The function of foliar scales in water conservation: an evaluation using tropical-mountain, evergreen shrubs of the species Rhododendron in section Schistanthe (Ericaceae)
Erik T. Nilsen A C , David W. Webb B and Zhe Bao A
+ Author Affiliations
- Author Affiliations
A Virginia Tech., Department of Biological Sciences, 2119 Derring Hall, Blacksburg, VA 24061, USA.
B University of Hawai’i, Botany Department, 3190 Maile Way, Honolulu, HI 96822, USA.
C Corresponding author. Email: enilsen@vt.edu
Australian Journal of Botany 62(5) 403-416 https://doi.org/10.1071/BT14072
Submitted: 17 April 2014 Accepted: 29 August 2014 Published: 8 October 2014
Abstract
Leaf scales (scarious trichomes) have putative significance to leaf water relations, energy balance, and gas exchange. A survey of leaf scales, stomata, and leaf morphology across 83 species of Rhododendron section Schistanthe in a common garden, at 1207-m elevation on Moana Loa, Hawai’i, was used to probe three possible functional models for scales on abaxial leaf surfaces. Scale density was commonly 10 mm–2, but densities up to 50 mm–2 occurred. The median stomatal density was 200 mm–2, but ranged up to 500 mm–2. Stomatal dispersion was grouped into four classes based on the proportion of stomata located under scales. Stomatal pore index decreased as scale density and scale importance factor increased. Thus, maximum stomatal conductance as represented by stomatal pore index decreased as the effect of scales on the leaf surface increased. Stomatal pore index increased as the elevation of the native range increased. However, the relative effects of scales on stomata peaked at mid-elevation. Principal components analysis indicated that the most important habitat factors determining both scale importance factor and stomatal pore index were elevation and growth form (epiphyte or terrestrial). Therefore, this survey indicated that scales serve a water conservation function, which is most effective at mid-elevation of the native range.
Additional keywords: leaf surface morphology, maximum stomatal conductance, scarious trichomes, stomatal density, stomatal dispersion, stomatal pore index.
References
Argent G (2006) ‘Rhododendrons of subgenus Vireya.’ (Royal Horticultural Society Publications: London)Aryal B, Neuner G (2012) Leaf wettability in Bilberry Vaccinium myrtillus L. as affected by altitude and openness of the growing site. Phyton – Annales Rei Botanicae 52, 245–262.
Beaulieu JM, Leitch IJ, Patel S, Pendharkar A, Knight CA (2008) Genome size is a strong predictor of cell size and stomatal density in angiosperms. New Phytologist 179, 975–986.
| Genome size is a strong predictor of cell size and stomatal density in angiosperms.Crossref | GoogleScholarGoogle Scholar | 18564303PubMed |
Behnke HD (1984) Plant trichomes – structure and ultrastructure: general terminology, taxonomic applications, and aspects of trichome-bacterial interactions in leaf tips of Discorea. In ‘Biology and chemistry of plant trichomes’. (Eds E Rodrigues, PL Healey, I Mehta) pp. 1–21. (Plenum Press: New York)
Benz BW, Martin CE (2006) Foliar trichomes, boundary layers, and gas exchange in 12 species of epiphytic Tillandsia (Bromeliaceae). Journal of Plant Physiology 163, 648–656.
| Foliar trichomes, boundary layers, and gas exchange in 12 species of epiphytic Tillandsia (Bromeliaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xkslalsrs%3D&md5=4aec2e2fd7266fa44140804327d80033CAS | 16545998PubMed |
Benzing DH (1976) Bromelian trichomes: structure, function, and ecological significance. Selbyana 1, 330–348.
Benzing DH, Henderson K, Kessel B, Sulak J (1976) The absorptive capacities of bromeliad trichomes. American Journal of Botany 63, 1009–1014.
| The absorptive capacities of bromeliad trichomes.Crossref | GoogleScholarGoogle Scholar |
Brewer CA, Smith WK (1997) Patterns of leaf surface wetness for mountain and subalpine plants. Plant, Cell & Environment 20, 1–11.
| Patterns of leaf surface wetness for mountain and subalpine plants.Crossref | GoogleScholarGoogle Scholar |
Brodribb TJ, Hill RS (1997) Imbricacy and stomatal wax plugs reduce maximum leaf conductance in southern hemisphere conifers. Australian Journal of Botany 45, 657–668.
| Imbricacy and stomatal wax plugs reduce maximum leaf conductance in southern hemisphere conifers.Crossref | GoogleScholarGoogle Scholar |
Brodribb TJ, Jordan GJ (2011) Water supply and demand remain balanced during leaf acclimation of Nothofagus cunninghamii trees. New Phytologist 192, 437–448.
| Water supply and demand remain balanced during leaf acclimation of Nothofagus cunninghamii trees.Crossref | GoogleScholarGoogle Scholar | 21679190PubMed |
Cai ZQ, Rijkers T, Bongers F (2005) Photosynthetic acclimation to light changes in tropical monsoon forest woody species differing in adult stature. Tree Physiology 25, 1023–1031.
| Photosynthetic acclimation to light changes in tropical monsoon forest woody species differing in adult stature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpt1elsLg%3D&md5=8b97b188d5d231a7ff5cba2346803990CAS | 15929933PubMed |
Carins Murphy MR, Jordan GJ, Brodribb TJ (2012) Differential leaf expansion can enable hydraulic acclimation to sun and shade. Plant, Cell & Environment 35, 1407–1418.
| Differential leaf expansion can enable hydraulic acclimation to sun and shade.Crossref | GoogleScholarGoogle Scholar |
Chamberlain D, Hyam R, Argent G, Fairweather G, Walter KS (1996) ‘The genus Rhododendron. Its classification and synonomy.’ (The Royal Botanical Garden: Edinburgh, UK)
Cordell S, Goldstein G, Mueller-Dombois D, Webb D, Vitousek PM (1998) Physiological and morphological variation in Metrosideros polymorpha, a dominant Hawaiian tree species, along an altitudinal gradient: the role of phenotypic plasticity. Oecologia 113, 188–196.
| Physiological and morphological variation in Metrosideros polymorpha, a dominant Hawaiian tree species, along an altitudinal gradient: the role of phenotypic plasticity.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 | 12204848PubMed |
Craven LA, Danet F, Veldkamp J, Goetsch LA, Hall BD (2010) Rhododendron section Shistanthe, the scientific name for Vireya rhododendrons (Ericaceae). Journal American Rhododendron Society 64, 190–192.
Ehleringer J (1984) Ecology and ecophysiology of leaf pubescence in North American desert plants. In ‘Biology and chemistry of plant trichomes’. (Eds E Rodriguez, PL Healey, I Mehta) pp. 113–132. (Plenum Press: New York)
Esau K (1960) ‘Anatomy of seed plants.’ (John Wiley & Sons Inc.: New York)
Feild TS, Zwieniecki MA, Donoghue MJ, Holbrook NM (1998) Stomatal plugs of Drimys winteri (Winteraceae) protect leaves from mist but not drought. Proceedings of the National Academy of Sciences,USA 95, 14 256–14 259.
| Stomatal plugs of Drimys winteri (Winteraceae) protect leaves from mist but not drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXns1Gmu7k%3D&md5=164dc543347478c50827fda183d922a5CAS |
Franks PJ, Drake PL, Beerling DJ (2009) Plasticity in maximum stomatal conductance constrained by negative correlation between stomatal size and density: an analysis using Eucalyptus globulus. Plant, Cell & Environment 32, 1737–1748.
| Plasticity in maximum stomatal conductance constrained by negative correlation between stomatal size and density: an analysis using Eucalyptus globulus.Crossref | GoogleScholarGoogle Scholar |
Glover BJ, Perez-Rodriguez M, Martin C (1998) Development of several epidermal cell types can be specified by the same MYB-related plant transcription factor. Development 125, 3497–3508.
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.
Hassiotou F, Evans JR, Ludwig M, Veneklaas EJ (2009) Stomatal crypts may facilitate diffusion of CO2 to adaxial mesophyll cells in thick sclerophylls. Plant, Cell & Environment 32, 1596–1611.
| Stomatal crypts may facilitate diffusion of CO2 to adaxial mesophyll cells in thick sclerophylls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVKhtbbK&md5=ed809893374fe0fce829fd8a5f27fdbcCAS |
Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424, 901–908.
| The role of stomata in sensing and driving environmental change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmsV2isLw%3D&md5=457ab6053a59f7b3b6221ca4432cb1bbCAS | 12931178PubMed |
Hogan KP, Smith AP, Araus JL, Saavedra A (1994) Ecotypic differentiation of gas-exchange responses and leaf anatomy in a tropical forest understory shrub from areas of contrasting rainfall regime. Tree Physiology 14, 819–831.
| Ecotypic differentiation of gas-exchange responses and leaf anatomy in a tropical forest understory shrub from areas of contrasting rainfall regime.Crossref | GoogleScholarGoogle Scholar | 14967651PubMed |
Jordan GJ, Weston PH, Carpenter RJ, Dillon RA, Brodribb TJ (2008) The evolutionary relations of sunken covered, and encrypted stomata to dry habitats in proteaceae. American Journal of Botany 95, 521–530.
| The evolutionary relations of sunken covered, and encrypted stomata to dry habitats in proteaceae.Crossref | GoogleScholarGoogle Scholar | 21632378PubMed |
Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecology Letters 7, 1225–1241.
| Conceptual issues in local adaptation.Crossref | GoogleScholarGoogle Scholar |
Kelly CC, Beerling DJ (1995) Plant life form, stomatal density and taxanomic relatedness: a reanalysis of Salisbury (1927). Functional Ecology 9, 422–431.
| Plant life form, stomatal density and taxanomic relatedness: a reanalysis of Salisbury (1927).Crossref | GoogleScholarGoogle Scholar |
Kenyon J, Walker J (1997) ‘Vireyas. A practical gardening guide.’ (Timber Press: Portland, OR)
Kofidis G, Bosabalidis AM (2008) Effects of altitude and season on glandular hairs and leaf structural traits of Nepeta nuda L. Botanical Studies (Taipei, Taiwan) 49, 363–372.
Kong GQ, Luo TX, Liu XS, Zhang L, Liang EY (2012) Annual ring widths are good predictors of changes in net primary productivity of alpine Rhododendron shrubs in the Sergyemla Mountains, southeast Tibet. Plant Ecology 213, 1843–1855.
| Annual ring widths are good predictors of changes in net primary productivity of alpine Rhododendron shrubs in the Sergyemla Mountains, southeast Tibet.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 |
Körner C, Allison A, Hilscher H (1983) Altitudinal variation in leaf diffusive conductance and leaf anatomy in heliophytes of montane New Guinea and their interaction with microclimate. Flora 174, 91–135.
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 |
Martin C, Glover BJ (2007) Functional aspects of cell patterning in aerial epidermis. Current Opinion in Plant Biology 10, 70–82.
| Functional aspects of cell patterning in aerial epidermis.Crossref | GoogleScholarGoogle Scholar | 17140837PubMed |
Mohammadian MA, Hill RS, Watling JR (2009) Stomatal plugs and their impact on fungal invasion in Agathis robusta. Australian Journal of Botany 57, 389–395.
| Stomatal plugs and their impact on fungal invasion in Agathis robusta.Crossref | GoogleScholarGoogle Scholar |
Moreno L, Bertiller MB, Carrera AL (2010) Changes in traits of shrub canopies across an aridity gradient in northern Patagonia, Argentina. Basic and Applied Ecology 11, 693–701.
| Changes in traits of shrub canopies across an aridity gradient in northern Patagonia, Argentina.Crossref | GoogleScholarGoogle Scholar |
Mott KA, Gibson AC, Oleary JW (1982) The adaptive significance of amphistomatic leaves. Plant, Cell & Environment 5, 455–460.
| The adaptive significance of amphistomatic leaves.Crossref | GoogleScholarGoogle Scholar |
Muller RN (1991) Growing-season water relations of Rhododendron maximum L and Kalmia latifolia L. Bulletin of the Torrey Botanical Club 118, 123–127.
| Growing-season water relations of Rhododendron maximum L and Kalmia latifolia L.Crossref | GoogleScholarGoogle Scholar |
Nilsen ET, Bao Y (1987) The influence of leaf age, season, and microclimate on the photosynthetic apparatus of Rhododendron maximum. 1. Chlorophylls. Photosynthetica 21, 535–542.
Nilsen ET, Webb DW (2007) Do scale type and density of Rhododendron species of section Vireya have any relationship to stomata. Journal American Rhododendron Society 61, 93–102.
Nobel PS (1999) ‘Physiochemical and environmental plant physiology.’ 2nd edn. (Academic Press: San Diego, CA)
Payne WW (1978) A glossary of plant hair terminology. Brittonia 30, 239–255.
| A glossary of plant hair terminology.Crossref | GoogleScholarGoogle Scholar |
Parlange J-Y, Waggoner PE (1970) Stomatal dimensions and resistance to diffusion. Plant Physiology 46, 337–342.
| Stomatal dimensions and resistance to diffusion.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cngvFKntg%3D%3D&md5=31cc6062278c88b810a648fc0ae4143cCAS | 16657461PubMed |
Raven JA (2002) Selection pressures on stomatal evolution. New Phytologist 153, 371–386.
| Selection pressures on stomatal evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1Wgt74%3D&md5=a9d63a02b6f158971aff1d660f045758CAS |
Ripley BS, Pammenter NW, Smith VR (1999) Function of leaf hairs revisited: the hair layer on leaves Arctotheca populifolia reduces photoinhibition, but leads to higher leaf temperatures caused by lower transpiration rates. Journal of Plant Physiology 155, 78–85.
| Function of leaf hairs revisited: the hair layer on leaves Arctotheca populifolia reduces photoinhibition, but leads to higher leaf temperatures caused by lower transpiration rates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXks1SltLg%3D&md5=bd52a23c4b0fdc36da9071c0601005a2CAS |
Royer DL (2001) Stomatal density and stomatal index as indicators of paleoatmospheric CO2 concentration. Review of Palaeobotany and Palynology 114, 1–28.
| Stomatal density and stomatal index as indicators of paleoatmospheric CO2 concentration.Crossref | GoogleScholarGoogle Scholar | 11295163PubMed |
Russo SE, Cannon WL, Elowsky C, Tan S, Davies SJ (2010) Variation in leaf stomatal traits of 28 tree species in relations to gas exchange along an edaphic gradient in a Bornean rain forest. American Journal of Botany 97, 1109–1120.
| Variation in leaf stomatal traits of 28 tree species in relations to gas exchange along an edaphic gradient in a Bornean rain forest.Crossref | GoogleScholarGoogle Scholar | 21616863PubMed |
Sack L, Cowan PD, Jaikumar N, Holbrook NM (2003) The ‘hydrology’ of leaves: co-ordination of structure and function in temperate woody species. Plant, Cell & Environment 26, 1343–1356.
| The ‘hydrology’ of leaves: co-ordination of structure and function in temperate woody species.Crossref | GoogleScholarGoogle Scholar |
Sakai WS, Sanford WG (1980) Ultrastructure of the water-absorbing trichomes of pineapple (Ananas comosus, Bromaliaceae). Annals of Botany 46, 7–11.
Salisbury EJ (1927) On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 215, 1–65.
| On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora.Crossref | GoogleScholarGoogle Scholar |
Sandquist DR, Ehleringer JR (2003) Population- and family-level variation of brittlebush (Encelia farinosa, Asteraceae) pubescence: its relation to drought and implications for selection in variable environments. American Journal of Botany 90, 1481–1486.
| Population- and family-level variation of brittlebush (Encelia farinosa, Asteraceae) pubescence: its relation to drought and implications for selection in variable environments.Crossref | GoogleScholarGoogle Scholar | 21659100PubMed |
Sarmiento G (1986) Ecological features of climate in high tropical mountains. In ‘High altitude tropical biogeography’. (Eds F Vuilleumeir, M Monasterio) pp. 11–46. (Oxford University Press: American Museum of Natural History: New York)
Sletvold N, Agren J (2012) Variation in tolerance to drought among Scandinavian populations of Arabidopsis lyrata. Evolutionary Ecology 26, 559–577.
| Variation in tolerance to drought among Scandinavian populations of Arabidopsis lyrata.Crossref | GoogleScholarGoogle Scholar |
Sleumer H (1966) An account of Rhododendron in Malesia. In ‘Flora Malesiana I’ (Senior Editor CGGJ Van Steenis). pp. 474–678. (Wolters-Noordhoff: Groningen, The Netherlands). [Reprinted as ‘An account of Rhododendron in Malesia’ with an introduction and index.]
Wagner GJ, Wang E, Shepherd RW (2004) New approaches for studying and exploiting an old protuberance, the plant trichome. Annals of Botany 93, 3–11.
| New approaches for studying and exploiting an old protuberance, the plant trichome.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3srps1KjsA%3D%3D&md5=a55b443306240595b5726fdeb2450b51CAS | 14678941PubMed |
Werker E (2000) Trichome diversity and development. Advances in Botanical Research 31, 1–35.
| Trichome diversity and development.Crossref | GoogleScholarGoogle Scholar |
Woodman RL, Fernandes GW (1991) Differential mechanical defense – herbivory, evapotranspiration, and leaf hairs. Oikos 60, 11–19.
| Differential mechanical defense – herbivory, evapotranspiration, and leaf hairs.Crossref | GoogleScholarGoogle Scholar |
Woodward FI (1986) Ecophysiological studies of the shrub Vaccinium myrtillus taken from a wide altitudinal range. Oecologia 70, 580–586.
| Ecophysiological studies of the shrub Vaccinium myrtillus taken from a wide altitudinal range.Crossref | GoogleScholarGoogle Scholar |
Woodward FI (1987) Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels. Nature 327, 617–618.
| Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels.Crossref | GoogleScholarGoogle Scholar |
Yang SK, Smith GL (1985) Further study on atmospheric lapse-rate regimes. Journal of the Atmospheric Sciences 42, 961–965.
| Further study on atmospheric lapse-rate regimes.Crossref | GoogleScholarGoogle Scholar |
Zhu Y, Siegwolf RTW, Durka W, Korner C (2010) Phylogenetically balanced evidence for structural and carbon isotope responses in plants along elevational gradients. Oecologia 162, 853–863.
| Phylogenetically balanced evidence for structural and carbon isotope responses in plants along elevational gradients.Crossref | GoogleScholarGoogle Scholar | 19997748PubMed |
