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Plant function and evolutionary biology
RESEARCH ARTICLE

Stomatal size and density trade-off varies with leaf phenology and species shade tolerance in a South Asian moist tropical forest

Abdullah Al-Nur Shanto Rahman A , Mizanur Rahman https://orcid.org/0000-0001-9011-2011 A , Mehedi Hasan Shimanto A , Mohammad Golam Kibria https://orcid.org/0000-0002-8644-6606 A and Mahmuda Islam https://orcid.org/0000-0003-3149-6582 A *
+ Author Affiliations
- Author Affiliations

A Department of Forestry and Environmental Science, Shahjalal University of Science and Technology, Sylhet 3114, Bangladesh.

* Correspondence to: mahmuda-fes@sust.edu

Handling Editor: Wieland Fricke

Functional Plant Biology 49(3) 307-318 https://doi.org/10.1071/FP21159
Submitted: 22 May 2021  Accepted: 18 January 2022   Published: 8 February 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

The density and guard cell length of stomata regulate the physiological processes in plants. Yet, the variation of stomatal characteristics among different functional groups of trees is not been well understood. Particularly, a comprehensive understanding of stomatal behaviour in Bangladeshi moist forest trees is lacking. The study investigated how abaxial stomatal density (SD) and guard cell length (GCL) vary among tree functional types and leaf phenological groups in a moist tropical forest of Bangladesh. Cluster dendrogram revealed three groups of species based on SD and GCL. The independent sample t-test showed that there was a significant difference in SD between evergreen and deciduous tree species (t = 4.18, P < 0.001) but no significant difference in GCL between the two phenological groups. ANOVA revealed no significant difference in SD among the light demanding, intermediate shade tolerant and shade tolerant species (F = 0.76, P = 0.47). However, GCL significantly differed among the three functional groups (F = 3.3, P < 0.05). Maximum theoretical stomatal conductance (gmax) varied between evergreen and deciduous species but did not vary with species shade tolerance. In general, there was a significant trade-off between SD and GCL. However, the inverse relationship was stronger in deciduous and shade tolerant species than in evergreen and shade intolerant species. Leaf dry matter content was positively related with SD and negatively related with GCL. Specific leaf area and leaf thickness were not related to the stomatal traits. Our analyses suggest that leaf phenology and species shade tolerance need to be considered while estimating gas exchange through the stomata in tropical moist forests.

Keywords: Bangladesh, functional groups, gmax, guard-cell length, leaf traits, stomatal density, stomatal traits, tropical forests.


References

Abrams MD, Kubiske ME (1990) Leaf structural characteristics of 31 hardwood and conifer tree species in central Wisconsin: Influence of light regime and shade-tolerance rank. Forest Ecology and Management 31, 245–253.
Leaf structural characteristics of 31 hardwood and conifer tree species in central Wisconsin: Influence of light regime and shade-tolerance rank.Crossref | GoogleScholarGoogle Scholar |

Al Afas N, Marron N, Ceulemans R (2007) Variability in Populus leaf anatomy and morphology in relation to canopy position, biomass production, and varietal taxon. Annals of Forest Science 64, 521–532.
Variability in Populus leaf anatomy and morphology in relation to canopy position, biomass production, and varietal taxon.Crossref | GoogleScholarGoogle Scholar |

Basu S, Ramegowda V, Kumar A, Pereira A (2016) Plant adaptation to drought stress [version 1; peer review: 3 approved]. F1000Research 5, 1554
Plant adaptation to drought stress [version 1; peer review: 3 approved].Crossref | GoogleScholarGoogle Scholar |

Bertolino LT, Caine RS, Gray JE (2019) Impact of stomatal density and morphology on water-use efficiency in a changing world. Frontiers in Plant Science 10, 225
Impact of stomatal density and morphology on water-use efficiency in a changing world.Crossref | GoogleScholarGoogle Scholar | 30894867PubMed |

Buckley TN (2005) The control of stomata by water balance. New Phytologist 168, 275–292.
The control of stomata by water balance.Crossref | GoogleScholarGoogle Scholar |

Camargo MAB, Marenco RA (2011) Density, size and distribution of stomata in 35 rainforest tree species in Central Amazonia. Acta Amazonica 41, 205–212.
Density, size and distribution of stomata in 35 rainforest tree species in Central Amazonia.Crossref | GoogleScholarGoogle Scholar |

Ducrey M (1992) Variation in leaf morphology and branching pattern of some tropical rain forest species from Guadeloupe (French West Indies) under semi-controlled light conditions. Annales des Sciences Forestières 49, 553–570.
Variation in leaf morphology and branching pattern of some tropical rain forest species from Guadeloupe (French West Indies) under semi-controlled light conditions.Crossref | GoogleScholarGoogle Scholar |

Elias P (1995) Stomata density and size of apple trees growing in irrigated and non irrigated conditions. Biologia 50, 115–118.

Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species.Crossref | GoogleScholarGoogle Scholar | 24306196PubMed |

Ferris R, Taylor G (1994) Stomatal characteristics of four native herbs following exposure to elevated CO2. Annals of Botany 73, 447–453.
Stomatal characteristics of four native herbs following exposure to elevated CO2.Crossref | GoogleScholarGoogle Scholar |

Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proceedings of the National Academy of Sciences of the United States of America 106, 10343–10347.
Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time.Crossref | GoogleScholarGoogle Scholar | 19506250PubMed |

Garnier E, Shipley B, Roumet C, Laurent G (2001) A standardized protocol for the determination of specific leaf area and leaf dry matter content. Functional Ecology 15, 688–695.
A standardized protocol for the determination of specific leaf area and leaf dry matter content.Crossref | GoogleScholarGoogle Scholar |

Hassan MM (1994) Forest soils of Bangladesh. Bangladesh Journal of Forest Science (Bangladesh) 23, 1–11.

Hasselquist NJ, Allen MF, Santiago LS (2010) Water relations of evergreen and drought-deciduous trees along a seasonally dry tropical forest chronosequence. Oecologia 164, 881–890.
Water relations of evergreen and drought-deciduous trees along a seasonally dry tropical forest chronosequence.Crossref | GoogleScholarGoogle Scholar | 20658152PubMed |

Henry C, John GP, Pan R, Bartlett MK, Fletcher LR, Scoffoni C, Sack L (2019) A stomatal safety-efficiency trade-off constrains responses to leaf dehydration. Nature Communications 10, 3398
A stomatal safety-efficiency trade-off constrains responses to leaf dehydration.Crossref | GoogleScholarGoogle Scholar | 31363097PubMed |

Holdridge LR (1967) ‘Life zone ecology.’ (Tropical Science Center: San Jose)

Hong T, Lin H, He D (2018) Characteristics and correlations of leaf stomata in different Aleurites Montana provenances. PLoS ONE 13, e0208899
Characteristics and correlations of leaf stomata in different Aleurites Montana provenances.Crossref | GoogleScholarGoogle Scholar | 30562378PubMed |

Islam M, Rahman M, Bräuning A (2018a) Long-term hydraulic adjustment of three tropical moist forest tree species to changing climate. Frontiers in Plant Science 9, 1761
Long-term hydraulic adjustment of three tropical moist forest tree species to changing climate.Crossref | GoogleScholarGoogle Scholar | 30564255PubMed |

Islam M, Rahman M, Bräuning A (2018b) Xylem anatomical responses of diffuse porous Chukrasia tabularis to climate in a South Asian moist tropical forest. Forest Ecology and Management 412, 9–20.
Xylem anatomical responses of diffuse porous Chukrasia tabularis to climate in a South Asian moist tropical forest.Crossref | GoogleScholarGoogle Scholar |

Islam M, Rahman M, Gebrekirstos A, Bräuning A (2021) Tree-ring δ18O climate signals vary among tree functional types in South Asian tropical moist forests. Science of the Total Environment 756, 143939
Tree-ring δ18O climate signals vary among tree functional types in South Asian tropical moist forests.Crossref | GoogleScholarGoogle Scholar |

Jarvis AJ, Mansfield TA, Davies WJ (1999) Stomatal behaviour, photosynthesis and transpiration under rising CO2. Plant, Cell & Environment 22, 639–648.
Stomatal behaviour, photosynthesis and transpiration under rising CO2.Crossref | GoogleScholarGoogle Scholar |

Kardiman R, Ræbild A (2018) Relationship between stomatal density, size and speed of opening in Sumatran rainforest species. Tree Physiology 38, 696–705.
Relationship between stomatal density, size and speed of opening in Sumatran rainforest species.Crossref | GoogleScholarGoogle Scholar | 29186586PubMed |

Khan A, Zheng J, Tan DK, Khan A, Akhtar K, Kong X, Munsif F, Iqbal A, Afridi MZ, Ullah A, Fahad S, Zhou R (2019) Changes in leaf structural and functional characteristics when changing planting density at different growth stages alters cotton lint yield under a new planting model. Agronomy 9, 859
Changes in leaf structural and functional characteristics when changing planting density at different growth stages alters cotton lint yield under a new planting model.Crossref | GoogleScholarGoogle Scholar |

Lawson T, Blatt MR (2014) Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiology 164, 1556–1570.
Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency.Crossref | GoogleScholarGoogle Scholar | 24578506PubMed |

Li Y, Johnson DA, Su Y, Cui J, Zhang T (2005) Specific leaf area and leaf dry matter content of plants growing in sand dunes. Botanical Bulletin of Academia Sinica 46, 127–134.
Specific leaf area and leaf dry matter content of plants growing in sand dunes.Crossref | GoogleScholarGoogle Scholar |

Liu C, He N, Zhang J, Li Y, Wang Q, Sack L, Yu G (2018) Variation of stomatal traits from cold temperate to tropical forests and association with water use efficiency. Functional Ecology 32, 20–28.
Variation of stomatal traits from cold temperate to tropical forests and association with water use efficiency.Crossref | GoogleScholarGoogle Scholar |

Liu C, Li Y, Xu L, Chen Z, He N (2019) Variation in leaf morphological, stomatal, and anatomical traits and their relationships in temperate and subtropical forests. Scientific Reports 9, 5803
Variation in leaf morphological, stomatal, and anatomical traits and their relationships in temperate and subtropical forests.Crossref | GoogleScholarGoogle Scholar | 30967600PubMed |

Loranger J, Shipley B (2010) Interspecific covariation between stomatal density and other functional leaf traits in a local flora. Botany 88, 30–38.
Interspecific covariation between stomatal density and other functional leaf traits in a local flora.Crossref | GoogleScholarGoogle Scholar |

Luomala E-M, Laitinen K, Sutinen S, Kellomäki S, Vapaavuori E (2005) Stomatal density, anatomy and nutrient concentrations of Scots pine needles are affected by elevated CO2 and temperature. Plant, Cell & Environment 28, 733–749.
Stomatal density, anatomy and nutrient concentrations of Scots pine needles are affected by elevated CO2 and temperature.Crossref | GoogleScholarGoogle Scholar |

McElwain JC, Yiotis C, Lawson T (2016) Using modern plant trait relationships between observed and theoretical maximum stomatal conductance and vein density to examine patterns of plant macroevolution. New Phytologist 209, 94–103.
Using modern plant trait relationships between observed and theoretical maximum stomatal conductance and vein density to examine patterns of plant macroevolution.Crossref | GoogleScholarGoogle Scholar |

Nishat A, Huq SMI, Barua SP, Reza AHMA, Khan ASM (Eds) (2002) ‘Bio-ecological zones of Bangladesh.’ (IUCN Bangladesh Country Office: Dhaka)

Onwuemet IC, Johnston M (2000) Influence of shade on stomatal density, leaf size and other leaf characteristics in the major tropical root crops, tannia, sweet potato, yam, cassava and taro. Experimental Agriculture 36, 509–516.
Influence of shade on stomatal density, leaf size and other leaf characteristics in the major tropical root crops, tannia, sweet potato, yam, cassava and taro.Crossref | GoogleScholarGoogle Scholar |

Orlović S, Guzina V, Krstić B, Merkulov L (1998) Genetic variability in anatomical, physiological and growth characteristics of hybrid poplar (Populus × euramericana Dode (Guinier)) and eastern cottonwood (Populus deltoides Bartr.) clones. Silvae Genetica 47, 183–190.

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 | 16657461PubMed |

Peel JR, Mandujano Sanchez MC, Lopez Portillo J, Golubov J (2017) Stomatal density, leaf area and plant size variation of Rhizophora mangle (Malpighiales: Rhizophoraceae) along a salinity gradient in the Mexican Caribbean. Revista de Biología Tropical 65, 701–712.
Stomatal density, leaf area and plant size variation of Rhizophora mangle (Malpighiales: Rhizophoraceae) along a salinity gradient in the Mexican Caribbean.Crossref | GoogleScholarGoogle Scholar |

Pemadasa MA (1979) Movements of abaxial and adaxial stomata. New Phytologist 82, 69–80.
Movements of abaxial and adaxial stomata.Crossref | GoogleScholarGoogle Scholar |

Poorter L, Bongers F (2006) Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87, 1733–1743.
Leaf traits are good predictors of plant performance across 53 rain forest species.Crossref | GoogleScholarGoogle Scholar | 16922323PubMed |

Poorter L, Castilho CV, Schietti J, Oliveira RS, Costa FRC (2018) Can traits predict individual growth performance? A test in a hyperdiverse tropical forest. New Phytologist 219, 109–121.
Can traits predict individual growth performance? A test in a hyperdiverse tropical forest.Crossref | GoogleScholarGoogle Scholar |

R Development Core Team (2020) R: a language and environment for statistical computing. (R Foundation for Statistical Computing: Vienna, Austria) Available at http://www.r-project.org/

Rahman M, Islam M, Bräuning A (2019) Species-specific growth resilience to drought in a mixed semi-deciduous tropical moist forest in South Asia. Forest Ecology and Management 433, 487–496.
Species-specific growth resilience to drought in a mixed semi-deciduous tropical moist forest in South Asia.Crossref | GoogleScholarGoogle Scholar |

Rahman M, Billah M, Rahman MO, Datta D, Ahsanuzzaman M, Islam M (2021) Disentangling the role of competition, light interception, and functional traits in tree growth rate variation in South Asian tropical moist forests. Forest Ecology and Management 483, 118908
Disentangling the role of competition, light interception, and functional traits in tree growth rate variation in South Asian tropical moist forests.Crossref | GoogleScholarGoogle Scholar |

Schlüter U, Muschak M, Berger D, Altmann T (2003) Photosynthetic performance of an Arabidopsis mutant with elevated stomatal density (sdd1-1) under different light regimes. Journal of Experimental Botany 54, 867–874.
Photosynthetic performance of an Arabidopsis mutant with elevated stomatal density (sdd1-1) under different light regimes.Crossref | GoogleScholarGoogle Scholar | 12554730PubMed |

Selaya NG, Anten NPR (2010) Leaves of pioneer and later-successional trees have similar lifetime carbon gain in tropical secondary forest. Ecology 91, 1102–1113.
Leaves of pioneer and later-successional trees have similar lifetime carbon gain in tropical secondary forest.Crossref | GoogleScholarGoogle Scholar | 20462124PubMed |

Sobuj NA, Rahman M (2011a) Assessment of plant diversity in Khadimnagar National Park of Bangladesh. International Journal of Environmental Sciences 2, 79–91.

Sobuj NA, Rahman M (2011b) Comparison of plant diversity of natural forest and plantations of Rema-Kalenga Wildlife Sanctuary of Bangladesh. Journal of Forest Science 27, 127–134.

Tanaka Y, Sugano SS, Shimada T, Hara-Nishimura I (2013) Enhancement of leaf photosynthetic capacity through increased stomatal density in Arabidopsis. New Phytologist 198, 757–764.
Enhancement of leaf photosynthetic capacity through increased stomatal density in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Tian M, Yu G, He N, Hou J (2016) Leaf morphological and anatomical traits from tropical to temperate coniferous forests: mechanisms and influencing factors. Scientific Reports 6, 19703
Leaf morphological and anatomical traits from tropical to temperate coniferous forests: mechanisms and influencing factors.Crossref | GoogleScholarGoogle Scholar | 26796339PubMed |

Ticha I (1982) Photosynthetic characteristics during ontogenesis of leaves. 7. Stomata density and sizes. Photosynthetica 16, 375–471.

Voleníková M, Tichá I (2001) Insertion profiles in stomatal density and sizes in Nicotiana tabacum L. plantlets. Biologia Plantarum 44, 161–165.
Insertion profiles in stomatal density and sizes in Nicotiana tabacum L. plantlets.Crossref | GoogleScholarGoogle Scholar |

Wang R, Yu G, He N, Wang Q, Zhao N, Xu Z, Ge J (2015) Latitudinal variation of leaf stomatal traits from species to community level in forests: Linkage with ecosystem productivity. Scientific Reports 5, 14454
Latitudinal variation of leaf stomatal traits from species to community level in forests: Linkage with ecosystem productivity.Crossref | GoogleScholarGoogle Scholar | 26403303PubMed |

Wu S, Zhao B (2017) Using clear nail polish to make Arabidopsis epidermal impressions for measuring the change of stomatal aperture size in immune response. In ‘Plant pattern recognition receptors: methods and protocols’. (Eds L Shan, P He) pp. 243–248. (Springer New York: New York, NY)
| Crossref |

Xu K, Guo L, Ye H (2019) A naturally optimized mass transfer process: the stomatal transpiration of plant leaves. Journal of Plant Physiology 234–235, 138–144.
A naturally optimized mass transfer process: the stomatal transpiration of plant leaves.Crossref | GoogleScholarGoogle Scholar | 30798115PubMed |

Yan Y-M, Fan Z-X, Fu P-L, Chen H, Lin L-X (2021) Size dependent associations between tree diameter growth rates and functional traits in an Asian tropical seasonal rainforest. Functional Plant Biology 48, 231–240.
Size dependent associations between tree diameter growth rates and functional traits in an Asian tropical seasonal rainforest.Crossref | GoogleScholarGoogle Scholar | 33119999PubMed |

Zhang L, Wang S, Yang X, Cui X, Niu H (2021) An intrinsic geometric constraint on morphological stomatal traits. Frontiers in Plant Science 12, 658702
An intrinsic geometric constraint on morphological stomatal traits.Crossref | GoogleScholarGoogle Scholar | 33968115PubMed |