The contrasting leaf functional traits between a karst forest and a nearby non-karst forest in south-west China
Pei-Li Fu
A B E , Shi-Dan Zhu C , Jiao-Lin Zhang A , Patrick M. Finnegan D , Yan-Juan Jiang A , Hua Lin A B , Ze-Xin Fan A B and Kun-Fang Cao C
+ Author Affiliations
- Author Affiliations
A CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Yunnan, 666303, China.
B Ailaoshan Station of Subtropical Forest Ecosystem Studies, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Jingdong, Yunnan, 676209, China.
C Plant Ecophysiology and Evolution Group, State Key Laboratory for Conservation and Utilisation of Subtropical Agro-bioresources and College of Forestry, Guangxi University, Nanning, Guangxi, 530004, China.
D School of Biological Sciences (M084), Faculty of Science, University of Western Australia, 35 Stirling Highway, Perth, WA 6009, Australia.
E Corresponding author. Email: fpl@xtbg.org.cn
Functional Plant Biology 46(10) 907-915 https://doi.org/10.1071/FP19103
Submitted: 15 April 2019 Accepted: 20 May 2019 Published: 26 June 2019
Abstract
Karst and non-karst forests occur in the same region in south-west China, but the soil water and mineral nutrients availability are different between the forests. Our hypothesis was that the leaves of karst trees would be better adapted to dry, nutrient-poor conditions than those of trees in a nearby non-karst forest. We compared the gas exchange, anatomical characteristics and mineral nutrient concentrations in leaves from 21 tree species in a tropical karst forest and 19 species in a nearby non-karst forest in south-west China. We found that the leaves of karst trees had higher P concentrations, photosynthetic capacity and water use efficiency, and greater adaxial and abaxial epidermis thickness than leaves of non-karst forest trees. Evergreen and deciduous trees differed more significantly in leaf functional traits in the karst forest than in the non-karst forest. The leaf palisade : spongy mesophyll thickness ratio was positively correlated with stomatal conductance and negatively correlated with photosynthetic water use efficiency in the karst forest but not in the non-karst forest. Our findings indicate that karst forest trees are more conservative in water use, whereas soil P deficiency could be a major limiting factor for the growth of non-karst forest trees.
Additional keywords: deciduous, evergreen, leaf anatomical traits, leaf P concentration, leaf palisade : spongy mesophyll thickness ratio.
References
Ackerly D (2004) Functional strategies of chaparral shrubs in relation to seasonal water deficit and disturbance. Ecological Monographs 74, 25–44.| Functional strategies of chaparral shrubs in relation to seasonal water deficit and disturbance.Crossref | GoogleScholarGoogle Scholar |
Baribault TW, Kobe RK, Finley AO (2012) Tropical tree growth is correlated with soil phosphorus, potassium, and calcium, though not for legumes. Ecological Monographs 82, 189–203.
| Tropical tree growth is correlated with soil phosphorus, potassium, and calcium, though not for legumes.Crossref | GoogleScholarGoogle Scholar |
Binks O, Meir P, Rowland L, da Costa ACL, Vasconcelos SS, de Oliveira AAR, Ferreira L, Christoffersen B, Nardini A, Mencuccini M (2016) Plasticity in leaf-level water relations of tropical rainforest trees in response to experimental drought. New Phytologist 211, 477–488.
| Plasticity in leaf-level water relations of tropical rainforest trees in response to experimental drought.Crossref | GoogleScholarGoogle Scholar | 27001030PubMed |
Bowman D, Prior LD (2005) Why do evergreen trees dominate the Australian seasonal tropics? Australian Journal of Botany 53, 379–399.
| Why do evergreen trees dominate the Australian seasonal tropics?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 |
Buckley TN, John GP, Scoffoni C, Sack L (2015) How does leaf anatomy influence water transport outside the xylem? Plant Physiology 168, 1616–1635.
| How does leaf anatomy influence water transport outside the xylem?Crossref | GoogleScholarGoogle Scholar | 26084922PubMed |
Cao K-F (2000) Leaf anatomy and chlorophyll concentration of 12 woody species in contrasting light conditions in a Bornean heath forest. Canadian Journal of Botany 78, 1245–1253.
| Leaf anatomy and chlorophyll concentration of 12 woody species in contrasting light conditions in a Bornean heath forest.Crossref | GoogleScholarGoogle Scholar |
Chen Y-J, Cao K-F, Schnitzer SA, Fan Z-X, Zhang J-L, Bongers F (2015) Water-use advantage for lianas over trees in tropical seasonal forests. New Phytologist 205, 128–136.
| Water-use advantage for lianas over trees in tropical seasonal forests.Crossref | GoogleScholarGoogle Scholar | 25264136PubMed |
Clements R, Sodhi NS, Schilthuizen M, Ng PKL (2006) Limestone karsts of Southeast Asia: imperiled arks of biodiversity. Bioscience 56, 733–742.
| Limestone karsts of Southeast Asia: imperiled arks of biodiversity.Crossref | GoogleScholarGoogle Scholar |
Du Y, Pan G, Li L, Hu Z, Wang X (2011) Leaf N/P ratio and nutrient reuse between dominant species and stands: predicting phosphorus deficiencies in Karst ecosystems, southwestern China. Environmental Earth Sciences 64, 299–309.
| Leaf N/P ratio and nutrient reuse between dominant species and stands: predicting phosphorus deficiencies in Karst ecosystems, southwestern China.Crossref | GoogleScholarGoogle Scholar |
Eamus D (1999) Ecophysiological traits of deciduous and evergreen woody species in the seasonally dry tropics. Trends in Ecology & Evolution 14, 11–16.
| Ecophysiological traits of deciduous and evergreen woody species in the seasonally dry tropics.Crossref | GoogleScholarGoogle Scholar |
Evans JR (1999) Leaf anatomy enables more equal access to light and CO2 between chloroplasts. New Phytologist 143, 93–104.
| Leaf anatomy enables more equal access to light and CO2 between chloroplasts.Crossref | GoogleScholarGoogle Scholar |
Fan D-Y, Jie S-L, Liu C-C, Zhang X-Y, Xu X-W, Zhang S-R, Xie Z-Q (2011) The trade-off between safety and efficiency in hydraulic architecture in 31 woody species in a karst area. Tree Physiology 31, 865–877.
| The trade-off between safety and efficiency in hydraulic architecture in 31 woody species in a karst area.Crossref | GoogleScholarGoogle Scholar | 21865304PubMed |
Fu P-L, Jiang Y-J, Wang A-Y, Brodribb TJ, Zhang J-L, Zhu S-D, Cao K-F (2012) Stem hydraulic traits and leaf water-stress tolerance are co-ordinated with the leaf phenology of angiosperm trees in an Asian tropical dry karst forest. Annals of Botany 110, 189–199.
| Stem hydraulic traits and leaf water-stress tolerance are co-ordinated with the leaf phenology of angiosperm trees in an Asian tropical dry karst forest.Crossref | GoogleScholarGoogle Scholar | 22585930PubMed |
Givnish TJ (2002) Adaptive significance of evergreen vs. deciduous leaves: solving the triple paradox. Silva Fennica 36, 703–743.
| Adaptive significance of evergreen vs. deciduous leaves: solving the triple paradox.Crossref | GoogleScholarGoogle Scholar |
Han WX, Fang JY, Reich PB, Ian Woodward F, Wang ZH (2011) Biogeography and variability of eleven mineral elements in plant leaves across gradients of climate, soil and plant functional type in China. Ecology Letters 14, 788–796.
| Biogeography and variability of eleven mineral elements in plant leaves across gradients of climate, soil and plant functional type in China.Crossref | GoogleScholarGoogle Scholar | 21692962PubMed |
He NP, Liu CC, Tian M, Li ML, Yang H, Yu GR, Guo DL, Smith MD, Yu Q, Hou JH (2018) Variation in leaf anatomical traits from tropical to cold-temperate forests and linkage to ecosystem functions. Functional Ecology 32, 10–19.
| Variation in leaf anatomical traits from tropical to cold-temperate forests and linkage to ecosystem functions.Crossref | GoogleScholarGoogle Scholar |
Huang W, Fu P-L, Jiang Y-J, Zhang J-L, Zhang S-B, Hu H, Cao K-F (2013) Differences in the responses of photosystem I and photosystem II of three tree species Cleistanthus sumatranus, Celtis philippensis and Pistacia weinmannifolia exposed to a prolonged drought in a tropical limestone forest. Tree Physiology 33, 211–220.
| Differences in the responses of photosystem I and photosystem II of three tree species Cleistanthus sumatranus, Celtis philippensis and Pistacia weinmannifolia exposed to a prolonged drought in a tropical limestone forest.Crossref | GoogleScholarGoogle Scholar | 23329334PubMed |
Kröber W, Heklau H, Bruelheide H (2015) Leaf morphology of 40 evergreen and deciduous broadleaved subtropical tree species and relationships to functional ecophysiological traits. Plant Biology 17, 373–383.
| Leaf morphology of 40 evergreen and deciduous broadleaved subtropical tree species and relationships to functional ecophysiological traits.Crossref | GoogleScholarGoogle Scholar | 25441614PubMed |
Li Q, Cao J, Yu L (2008) Biogeochemical effect of karst soil on the element concentrations in the leaves of two species of Flos Lonicerae. Plant, Soil and Environment 54, 486–492.
| Biogeochemical effect of karst soil on the element concentrations in the leaves of two species of Flos Lonicerae.Crossref | GoogleScholarGoogle Scholar |
Liu CC, Liu YG, Guo K, Fan DY, Li GG, Zheng YR, Yu LF, Yang R (2011) Effect of drought on pigments, osmotic adjustment and antioxidant enzymes in six woody plant species in karst habitats of southwestern China. Environmental and Experimental Botany 71, 174–183.
| Effect of drought on pigments, osmotic adjustment and antioxidant enzymes in six woody plant species in karst habitats of southwestern China.Crossref | GoogleScholarGoogle Scholar |
Liu C, Liu Y, Guo K, Wang S, Yang Y (2014) Concentrations and resorption patterns of 13 nutrients in different plant functional types in the karst region of south-western China. Annals of Botany 113, 873–885.
| Concentrations and resorption patterns of 13 nutrients in different plant functional types in the karst region of south-western China.Crossref | GoogleScholarGoogle Scholar | 24573643PubMed |
Nieuwenhuize J, Maas YEM, Middelburg JJ (1994) Rapid analysis of organic carbon and nitrogen in particulate materials. Marine Chemistry 45, 217–224.
| Rapid analysis of organic carbon and nitrogen in particulate materials.Crossref | GoogleScholarGoogle Scholar |
Niinemets Ü, Kull K (2005) Co-limitation of plant primary productivity by nitrogen and phosphorus in a species-rich wooded meadow on calcareous soils. Acta Oecologica 28, 345–356.
| Co-limitation of plant primary productivity by nitrogen and phosphorus in a species-rich wooded meadow on calcareous soils.Crossref | GoogleScholarGoogle Scholar |
Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, de Vos AC, Buchmann N, et al. (2013) New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61, 167–234.
| New handbook for standardised measurement of plant functional traits worldwide.Crossref | GoogleScholarGoogle Scholar |
Querejeta JI, Estrada-Medina H, Allen MF, Jiménez-Osornio JJ (2007) Water source partitioning among trees growing on shallow karst soils in a seasonally dry tropical climate. Oecologia 152, 26–36.
| Water source partitioning among trees growing on shallow karst soils in a seasonally dry tropical climate.Crossref | GoogleScholarGoogle Scholar | 17216213PubMed |
R Core Team (2018) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing, Vienna, Austria) Available at https://www.R-project.org/
Rossatto DR, Carvalho FA, Haridasan M (2015) Soil and leaf nutrient concentration of tree species support deciduous forests on limestone outcrops as a eutrophic ecosystem. Acta Botanica Brasílica 29, 231–238.
| Soil and leaf nutrient concentration of tree species support deciduous forests on limestone outcrops as a eutrophic ecosystem.Crossref | GoogleScholarGoogle Scholar |
Sack L, Frole K (2006) Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees. Ecology 87, 483–491.
| Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees.Crossref | GoogleScholarGoogle Scholar | 16637372PubMed |
Schwinning S (2008) The water relations of two evergreen tree species in a karst savanna. Oecologia 158, 373–383.
| The water relations of two evergreen tree species in a karst savanna.Crossref | GoogleScholarGoogle Scholar | 18830633PubMed |
Tomlinson KW, Poorter L, Sterck FJ, Borghetti F, Ward D, de Bie S, van Langevelde F (2013) Leaf adaptations of evergreen and deciduous trees of semi-arid and humid savannas on three continents. Journal of Ecology 101, 430–440.
| Leaf adaptations of evergreen and deciduous trees of semi-arid and humid savannas on three continents.Crossref | GoogleScholarGoogle Scholar |
Vitousek PM, Sanford RL (1986) Nutrient cycling in moist tropical forest. Annual Review of Ecology and Systematics 17, 137–167.
| Nutrient cycling in moist tropical forest.Crossref | GoogleScholarGoogle Scholar |
Vogelmann TC (1993) Plant tissue optics. Annual Review of Plant Biology 44, 231–251.
| Plant tissue optics.Crossref | GoogleScholarGoogle Scholar |
Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15, 1–19.
| The fate of phosphorus during pedogenesis.Crossref | GoogleScholarGoogle Scholar |
Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biological Reviews of the Cambridge Philosophical Society 81, 259–291.
| Bivariate line-fitting methods for allometry.Crossref | GoogleScholarGoogle Scholar | 16573844PubMed |
Wei L-Y, Zeng D-J, Lv S-H, Zhang JL, Jiao JF, You YM, Li XK (2011) Variation in structural and physiological leaf traits of eight species in karst desertification area of China. Photosynthetica 49, 43–47.
| Variation in structural and physiological leaf traits of eight species in karst desertification area of China.Crossref | GoogleScholarGoogle Scholar |
Westoby M, Wright IJ (2006) Land-plant ecology on the basis of functional traits. Trends in Ecology & Evolution 21, 261–268.
| Land-plant ecology on the basis of functional traits.Crossref | GoogleScholarGoogle Scholar |
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, et al. (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.
| The worldwide leaf economics spectrum.Crossref | GoogleScholarGoogle Scholar | 15103368PubMed |
Yuan D-X (1991) ‘Karst of China.’ (Geological Publishing House: Beijing). [In Chinese]
Zhang G-C (2006) A research on soil principal nutrient components of typical forest communities in Xishuangbanna. Master’s thesis, Graduate University of Chinese Academy of Sciences, Beijing, China. [In Chinese]
Zhang J-L, Zhu J-J, Cao K-F (2007) Seasonal variation in photosynthesis in six woody species with different leaf phenology in a valley savanna in southwestern China. Trees 21, 631–643.
| Seasonal variation in photosynthesis in six woody species with different leaf phenology in a valley savanna in southwestern China.Crossref | GoogleScholarGoogle Scholar |
Zhang JL, Meng LZ, Cao KF (2009) Sustained diurnal photosynthetic depression in uppermost-canopy leaves of four dipterocarp species in the rainy and dry seasons: does photorespiration play a role in photoprotection? Tree Physiology 29, 217–228.
| Sustained diurnal photosynthetic depression in uppermost-canopy leaves of four dipterocarp species in the rainy and dry seasons: does photorespiration play a role in photoprotection?Crossref | GoogleScholarGoogle Scholar | 19203947PubMed |
Zhang J-L, Poorter L, Cao K-F (2012) Productive leaf functional traits of Chinese savanna species. Plant Ecology 213, 1449–1460.
| Productive leaf functional traits of Chinese savanna species.Crossref | GoogleScholarGoogle Scholar |
Zhu H, Wang H, Li B, Sirirugsa P (2003) Biogeography and floristic affinities of the limestone flora in Southern Yunnan, China. Annals of the Missouri Botanical Garden 90, 444–465.
| Biogeography and floristic affinities of the limestone flora in Southern Yunnan, China.Crossref | GoogleScholarGoogle Scholar |
Zhu H, Cao M, Hu HB (2006) Geological history, flora, and vegetation of Xishuangbanna, southern Yunnan, China. Biotropica 38, 310–317.
| Geological history, flora, and vegetation of Xishuangbanna, southern Yunnan, China.Crossref | GoogleScholarGoogle Scholar |
Zhu SD, Chen YJ, Fu PL, Cao KF (2017) Different hydraulic traits of woody plants from tropical forests with contrasting soil water availability. Tree Physiology 37, 1469–1477.
| Different hydraulic traits of woody plants from tropical forests with contrasting soil water availability.Crossref | GoogleScholarGoogle Scholar | 28985366PubMed |
