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Extended Leaf Senescence Promotes Carbon Gain and Nutrient Resorption: Importance of Maintaining Winter Photosynthesis in Subtropical Forests

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Extended Leaf Senescence Promotes Carbon Gain and Nutrient Resorption: Importance of Maintaining Winter Photosynthesis in Subtropical Forests Oecologia DOI 10.1007/s00442-013-2672-1 PHYSIOLOGICAL ECOLOGY - ORIGINAL RESEARCH Extended leaf senescence promotes carbon gain and nutrient resorption: importance of maintaining winter photosynthesis in subtropical forests Yong-Jiang Zhang • Qiu-Yun Yang • David W. Lee • Guillermo Goldstein • Kun-Fang Cao Received: 18 September 2012 / Accepted: 17 April 2013 Ó Springer-Verlag Berlin Heidelberg 2013 Abstract The relative advantages of being deciduous or the hypothesis that anthocyanin accumulation and/or evergreen in subtropical forests and the relationship between extended leaf senescence help in nutrient resorption. Sub- leaf phenology and nutrient resorption efficiency are not well stantial winter carbon gain and efficient nutrient resorption understood. The most successful deciduous species (Lyonia may partially explain the success of L. ovalifolia versus that ovalifolia) in an evergreen-dominated subtropical montane of the other deciduous species in this subtropical forest. The cloud forest in southwest (SW) China maintains red se- importance of maintaining a positive carbon balance for nescing leaves throughout much of the winter. The aim of ecological success in this forest also provides indirect evi- this study was to investigate whether red senescing leaves of dence for the dominance of evergreen species in the sub- this species were able to assimilate carbon in winter, to infer tropical forests of SW China. the importance of maintaining a positive winter carbon balance in subtropical forests, and to test whether an exten- Keywords Deciduousness Á Leaf phenology Á Carbon ded leaf life span is associated with enhanced nutrient balance Á Anthocyanin Á Cloud forest resorption and yearly carbon gain. The red senescing leaves of L. ovalifolia assimilated considerable carbon during part of the winter, resulting in a higher yearly carbon gain than co- Introduction occurring deciduous species. Its leaf N and P resorption efficiency was higher than for co-occurring non-anthocyanic Deciduous trees are defined as trees that remain completely deciduous species that dropped leaves in autumn, supporting leafless for a certain period of time during the year (for a Communicated by Andrea Polle. Y.-J. Zhang Á Q.-Y. Yang Á K.-F. Cao (&) D. W. Lee Key Laboratory of Tropical Forest Ecology, Xishuangbanna Department of Biological Sciences, Florida International Tropical Botanical Garden, Chinese Academy of Sciences, University, Miami, FL 33199, USA 666303 Mengla, Yunnan, China e-mail: [email protected] G. Goldstein Departamento de Ecologia, Genetica y Evolucion, Facultad de Y.-J. Zhang Á G. Goldstein (&) Ciencias Exactas y Naturales, Universidad de Buenos Aires, Department of Biology, University of Miami, PO Box 249118, Ciudad Universitaria, Nun˜ez, Buenos Aires, Argentina Coral Gables, FL 33124, USA e-mail: [email protected] K.-F. Cao State Key Laboratory for Conservation and Utilization Y.-J. Zhang Á Q.-Y. Yang of Subtropical Agro-bioresources, The Key Laboratory Ailaoshan Station for Subtropical Forest Ecosystem Studies, of Ministry of Education for Microbial and Plant Genetic Chinese Academy of Sciences, 676200 Jingdong, Yunnan, China Engineering, and College of Forestry, Guangxi University, 530004 Nanning, Guangxi, China Y.-J. Zhang Graduate University of Chinese Academy of Sciences, 100039 Beijing, China 123 Oecologia review, see Kikuzawa and Lechowicz 2011). The habit of anthocyanins reduce photo-damage to protect the physio- deciduousness originated in the Cretaceous period when logical processes of nutrient resorption (Feild et al. 2001; angiosperms spread from low-latitude to mid-latitude Lee et al. 2003; Hoch et al. 2003). That contention is based regions (Axelrod 1966; Wolfe 1987). Deciduousness is on the reasoning that free radicals induced by photo-oxi- thought to be an adaptation to the seasonal low tempera- dation oxidize the products of chlorophyll degradation tures in the mid-latitude region of the northern hemisphere, (Matile et al. 1999), thereby interrupting the resorption or to the seasonal drought in some tropical or subtropical process of nutrients. Three anthocyanic deciduous species regions (Givnish 2002). Being deciduous avoids the recycled more N than acyanic mutants (Hoch et al. 2003), investment in low-temperature (or drought) resistance (e.g., and leaf anthocyanin content was negatively correlated high nitrogen partitioning to structural components; with leaf N concentration in senescent leaves of deciduous increasing osmo-regulation and membrane phospholipids species in New England, USA (Lee et al. 2003), supporting in acclimation), at a cost of a relatively short period of this hypothesis. Photo-protection by anthocyanins will carbon assimilation (Givnish 2002). Therefore, whether allow senescing leaves to maintain some degree of carbon evergreen trees are able to assimilate considerable carbon assimilation, at least during the early stage of leaf senes- during the unfavorable season is an important factor in cence. The carbon assimilation of senescing leaves has not determining the relative dominance of evergreen or been investigated, probably because the senescence process deciduous trees in a forest ecosystem. The influence of an is usually short. Carbon assimilation by senescing leaves, unfavorable season on tree carbon assimilation has been however, could be of importance to some deciduous spe- investigated in tropical, temperate, boreal, and Mediterra- cies with prolonged senescence. nean forests/shrublands (Malhi et al. 1999; Oliveira and Lyonia ovalifolia Drude var. ovalifolia (Ericaceae), the Penuelas 2004; Taneda and Tateno 2005), but not in sub- most common deciduous tree species in the subtropical tropical forests. In the Asian subtropics, tree photosynthesis evergreen broadleaf forest of Ailao Mountain in SW China might be negatively affected by low temperatures in winter (Qiu and Xie 1998), maintains red leaves on trees for a and high cloud cover (low incoming solar radiation) in long period in winter (more than 2 months) when other summer. The advantages of being deciduous or evergreen deciduous trees are leafless. The objectives of this study in subtropical forests are poorly understood. were: (1) to determine the winter photosynthetic perfor- China harbors the largest area of subtropical broadleaf mance of Lyonia ovalifolia red senescing leaves; (2) to forests in the world (Wu 1980; Song et al. 2005). Ever- infer the relative contribution of winter carbon gain to the green broadleaf trees dominate the forests from 1,000 to yearly carbon balance of L. ovalifolia and the importance 2,600 m in the subtropical area of southwest (SW) China, of maintaining positive winter carbon balances for trees in while subtropical forests from southeast (SE) China at subtropical forests of SW China; and (3) to test whether L. similar elevations are dominated by deciduous trees (Wu ovalifolia with extended leaf senescence and anthocyanin 1980). The subtropical area in SW China has milder win- accumulation has higher nutrient resorption efficiency than ters than SE China because the Tibetan Plateau and Yun- co-occurring deciduous species without extended leaf nan–Guizhou Plateau prevent cold fronts from moving senescence and anthocyanin accumulation. south in western China. If the medium and high elevation subtropical forests in SW China are dominated by ever- green broadleaf trees owing to a mild winter, it is reason- Materials and methods able to hypothesize that some coexisting deciduous species are subjected to selective pressures to extend their leaf life Study site spans to partially utilize autumn and winter solar radiation. Many deciduous species accumulate anthocyanins dur- This study was performed in an evergreen broadleaf forest ing leaf senescence (e.g., Matile 2000; Feild et al. 2001; at the Ailaoshan Station for Subtropical Evergreen Lee et al. 2003). There is some evidence that anthocyanins Broadleaf Forest Ecosystem Studies (24°320N, 101°010E, in leaves can act as a light-attenuation screen (Feild et al. elevation 2,460 m), located at Ailao Mountain, Jingdong 2001; Gould et al. 2002; Gould 2004; Hughes et al. 2005) County, Yunnan Province, SW China. The station is a or antioxidants (Hoch et al. 2001; Neill et al. 2002; Neill member of the Chinese Ecosystem Research Network and Gould 2003; Kytridis and Manetas 2006) to reduce (CERN), and the Chinese National Ecosystem Observation photo-inhibition and photo-oxidation. Since the leaves will and Research Network (CEORN). Annual average tem- senesce anyway, anthocyanin synthesis for photo-protec- perature at the study site is 11.3 °C, and annual average tion would be costly and without an apparent adaptive precipitation is 1,931 mm (5-year average; Qiu and Xie value. One hypothesis explaining the adaptive significance 1998). The weather in 2009, when we conducted the of anthocyanin synthesis in senescing leaves is that present study, is shown in Fig. 1. Sunshine duration in the 123 Oecologia 400 30 D. Don, Betula alnoides Hamilt, Populus yunnanensis Dode, (a) Rainfall Clethra brammeriana Hand.-Mazz.) were also studied for 25 Maximum comparison. Leaves of these four deciduous species turn 300 C) 20 o yellow and drop in October or early November. Sun-exposed trees (2–3 m high) on the forest edges were chosen for the 15 200 Mean physiological measurements and to minimize shading 10 effects. We performed the physiological measurements from April 2009 to February 2010. Rainfall (mm) Rainfall 5 100 Minimum Air temperature ( Air temperature 0 Gas exchange
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