein.  Phylogenies and the Comparative Method , 1985, The American Naturalist.

[103]  P. Baas,et al.  A Comparison of the Ecological Wood Anatomy of the Floras of Southern California and Israel , 1985 .

[104]  Josefina Barajas-Morales.  Wood Structural Differences between Trees of Two Tropical Forests in Mexico , 1985 .

[105]  P. M. Rury.  Systematic and Ecological Wood Anatomy of the Erythroxylaceae , 1985 .

[106]  D. Hoekman,et al.  Ecological Wood Anatomy of the Woody Southern Californian Flora , 1985 .

[107]  S. Carlquist.  Vasicentric Tracheids as a Drought Survival Mechanism in the Woody Flora of Southern California and Similar Regions; Review of Vasicentric Tracheids , 1985 .

[108]  M. Zimmermann,et al.  The hydraulic architecture of eastern hemlock (Tsuga canadensis) , 1984 .

[109]  S. Carlquist.  Vessel Grouping in Dicotyledon Wood , 1984 .

[110]  M. Zimmermann,et al.  The control of vessel size and density along the plant axis: a new hypothesis , 1983 .

[111]  A. Fahn,et al.  Some Ecological Trends in Vessel Characters , 1983 .

[112]  S. Carlquist.  The use of ethylenediamine in softening hard plant structures for paraffin sectioning. , 1982, Stain technology.

[113]  P. Sen,et al.  Introduction to bivariate and multivariate analysis , 1981 .

[114]  J. P. Holt,et al.  Geometric similarity of aorta, venae cavae, and certain of their branches in mammals. , 1981, The American journal of physiology.

[115]  S. Carlquist.  Further Concepts in Ecological Wood Anatomy, with Comments on Recent Work in Wood Anatomy and Evolution , 1980 .

[116]  K Schmidt-Nielsen,et al.  Scaling in biology: the consequences of size. , 1975, The Journal of experimental zoology.

[117]  S. Carlquist.  Wood Anatomy of Lobelioideae (Campanulaceae) , 1969 .

[118]  V. I. Cheadle.  The Anatomy of Plants , 1961 .

[119]  F. O. Bower,et al.  Comparative Anatomy of the Vegetative Organs of the Phanerogams and Ferns , 2009, Nature.

[120]  F. Bower,et al.  Comparative anatomy of the vegetative organs of the phanerogams and ferns / by A. de Bary ; translated and annotated by F.O. Bower and D.H. Scott ; with 241 woodcuts and an index. , 1884 .