Detection of the different characteristics of year-to-year variation in foliage phenology among deciduous broad-leaved tree species by using daily continuous canopy surface images
Introduction
Changes in plant phenology, such as advanced or delayed timings of the start of leaf-expansion (SLE) and the end of leaf-fall (ELF) (e.g., Cong et al., 2013, Jeong et al., 2011, Zeng et al., 2011), may alter ecosystem functions such as water, energy, and carbon exchanges between the land surface and the atmosphere in terrestrial ecosystems by changing physical properties (e.g., solar albedo and evapotranspiration) and biological processes (e.g., CO2 uptake by photosynthesis) (Barford et al., 2001, Churkina et al., 2005, Lawrence and Slingo, 2004a, Lawrence and Slingo, 2004b, Myneni et al., 1997). Long-term trends of advanced SLE and delayed ELF showed different characteristics among each region at a continental scale. For example, the long-term trend of delayed ELF (e.g., 2.2 days per decade from 1986 to 2005 in China [Chen and Xu, 2012], and 1.6 days per decade from 1959 to 1993 in Europe [Menzel and Fabian, 1999]) was slower than the long-term trend of advanced SLE (e.g., 4 days per decade from 1986 to 2005 in China [Chen and Xu, 2012], and 2.0 days per decade from 1959 to 1993 in Europe [Menzel and Fabian, 1999]) in temperate climate regions across Europe and China, whereas the long-term trend of delayed ELF (1.6 days per decade from 1953 to 2000 [Matsumoto et al., 2003] and 2.7 days per decade from 1961 to 2011 [Nagai et al., 2013a]) was faster than the long-term trend of advanced SLE (0.9 days per decade from 1953 to 2000 [Matsumoto et al., 2003]) in Japan. These local phenological changes may alter ecosystem services, such as carbon stock and climate control, on a regional to a global scale (Peñuelas et al., 2009).
Sensitivity of foliage phenology under environmental changes shows different characteristics among temperate deciduous tree species (Fu et al., 2013, Morin et al., 2010, Vitasse et al., 2009a, Vitasse et al., 2009b). For instance, Vitasse et al. (2009a) reported that the phenological sensitivity of leaf unfolding to temperature for oak was stronger than that for beech in southern France. These differences in species-specific phenological response to environmental changes may affect the competition for light among the tree species, and it may also therefore affect the distribution of tree species in temperate mixed-species deciduous forests (Kramer et al., 2000). Urbanski et al. (2007) suggested that the change of spatial distribution of tree species might alter the net ecosystem production in a mixed deciduous forest. These reports suggest that consideration of the differences in the species-specific phenological response to environmental change in each region would provide us with useful information to predict the response of ecosystem services to rapid environmental change.
Recently, automatically captured digital camera images have been applied to continuous phenological observations because such observations make it possible to collect automated data at high temporal resolution in multiple ecosystems with low operating costs (e.g., Alberton et al., 2014, Crimmins and Crimmins, 2008, Migliavacca et al., 2011, Richardson et al., 2007, Sonnentag et al., 2012). Temporal changes in RGB color information (the digital intensity value of red, green, and blue), which is extracted from the images, allow researchers to detect foliage phenological changes such as leaf-expansion and leaf senescence (e.g., Henneken et al., 2013, Ide and Oguma, 2010, Nagai et al., 2013b, Zhao et al., 2012). Some studies have used the greenness index for estimation of the green-up date (Ahrends et al., 2008, Ahrends et al., 2009, Ide and Oguma, 2010, Richardson et al., 2007). Although the image-analysis methods for the detection of the timing of phenological changes, such as leaf-expansion, leaf-coloring, and leaf-fall, have been developed by such previous studies (e.g., Nagai et al., 2011), the evaluation of the long-term variation in the timings of these phenological events in each deciduous tree species based on this type of image analysis has not yet been sufficiently investigated.
In this study, (1) we investigated the year-to-year variation in the timings of SLE and ELF for four tree species (redvein maple: Acer rufinerve, Erman's birch: Betula ermanii, Miyama cherry: Prunus maximowiczii, and white oak: Quercus crispula) in a cool-temperate deciduous broad-leaved forest in Japan by using daily continuous canopy surface images from 2004 to 2013, (2) we also investigated the differences of the phenological sensitivity in the timings of SLE and ELF to air temperature among the tree species, and (3) we discussed the usefulness and problems of using canopy surface images for phenological observations in a forest ecosystem. Our aim was to provide robust evidence of the usefulness of daily continuous canopy surface images for continuous observation of the interannual variation in foliage phenology among various tree species within a deciduous broad-leaved forest.
Section snippets
Study site
The study site is located in a cool-temperate deciduous broad-leaved forest in Takayama, Japan (TKY site; 36°08′46″N, 137°25′23″E, 1420 m above sea level; Nagai et al., 2013a). The dominant tree species are 50–60-year-old Q. crispula and B. ermanii (Ohtsuka et al., 2009). The height of the dominant trees ranges from 13 to 20 m (Nasahara et al., 2008). An evergreen dwarf bamboo species (Sasa senanensis) covers the forest floor, and its height is about 1.5 m (Ohtsuka et al., 2009). The annual mean
Year-to-year variation in the timings of SLE and ELF
Year-to-year variations in the timings of SLE and ELF for the canopy and the individual ROI trees are shown in Fig. 2. The average date of the timings of SLE and ELF for each individual tree species from 2004 to 2013 is summarized in Table 1. The timings of SLE of A. rufinerve and P. maximowiczii were generally 3–5 days earlier than those of B. ermanii and Q. crispula every year (Fig. 2a). The timing of SLE of Q. crispula tended to be earlier than that of B. ermanii. Year-to-year patterns in the
Utilization of a downward-pointing digital camera with a fish-eye lens for phenological observations
We observed simultaneously the seasonal changes in foliage phenology of the various broad-leaved trees by using a downward-viewing hemispheric image. However, the phenological observation by using the downward-viewing images has a disadvantage that a downward-viewing image captures not only canopy foliage but also understory foliage (e.g., Mizunuma et al., 2012). This fact suggests that the understory foliage within the image is misleading for detection of the timings of SLE and ELF. Here, we
Conclusions
We showed (1) the year-to-year variations of foliage phenology among different deciduous broad-leaved tree species, and (2) the different characteristics of their phenological sensitivity to air temperature among the tree species by using the digital camera monitoring for 10 years. The images have much more information than the recorded dates which potentially lead to new findings of the long-term spatial and temporal changes in ecosystem structure. For instance, the sideways-looking images at
Acknowledgments
We thank K. Kurumado, Y. Miyamoto, S. Yoshitake (Takayama Field Station of River Basin Research Center, Gifu University), and H.M. Noda (National Institute for Environmental Studies), for their assistance in our observations. We also thank all PEN members for their cooperation. We thank the editor and an anonymous reviewer for their kind and constructive comments. T. Inoue and S. Nagai were supported by KAKENHI (25281014; Grant-in-Aid for Scientific Research B by the Japan Society for the
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