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DO ENVIRONMENTAL FACTORS AFFECT THE TAXONOMIC RELIABILITY OF LEAF CUTICULAR MICROMORPHOLOGICAL CHARACTERS? A CASE STUDY IN PODOCARPACEAE

Published online by Cambridge University Press:  02 August 2017

J. A. R. Clugston ,
C. E. Jeffree ,
A. Ahrends  and
R. R. Mill
J. A. R. Clugston
Affiliation:
Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, Scotland, UK. Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3JH, Scotland, UK.
C. E. Jeffree
Affiliation:
Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3JH, Scotland, UK.
A. Ahrends
Affiliation:
Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, Scotland, UK.
R. R. Mill*
Affiliation:
Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, Scotland, UK.
*
E-mail for correspondence: r.mill@rbge.ac.uk
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Abstract

Leaf cuticle micromorphology has been cited as an important set of taxonomic characters in gymnosperms, but previous studies have largely been based on small sample sizes. The premise of this study was to understand whether external factors affect cuticular micromorphology of Podocarpaceae. Two example species, Prumnopitys andina and Podocarpus salignus, were studied. Of 21 sampled characters, nine (c.43% of the total) were visually assessed as being moderately reliable or highly reliable for taxonomic discrimination for both species, with an additional six (c.29%) being moderately reliable or highly reliable for only one or other of the example species, and six characters (c.29%) unreliable for both. Seven of the most variable stomatal characters were selected for further analysis to establish whether environmental factors affect them. The relationship between these seven stomatal characters, the environment and climate was analysed using the R ‘vegan’ package and climate data gathered from WorldClim. Our results showed that both species had larger stomata in moist and shady conditions, and a higher density of (smaller) stomata in sunny and drier conditions. An additional novel finding was the presence of stomata on the adaxial leaf surface in 46% of samples of Prumnopitys andina: the first record of adaxial stomata in this species, highlighting the necessity of studying multiple samples of a given species. In conclusion, these results indicate that larger sample sizes than have hitherto been employed in cuticle micromorphological studies are necessary to fully document the amount of phenotypic variation that exists.

Keywords

Climatecultivationcuticular micromorphologyenvironmentPodocarpusprincipal components analysisPrumnopitysRsample sizestomatavariation
Type
Articles
Information
Edinburgh Journal of Botany , Volume 74 , Issue 3 , November 2017 , pp. 299 - 343
Copyright
Copyright © Trustees of the Royal Botanic Garden Edinburgh (2017) 

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References

Aasamaa, K., Sober, A. & Rahi, M. (2001). Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Austral. J. Pl. Physiol. 28 (8): 765–774.Google Scholar
Allen, M. T. & Pearcy, R. W. (2000). Stomatal behavior and photosynthetic performance under dynamic light regimes in a seasonally dry tropical rain forest. Oecologia 122 (4): 470–478.Google Scholar
Alvin, K. & Boulter, M. C. (1974). A controlled method of comparative study for Taxodiaceous leaf cuticles. Bot. J. Linn. Soc. 69 (4): 277–286.Google Scholar
Bakker, J. C. (1991). Effects of humidity on stomatal density and its relation to leaf conductance. Sci. Hort. 48 (3–4): 205–212.Google Scholar
Barone Lumaga, M. R., Moretti, A. & De Luca, P. (1999). Morphological aspects of stomata, cuticle and chloroplasts in Ceratozamia kuesteriana Regel (Zamiaceae). Pl. Biosyst. 133 (1): 47–53.Google Scholar
Berkeley Natural History Museums (2017). University of California Botanical Garden TAPIR Provider. Online GBIF occurrence dataset. Available: http://www.gbif.org/occurrence/67028166 (downloaded 2 May 2017).Google Scholar
Carpenter, R. J. (1994). Cuticular morphology and aspects of the ecology and fossil history of North Queensland rainforest Proteaceae. Bot. J. Linn. Soc. 116 (4): 249–303.Google Scholar
Carpenter, R. J., Hill, R. S. & Jordan, G. J. (2005). Leaf cuticular morphology links Platanaceae and Proteaceae. Int. J. Pl. Sci. 166 (5): 843–855.Google Scholar
Chagnoux, S. (2017). The vascular plants collection (P) at the Herbarium of the Muséum national d'Histoire naturelle (MNHN – Paris). Version 69.9. MNHN – Muséum national d'Histoire naturelle. Online GBIF occurrence dataset. Available: http://doi.org/10.15468/nc6rxy (downloaded from GBIF.org 2 May 2017).Google Scholar
Council of Heads of Australasian Herbaria (2017). Australia's Virtual Herbarium, 9 April 2017. Online GBIF occurrence dataset. Available: http://www.gbif.org/occurrence/995382962 (downloaded 2 May 2017).Google Scholar
Creuwels, J. (2017). Naturalis Biodiversity Center (NL) – Botany. Naturalis Biodiversity Center. Online GBIF occurrence dataset. Available: http://doi.org/10.15468/ib5ypt (downloaded via GBIF.org 2 May 2017).Google Scholar
Dean, E. A. & Starbuck, T. (2016). DAV UC Davis Center for Plant Diversity. University of California, Davis. Online GBIF occurrence dataset. Available: http://doi.org/10.15468/z77ps7 (downloaded via GBIF.org 2 May 2017).Google Scholar
García San León, D. (2017). SANT Herbarium vascular plants collection. Herbario SANT, Universidade de Santiago de Compostela. Online GBIF occurrence dataset. Available: http://doi.org/10.15468/dgbpla (downloaded via GBIF.org 2 May 2017).CrossRefGoogle Scholar
Gardner, M. (2013). Conifers – collecting for safe keeping. Botanics 54: 6–7.Google Scholar
Global Administrative Areas (2012). GADM database of Global Administrative Areas. Online. Available: http://www.gadm.org Google Scholar
Hardin, J. W. & Murrell, Z. E. (1997). Foliar micromorphology of Cornus . J. Torrey Bot. Soc. 124 (2): 124–139.Google Scholar
Herbarium Berolinense (2017). Botanic Garden and Botanical Museum Berlin-Dahlem. Online GBIF occurrence dataset. Available: http://doi.org/10.15468/dlwwhz (downloaded via GBIF.org 2 May 2017).Google Scholar
Herbarium Senckenbergianum (2017). Online GBIF occurrence dataset. Available: http://doi.org/10.15468/ucmdjy (downloaded via GBIF.org 2 May 2017).Google Scholar
Hetherington, A. M. & Woodward, F. I. (2003). The role of stomata in sensing and driving environmental change. Nature 424 (6951): 901–908.Google Scholar
Hijmans, R. J. & Etten, J. van (2013). raster: geographic data analysis and modelling. R package version 2.1-37. Online. Available: http://CRAN.R-project.org/package=raster Google Scholar
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25 (15): 1975–1978.Google Scholar
Hill, R. S. & Carpenter, R. J. (1991). Evolution of Acmopyle and Dacrycarpus (Podocarpaceae) foliage as inferred from macrofossils in south-eastern Australia. Austral. Syst. Bot. 4 (3): 449–479.Google Scholar
Ickert-Bond, S. M. (2000). Cuticle micromorphology of Pinus krempfii Lecomte (Pinaceae) and additional species from Southeast Asia. Int. J. Pl. Sci. 161 (2): 301–317.Google Scholar
Instituto de Botánica Darwinion (2017). Instituto de Botánica Darwinion – CONICET. Online GBIF occurrence dataset. Available: http://doi.org/10.15468/vtfbe3 (downloaded via GBIF.org 2 May 2017).Google Scholar
Kim, K., Whang, S. S. & Hill, R. S. (1999). Cuticle micromorphology of leaves of Pinus (Pinaceae) in east and south-east Asia. Bot. J. Linn. Soc. 129 (1): 55–74.Google Scholar
Leng, Q., Yang, H., Yang, Q. & Zhou, J. (2001). Variation of cuticle micromorphology of Metasequoia glyptostroboides (Taxodiaceae). Bot. J. Linn. Soc. 136 (2): 207–219.Google Scholar
Ma, Q.-W., Ferguson, D. K., Li, F.-L., & Li, C.-S. (2009). Leaf epidermal structures of extant plants of Cunninghamia and Taiwania (Cupressaceae sensu lato) and their taxonomic application. Rev. Palaeobot. Palynol. 155 (1): 15–24.Google Scholar
Magill, B., Solomon, J. & Stimmel, H. (2016). Tropicos specimen data, Missouri Botanical Garden. Online GBIF occurrence dataset. Available: http://doi.org/10.15468/hja69f (downloaded via GBIF.org 2 May 2017).Google Scholar
Martin, P. & Heughebaert, A. (2017). Herbarium of Namur. Université de Namur Département de Biologie. Online GBIF occurrence dataset. Available: http://doi.org/10.15468/xy0eoi (downloaded via GBIF.org 2 May 2017).Google Scholar
McNeilly, T., Ashraf, M. & Veltkamp, C. (1987). Leaf micromorphology of sea cliff and inland plants of Agrostis stolonifera L., Dactylis glomerata L., and Holcus lanatus L. New Phytol. 106 (2): 261–269.Google Scholar
Mickle, J. E., Barone Lumaga, M.R., Moretti, A. & De Luca, P. (2011). Scanning electron microscopy studies of cuticle micromorphology in Cycas L. (Cycadaceae). Pl. Biosyst. 145 (1): 191–201.Google Scholar
Mill, R. R. & Stark Schilling, D. M. (2009). Cuticle micromorphology of Saxegothaea (Podocarpaceae). Bot. J. Linn. Soc. 159 (1): 58–67.Google Scholar
Mitton, J. B., Grant, M. C., & Yoshino, A. M. (1998). Variation in allozymes and stomatal size in pinyon (Pinus edulis, Pinaceae), associated with soil moisture. Amer. J. Bot. 85 (9): 1262–1265.Google Scholar
Mott, K. A., Gibson, A. C. & O'Leary, J. W. (1982). The adaptive significance of amphistomatic leaves. Pl. Cell Environm. 5 (6): 455–460.Google Scholar
Oksanen, J. F., Blanchet, G., Kindt, R., Legendre, P., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H. & Wagner, H. (2013). Vegan: Community Ecology Package. R package version 2.0-7. Online. Available: http://CRAN.R-project.org/package=vegan Google Scholar
Orrell, T. & Hollowell, T. (2017). NMNH Extant Specimen Records. Version 1.7. National Museum of Natural History, Smithsonian Institution. Online GBIF occurrence dataset. Available: http://doi.org/10.15468/hnhrg3 (downloaded via GBIF.org 2 May 2017).Google Scholar
Pole, M. (2010). Cuticle morphology of Australasian Sapindaceae. Bot. J. Linn. Soc. 164 (3): 264–292.Google Scholar
Poole, I., Meyers, J. D. B., Lawson, T. & Raven, J. A. (1996). Variations in stomatal density and index: implications for palaeoclimatic reconstructions. Pl. Cell Environm. 19 (6): 705–712.Google Scholar
R Core Team (2013). R: a Language and Environment for Statistical Computing, Version 3.0.1. Vienna: R Foundation for Statistical Computing. Online. Available: http://www.R-project.org/ Google Scholar
Ramirez, J. & Tulig, M. (2015). The New York Botanical Garden Herbarium (NY) – Vascular Plant Collection. Version 2.1. The New York Botanical Garden. Online GBIF occurrence dataset. Available: http://doi.org/10.15468/6e8nje (downloaded via GBIF.org 2 May 2017).Google Scholar
Rasband, W. S. (1997–2012). ImageJ, version 1.47u. Bethesda, Maryland: National Institutes of Health. Online. Available: https://imagej.nih.gov/ij/ (accessed 25 June 2013).Google Scholar
Real Jardín Botánico de Madrid (2016). Vascular Plant Herbarium (MA). Real Jardín Botánico (CSIC). Online GBIF occurrence dataset. Available: http://doi.org/10.15468/mug7kr (downloaded via GBIF.org 2 May 2017).Google Scholar
Royal Botanic Garden Edinburgh (2017a). Royal Botanic Garden Edinburgh Herbarium (E). Online GBIF occurrence dataset. Available: http://doi.org/10.15468/ypoair (downloaded via GBIF.org 2 May 2017).Google Scholar
Royal Botanic Garden Edinburgh (2017b). Royal Botanic Garden Edinburgh Living Plant Collections (E). Online GBIF occurrence dataset. Available: http://doi.org/10.15468/bkzv1l (downloaded via GBIF.org 2 May 2017).Google Scholar
Royal Botanic Gardens, Kew (2016). Royal Botanic Gardens, Kew – Herbarium Specimens. Online GBIF occurrence dataset. Available: http://doi.org/10.15468/ly60bx (downloaded via GBIF.org 2 May 2017).Google Scholar
Schulze, E.-D., Hall, A. E., Lange, O. L., Evenari, M., Kappen, L. & Buschbom, U. (1980). Long-term effects of drought on wild and cultivated plants in the Negev desert. Oecologia 45 (1): 11–18.Google Scholar
Sharma, G. K., & Dunn, D. B. (1968). Effect of environment on the cuticular features in Kalanchoe fedschenkoi . Bull. Torrey Bot. Club 95 (5): 464–473.Google Scholar
Stark Schilling, D. M. & Mill, R. R. (2011). Cuticle micromorphology of Caribbean and Central American species of Podocarpus (Podocarpaceae). Int. J. Pl. Sci. 172 (5): 601–631.Google Scholar
Stockey, R. A. & Atkinson, I. J. (1993). Cuticle micromorphology of Agathis Salisbury. Int. J. Pl. Sci. 154 (1): 187–224.Google Scholar
Stockey, R. A. & Frevel, B. J. (1997). Cuticle micromorphology of Prumnopitys Philippi (Podocarpaceae). Int. J. Pl. Sci. 158 (2): 198–221.Google Scholar
Stockey, R. A. & Ko, H. (1986). Cuticle micromorphology of Araucaria de Jussieu. Bot. Gaz. 147 (4): 508–548.Google Scholar
Stockey, R. A. & Ko, H. (1988). Cuticle micromorphology of some New Caledonian podocarps. Bot. Gaz. 149 (2): 240–252.Google Scholar
Stockey, R. A. & Ko, H. (1990). Cuticle micromorphology of Dacrydium (Podocarpaceae) from New Caledonia. Bot. Gaz. 151 (1): 138–149.Google Scholar
Stockey, R. A., Ko, H. & Woltz, P. (1992). Cuticle micromorphology of Falcatifolium de Laubenfels (Podocarpaceae). Int. J. Pl. Sci. 153 (4): 589–601.Google Scholar
Stockey, R. A., Ko, H. & Woltz, P. (1995). Cuticle micromorphology of Parasitaxus de Laubenfels (Podocarpaceae). Int. J. Pl. Sci. 156 (5): 723–730.Google Scholar
Stockey, R. A., Frevel, B. J. & Woltz, P. (1998). Cuticle micromorphology of Podocarpus, subgenus Podocarpus, section Scytopodium (Podocarpaceae) of Madagascar and South Africa. Int. J. Pl. Sci. 159 (6): 923–940.Google Scholar
Telenius, A. & Shah, M. (2016). Phanerogamic Botanical Collections (S). GBIF-Sweden. Occurrence dataset. Available: http://doi.org/10.15468/yo3mmu (accessed via GBIF.org 2 May 2017).Google Scholar
Vu, V. Q. (2011). ggbiplot: a ggplot2 based biplot. R package version 0.55. Online. Available: http://github.com/vqv/ggbiplot (accessed 11 March 2017).Google Scholar
Whang, S. S., Pak, J.-H., Hill, R. S. & Kim, K. (2001). Cuticle micromorphology of leaves of Pinus (Pinaceae) from Mexico and Central America. Bot. J. Linn. Soc. 135 (4): 349–373.Google Scholar
Whang, S. S., Kim, K. & Hill, R. S. (2004). Cuticle micromorphology of leaves of Pinus (Pinaceae) from North America. Bot. J. Linn. Soc. 144 (3): 303–320.Google Scholar
Whiting, M. (2009). Cuticular micromorphology of Podocarpus as a systematic tool. M.Sc. dissertation, University of Edinburgh and Royal Botanic Garden Edinburgh.Google Scholar
Williams, J. (2011). Colección de Herbario. Facultad de Ciencias Naturales y Museo – U.N.L.P. Online GBIF occurrence dataset. Available: http://doi.org/10.15468/i9bj5r (downloaded via GBIF.org 2 May 2017).Google Scholar
Wilton, A. (2017). Allan Herbarium (CHR). Landcare Research. Online GBIF occurrence dataset. Available: http://doi.org/10.15468/x5ucvh (downloaded via GBIF.org 2 May 2017).Google Scholar
Xiang, Q. & Farjon, A. (2003). Cuticle morphology of a newly discovered conifer, Xanthocyparis vietnamensis (Cupressaceae), and a comparison with some of its nearest relatives. Bot. J. Linn. Soc. 143 (3): 315–322.Google Scholar
Xiang, Q. & Fu, L. (1998). SEM observation on the structure of cuticles on leaf inner surface on Abies (Pinaceae) and its significance in systematics. Acta Phytotax. Sin. 36 (5): 441–448.Google Scholar
Zhang, L., Niu, H., Wang, S., Zhu, X., Luo, C., Li, Y. & Zhao, X. (2012). Gene or environment? Species‐specific control of stomatal density and length. Ecol. Evol. 2 (5): 1065–1070.Google Scholar
Zou, P., Liao, J.-P. & Zhang, D.-X. (2008). Leaf epidermal micromorphology of Cercis (Fabaceae: Caesalpinioideae). Bot. J. Linn. Soc. 158 (3): 539–547.Google Scholar