Hydraulic Consequences of Vessel Evolution in Angiosperms

We tested two hypotheses for how vessel evolution in angiosperms influenced xylem function. First, the transition to vessels decreased resistance to flow—often considered the driving force for their evolution. Second, the transition to vessels compromised safety from cavitation—a constraint emerging from the “pit area hypothesis” for vulnerability to cavitation. Data were obtained from branch wood of 17 basal taxa with vessels and two eudicots possessing “primitive” perforation plates. Results were compared with previous data from vesselless angiosperms and eudicots with simple perforation plates. Contrary to the first hypothesis, basal taxa did not have significantly lower sapwood‐specific resistivity than vesselless angiosperms, despite vessels being wider than tracheids. Eudicot resistivity was ca. 4.5 times lower. On a vessel‐area basis, resistivity of “primitive” vessels ( \documentclass{aastex} \usepackage{amsbsy} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{bm} \usepackage{mathrsfs} \usepackage{pifont} \usepackage{stmaryrd} \usepackage{textcomp} \usepackage{portland,xspace} \usepackage{amsmath,amsxtra} \usepackage[OT2,OT1]{fontenc} \newcommand\cyr{ \renewcommand\rmdefault{wncyr} \renewcommand\sfdefault{wncyss} \renewcommand\encodingdefault{OT2} \normalfont \selectfont} \DeclareTextFontCommand{\textcyr}{\cyr} \pagestyle{empty} \DeclareMathSizes{10}{9}{7}{6} \begin{document} \landscape $$435\pm 104$$ \end{document} MPa s m−2) was lower than angiosperm tracheids ( \documentclass{aastex} \usepackage{amsbsy} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{bm} \usepackage{mathrsfs} \usepackage{pifont} \usepackage{stmaryrd} \usepackage{textcomp} \usepackage{portland,xspace} \usepackage{amsmath,amsxtra} \usepackage[OT2,OT1]{fontenc} \newcommand\cyr{ \renewcommand\rmdefault{wncyr} \renewcommand\sfdefault{wncyss} \renewcommand\encodingdefault{OT2} \normalfont \selectfont} \DeclareTextFontCommand{\textcyr}{\cyr} \pagestyle{empty} \DeclareMathSizes{10}{9}{7}{6} \begin{document} \landscape $$906\pm 89$$ \end{document} MPa s m−2) but still greater than eudicot vessels ( \documentclass{aastex} \usepackage{amsbsy} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{bm} \usepackage{mathrsfs} \usepackage{pifont} \usepackage{stmaryrd} \usepackage{textcomp} \usepackage{portland,xspace} \usepackage{amsmath,amsxtra} \usepackage[OT2,OT1]{fontenc} \newcommand\cyr{ \renewcommand\rmdefault{wncyr} \renewcommand\sfdefault{wncyss} \renewcommand\encodingdefault{OT2} \normalfont \selectfont} \DeclareTextFontCommand{\textcyr}{\cyr} \pagestyle{empty} \DeclareMathSizes{10}{9}{7}{6} \begin{document} \landscape $$91\pm 9$$ \end{document} MPa s m−2). High resistivity of primitive vessels could be attributed to their being shorter per diameter than eudicots and to high perforation plate resistivity ( \documentclass{aastex} \usepackage{amsbsy} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{bm} \usepackage{mathrsfs} \usepackage{pifont} \usepackage{stmaryrd} \usepackage{textcomp} \usepackage{portland,xspace} \usepackage{amsmath,amsxtra} \usepackage[OT2,OT1]{fontenc} \newcommand\cyr{ \renewcommand\rmdefault{wncyr} \renewcommand\sfdefault{wncyss} \renewcommand\encodingdefault{OT2} \normalfont \selectfont} \DeclareTextFontCommand{\textcyr}{\cyr} \pagestyle{empty} \DeclareMathSizes{10}{9}{7}{6} \begin{document} \landscape $$57\% \pm 15\% $$ \end{document} of total) in the species with scalariform plates. In support of the second hypothesis, primitive vessels had a cavitation pressure 1.4 MPa more vulnerable than angiosperm tracheids. This “vulnerability bottleneck” may have been even more extreme without a shift in vessels to less porous interconduit pit membranes. Vessel evolution was not driven by lower flow resistance, and it may have been limited to wet habitats by cavitation risk. A subtle, context‐dependent advantage to primitive vessels is consistent with the distribution of the vesselless condition in the angiosperm tree. The results imply that truly efficient and safe vessels evolved much later than vessels per se, perhaps in concordance with larger radiations among core angiosperms.