A comparison of xylem vessel metrics between tropical and temperate Rhododendron species across elevation ranges
Tatpong Tulyananda A and Erik T. Nilsen A BA Department of Biological Sciences, Virginia Tech, Blacksburg, VA 24061, USA.
B Corresponding author. Email: enilsen@vt.edu
Australian Journal of Botany 65(4) 389-399 https://doi.org/10.1071/BT16261
Submitted: 29 December 2016 Accepted: 5 June 2017 Published: 20 July 2017
Abstract
Research on tree vascular traits has demonstrated an important trade-off between safety and efficiency of wood, such that tropical trees have more efficient xylem than temperate trees. However, this trade-off is equivocal for plants with non-tree architecture. So as to test the trade-off between safety and efficiency in evergreen shrubs, xylem traits of temperate and tropical Rhododendrons were compared. Rhododendron diversified from the temperate zone of Asia into the Malesian tropical zone, which makes this monophyletic group an excellent subject for testing the trade-off in vessel structure in evergreen shrubs. We hypothesised that twig wood of temperate Rhododendron species would have safe twig xylem, whereas that of tropical Rhododendron species would be more efficient. In the present study, safety refers to protection against freeze–thaw-induced embolism. Twig wood anatomy of accessions representing 60 species of Rhododendron was assayed. Most vessel traits of temperate species were significantly safer than those of tropical species, supporting the trade-off in this group. Some safety metrics of the twig xylem increased with an increase in native-range elevation. The adaptive changes in twig wood metrics were small, which means that stomatal conductance is constrained by limited hydraulic conductance in both temperate and tropical species of Rhododendron. This constraint has significant implications to the ecology of Rhododendron.
Additional keywords: kurtosis, safety-efficiency trade-off, skewness, theoretical water transport, tropical diversification, vessel diameter.
References
Anderegg WR, Klein L, Bartlett TM, 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 |
Argent G (2015) ‘Rhododendrons of subgenus Vireya.’ (Royal Horticultural Society Publications: London)
Brantley S, Ford CR, Vose JM (2013) Future species composition will affect forest water use after loss of eastern hemlock from southern Appalachian forests. Ecological Applications 23, 777–790.
| Future species composition will affect forest water use after loss of eastern hemlock from southern Appalachian forests.Crossref | GoogleScholarGoogle Scholar |
Brodribb T (2009) Xylem hydraulic physiology: the functional backbone of terrestrial plant productivity. Plant Science 177, 245–251.
| Xylem hydraulic physiology: the functional backbone of terrestrial plant productivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpt1Kgsro%3D&md5=f5527b0b837f509056379015afaaba26CAS |
Brown GK, Craven LA, Udovicic F, Ladiges PY (2006) Phylogeny of Rhododendron section Vireya (Ericaceae) based on two non-coding regions of cpDNA. Plant Systematics and Evolution 257, 57–93.
| Phylogeny of Rhododendron section Vireya (Ericaceae) based on two non-coding regions of cpDNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVajsbY%3D&md5=70477ee52ddde387e1659fe6c372dd26CAS |
Castro-Díez P, Puyravaud JP, Cornelissen JHC, Villar-Salvador P (1998) Stem anatomy and relative growth rate in seedlings of a wide range of woody plant species and types. Oecologia 116, 57–66.
| Stem anatomy and relative growth rate in seedlings of a wide range of woody plant species and types.Crossref | GoogleScholarGoogle Scholar |
Charrier G, Charra-Vaskou K, Kasuga J, Cochard H, Mayr S, Ameglio T (2014) Freeze–thaw stress: effects of temperature on hydraulic conductivity and ultrasonic activity in ten woody angiosperms. Plant Physiology 164, 992–998.
| Freeze–thaw stress: effects of temperature on hydraulic conductivity and ultrasonic activity in ten woody angiosperms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXks1Smu7k%3D&md5=6dce86db3a14184f362ae0a9698d6295CAS |
Chenlemuge T, Schuldt B, Dulamsuren C, Hertel D, Leuschner C, Hauck M (2015) Stem increment and hydraulic architecture of a boreal conifer (Larix sibirica) under contrasting macroclimates. Trees-Structure and Function 29, 623–636.
| Stem increment and hydraulic architecture of a boreal conifer (Larix sibirica) under contrasting macroclimates.Crossref | GoogleScholarGoogle Scholar |
Choat B, Medek DE, Stuart SA, Pasquet-Kok J, Egerton JJG, Salari H, Sack L, Ball MC (2011) Xylem traits mediate a trade-off between resistance to freeze-thaw-induced embolism and photosynthetic capacity in overwintering evergreens. New Phytologist 191, 996–1005.
| Xylem traits mediate a trade-off between resistance to freeze-thaw-induced embolism and photosynthetic capacity in overwintering evergreens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1WmsbbM&md5=8283f4cf3e7f97344382d35ad946b842CAS |
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 |
Cordero RA, Nilsen ET (2002) Effects of summer drought and winter freezing on stem hydraulic conductivity of Rhododendron species from contrasting climates. Tree Physiology 22, 919–928.
| Effects of summer drought and winter freezing on stem hydraulic conductivity of Rhododendron species from contrasting climates.Crossref | GoogleScholarGoogle Scholar |
Davis SD, Sperry JS, Hacke UG (1999) The relationship between xylem conduit diameter and cavitation caused by freezing. American Journal of Botany 86, 1367–1372.
| The relationship between xylem conduit diameter and cavitation caused by freezing.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3Mngs1Gnug%3D%3D&md5=d185923497c2b4e3628c92f8cc942126CAS |
Feild TS, Brodribb T (2001) Stem water transport and freeze–thaw xylem embolism in conifers and angiosperms in a Tasmanian treeline heath. Oecologia 127, 314–320.
| Stem water transport and freeze–thaw xylem embolism in conifers and angiosperms in a Tasmanian treeline heath.Crossref | GoogleScholarGoogle Scholar |
Gärtner H, Lucchinetti S, Schweingruber FH (2014) New perspectives for wood anatomical analysis in dendrosciences: the GSL1-microtome. Dendrochronologia 32, 47–51.
| New perspectives for wood anatomical analysis in dendrosciences: the GSL1-microtome.Crossref | GoogleScholarGoogle Scholar |
Gleason SM, Westoby M, Jansen S, Choat B, Hacke UG, Pratt RB, Bhaskar R, Brodribb TJ, Bucci SJ, Cao KF, Cochard H, Delzon S, Domec JC, Fan Z, Field ZX, Jacobsen TS, Johnson AL, Lens DM, Maherali F, Martinez-Vilalta H, Mayr J, Mc S, Culloh KA, Mencuccini M, Mitchell PJ, Morris H, Nardini A, Pittermann AJ, Plavcova L, Schreiber SG, Sperry JS, Wright IJ, Zanne AE (2016) Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world’s woody plant species. New Phytologist 209, 123–136.
| Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world’s woody plant species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvFKhsLjE&md5=25e1e99cc892f41dcf9b1990be2d7125CAS |
Goetsch LA, Eckert AJ, Hall BD, Hoot SB (2005) The molecular systematics of Rhododendron (Ericaceae): a phylogeny based upon RPB2 gene sequences. Systematic Botany 30, 616–626.
| The molecular systematics of Rhododendron (Ericaceae): a phylogeny based upon RPB2 gene sequences.Crossref | GoogleScholarGoogle Scholar |
Goetsch LA, Craven LA, Hall BD (2011) Major speciation accompanied the dispersal of Vireya rhododendrons (Ericaceae, Rhododendron sect. Schistanthe) through the Malayan archipelago: evidence from nuclear gene sequences. Taxon 60, 1015–1028.
Hacke U, Sperry JS (2001) Functional and ecological xylem anatomy. Perspectives in Plant Ecology, Evolution and Systematics 4, 97–115.
| Functional and ecological xylem anatomy.Crossref | GoogleScholarGoogle Scholar |
Hacke U, 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, Jacobsen AL, Pratt RB (2009) Xylem function of arid-land shrubs from California, USA: an ecological and evolutionary analysis. Plant, Cell & Environment 32, 1324–1333.
| Xylem function of arid-land shrubs from California, USA: an ecological and evolutionary analysis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MnitVKksQ%3D%3D&md5=6f134199ba4e62739328ab1defaf9a0aCAS |
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 |
Körner C (2007) The use of ‘altitude’ in ecological research. Trends in Ecology & Evolution 22, 569–574.
| The use of ‘altitude’ in ecological research.Crossref | GoogleScholarGoogle Scholar |
Kurashige Y, Etoh J-I, Handa T, Takayangi K, Yukawa T (2001) Sectional relationships in the genus Rhododendron (Ericaceae): evidence from matK and trnK intron sequences. Plant Systematics and Evolution 228, 1–14.
| Sectional relationships in the genus Rhododendron (Ericaceae): evidence from matK and trnK intron sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslSksLw%3D&md5=769a9f1f1443de90cc8ff09bd7814783CAS |
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 |
Lipp CC, Nilsen ET (1997) The impact of subcanopy light environment on the hydraulic vulnerability of Rhododendron maximum to freeze–thaw cycles and drought. Plant, Cell & Environment 20, 1264–1272.
| The impact of subcanopy light environment on the hydraulic vulnerability of Rhododendron maximum to freeze–thaw cycles and drought.Crossref | GoogleScholarGoogle Scholar |
McCulloh KA, 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. New Phytologist 186, 439–450.
| Moving water well: comparing hydraulic efficiency in twigs and trunks of coniferous, ring-porous and diffuse-porous saplings.Crossref | GoogleScholarGoogle Scholar |
Medeiros JS, Pockman WT (2014) Freezing regime and trade-offs with water transport efficiency generate variation in xylem structure across diploid populations of Larrea sp. (Zygophyllaceae). American Journal of Botany 101, 598–607.
| Freezing regime and trade-offs with water transport efficiency generate variation in xylem structure across diploid populations of Larrea sp. (Zygophyllaceae).Crossref | GoogleScholarGoogle Scholar |
Meinzer FC, McCulloh KA, Lachenbruch B, Woodruff DR, Johnson DM (2010) The blind men and the elephant: the impact of context and scale in evaluating conflicts between plant hydraulic safety and efficiency. Oecologia 164, 287–296.
| The blind men and the elephant: the impact of context and scale in evaluating conflicts between plant hydraulic safety and efficiency.Crossref | GoogleScholarGoogle Scholar |
Minder JR, Mote PW, Lundquist JD (2010) Surface temperature lapse rates over complex terrain: lessons from the Cascade Mountains. Journal of Geophysical Research 115, D14122
| Surface temperature lapse rates over complex terrain: lessons from the Cascade Mountains.Crossref | GoogleScholarGoogle Scholar |
Nabeshima E, Kubo T, Yasue K, Hiura T, Funada R (2015) Changes in radial growth of earlywood in Quercus crispula between 1970 and 2004 reflect climate change. Trees-Structure and Function 29, 1273–1281.
| Changes in radial growth of earlywood in Quercus crispula between 1970 and 2004 reflect climate change.Crossref | GoogleScholarGoogle Scholar |
Nilsen ET (1986) Quantitative phenology and leaf survivorship of Rhododendron maximum L. in contrasting irradiance environments of the Appalachian mountains. American Journal of Botany 73, 822–831.
| Quantitative phenology and leaf survivorship of Rhododendron maximum L. in contrasting irradiance environments of the Appalachian mountains.Crossref | GoogleScholarGoogle Scholar |
Nilsen ET (1992) Thermonastic leaf movements: a synthesis of research with Rhododendron. Botanical Journal of the Linnean Society 110, 205–233.
| Thermonastic leaf movements: a synthesis of research with Rhododendron.Crossref | GoogleScholarGoogle Scholar |
Nilsen ET, Stetler DA, Gassman CA (1988) The influence of age and microclimate on the photochemistry of Rhododendron maximum leaves II. Chloroplast structure and photosynthetic light response. American Journal of Botany 75, 1526–1534.
| The influence of age and microclimate on the photochemistry of Rhododendron maximum leaves II. Chloroplast structure and photosynthetic light response.Crossref | GoogleScholarGoogle Scholar |
Noshiro S, Suzuki M (1995) Ecological wood anatomy of Nepalese Rhododendron (Ericaceae). 2. Intraspecific variation. Journal of Plant Research 108, 217–233.
| Ecological wood anatomy of Nepalese Rhododendron (Ericaceae). 2. Intraspecific variation.Crossref | GoogleScholarGoogle Scholar |
Noshiro S, Suzuki M, Ohba H (1995) Ecological wood anatomy of Nepalese Rhododendron (Ericaceae). 1. Interspecific variation. Journal of Plant Research 108, 1–9.
| Ecological wood anatomy of Nepalese Rhododendron (Ericaceae). 1. Interspecific variation.Crossref | GoogleScholarGoogle Scholar |
Olson ME, Rosell JA, Leon C, Zamora S, Weeks A, Alvarado-Cardenas LO, Cacho NI, Grant J (2013) Convergent vessel diameter-stem diameter scaling across five clades of new and old world eudicots from desert to rain forest. International Journal of Plant Sciences 174, 1062–1078.
| Convergent vessel diameter-stem diameter scaling across five clades of new and old world eudicots from desert to rain forest.Crossref | GoogleScholarGoogle Scholar |
Pittermann J, Sperry JS (2003) Tracheid diameter is the key trait determining the extent of freezing-induced embolism in conifers. Tree Physiology 23, 907–914.
| Tracheid diameter is the key trait determining the extent of freezing-induced embolism in conifers.Crossref | GoogleScholarGoogle Scholar |
Reinhardt K, Smith WK (2016) Chlorophyll fluorescence and photosynthetic gas exchange under direct versus diffuse light in evergreen conifer (Picea pungens) shoots and broadleaf shrub (Rhododendron ponticum) leaves. Plant Ecology 217, 443–450.
| Chlorophyll fluorescence and photosynthetic gas exchange under direct versus diffuse light in evergreen conifer (Picea pungens) shoots and broadleaf shrub (Rhododendron ponticum) leaves.Crossref | GoogleScholarGoogle Scholar |
Sperry JS, Saliendra NZ (1994) Intra- and inter-plant variation in xylem cavitation in Betula occidentalis. Plant, Cell & Environment 17, 1233–1241.
| Intra- and inter-plant variation in xylem cavitation in Betula occidentalis.Crossref | GoogleScholarGoogle Scholar |
Sperry JS, Sullivan JEM (1992) Xylem embolism in response to freeze thaw cycles and water stress in ring-porous, diffuse-porous, and conifer species. Plant Physiology 100, 605–613.
| Xylem embolism in response to freeze thaw cycles and water stress in ring-porous, diffuse-porous, and conifer species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cngvVWrsA%3D%3D&md5=ea40780ad6f1f07a755d47a766fc9c2eCAS |
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 |
Umebayashi T, Utsumi Y, Koga S, Murata I, Fukuda K (2016) Differences in drought- and freeze-induced embolisms in deciduous ring-porous plant species in Japan. Planta 244, 753–760.
| Differences in drought- and freeze-induced embolisms in deciduous ring-porous plant species in Japan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtFSgu7fJ&md5=296d73c5d5833cad0cb9d9e88911ad59CAS |
Wang J, Ives NE, Lechowicz MJ (1992) The relation of foliar phenology to xylem embolism in trees. Functional Ecology 6, 469–475.
| The relation of foliar phenology to xylem embolism in trees.Crossref | GoogleScholarGoogle Scholar |
Zanne AE, Tank DC, Cornwell WK, Eastman JM, Smith SA, FitzJohn RG, McGlinn DJ, O’Meara BC, Moles AT, Reich PB, Royer DL, Soltis DE, Stevens PF, Westoby M, Wright IJ, Aarssen L, Bertin RI, Calaminus A, Govaerts R, Hemmings F, Leishman MR, Oleksyn J, Soltis PS, Swenson NG, Warman L, Beaulieu JM (2014) Three keys to the radiation of angiosperms into freezing environments. Nature 506, 89–92.
| Three keys to the radiation of angiosperms into freezing environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsl2msb8%3D&md5=4280998ee1bd7565a4f92db5299af75aCAS |