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Ecology |
Forestry and Forest Products Research Institute, Tsukuba, 305-8687, Japan; Faculty of Agriculture, Kochi University, Nankoku, 783-8502, Japan; Hokkaido University Forests, FSC, Sapporo, 060-0809, Japan; Ehime Kindergarten, Matsuyama, 790-0003, Japan
Received for publication November 28, 2005. Accepted for publication March 5, 2007.
ABSTRACT
Tree species can generally be classified into two groups, heterobaric and homobaric leafed species, according to whether bundle-sheath extensions (BSEs) are found in the leaf (heterobaric leaf) or not (homobaric leaf). In this study, we study whether the leaf type is related to the growth environment and/or life form type, even in a tropical rain forest, where most trees have evergreen leaves that are generally homobaric. Accordingly, we investigated the distribution of leaf morphological differences across different life forms of 250 tree species in 45 families in a tropical rainforest. In total, 151 species (60%) in 36 families had homobaric leaves, and 99 species (40%) in 21 families had heterobaric leaves. We found that the proportion of heterobaric and homobaric leaf species differed clearly across taxonomic groups and life form types, which were divided into five life form types by their mature tree heights (understory, subcanopy, canopy, and emergent species) and as canopy gap species. Most understory (94%) and subcanopy (83%) species such as Annonaceae had homobaric leaves. In contrast, heterobaric leaf trees appeared more frequently in the canopy species (43%), the emergent species (96%) (such as Dipterocarpaceae), and the canopy gap species (62%). Our results suggest that tree species in the tropical rainforest adapt to spatial differences in the environmental conditions experienced at the mature height of each tree species, such as light intensity and vapor pressure difference, by having differing leaf types (heterobaric or homobaric) because these types potentially have different physiological and/or mechanical functions.
Key Words: bundle-sheath extension • heterobaric leaf • homobaric leaf • life form type • morphology • tropical forest
The morphological characteristics of plant organs are important in adaptation to growth environments because they are central to functions such as photosynthesis, movement of water, and absorption by root (Esau, 1960
; Larcher, 2003
). Plant leaves display diverse morphological characteristics across species, including their shape, size, and structure (Gifford and Foster, 1989
; Thomas and Ickes, 1995
; Dominy et al., 2003
; Kenzo et al., 2004
). Tree species can be classified into two groups, heterobaric and homobaric leaf species, according to the occurrence of bundle-sheath extensions (BSEs) in the leaf (Neger, 1918
; Wylie, 1951
; Terashima, 1992
). BSEs are formed by parenchyma or sclerenchyma cells of the vascular bundle sheath, which extend to the epidermis on both sides of the leaf in heterobaric leaf trees (Wylie, 1943
, 1952
). As a result, the mesophyll of heterobaric leaves is separated into many small "bundle-sheath extension compartments" by BSEs (Terashima, 1992
). In contrast, homobaric leaves lack BSEs and the internal structure of the leaf is relatively homogenous.
These leaf types differ not only in structural traits but also in mechanical and functional characteristics. For example, BSEs in heterobaric leaves may give mechanical support to the leaf blade (Wylie, 1952
; Esau, 1960
), act as a water conduit (Wylie, 1943
), or cause non-uniform photosynthesis (Siebke and Weis, 1995
; Mott and Buckley, 2000
; West et al., 2005
). Homobaric leaves, in contrast, have larger lateral movements of gases in the leaf than heterobaric leaves (Parkhurst, 1994
; Rhizopoulou and Psaras, 2003
; Pieruschka et al., 2005
, 2006
; but see Morison et al., 2005
).
These morphological and functional differences between the two leaf types may relate to their growth environments and/or life form type (such as emergent, canopy, subcanopy, understory, and canopy gap species). Recent studies documented the strong ecological linkage among growth environments and/or life form (or adult tree size) with respect to tree growth and leaf physiological and morphological characteristics (e.g., Thomas and Bazzaz, 1999
; Reich, 2000
; Thomas, 2003
; Sack et al., 2005
; King et al., 2006
; Sack and Frole, 2006
). Some authors have suggested that heterobaric leaf trees will preferentially be found in deciduous forests, which have dry and/or cold seasons (Wylie, 1952
; Terashima, 1992
). In contrast, the proportion of homobaric leaf trees may increase in wet and warm regions, which are usually dominated by evergreen tree species. Many more evergreen tree species have homobaric leaves than deciduous tree species (Wylie, 1952
; McClendon, 1992
; Kashimura et al., 2000
; Boeger et al., 2004
). Consequently, in the tropical rainforest, most tree species may have homobaric leaves because the forest condition is humid all year round and consists mainly of evergreen trees, compared with other forest biomes.
In this study, we suppose that leaf type is correlated with growth environment and/or life form type rather than with forest biome, even in a tropical rainforest in which most trees have evergreen leaves. The spatial distribution of microenvironmental factors such as light intensity, temperature, and humidity varies significantly even in a humid tropical rainforest (Whitmore, 1984
, 1998
). In particular, the upper canopy of the forest undergoes significant desiccating conditions because of the high light intensities, high temperature, and low humidity, whereas the interior of tropical rainforest is light-deficient and humid (Aoki et al., 1978
; Yoda, 1978
; Kumagai et al., 2001
). Canopy gaps are also dry and are exposed to high irradiance compared with the forest floor under the closed canopy (Whitmore, 1998
). As a result of the frequent water stress conditions in the canopy and in canopy gaps, most tree species may display heterobaric leaves even in tropical rainforests. On the other hand, homobaric leaf trees should be better represented in forest understory species because of the humid environment. If the proportion of species of each leaf type varies with location in the forest, this may also influence stand-level photosynthesis and transpiration traits, which may differ between leaf types (Terashima, 1992
). However, only limited information is available on the distribution pattern and/or environmental response to different growth conditions of heterobaric and homobaric leaf trees.
In the present work, we investigated the distribution of leaf morphological differences across ecological types, distinguishing between heterobaric and homobaric leaf species, in different life forms of 250 tree species in 45 families in a tropical rainforest, which has high species richness, many life forms and complex microenvironments. In particular, we focused on the relation between each leaf type and their life form types, such as emergent, canopy, subcanopy, understory, and canopy gap species.
MATERIALS AND METHODS
Study site
The study was carried out in the Canopy Biology Plot (8 ha, 200 x 400 m; Inoue et al., 1994
) and in the Canopy Crane Plot (4 ha, 200 x 200 m; Sakai et al., 2002
) in a lowland mixed dipterocarp forest in Lambir Hills National Park, Sarawak, Malaysia (4°12' N, 113°50' E, 150–250 m a.s.l.), in 2005. The mean height of the canopy in the stand was about 30–40 m; some emergent trees reached 50–70 m. The area has a humid tropical climate, with weak seasonal changes in rainfall and temperature (Kato et al., 1995
). The annual precipitation at the Canopy Crane Plot (there is one weather station) averaged 2540 mm from 2000 to 2004. The average annual temperature from 2000 to 2003 was 26.3°C, with monthly means that varied from 25.6°C in February to 27.0°C in May.
Plant material
We collected the leaves of 434 individuals of 250 tree species in 127 genera in 45 families, from forest understory to emergent tree class and at a canopy gap in the plots (see Appendix). We used fully expanded and apparently nonsenescing leaves taken from the top of the crown. To collect leaf samples, we used a canopy observation system, including tree towers and aerial walkways at the Canopy Biology Plot (Inoue et al., 1994
) and an 85 m canopy crane at the Crane Plot (Sakai et al., 2002
). The canopy crane system provides three-dimensional access to the forest (Ozanne et al., 2003
). Between two and five leaves of each species in the plots were sampled for microscopic observations. Nomenclature was checked in the Angiosperm Phylogeny Website, version 6 (http://www.mobot.org/MOBOT/Research/APweb) and in flora records of the study area (Anderson, 1980
; Soepadmo and Wong, 1995
; Soepadmo et al., 1996
, 2002
, 2004
; Nagamasu and Momose, 1997
; Soepadmo and Saw, 2000
).
Sampling at growth stages between seedling and mature tree
To analyze the occurrence of BSEs in different growth stages and individuals, we selected 42 species in 22 genera in 14 families, such as Burseraceae, Dipterocarpaceae, Euphorbiaceae, and Moraceae, from the 250 species (see Appendix). The species selected are mainly typical canopy and emergent trees in the forest. In the survey, we mainly compared leaf type between seedlings (DBH < 3 cm) grown under dark forest understory and mature canopy individuals that had reached the bright canopy layer. Canopy openness on the sampled seedlings, which was calculated from a hemisphere photograph (Kenzo et al., 2006
), was less than 10%. In total, samples from 226 individuals were collected for this study (see Appendix).
Leaf collection and occurrence of BSEs
Collected fresh leaves were observed in transmitted light and then fixed in FAA (40% formaldehyde : acetic acid : 70% ethanol; 2 : 1 : 17, v/v). Transverse slices were also prepared and observed with a light microscope (AFX-IIA, Nikon, Tokyo, Japan) equipped with a camera (DS-5M-L1, Nikon, Tokyo, Japan). Some samples were observed using a low-vacuum scanning electron microscope (JSM-5310LV; JEOL) at an accelerating voltage of 15 kV (Fig. 2).
|
; Beyschlag et al., 1992
, 1994
; Hiromi et al., 1999
) to separate the leaf types of 24 species in 14 families (see Appendix). Immediately after detachment from the tree, the leaf sample was immersed in either 30 mL or 100 mL 1% fuchsin acid solution, in a 50 mL or 200 mL syringe, respectively. Air bubbles in the syringe were removed through the syringe outlet. The water column in the syringe was pushed inward by the piston, so that water penetrated into the leaf via the stomatal pores. The infiltrated leaves were removed from the syringe and dried on blotting paper. If the leaf is heterobaric, then the compartments become visible, especially in the afternoon (Hiromi et al., 1999
; Küppers et al., 1999
; Fig. 3a). In homobaric leaves, liquid dyes diffuse, and the dye spots gradually expand into the whole leaf (Hiromi et al., 1999
; Fig. 3b, c).
|
|
; Soepadmo and Wong, 1995
; Soepadmo et al., 1996
, 2002
, 2004
; Nagamasu and Momose, 1997
; Sakai et al., 1999
; Soepadmo and Saw, 2000
; Lee et al., 2002
). Thereafter, the tree species were classified into four categories by mature height (Sakai et al., 1999
): forest understory (<12.5 m), subcanopy (12.5–27.5 m), canopy (>27.5–42.5 m), and emergent (>42.5 m) species. We collected 49, 78, 53, and 49 tree species from the forest understory, subcanopy, canopy, and emergent species, respectively (Table 1). Tree species that grow mainly in canopy gaps were classified independently (canopy gap species; 21 species), regardless of their height.
|
The leaf types, heterobaric or homobaric, from seedling to mature tree in 226 individuals in 42 species in 14 families did not vary between growth stages and individuals. However, the interval of BSEs on 36 studied species was usually denser in leaves of canopy individuals than in leaves of understory seedlings (Fig. 4).
|
2 test, P < 0.0001, df = 4, N = 250 species; SPSS version 11.5, SPSS, Inc., Chicago, Illinois, USA). The proportion of heterobaric leaf trees was only 6% for forest understory species and 17% for subcanopy species. The proportion increased to 43% for canopy species and reached 96% for emergent species. The proportion in the canopy gap species was also quite high (62%).
We also found a significant relation between taxonomic group (family) and leaf type (2 test, P < 0.0001, df = 13, N = 184 species, in 14 families with >five species sampled for each family in this study; SPSS version 11.5; Table 2). All species of Dipterocarpaceae, consisting mainly of canopy and emergent tree, were classified as heterobaric leaf trees. In contrast, Annonaceae, Rubiaceae and Melastomataceae, which appeared mainly in the forest understory, had only homobaric leaves (Table 2). However, seven families, such as Euphorbiaceae, Lauraceae, Burseraceae, and Sapotaceae, included trees of both leaf types. Tree species of both leaf types were even found in the same genus within these families: for example, genus Macaranga in Euphorbiaceae and Santiria in Burseraceae included both leaf types (see Appendix).
|
The leaf type of tree species, either heterobaric or homobaric leaf, may depend on life form types in the tropical rainforest. In general, evergreen tree species tend to have homobaric leaves compared with deciduous tree species (Wylie, 1952
). Nevertheless, upper canopy and gap species, especially the most emergent species in the tropical rainforest, displayed heterobaric leaves even from the small seedling stage (Fig. 4, Table 1).
The difference in the distribution of leaf types along with mature tree height may be related to the steep microenvironment gradient with forest height. In canopy conditions in a tropical rainforest, tree leaves suffer strong desiccating conditions from the higher vapor pressure difference (VPD), temperature, and stronger winds than leaves in the understory (Aoki et al., 1978
; Yoda, 1978
; Chazdon et al., 1996
). The presence of BSEs might confer an advantage on heterobaric leaves over homobaric leaves in the high-stress canopy environment. BSEs may be responsible for rapid stomatal response to drought signals, such as reduction of water potential in the mesophyll or a higher concentration of abscisic acid (ABA) by rapid transportation of these signals via the transpiration stream in BSEs (Terashima, 1992
). BSEs may also contribute to the support and protection of the leaf blade against collapse after severe dehydration or other stress (Wylie, 1943
, 1951
, 1952
; Lucas et al., 1991
; Choong et al., 1992
; Terashima, 1992
), may protect against evaporation following injury to the leaf blade (Aldea et al., 2005
), and may guide sunlight to thicker sun leaves (Karabourniotis et al., 2000
; Nikolopoulos et al., 2002
). The higher proportion of heterobaric leaf trees in the gap species may also be related to their dry and sunny growth environment, just as in the upper canopy conditions.
Conversely, the understory of a tropical rainforest is more suited to homobaric leaves, which may tend to have greater leaf performance in shade condition than heterobaric leaves. Light environments in the tropical rainforest change significantly with decreasing forest height, usually with only a low percentage of the sunlight reaching the forest floor (Yoda, 1978
; Chazdon, 1988
; Chazdon et al., 1996
). Under such conditions, most growing plants that reproduce in the understory have greater leaf performance in the shade (Whitmore, 1998
). The lack of BSEs may improve the ability to use available sunflecks, because lateral CO2 diffusion from shaded to illuminated areas of the homobaric leaf will enhance photosynthesis (Lawson and Morison, 2006
; Pieruschka et al., 2006
). Homobaric leaves also increase their proportion of photosynthetically active leaf areas (Terashima, 1992
). In a study of BSEs in 31 temperate heterobaric leaf tree species, Nikolopoulos et al. (2002)
reported that the photosynthetically active leaf area ranged from 91% to 48% according to an increasing density of BSEs. These characteristics could contribute to the photosynthetic efficiency under limited light. Even heterobaric leaves growing under shaded conditions, as in the seedling stage under the understory and the mature stage in the inner crown, generally have larger BSE compartments than heterobaric leaves growing under sunny conditions in the same species (Fig. 4; Crocker, 1919
; Wylie, 1951
; Roth, 1984
; Koike et al., 1997
; Nikolopoulos et al., 2002
). Some authors have also found that species of temperate deciduous trees with thicker leaves tend to have denser BSEs (Wylie, 1952
; Nikolopoulos et al., 2002
). However, some understory trees such as the genus Goniothalamus in this study, had very thick leaves (more than 400 µm), but they were homobaric. Future study may be still needed on the relation between leaf thickness and BSE occurrence in the leaves.
The tree leaf type, whether heterobaric or homobaric, is also related to the taxonomic group (family and/or genus), which is usually reflected by life form type and/or growth habitat at around the mature stage. Families mainly appearing in the canopy layer, such as Dipterocarpaceae, tend to have heterobaric leaves. In contrast, families mainly appearing in the forest understory, such as Annonaceae, Rubiaceae, and Melastomataceae, tend to have homobaric leaves (Table 2, Appendix). However, families such as Euphorbiaceae, Lauraceae, Burseraceae, and Sapotaceae, which include tree species of various life form types, from understory to emergent, included both heterobaric and homobaric leaf trees (Table 2, Appendix). Furthermore, some genera in these families, such as Macaranga (Euphorbiaceae) and Santiria (Burseraceae), included trees of both leaf types (see Appendix). The leaf type in a single species does not change through its growth stages or between individuals. These results suggest that the leaf type in each species depends on the growth habitats and/or life form types at the mature height of each tree species, which are in turn commonly related to the forest microenvironments at the adult tree stage. In addition, it is reported that in tropical rainforest species, the interspecific leaf physiological properties of seedlings, such as the photosynthetic rate, are significantly related to the adult tree habitat, even if the seedlings themselves were grown in the same environment (Thomas and Bazzaz, 1999
; Cai et al., 2005
; Martínez-Garza and Howe, 2005
). Our results, showing that the leaf type is fixed throughout the stages, from seedlings to mature individuals, of the same species, may reflect these interspecific differences in leaf physiological traits at the seedling stage.
In conclusion, we found a clear distribution pattern for the leaf type, categorized as either heterobaric or homobaric leaves, in the growth environment and/or life form types and in the taxonomic groups, in this tropical rain forest. Our results suggest that tropical tree species might adapt to the spatial gradient of the physical variables, such as light intensity and VPD, at the mature height of each tree species by having different leaf types—heterobaric or homobaric—which may have different physiological and mechanical functions. To study this phenomenon further, the functional roles of each leaf in the various environments must be determined.
APPENDIX. List of tree species of a Malaysian lowland tropical rainforest with leaf type, life form, and total sampling number of individuals and leaves
FOOTNOTES
1 The authors thank the Forest Department Sarawak and Sarawak Forestry Corporation and Prof. T. Nakashizuka, Prof. K. Ogino, Dr. M. Sano, Mr. M. Yoshimura, Dr. K. Kamiya, Mr. S. Kashimura, and Dr. K. Yazaki for their kind support of this study. Dr. L. Sack and anonymous reviewers made valuable suggestions to improve the manuscript. Prof. M. Suzuki, Dr. K. Kuraji, and Dr. T. Kumagai provided the climate data. Dr. H. Nagamasu and Dr. K. Momose identified tree species in the plots and gave us some leaf samples. This research was partly supported by a Project of the Research Institute for Humanity and Nature (P2–2); Grant-in-Aid for Scientific Research (no. 16310017) from the Ministry of Education, Science and Culture, Japan; and by the Japan Society for Promotion of Science (JSPS) Research Fellowships for Young Scientists (T.I.). 
6 Author for correspondence (mona{at}affrc.go.jp
)
LITERATURE CITED
Aldea M. Hamilton J. G. Resti J. P. Zangerl A. R. Berenbaum M. R. Delucia E. H.. 2005. Indirect effect of insect herbivory on leaf gas exchange in soybean. Plant, Cell & Environment 28: 402-411.[CrossRef]
Anderson J. A. R.. 1980. A check list of the trees of Sarawak Forest Department Sarawak, Kuching, Malaysia.
Aoki M. Yabuki K. Koyama H.. 1978. Micrometeorology of Pasoh forest. Malayan Nature Journal 30: 149-159.
APG II.. 2003. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants. Botanical Journal of the Linnean Society 141: 399-436.[CrossRef][ISI]
Beyschlag W. Kresse F. Ryel R. J. Pfanz H.. 1994. Stomatal patchiness in conifers: experiments with Picea abies (L.) Karst. and Abies alba Mill. Trees 8: 132-138.
Beyschlag W. Pfanz H.. 1990. A fast method to detect the occurrence of nonhomogeneous distribution of stomatal aperture in heterobaric plant leaves. Oecologia 82: 52-55.[CrossRef][ISI]
Beyschlag W. Pfanz H. Ryel R. J.. 1992. Stomatal patchiness in Mediterranean evergreen sclerophylls. Phenomenology and consequence for the interpretation of the midday depression in photosynthesia and transpiration. Planta 187: 546-553.[ISI]
Boeger M. R. T. Alves L. C. Negrelle R. R. B.. 2004. Leaf morphology of 89 tree species from a lowland tropical rain forest (Atlantic forest) in south Brazil. Brazilian Archives of Biology and Technology 47: 933-943.[ISI]
Cai Z.-Q. 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.[ISI][Medline]
Chazdon R. L.. 1988. Sunflecks and their importance to forest understory plants. Advanced Ecological Research 18: 1-63.
Chazdon R. L. Pearcy R. W. Lee D. W. Fetcher N.. 1996. Photosynthetic responses of tropical forest plants to contrasting light environments. In S. S. Mulkey, R. L. Chazdon, and A. P. Smith [eds.], Tropical forest plant ecophysiology 5-55 Chapman and Hall, New York, New York, USA.
Choong M. F. Lucas P. W. Ong J. S. Y. Pereira B. Tan H. T. W. Turner I. M.. 1992. Leaf fracture toughness and sclerophylly: their correlations and ecological implications. New Phytologist 121: 597-610.[CrossRef][ISI]
Crocker Wm.. 1919. Aeration systems of leaves. Botanical Gazette 67: 517-518.
Dominy N. J. Lucas P. W. Wright S. J.. 2003. Mechanics and chemistry of rain forest leaves: canopy and understory compared. Journal of Experimental Botany 54: 2007-2014.
Esau K.. 1960. Anatomy of seed plants Wiley, New York, New York, USA.
Fly K. E. Walker R. B.. 1967. A pressure-infiltration method for estimating stomatal opening in conifers. Ecology 48: 155-157.[CrossRef][ISI]
Gifford A. M. Foster E. M.. 1989. Morphology and evolution of vascular plants Freeman, New York, New York, USA.
Hiromi T. Ninomiya I. Koike T. Ogino K.. 1999. Regulation of transpiration by patchy stomatal opening in canopy tree species of Dipterocarpaceae in tropical rainforest, Sarawak, Malaysia. Japanese Journal of Ecology 49: 83-91 (in Japanese with English abstract).
Inoue T. Yumoto T. Hamid A. A. Ogino K. Lee H. S.. 1994. Construction of a canopy observation system in the tropical rainforest of Sarawak. In T. Inoue and A. A. Hamid [eds.], Canopy biology program in Sarawak. I. Plant reproductive systems and animal seasonal dynamics 4-21 Center for Ecological Research, Kyoto University, Otsu, Japan.
Karabourniotis G. Bornman J. F. Nikolopoulos D.. 2000. A possible optical role of the bundle sheath extensions of some heterobaric leaves of Vitis vinifera and Quercus coccifera. Plant, Cell & Environment 23: 423-430.[CrossRef]
Kashimura S. Hiromi T. Ninomiya I.. 2000. The leaf anatomical structure of broadleaf plant. Homobaric leaf and heterobaric leaf. Bulletin of the Ehime University Forest 38: 23-36 (in Japanese with English abstract).
Kato M. Inoue T. Hamid A. A. Nagamitsu T. Merdek M. B. Nona A. R. Itino T. Yamane S. Yumoto T.. 1995. Seasonality and vertical structure of light-attracted insect communities in a dipterocarp forest in Sarawak. Researches on Population Ecology 37: 59-79.[CrossRef][ISI]
Kenzo T. Ichie T. Yoneda R. Kitahashi Y. Watanabe Y. Ninomiya I. Koike T.. 2004. Interspecific variation of photosynthesis and leaf characteristics in five canopy trees of Dipterocarpaceae in a tropical rain forest. Tree Physiology 24: 1187-1192.[ISI][Medline]
Kenzo T. Ichie T. Yoneda R. Watanabe Y. Ninomiya I. Koike T.. 2006. Changes in photosynthesis and leaf characteristics with height from seedlings to mature canopy trees in five dipterocarp species in a tropical rain forest. Tree Physiology 26: 865-873.[ISI][Medline]
King D. A. Davies S. J. Noor N. S. M.. 2006. Growth and mortality are related to adult tree size in a Malaysian mixed dipterocarp forest. Forest Ecology and Management 223: 152-158.[CrossRef][ISI]
Koike T. Miyashita N. Toda H.. 1997. Effect of leaf structural characteristics in successional deciduous broadleaved tree seedlings and their silvicultural meaning. Forest Resources Environment 35: 9-25.
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. Journal of Forest Research 6: 257-264.[CrossRef]
Küppers M. Heiland I. Schneider H. Neugebauer P. J.. 1999. Light-flecks cause non-uniform stomatal opening—studies with special emphasis on Fagas sylvatica L. Trees 14: 130-144.
Larcher W.. 2003. Physiological plant ecology, 4th ed Springer-Verlag, New York, New York, USA.
Lawson T. Morison J.. 2006. Visualising patterns of CO2 diffusion in leaves. New Phytologist 169: 641-643.[CrossRef][ISI][Medline]
Lee H. S. Ashton P. S. Yamakura T. Tan S. Davies S. J. Itho A. Chai E. O. K. Ohkubo T. LaFrankie J. V.. 2002. The 52-hectare forest research plot at Lambir Hills, Sarawak, Malaysia: tree distribution maps, diameter tables and species documentation Forest Department Sarawak, Arnold Arboretum–CTFS Asia Program and Smithsonian Tropical Research Institute; Lee Miing Press, Kuching, Malaysia.
Lucas P. W. Choong M. F. Tan H. T. W. Turner I. M. Berrick A. J.. 1991. The fracture toughness of the leaf of the dicotyledon Calophyllum inophyllum L. (Guttiferae). Philosophical Transactions of the Royal Society of London, B, Biological Sciences 334: 95-106.[CrossRef]
Martínez-Garza C. Howe H. F.. 2005. Developmental strategy or immediate responses in leaf traits of tropical tree species?. International Journal of Plant Sciences 166: 41-48.[CrossRef][ISI]
McClendon J. H.. 1992. Photographic survey of the occurrence of bundle-sheath extensions in deciduous dicots. Plant Physiology 99: 1677-1679.
Morison J. I. L. Gallouet E. Lawson T. Cornic G. Herbin R. Baker N. R.. 2005. Lateral diffusion of CO2 in leaves is not sufficient to support photosynthesis. Plant Physiology 139: 254-266.
Mott K. A. Buckley T. N.. 2000. Patchy stomatal conductance: emergent collective behavior of stomata. Trends in Plant Science 5: 258-262.[CrossRef][ISI][Medline]
Nagamasu H. Momose K.. 1997. Flora of Lambir Hills National Park, Sarawak, with special reference to the Canopy Biology Plot. In T. Inoue and A. A. Hamid [eds.], Canopy biology program in Sarawak. II. General flowering of tropical forests in Sarawak 20-67 Center for Ecological Research, Kyoto University, Otsu, Japan.
Neger F. W.. 1918. Die Wegsamkeit der Laubblätter für Gase. Flora 111: 152-161.
Nikolopoulos D. Liakopoulos G. Drossopoulos I. Karabourniotis G.. 2002. The relationship between anatomy and photosynthetic performance of heterobaric leaves. Plant Physiology 129: 235-243.
Ozanne C. M. P. Anhuf D. Boulter S. L. Kitching R. L. Köner C. Meinzer F. C. Mitchell A. W. Nakashizuka T. Silva Dias P. L. Stork N. E. Wright S. J. Yoshimura M.. 2003. Biodiversity meets the atmosphere: a global view of forest canopies. Science 301: 183-186.
Parkhurst D. F.. 1994. Diffusion of CO2 and other gases inside leaves. New Phytologist 126: 449-479.[CrossRef][ISI]
Pieruschka R. Schurr U. Jahnke S.. 2005. Lateral gas diffusion inside leaves. Journal of Experimental Botany 56: 857-867.
Pieruschka R. Schurr U. Jensen M. Wolff W. F. Jahnke S.. 2006. Lateral diffusion of CO2 from shaded to illuminated leaf parts affects photosynthesis inside homobaric leaves. New Phytologist 169: 779-787.[CrossRef][ISI][Medline]
Reich P. B.. 2000. Do tall trees scale physiological heights?. Trends in Ecology and Evolution 15: 41-42.[CrossRef]
Rhizopoulou S. Psaras G. K.. 2003. Development and structure of drought-tolerant leaves of the Mediterranean shrub Capparis spinosa L. Annals of Botany 92: 1-7.
Roth I.. 1984. Stratification of tropical forests as seen in leaf structure Dr. W. Junk, The Hague, Netherlands.
Sack L. Frole K.. 2006. Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees. Ecology 87: 483-491.[CrossRef][ISI][Medline]
Sack L. Tyree M. T. Holbrook N. M.. 2005. Leaf hydraulic architecture correlates with regeneration irradiance in tropical rainforest trees. New Phytologist 167: 403-413.[CrossRef][ISI][Medline]
Sakai S. Momose K. Yumoto T. Nagamitsu T. Nagamasu H. Hamid A. A. Nakashizuka T.. 1999. Plant reproductive phenology over four years including an episode of general flowering in a lowland dipterocarp forest, Sarawak, Malaysia. American Journal of Botany 86: 1414-1436.
Sakai S. Nakashizuka T. Ichie T. Nomura M. Chong L.. 2002. Lambir hills canopy crane, Malaysia. In A. W. Mitchell, K. Secoy, and T. Jackson [eds.], The global canopy handbook 77-79 Global Canopy Programme, Oxford, UK.
Siebke K. Weis E.. 1995. Assimilation images of leaves of Glechoma hederacea: analysis of non-synchronous stomata related oscillations. Planta 196: 155-165.[ISI]
Soepadmo E. Saw L. G.. 2000. Tree flora of Saba and Sarawak, vol. 3 Ampang Press Sdn. Bhd., Kuala Lumpur, Malaysia.
Soepadmo E. Saw L. G. Chung R. C. K.. 2002. Tree flora of Saba and Sarawak, vol. 4 Ampang Press Sdn. Bhd., Kuala Lumpur, Malaysia.
Soepadmo E. Saw L. G. Chung R. C. K.. 2004. Tree flora of Saba and Sarawak, vol. 5 Ampang Press Sdn. Bhd., Kuala Lumpur, Malaysia.
Soepadmo E. Wong K. M.. 1995. Tree flora of Saba and Sarawak, vol. 1 Ampang Press Sdn. Bhd., Kuala Lumpur, Malaysia.
Soepadmo E. Wong K. M. Saw L. G.. 1996. Tree flora of Saba and Sarawak, vol. 2 Ampang Press Sdn. Bhd., Kuala Lumpur, Malaysia.
Terashima I.. 1992. Anatomy of non-uniform leaf photosynthesis. Photosynthesis Research 31: 195-212.[CrossRef][ISI]
Thomas S. C.. 2003. Comparative biology of tropical trees: a perspective from Pasoh. In T. Okuda, N. Manokaran, Y. Matsumoto, K. Niiyama, S. C. Thomas, and P. S. Ashton [eds.], Pasoh: ecology of a lowland rain forest in Southeast Asia 171-194 Springer-Verlag, Tokyo, Japan.
Thomas S. C. Bazzaz F. A.. 1999. Asymptotic height as a predictor of photosynthetic characteristics in Malaysian rain forest trees. Ecology 80: 1607-1622.[CrossRef][ISI]
Thomas S. C. Ickes K.. 1995. Ontogenetic changes in leaf size in Malaysian rain forest trees. Biotropica 27: 427-434.[CrossRef][ISI]
West J. D. Peak D. Peterson J. Q. Mott K. A.. 2005. Dynamics of stomatal patches for a single surface of Xanthium strumarium L. leaves observed with fluorescence and thermal image. Plant, Cell & Environment 28: 633-641.[CrossRef]
Whitmore T. C.. 1984. Tropical rain forest of the Far East, 2nd ed Oxford University Press, Oxford, UK.
Whitmore T. C.. 1998. An introduction to tropical rain forests, 2nd ed Oxford University Press, Oxford, UK.
Wylie R. B.. 1943. The role of the epidermis in foliar organization and its relations to the minor venation. American Journal of Botany 30: 273-280.[CrossRef][ISI]
Wylie R. B.. 1951. Principles of foliar organization shown by sun–shade leaves from ten species of deciduous dicotyledonous trees. American Journal of Botany 38: 355-361.[CrossRef][ISI]
Wylie R. B.. 1952. The bundle sheath extension in leaves of dicotyledons. American Journal of Botany 39: 645-651.[CrossRef][ISI]
Yoda K.. 1978. Three-dimensional distribution of light intensity in a tropical rain forest of West Malaysia. Malayan Nature Journal 30: 161-177.
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