Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Xylem vessel length and distribution: does analysis method matter? A study using Acacia

Virginia G. Williamson A B D and John A. Milburn A C
+ Author Affiliations
- Author Affiliations

A Department of Botany, The University of New England, Armidale, NSW 2351, Australia.

B Present address: School of Ecosystem and Forest Sciences, The University of Melbourne, Richmond, Vic. 3121, Australia.

C Deceased.

D Corresponding author. Email: vgw@unimelb.edu.au

Australian Journal of Botany 65(3) 292-303 https://doi.org/10.1071/BT16220
Submitted: 9 November 2016  Accepted: 21 April 2017   Published: 6 June 2017

Abstract

Knowledge of xylem vessel length is important for several reasons, including the accurate calculation and comparison of hydraulic conductivity studies in excised stems. Vessel length data and distributions are also relevant in some anatomical, ecological, evolutionary, pathological and compatible hydraulic studies. However, determining vessel length is tedious, so is often either avoided or undertaken arbitrarily in hydraulic conductivity studies. We examined four injection media (paints and inks) under transmission electron microscopy to ascertain which was most suitable for determining vessel length. Hunt’s Speedball India ink, with evenly distributed, uniform spherical carbon particles of 33 nm, would avoid premature vessel blockage and, therefore, coupled with the fact that it is non-toxic, is the preferred medium to determine vessel length in Acacia amoena Wendl. terminal stems. The longest vessel was 10 cm, which accounted for 0.4% of vessels. Vessel length distributions were then determined and compared using the same dataset and four established methods. All four methods produced distributions which indicated that the most common vessel length class was short (0–2 cm), and no method was significantly different from the other; however, for ease of calculation, the Christman et al. (2009) method is recommended. Whether vessel length or distribution is necessary for hydraulic-conductivity studies will depend on whether or not merely indicative rates of flow are required, but to provide comparative information for global datasets, then they are needed.

Additional keywords: Hagen–Poiseuille, pit membranes, safety versus efficiency, transmission electron microscopy, xylem anatomy.


References

Aloni R (2015) Ecophysiological implications of vascular differentiation and plant evolution. Trees 29, 1–16.
Ecophysiological implications of vascular differentiation and plant evolution.Crossref | GoogleScholarGoogle Scholar |

Anderegg WRL, Klein T, Bartlett M, Sack L, Pellegrini AFA, Choat B, Jansen S (2016) Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe. Proceedings of the National Academy of Sciences of the United States of America 113, 5024–5029.
Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xmt1Shtbk%3D&md5=0da97103c920adadb742d48be1cc43eaCAS |

André J-P (2005) ‘Vascular organization of angiosperms. A new vision.’ (Science Publishers: Enfield, NH)

Arndt CH (1929) The movement of sap in Coffea arabica L. American Journal of Botany 16, 179–191.
The movement of sap in Coffea arabica L.Crossref | GoogleScholarGoogle Scholar |

Briggs GE (1967) ‘Movement of water in plants.’ (Blackwell Scientific Publications: Oxford, UK)

Brodersen CR, McElrone AJ, Choat B, Matthews MA, Shackel KA (2010) The dynamics of embolism repair in xylem: in vivo visualizations using high-resolution computed tomography. Plant Physiology 154, 1088–1095.
The dynamics of embolism repair in xylem: in vivo visualizations using high-resolution computed tomography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsV2nsbfL&md5=067f4238f4041f4fb5f793f6fdbef5ddCAS |

Brodersen CR, Lee EF, Choat B, Jansen S, Phillips RJ, Shackel KA, McElrone AJ, Matthews MA (2011) Automated analysis of three-dimensional xylem networks using high-resolution computed tomography. New Phytologist 191, 1168–1179.
Automated analysis of three-dimensional xylem networks using high-resolution computed tomography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Wmtr7I&md5=9160528aaf0cc0ace7e67651ade516aaCAS |

Cai J, Tyree MT (2014) Measuring vessel length in vascular plants: can we divine the truth? History, theory, methods, and contrasting models. Trees 28, 643–655.
Measuring vessel length in vascular plants: can we divine the truth? History, theory, methods, and contrasting models.Crossref | GoogleScholarGoogle Scholar |

Carlquist S (1985) Vasicentric tracheids as a drought survival mechanism in the woody flora of southern California and similar regions; review of vasicentric tracheids. Aliso 11, 30–68.

Carlquist S (2001) ‘Comparative wood anatomy: systematic, ecological, and evolutionary aspects of dicotyledon wood.’ (Springer-Verlag: Berlin)

Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE (2009) Towards a worldwide wood economics spectrum. Ecology Letters 12, 351–366.
Towards a worldwide wood economics spectrum.Crossref | GoogleScholarGoogle Scholar |

Choat B, Ball M, Luly J, Holtum J (2003) Pit membrane porosity and water stress-induced cavitation in four co-existing dry rainforest tree species. Plant Physiology 131, 41–48.
Pit membrane porosity and water stress-induced cavitation in four co-existing dry rainforest tree species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnvVGhsg%3D%3D&md5=5cb248bd8483c355979396dba17e958cCAS |

Choat B, Jansen S, Zwieniecki MA, Smets E, Holbrook NM (2004) Changes in pit membrane porosity due to deflection and stretching: the role of vestured pits. Journal of Experimental Botany 55, 1569–1575.
Changes in pit membrane porosity due to deflection and stretching: the role of vestured pits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlOqu7g%3D&md5=51dc6e633555b4022f59ae4020ced0c6CAS |

Choat B, Drayton WM, Brodersen C, Matthews MA, Shackel KA, Wada H, McElrone AJ (2010) Measurement of vulnerability to water stress-induced cavitation in grapevine: a comparison of four techniques applied to a long-vesseled species. Plant, Cell & Environment 33, 1502–1512.

Christman MA, Sperry JS, Adler FR (2009) Testing the ‘rare pit’ hypothesis for xylem cavitation resistance in three species of Acer. New Phytologist 182, 664–674.
Testing the ‘rare pit’ hypothesis for xylem cavitation resistance in three species of Acer.Crossref | GoogleScholarGoogle Scholar |

Cochard H, Delzon S, Badel E (2015) X-ray microtomography (micro-CT): a reference technology for high-resolution quantification of xylem embolism in trees. Plant, Cell & Environment 38, 201–206.
X-ray microtomography (micro-CT): a reference technology for high-resolution quantification of xylem embolism in trees.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cfjsFynug%3D%3D&md5=68bdabbd9a5c1d45e3169d58965bf83bCAS |

Cohen S, Bennink J, Tyree M (2003) Air method measurements of apple vessel length distributions with improved apparatus and theory. Journal of Experimental Botany 54, 1889–1897.
Air method measurements of apple vessel length distributions with improved apparatus and theory.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsl2ksbY%3D&md5=beb4bc1b3e5b4cb66f35c84a1f07f7d4CAS |

Crombie DS, Milburn JA, Hipkins MF (1985) Maximum sustainable xylem sap tensions in Rhododendron and other species. Planta 163, 27–33.
Maximum sustainable xylem sap tensions in Rhododendron and other species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2c7osVWitQ%3D%3D&md5=83cdc799d373bbe0cd55fcb2aac05210CAS |

Damunupola JW, Ratnayake K, Joyce DC, Irving DE (2011) Characterisation of xylem conduits and their possible role in limiting the vase life of cut Acacia holosericea (Mimosaceae) foliage stems. Functional Plant Biology 38, 614–623.
Characterisation of xylem conduits and their possible role in limiting the vase life of cut Acacia holosericea (Mimosaceae) foliage stems.Crossref | GoogleScholarGoogle Scholar |

Evert RF (2006) ‘Esau’s plant anatomy: meristems, cells, and tissues of the plant body: their structure, function, and development.’ (John Wiley & Sons: Hoboken, NJ)

Ewart AJ (1908) The ascent of water in trees. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 199, 341–392.
The ascent of water in trees.Crossref | GoogleScholarGoogle Scholar |

Ewers FW, Fisher JB (1989) Techniques for measuring vessel lengths and diameters in stems of woody plants. American Journal of Botany 76, 645–656.
Techniques for measuring vessel lengths and diameters in stems of woody plants.Crossref | GoogleScholarGoogle Scholar |

Greenidge KNH (1952) An approach to the study of vessel length in hardwood species. American Journal of Botany 39, 570–574.
An approach to the study of vessel length in hardwood species.Crossref | GoogleScholarGoogle Scholar |

Hacke UG, Sperry JS, Wheeler JK, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiology 26, 689–701.
Scaling of angiosperm xylem structure with safety and efficiency.Crossref | GoogleScholarGoogle Scholar |

Hacke UG, Sperry JS, Feild TS, Sano Y, Sikkema EH, Pitterman J (2007) Water transport in vesselless angiosperms: conducting efficiency and cavitation safety. International Journal of Plant Sciences 168, 1113–1126.
Water transport in vesselless angiosperms: conducting efficiency and cavitation safety.Crossref | GoogleScholarGoogle Scholar |

Handley WRC (1936) Some observations on the problem of vessel length determination in woody dicotyledons. New Phytologist 35, 456–471.
Some observations on the problem of vessel length determination in woody dicotyledons.Crossref | GoogleScholarGoogle Scholar |

Hargrave KR, Kolb KJ, Ewers FW, Davis SD (1994) Conduit diameter and drought-induced embolism in Salvia mellifera Greene (Labiatae). New Phytologist 126, 695–705.
Conduit diameter and drought-induced embolism in Salvia mellifera Greene (Labiatae).Crossref | GoogleScholarGoogle Scholar |

Hoffmann WA, Marchin RM, Abit P, Lau OL (2011) Hydraulic failure and tree dieback are associated with high wood density in a temperate forest under extreme drought. Global Change Biology 17, 2731–2742.
Hydraulic failure and tree dieback are associated with high wood density in a temperate forest under extreme drought.Crossref | GoogleScholarGoogle Scholar |

Hopkins DL (1989) Xylella fastidiosa: xylem-limited bacterial pathogen of plants. Annual Review of Phytopathology 27, 271–290.
Xylella fastidiosa: xylem-limited bacterial pathogen of plants.Crossref | GoogleScholarGoogle Scholar |

Jacobsen AL, Pratt RB, Tobin MF, Hacke UG, Ewers FW (2012) A global analysis of xylem vessel length in woody plants. American Journal of Botany 99, 1583–1591.
A global analysis of xylem vessel length in woody plants.Crossref | GoogleScholarGoogle Scholar |

Jansen S, Baas P, Gasson P, Smet E (2003) Vestured pits: do they promote safer water transport? International Journal of Plant Sciences 164, 405–413.
Vestured pits: do they promote safer water transport?Crossref | GoogleScholarGoogle Scholar |

Jansen S, Choat B, Pletsers A (2009) Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms. American Journal of Botany 96, 409–419.
Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms.Crossref | GoogleScholarGoogle Scholar |

Lens F, Sperry S, 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 Phytologist 190, 709–723.
Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer.Crossref | GoogleScholarGoogle Scholar |

Lens F, Tixier A, Cochard H, Sperry JS, Jansen S, Herbette S (2013) Embolism resistance as a key mechanism to understand adaptive plant strategies. Current Opinion in Plant Biology 16, 287–292.
Embolism resistance as a key mechanism to understand adaptive plant strategies.Crossref | GoogleScholarGoogle Scholar |

Middleton TM (1989) Modification of the latex paint infusion technique for the determination of vessel length in hardwoods. Wood Science and Technology 23, 299–302.
Modification of the latex paint infusion technique for the determination of vessel length in hardwoods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXjvVersw%3D%3D&md5=e211b1933aeaf8cf22dbbb585aac643eCAS |

Middleton TM, Butterfield BG (1990) Vessel length distribution in the stems of three New Zealand species of Nothofagus. Wood Science and Technology 24, 17–22.
Vessel length distribution in the stems of three New Zealand species of Nothofagus.Crossref | GoogleScholarGoogle Scholar |

Milburn JA (1979) ‘Water flow in plants.’ (Longman Group: London)

Milburn JA, Covey-Crump PAK (1971) A simple method for the determination of conduit length and distribution in stems. New Phytologist 70, 427–434.
A simple method for the determination of conduit length and distribution in stems.Crossref | GoogleScholarGoogle Scholar |

Milburn JA, McLaughlin ME (1974) Studies of cavitation in isolated vascular bundles and whole leaves of Plantago major L. New Phytologist 73, 861–871.
Studies of cavitation in isolated vascular bundles and whole leaves of Plantago major L.Crossref | GoogleScholarGoogle Scholar |

Petit G, Anfodillo T (2011) 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). Oecologia 165, 271–274.
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).Crossref | GoogleScholarGoogle Scholar |

Poot P, Veneklaas EJ (2013) Species distribution and crown decline are associated with contrasting water relations in four common sympatric eucalypt species in southwestern Australia. Plant and Soil 364, 409–423.
Species distribution and crown decline are associated with contrasting water relations in four common sympatric eucalypt species in southwestern Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXit1Gksb8%3D&md5=c21a9e89cc3c8b6860916cdd88025634CAS |

Ranasinghe MS, Milburn JA (1995) Xylem conduction and cavitation in Hevea brasiliensis. Journal of Experimental Botany 46, 1693–1700.
Xylem conduction and cavitation in Hevea brasiliensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpvV2lt7g%3D&md5=b04a3ad641dee60ab1d4bcc839978b64CAS |

Rappel L (1985) The factors leading to senescence in cut flowers of Acacia. BSc(Hons) Thesis, University of New England, Armidale, NSW, Australia.

Ritman K (1988) Plant water relations: investigations into acoustic emission and transmission. PhD Thesis, University of New England, Armidale, NSW, Australia.

Ritman KT, Milburn JA (1988) Acoustic emissions from plants: ultrasonic and audible compared. Journal of Experimental Botany 39, 1237–1248.
Acoustic emissions from plants: ultrasonic and audible compared.Crossref | GoogleScholarGoogle Scholar |

Rohde E, Vogt C, Heineman WR (1998) The analysis of fountain pen inks by capillary electrophoresis with ultraviolet/visible absorbance and laser-induced fluorescence detection. Electrophoresis 19, 31–41.
The analysis of fountain pen inks by capillary electrophoresis with ultraviolet/visible absorbance and laser-induced fluorescence detection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhsVOlsr0%3D&md5=458f05766e1e40be7cc455166c69ab73CAS |

Scholz A, Klepsch M, Karimi Z, Jansen S (2013) How to quantify conduits in wood? Frontiers in Plant Science 4, 1–11.
How to quantify conduits in wood?Crossref | GoogleScholarGoogle Scholar |

Skene DS, Balodis V (1968) A study of vessel length in Eucalyptus obliqua L’Herit. Journal of Experimental Botany 19, 825–830.
A study of vessel length in Eucalyptus obliqua L’Herit.Crossref | GoogleScholarGoogle Scholar |

Sperry JS (n.d.) ‘Sperry lab methods and computer programs.’ (Department of Biology, University of Utah) Available at http://biologylabs.utah.edu/sperry/methods.html [Accessed 7 October 2016]

Sperry JS, Tyree MT (1988) Mechanism of water stress-induced xylem embolism. Plant Physiology 88, 581–587.
Mechanism of water stress-induced xylem embolism.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhvVGjtQ%3D%3D&md5=11b307e2e11a6c004e0c403f842b5777CAS |

Sperry JS, Hacke UG, Wheeler JK (2005) Comparative analysis of end wall resistivity in xylem conduits. Plant, Cell & Environment 28, 456–465.
Comparative analysis of end wall resistivity in xylem conduits.Crossref | GoogleScholarGoogle Scholar |

Sperry JS, Hacke UG, Pittermann J (2006) Size and function in conifer tracheids and angiosperm vessels. American Journal of Botany 93, 1490–1500.
Size and function in conifer tracheids and angiosperm vessels.Crossref | GoogleScholarGoogle Scholar |

Sperry JS, Hacke UG, Feild TS, Sano Y, Sikkema EH (2007) Hydraulic consequences of vessel evolution in angiosperms. International Journal of Plant Sciences 168, 1127–1139.
Hydraulic consequences of vessel evolution in angiosperms.Crossref | GoogleScholarGoogle Scholar |

Strasburger E (1924) ‘Handbook of practical botany.’ (George Allen & Unwin: London)

Swartz HM, Liu KJ, Goda F, Walczak T (1994) India ink: a potential clinically applicable EPR oximetry probe. Magnetic Resonance in Medicine 31, 229–232.
India ink: a potential clinically applicable EPR oximetry probe.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c7otVOmtA%3D%3D&md5=e5f795a1ab9477e10046e227bf7fbd40CAS |

Torres-Ruiz JM, Jansen S, Choat B, McElrone AJ, Cochard H, Brodribb TJ, Badel E, Burlett R, Bouche PS, Brodersen CR, Li S, Morris H, Delzon S (2015) Direct X-ray microtomography observation confirms the induction of embolism upon xylem cutting under tension. Plant Physiology 167, 40–43.
Direct X-ray microtomography observation confirms the induction of embolism upon xylem cutting under tension.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkt1Wmtbs%3D&md5=b1a42dc3e4a438eabb7089eb2958b414CAS |

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, 103–110.
Diminished vessel diameter as a possible factor in the decline of European ash (Fraxinus excelsior L.).Crossref | GoogleScholarGoogle Scholar |

Tyree MT (1993) Theory of vessel length determination: the problem of nonrandom vessel ends. Canadian Journal of Botany 71, 297–302.
Theory of vessel length determination: the problem of nonrandom vessel ends.Crossref | GoogleScholarGoogle Scholar |

Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Plant Molecular Biology 40, 19–36.
Vulnerability of xylem to cavitation and embolism.Crossref | GoogleScholarGoogle Scholar |

Tyree MT, MacGregor ME, Petrov A, Upenieks MI (1978) A comparison of systematic errors between the Richards and Hammel methods of measuring tissue-water relations parameters. Canadian Journal of Botany 56, 2153–2161.
A comparison of systematic errors between the Richards and Hammel methods of measuring tissue-water relations parameters.Crossref | GoogleScholarGoogle Scholar |

Tyree MT, Cochard H, Cruiziat P (2003) The water-filled versus air-filled status of vessels cut open in air: the ‘Scholander assumption’ revisited. Plant, Cell & Environment 26, 613–621.
The water-filled versus air-filled status of vessels cut open in air: the ‘Scholander assumption’ revisited.Crossref | GoogleScholarGoogle Scholar |

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 & Environment 28, 800–812.
Inter-vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade-off in xylem transport.Crossref | GoogleScholarGoogle Scholar |

Wheeler JK, Huggett BA, Tofte AN, Rockwell FE, Holbrook NM (2013) Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism. Plant, Cell & Environment 36, 1938–1949.

Williamson VG (1996) Physiological and microbiological processes of cut flower senescence in two Australian native genera, Acacia and Boronia. PhD Thesis, University of New England, Armidale, NSW, Australia.

Williamson VG, Milburn JA (1995) Cavitation events in cut stems kept in water: implications for cut flower senescence. Scientia Horticulturae 64, 219–232.
Cavitation events in cut stems kept in water: implications for cut flower senescence.Crossref | GoogleScholarGoogle Scholar |

Zimmermann MH (1978) Hydraulic architecture of some diffuse-porous trees. Canadian Journal of Botany 56, 2286–2295.
Hydraulic architecture of some diffuse-porous trees.Crossref | GoogleScholarGoogle Scholar |

Zimmermann MH (1983) ‘Xylem structure and the ascent of sap.’ (Springer-Verlag: Berlin)

Zimmermann MH, Jeje AA (1981) Vessel length distribution in stems of some American woody plants. Canadian Journal of Botany 59, 1882–1892.
Vessel length distribution in stems of some American woody plants.Crossref | GoogleScholarGoogle Scholar |

Zimmermann MH, Milburn JA (1982) Transport and storage of water. In ‘Physiological plant ecology. Vol. II’. (Eds OL Lange, PS Nobel, CB Osmond, H Ziegler) pp. 135–151. (Springer-Verlag: Berlin)

Zimmermann MH, Potter D (1982) Vessel length distribution in branches, stem and roots of Acer rubrum L. IAWA Bulletin 3, 103–109.

Zimmermann MH, Tomlinson PB (1968) Vascular construction and development in the aerial stem of Prionium (Juncaceae). American Journal of Botany 55, 1100–1109.
Vascular construction and development in the aerial stem of Prionium (Juncaceae).Crossref | GoogleScholarGoogle Scholar |

Zweypfenning RCVJ (1978) A hypothesis on the function of vestured pits. IAWA Bulletin 1, 13–15.