Abstract
The vertical structure of a tropical rain forest is complex and multilayered, with strong variation of micro-environment with height up to the canopy. We investigated the relation between morphological traits of leaf surfaces and tree ecological characteristics in a Malaysian tropical rain forest. The shapes and densities of stomata and trichomes on the abaxial leaf surfaces and their relation with leaf characteristics such as leaf area and leaf mass per area (LMA) were studied in 136 tree species in 35 families with different growth forms in the tropical moist forest. Leaf physiological properties were also measured in 50 canopy and emergent species. Most tree species had flat type (40.4 %) or mound type (39.7 %) stomata. In addition, 84 species (61.76 %) in 22 families had trichomes, including those with glandular (17.65 %) and non-glandular trichomes (44.11 %). Most leaf characteristics significantly varied among the growth form types: species in canopy and emergent layers and canopy gap conditions had higher stomatal density, stomatal pore index (SPI), trichome density and LMA than species in understory and subcanopy layers, though the relation of phylogenetically independent contrasts to each characteristic was not statistically significant, except for leaf stomatal density, SPI and LMA. Intrinsic water use efficiency in canopy and emergent tree species with higher trichome densities was greater than in species with lower trichome densities. These results suggest that tree species in tropical rain forests adapt to a spatial difference in their growth forms, which are considerably affected by phylogenetic context, by having different stomatal and trichome shapes and/or densities.
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Agrawal AA, Fishbein M, Jetter R, Salminen JP, Goldstein JB, Freitag AE, Sparks JP (2009) Phylogenetic ecology of leaf surface traits in the milkweeds (Asclepias spp.): chemistry, ecophysiology, and insect behavior. New Phytol 183:848–867
Aiba M, Nakashizuka T (2007) Differences in the dry-mass cost of sapling vertical growth among 56 woody species co-occurring in a Bornean tropical rain forest. Funct Ecol 21:41–49
Aronne G, De Micco V (2001) Seasonal dimorphism in the Mediterranean Cistus incanus L. subsp. incanus. Ann Bot 87:789–794
Bacon MA (2004) Water use efficiency in plant biology. Blackwell, Oxford
Basset Y, Aberlenc H-P, Barrios H, Curletti G, Bérenger J-M, Besco J-P, Causse P, Haug A, Hennion A-S, Lesobre L, Marquès F, O’meara R (2001) Stratification and diel activity of arthropods in a lowland rainforest in Gabon. Biol J Linnean Soc 72:585–607
Beerling DJ, Chaloner WG (1993) Stomatal density responses of Egyptian Olea europaea L. Leaves to CO2 change since 1327 BC. Ann Bot 71:431–435
Boeger MRT, Alves LC, Negrelle RRB (2004) Leaf morphology of 89 tree species from a lowland tropical rain forest (Atlantic forest) in South Brazil. Braz Arch Biol Technol 47:933–943
Chapman VJ (1976) Mangrove vegetation. J Cramer, Leuterhausen
Charles E, Basset Y (2005) Vertical stratification of leaf-beetle assemblages (Coleoptera: Chrysomelidae) in two forest types in Panama. J Trop Ecol 21:329–336
Coley PD (1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol Monogr 53:209–233
Davies SJ (1998) Photosynthesis of nine pioneer Macaranga species from Borneo in relation to life history. Ecology 79:2292–2308
De Micco V, Aronne G (2012) Morpho-anatomical traits for plant adaptation to drought. In: Aroca R (ed) Plant responses to drought stress, from morphological to molecular features. Springer, Berlin, pp 37–61
Deng M, Li Q, Yang S, Liu YC, Xu J (2013) Comparative morphology of leaf epidermis in the genus Lithocarpus and its implication in leaf epidermal feature evolution in Fagaceae. Plant Syst Evol 299:659–681
Ehleringer J (1984) Ecology and ecophysiology of leaf pubescence in North American desert plants. In: Rodrigues E, Healey PL, Mehta I (eds) Biology and chemistry of plant trichomes. Plenum Press, New York, pp 113–132
Ehleringer JR, Björkman O (1978) Pubescence and leaf spectral characteristics in a desert shrub, Encelia farinosa. Oecologia 36:151–162
Ehleringer J, Björkman O, Mooney HA (1976) Leaf pubescence: Effects on absorptance and photosynthesis in a desert shrub. Science 191:376–377
Ehleringer JR, Mooney HA (1978) Leaf hairs: Effects on physiological activity and adaptive value to a desert shrub. Oecologia 37:183–200
Eller BM, Willi P (1977) The significance of leaf pubescence for the absorption of global radiation by Tussilago farfara L. Oecologia 29:179–187
Evert RF (2006) Esau’s plant anatomy: meristems, cells, and tissues of the plant body: their structure, function, and development, 3rd edn. Wiley, New Jersey
Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15
Fernández V, Sancho-Knapik D, Guzmán P, Peguero-Pina JJ, Gil L, Karabourniotis G, Khayet M, Fasseas C, Heredia-Guerrero JA, Heredia A, Gil-Pelegrín E (2014) Wettability, polarity, and water absorption of holm oak leaves: effect of leaf side and age. Plant Physiol 166:168–180
Franks PJ, Beerling DJ (2009) CO2-forced evolution of plant gas exchange capacity and water-use efficiency over the Phanerozoic. Geobiology 7:227–236
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 Environ 32:1737–1748
Garland T Jr, Dickerman AW, Janis CM, Jones JA (1993) Phylogenetic analysis of covariance by computer simulation. Syst Biol 42:265–292
Gifford AM, Foster EM (1989) Morphology and evolution of vascular plants. W.H. Freeman, New York
Givnish TJ (1984) Leaf and canopy adaptations in tropical forests. In: Medina E, Mooney HA, Vazquez-Yanes C (eds) Physiological ecology of plants of the wet tropics. Junk, The Hague, pp 51–84
Gregoriou K, Pontikis K, Vemmos S (2007) Effects of reduced irradiance on leaf morphology, photosynthetic capacity, and fruit yield in olive (Olea europaea L.). Photosynthetica 45:172–181
Grubb PJ, Grubb EAA, Miyata I (1975) Leaf structure and function in evergreen trees and shrubs of Japanese warm temperate rain forest. I. The structure of the lamina. Bog Mag Tokyo 88:197–211
Gutschick VP (1999) Biotic and abiotic consequences of differences in leaf structure. New Phytol 143:3–18
Hill RS (1998) Fossil evidence for the onset of xeromorphy and scleromorphy in Australian Proteaceae. Austral Syst Bot 11:391–400
Hiromi T, Ichie T, Kenzo T, Ninomiya I (2012) Interspecific variation in leaf water use associated with drought tolerance in four emergent dipterocarp species of a tropical rain forest in Borneo. J For Res 17:369–377
Hoof J, Sack L, Webb DT, Nilsen ET (2008) Contrasting structure and function of pubescent and glabrous varieties of Hawaiian Metrosideros polymorpha (Myrtaceae) at high elevation. Biotropica 40:113–118
Inoue Y, Kenzo T, Tanaka-Oda A, Yoneyama A, Ichie T (2015) Leaf water use in heterobaric and homobaric leafed canopy tree species in a Malaysian tropical rain forest. Photosynthetica 53:177–186
Ishida A, Toma T, Matsumoto Y, Yap SK, Maruyama Y (1996) Diurnal changes in leaf gas exchange characteristics in the uppermost canopy of a rain forest tree, Dryobalanops aromatica Gaertn. f. Tree Physiol 16:779–785
Ishida A, Nakano T, Uemura A, Yamashita N, Tanabe H, Koike N (2001) Light-use properties in two sun-adapted shrubs with contrasting canopy structures. Tree Physiol 21:497–504
Kamoi T, Kenzo T, Kuraji K, Momose K (2008) Abortion of reproductive organs as an adaptation to fluctuating daily carbohydrate production. Oecologia 154:663–677
Karabourniotis G, Papadopoulos K, Papamarkou M, Manetas Y (1992) Ultraviolet-B radiation absorbing capacity of leaf hairs. Physiol Plant 86:414–418
Kato M, Inoue T, Hamid AA, Nagamitsu T, Merdek MB, Nona AR, Itino T, Yamane S, Yumoto T (1995) Seasonality and vertical structure of light-attracted insect communities in a dipterocarp forest in Sarawak. Res Popul Ecol 37:59–79
Kenzo T, Ichie T, Yoneda R, Kitahashi Y, Watanabe Y, Ninomiya I, Koike T (2004) Interspecific variation of photosynthesis and leaf characteristics in canopy trees of five species of Dipterocarpaceae in a tropical rain forest. Tree Physiol 24:1187–1192
Kenzo T, Ichie T, Watanabe Y, Yoneda R, Ninomiya I, Koike T (2006) Changes in photosynthesis and leaf characteristics with tree height in five dipterocarp species in a tropical rain forest. Tree Physiol 26:865–873
Kenzo T, Ichie T, Watanabe Y, Hiromi T (2007) Ecological distribution of homobaric and heterobaric leaves in tree species of Malaysian lowland tropical rainforest. Am J Bot 94:764–775
Kenzo T, Yoneda R, Azani MA, Majid NM (2008) Changes in leaf water use after removal of leaf lower surface hairs on Mallotus macrostachyus (Euphorbiaceae) in a tropical secondary forest in Malaysia. J For Res 13:137–142
Kenzo T, Yoneda R, Sano M, Araki M, Shimizu A, Tanaka-Oda A, Chann S (2012) Variations in leaf photosynthetic and morphological traits with tree height in various tree species in a Cambodian tropical dry evergreen forest. Jpn Agric Res Q 46:167–180
Kenzo T, Inoue Y, Yoshimura M, Yamashita M, Tanaka-Oda A, Ichie T (2015) Height-related changes in leaf photosynthetic traits in diverse Bornean tropical rain forest trees. Oecologia 177:191–202
Kitahashi Y, Ichie T, Maruyama Y, Kenzo T, Kitaoka S, Matsuki S, Chong L, Nakashizuka T, Koike T (2008) Photosynthetic water use efficiency in tree crowns of Shorea beccariana and Dryobalanops aromatica in a tropical rain forest in Sarawak, East Malaysia. Photosynthetica 46:151–155
Koch GW, Stillet SC, Jennings GM, Davis SD (2004) The limits to tree height. Nature 428:851–854
Koike T, Watanabe T, Toda H, Haibara K (1998) Morphological diversity of stomata of representative broadleaved trees in a temperate region: detection with the Sump method. For Resour Environ 36:57–65
Kumagai T, Kuraji K, Noguchi H, Tanaka Y, Tanaka K, Suzuki M (2001) Vertical profiles of environmental factors within tropical rainforest, Lambir Hills National Park, Sarawak, Malaysia. J For Res 6:257–264
Kume T, Tanaka N, Kuraji K, Komatsu H, Yoshifuji N, Saitoh TM, Suzuki M, Kumagai T (2011) Ten-year evapotranspiration estimates in a Bornean tropical rainforest. Agr For Meteorol 151:1183–1192
Larcher W (2003) Physiological plant ecology, 4th edn. Springer, New York
Levin DA (1973) The role of trichomes in plant defense. Q Rev Biol 48:3–15
Marquis RJ (1992) The selective impact of herbivory. In: Fritz RS, Simmseds EL (eds) Plant resistance to herbivores and pathogens. Ecology, evolution, and genetics. University of Chicago Press, Chicago, pp 301–325
Niinemets U, Keenan T (2014) Photosynthetic responses to stress in Mediterranean evergreens: mechanisms and models. Environ Exp Bot 103:24–41
O’Leary MH (1988) Carbon isotopes in photosynthesis. Bioscience 38:328–336
Pérez-Estrada LB, Cano-Santana Z, Oyama K (2000) Variation in leaf trichomes of Wigandia urens: Environmental factors and physiological consequences. Tree Physiol 20:629–632
Pierce S (2007) The Jeweled Armor of Tillandsia—multifaceted or elongated trichomes provide photoprotection. Aliso 23:44–52
Pierce S, Maxwell K, Griffiths H, Winter K (2001) Hydrophobic trichome layers and epicuticular wax powders in Bromeliaceae. Am J Bot 88:1371–1389
Poorter L, Bongers F (2006) Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87:1733–1743
Poorter L, Kwant R, Hernández R, Medina E, Werger MJA (2000) Leaf optical properties in Venezuelan cloud forest trees. Tree Physiol 20:519–526
Pyykkö M (1979) Morphology and anatomy of leaves from some woody plants in a humid tropical rainforest of Venezuelan Guayana. Acta Bot Fenn 112:1–41
Raven JA (2002) Selection pressures on stomatal evolution. New Phytol 153:371–386
Richards PW (1952) The tropical rain forest: an ecological study. Cambridge University Press, Cambridge
Rodríguez E, Healey PL, Mentha I (1984) Biology and chemistry of plant trichomes. Plenum Press, New York
Roth I (1984) Stratification of tropical forests as seen in leaf structure. Dr W Junk Publishers, Hague
Roth I (1990) Leaf structure of a Venezuelan cloud forest in relation to the microclimate. Gebrüder Borntraeger, Berlin
Roth-Nebelsick A (2007) Computer-based studies of diffusion through stomata of different architecture. Ann Bot 100:23–32
Roy BA, Stanton ML, Eppley SM (1999) Effects of environmental stress on leaf hair density and consequences for selection. J Evol Biol 12:1089–1103
Russo SE, Cannon WL, Elowsky C, Tan S, Davies SJ (2010) Variation in leaf stomatal traits of 28 tree species in relation to gas exchange along an edaphic gradient in a Bornean rain forest. Am J Bot 97:1109–1120
Ryan MG, Yoder BJ (1997) Hydraulic limits to tree height and tree growth: What keeps trees from growing beyond a certain height? Bioscience 47:235–242
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 Environ 26:1343–1356
Sack L, Tyree MT, Holbrook NM (2005) Leaf hydraulic architecture correlates with regeneration irradiance in tropical rainforest trees. New Phytol 167:403–413
Sack L, Melcher PJ, Liu WH, Middleton E, Pardee T (2006) How strong is intracanopy leaf plasticity in temperate deciduous trees? Am J Bot 93:829–839
Sakai S, Momose K, Yumoto T, Nagamitsu T, Nagamasu H, Hamid AA, Nakashizuka T (1999) Plant reproductive phenology over four years including an episode of general flowering in a lowland dipterocarp forest, Sarawak, Malaysia. Am J Bot 86:1414–1436
Salisbury EJ (1927) On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora. Philos Trans R Soc B-Biol Sci 216:1–65
Schreuder MDJ, Brewer CA, Heine C (2001) Modelled influences of non-exchanging trichomes on leaf boundary layers and gas exchange. J Theor Biol 210:23–32
Sobrado MA, Medina E (1980) General morphology, anatomical structure, and nutrient content of sclerophyllous leaves of the ‘bana’ vegetation of amazonas. Oecologia 45:341–345
Sosnovsky Y (2015) Microscopical investigation of the leaf architecture in greenhouse-cultivated Ficus (Moraceae). Plant Syst Evol 301:1669–1692
Sutton SL, Hudson PJ (1980) The vertical distribution of small flying insects in the lowland rain forest of Zaïre. Zool J Linn Soc 68:111–123
Tan GCH, Ong BL, Turner IM (1994) The photosynthetic performance of six early successional tropical tree species. Photosynthetica 30:201–206
Turner IM (2001) The ecology of trees in the tropical rain forest. Cambridge University Press, Cambridge
Wagner GJ (1991) Secreting glandular trichomes: more than just hairs. Plant Physiol 96:675–679
Wagner GJ, Wang E, Shepherd RW (2004) New approaches for studying and exploiting an old protuberance, the plant trichome. Ann Bot-Lond 93:3–11
Wallace LL, Dunn EL (1980) Comparative photosynthesis of three gap phase successional tree species. Oecologia 45:331–340
Walter N (1973) Vegetation of the earth. Springer, New York, pp 42–45
Webb CO, Donoghue MJ (2005a) Phylomatic: a database for applied phylogenetics (http://www.phylodiversity.net/phylomatic/)
Webb CO, Donoghue MJ (2005b) Phylomatic: tree assembly for applied phylogenetics. Mol Ecol Notes 5:181–183
Webb CO, Ackerly DD, Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24:2098
Weerasinghe LK, Creek D, Crous KY, Xiang S, Liddell MJ, Turnbull MH, Atkin OK (2014) Canopy position affects the relationships between leaf respiration and associated traits in a tropical rainforest in Far North Queensland. Tree Physiol 34:564–584
Whitmore TC (1998) An introduction to tropical rain forests, 2nd edn. Oxford University Press, Oxford
Wilkens RT, Shea GO, Halbreich S, Stamp NE (1996) Resource availability and the trichome defenses of tomato plants. Oecologia 106:181–191
Willmer C, Fricker M (1996) Stomata, 2nd edn. Chapman and Hall, London
Woodward FI (1987) Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels. Nature 327:617–618
Wuenscher JE (1970) The effect of leaf hairs of Verbascum thapsus on leaf energy exchange. New Phytol 69:65–73
Xu Z, Zhou G (2008) Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J Exp Bot 59:3317–3325
Yoda K (1978) Three-dimensional distribution of light intensity in a tropical rain forest of West Malaysia. Malay Nat J 30:161–177
Acknowledgments
We thank the Forest Department, Sarawak, and Sarawak Forestry Corporation, and also Prof. T. Nakashizuka, Prof. N. Yamamura, Prof. S. Fujiwara, Dr. Y. Watanabe, Dr. M. Aiba and Ms. Y. Kuzume for their kind support of this study. Climate data was provided by Dr. T. Kume. Dr. H. Nagamasu and Dr. K. Momose identified tree species in the plots. This research was partly supported by a Project of the Research Institute for Humanity and Nature (P2-5, D-04): a Grant-in-Aid for Scientific Research (Nos. 23255002, 24405032) from the Ministry of Education, Science and Culture, Japan: the Environment Research and Technology Development Fund (RF-1010, S-9) of the Ministry of the Environment, Japan.
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Ichie, T., Inoue, Y., Takahashi, N. et al. Ecological distribution of leaf stomata and trichomes among tree species in a Malaysian lowland tropical rain forest. J Plant Res 129, 625–635 (2016). https://doi.org/10.1007/s10265-016-0795-2
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DOI: https://doi.org/10.1007/s10265-016-0795-2