Ecol Res (2015) 30: 867–877 DOI 10.1007/s11284-015-1286-y
O R I GI N A L A R T IC L E
Vilanee Suchewaboripont • Masaki Ando Yasuo Iimura • Shinpei Yoshitake • Toshiyuki Ohtsuka
The effect of canopy structure on soil respiration in an old-growth beechoak forest in central Japan
Received: 4 February 2015 / Accepted: 1 June 2015 / Published online: 18 June 2015 The Ecological Society of Japan 2015
Abstract Soil respiration (Rs) is a key component in the estimation of the net ecosystem production (NEP) of oldgrowth forests, which are generally thought to have ceased carbon accumulation. The objectives of the present study were to characterize the spatial and temporal patterns of Rs, and to identify the determinants of the spatial and temporal variability of Rs, using general linear mixed models (GLMM), in an old-growth beech-oak forest. GLMM analyses identified monthly effect as a significant explanatory variable for temporal variation, as well as gap/canopy and soil water content (SWC) as explanatory variables for spatial variation, in Rs. The complexity of vertical structure in the forest was reflected in the spatial pattern of Rs, which was higher in canopy areas than in gap areas during the growing season, except in November. This spatial pattern was not affected by soil temperature. Moreover, SWC did not differ between gap and canopy areas, although SWC partially explained the spatial heterogeneity in Rs. The carbon:nitrogen ratios of soil organic matter in canopy areas were significantly higher than those in gap areas. Fine root biomass was 1.7-fold greater in canopy areas than in gap areas, likely because of the higher Rs in canopy areas, and root respiration made a much large contribution to Rs than heterotrophic respiration. The different patterns of fine root biomass between gap and canopy areas mainly V. Suchewaboripont Æ T. Ohtsuka United Graduate School of Agricultural Science, Gifu University, 1-1 Yanagido, Gifu 501-1193, Japan V. Suchewaboripont (&) Æ S. Yoshitake Æ T. Ohtsuka River Basin Research Center, Gifu University, 1-1 Yanagido, Gifu 501-1193, Japan E-mail:
[email protected] Tel.: +81 58-293-2065 M. Ando Laboratory of Forest Ecology, Faculty of Applied Biological Sciences, Gifu University, 1-1 Yanagido, Gifu 501-1193, Japan Y. Iimura School of Environmental Science, The University of Shiga Prefecture, Hikone, Shiga 522-8533, Japan
control the spatial heterogeneity in Rs; thus, it is worth considering the gap/canopy variability in Rs when evaluating annual efflux in old-growth forests. Keywords Soil respiration Æ Spatial variation Æ Gap/canopy structure Æ Fine root Æ Old-growth forest
Introduction Odum (1969) hypothesized that changes in the structural and functional characteristics of developing ecosystems occur during ecological successions. Accordingly, the balance of ecosystem production and respiration (the P:R ratio) should be a functional index of the relative maturity of the system. In general, the net primary production (NPP) of forest ecosystems typically changes with age, and declines substantially after peaking relatively early during stand development (Ryan et al. 1997; Binkley et al. 2002). Therefore, during the early stages of succession, the P:R ratio is greater than one and then approaches one as succession proceeds to the mature or climax stages. Consequently, net ecosystem production (NEP) increases during early succession, and gradually decreases to near zero in mature ecosystems. Gough et al. (2008) also supported Odum’s prediction by demonstrating declines in carbon (C) storage in aging forest stands by assessing annual forest C storage using ecological and meteorological approaches in mixed-deciduous forests of the United States, although considerable variability was found between study sites. In contrast, several recent studies showed that older forests can maintain significant C sinks (Luyssaert et al. 2008; Wirth et al. 2009) because of the complexity of their canopy structures, which are generated through the death of canopy trees, followed by juvenile regeneration in gaps. Hardiman et al. (2011) recently investigated the relationships between the structural complexity of canopies and the NPP of wood in a maturing deciduous forest in the USA. In contrast to Odum’s theory that NEP declines to zero partly because of declining NPP in older
868
stands, they hypothesized that canopy structure increases with stand age and is positively correlated with stand production. Accordingly, they showed that older forests exhibited higher productivity than young forests because of the appearance of canopy complexity (Hardiman et al. 2011, 2013), which resulted from small numbers of large trees and very large numbers of small trees. Forest maturity potentially alters soil respiration because of the structural complexity of the canopy; however, few investigators have characterized respiratory efflux in old-growth forests. Soil respiration (Rs) is an important parameter for estimating NEP because NEP is determined by a balance between autotrophic photosynthetic assimilation (NPP) and respiratory efflux from heterotrophs (Rh), and most Rh is released from the soil in forest ecosystems with detritus-based trophic systems (Sulzman et al. 2005; Fekete et al. 2014). In temperate deciduous forests, temporal (seasonal) variation in Rs has been well documented, and soil temperature (Ts) is the principle factor controlling the seasonal variation in Rs (Lloyd and Taylor 1994; Mo et al. 2005; Hashimoto et al. 2009). An exponential (Q10) relationship between Ts and Rs has been used to evaluate the annual Rs flux in temperate deciduous forests in the absence of soil moisture limitations (Mo et al. 2005; Ohtsuka et al. 2010). Spatial variation in Rs is also influenced by, for example, Ts (Schatz et al. 2012), soil water content (SWC) (Jia et al. 2003), soil properties (Scott-Denton et al. 2003; Saiz et al. 2006; Ngao et al. 2012), and root biomass (Stoyan et al. 2000; Søe and Buchmann 2005; Adachi et al. 2006; Knohl et al. 2008; Hojjati and Lamersdorf 2010). However, there are few studies of the role of canopy structural complexity in the spatial variability in Rs (Schatz et al. 2012). Thus, canopy structural complexity, particularly gaps and canopies, makes it difficult to obtain accurate assessments of the annual Rs flux and NEP in old-growth forests (Irvine and Law 2002; Hojjati and Lamersdorf 2010). In the old-growth beech forests of cool temperate regions in Japan, characterizations of structure have
shown the presence of clearly defined gap and canopy areas due to the deaths of large canopy trees (Nakashizuka and Numata 1982). Although small tree regeneration occurs in these gap areas, dense dwarf bamboo (Sasa sp.) limits the regeneration of small trees in some gaps. Although previous studies showed spatial variations in Rs in old-growth forests (Jordan et al. 2009), the relationship between Rs and canopy structures remains unclear. In central Japan, large areas of the lower slopes of Mt. Hakusan (a temperate region) are covered with old-growth beech and oak forests (Kato and Komiyama 1999) that are more than 250 years old, with canopy tree trunks reaching diameters up to 200 cm (Suchewaboripont et al. 2015). In the present study, we performed ecological inventories of C cycling in these old-growth temperate deciduous forests, and characterized the spatial pattern of Rs in an old-growth beech-oak forest on Mt. Hakusan during the growing season. Subsequently, we examined the effects of environmental factors on heterogeneities in Rs and hypothesized that gap/canopy structures may influence the spatial variability in Rs. Finally, we compared Rs and related factors between gaps and canopies, and identified determinants of the spatial and temporal variability in Rs using generalized linear mixed models (GLMM).
Methods Study site The study site (369¢N, 13649¢E, 1330 m a.s.l.) is located on the mid slope of Mt. Hakusan (Fig. 1), where primary, deciduous broad-leaved forests have become established around the Ohshirakawa river basin (840–1600 m a.s.l.) since the last eruption of Mt. Hakusan in 1659 (Japan Meteorological Agency; JMA). This area has been protected by the creation of Hakusan National Park, which is under the management of the Forest Agency of Japan and the Ministry of Environ-
Fig. 1 The study site was located on a mid-slope of Mt. Hakusan (1330 m a.s.l.), central Japan (a). Primary, broad-leaved deciduous forests were established around the Ohshirakawa river basin from 840 to 1600 m a.s.l. (b); gray lines show contour intervals of 100-m elevation
869
ment of Japan. There was no evidence of human disturbance in this area prior to the construction of the Ohshirakawa dam (approximately 800 m from the study site) in the 1960s. C cycling was examined in a permanent 1-ha (100 m · 100 m) plot of primary forest during July 2011. This plot is situated on an east-facing, gentle slope (average slope of 3 degrees), and the canopy layer is dominated by Fagus crenata (beech, 47.6 % of the basal area) and Quercus mongolica var. crispula (oak, 37.4 % of the basal area) trees with diameters at breast height (DBHs) of ‡25 cm and heights of approximately 25–30 m. The sub-tree layer mainly comprises beech, Acer tenuifolium, and Viburnum furcatum, with high stem densities and heights of 10–15 m. The aboveground biomass (except for leaves) of the canopy trees is extremely large (446.8 Mg ha1), whereas that of the sub-trees is only 17.9 Mg ha1. Evergreen dwarf bamboo (Sasa kurilensis) of 1.5–2.0 m height sparsely covers the forest floor. A dead oak tree (DBH = 74.5 cm) near the study plot was over 258-years-old. The soil in the study plot is a volcagogenous regosol with a thin A layer of 0–18 cm and a B layer of 19–24 cm (Suchewaboripont et al. 2015). Air temperature was monitored in the study plot by installing a weather station, but it was interpolated according to the relationship between air temperature at the Shirakawa weather station (3616¢N, 13654¢E, 748 m a.s.l.) and at the study site during the deep snow season because the air temperature sensor was buried. The annual mean air-temperature in 2012 was 5.8 C, with a maximum daily temperature of 21.5 C during August and a minimum daily temperature of 9.9 C during February. Annual precipitation in 2012 was 2262 mm (Miboro weather station; 369¢N, 13654¢E, 640 m a.s.l.). This area has heavy snowfall from November to April, with accumulated depths of 2.9 and >4 m in 2012 and 2013, respectively. Measurement of soil respiration Chambers of 23.5-cm diameter and 16.5-cm height were installed at a soil depth of 1 cm at 100 locations in 100
subplots (10 · 10 m2) of the 1-ha permanent plot. Chamber lids were kept open to collect litter and rainfall (Fig. 2), and vegetation from the chambers was clipped during the experiment to avoid effluxes that did not originate from the soil. CO2 efflux from the soil (Rs) in the chambers was measured using the soda lime technique (Keith and Wong 2006). Soda lime granules consisted of Ca(OH)2 (80 %) and NaOH (3 %), and the size of the granules ranged from 1.5–3.5 mm (Soda lime Granular No. 1, Kishida Chemical Co., Ltd., Osaka, Japan). Briefly, about 7 g of soda lime granules was placed in a small glass pot of 3.2-cm diameter and oven-dried at 105 C for 24 h. Glass pots containing dry soda lime granules were weighed to an accuracy of 0.1 mg and then sealed until transported to the study field. Subsequently, dried soda lime was rehydrated with 3 ml of water using a fine spray prior to placement in the chambers (Fig. 2) at approximately noon. The time of incubation was calculated by recording the times at which the chambers were closed and opened. After 24 h, the glass pots were collected, sealed, and transported to the laboratory. Glass pots were then oven-dried at 105 C for 24 h to a constant weight and re-weighed. Blank measurements were made to account for CO2 absorption by the soda lime during the experimental procedure. Five blank chambers with sealed bases were treated in the same manner as the sample chambers in the soil. Rs was measured as a daily integrated value using the following equation: Rs g m2 day1 of C
¼
ðWs Wb Þ 1:69 24 12 ; chamber area H 44
where Ws is the sample weight gain (g) of soda lime, Wb is the mean blank weight gain (g) of soda lime, and H represents exposure times (h). Rs values were determined monthly during the snow-free period of 2012 (5–6 June, 9–10 July, 7–8 August, 30–31 August, 3–4 October, and 5–6 November). The accuracy of the soda lime method was verified by comparison with infrared gas analyzer (IRGA) measurements by Keith and Wong (2006) and Hirota et al.
Fig. 2 A chamber for measuring CO2 efflux from soil. A small glass pot with dried soda lime granules was placed in the chamber of 23.5cm diameter (a). The soda lime was then rehydrated prior to measurement, and it was closed with a lid for 1 day (b)
870
Fig. 3 Air and soil (Ts) temperatures and soil water content (SWC) were monitored in the study plot by a weather tower during 2012; air temperature, dashed line; Ts, solid line; arrows indicate the days of soil respiration measurements (a). Air temperature in the snowy season was interpolated from the relationship between the air temperature at the Shirakawa station (3616¢N, 13654¢E, 748 m a.s.l.) of the Japan Meteorological Agency (JMA) and at the study site. Daily precipitation data (bar) were provided by the Miboro station (369¢N, 13654¢E, 640 m a.s.l.) of JMA (b)
(2011). The accuracy of the soda lime method was reported to be quantitatively similar to that of an IRGA measurement from a portable photosynthesis system (LI-6200, LI-COR Biosciences, Lincoln, NE, USA), with a 1:1 linear regression (Keith and Wong 2006). Moreover, Hirota et al. (2011) compared the rate of Rs using soda lime and an IRGA (GMP343, Vaisala, Helsinki, Finland) connected to an automatic open-close chamber (AOCC) system. Although the soda lime method tended to overestimate Rs compared with the IRGA method, the linear relationship between the two methods was not significantly different from 1:1 (Hirota et al. 2011). Measurement of environmental parameters Ts was measured at a depth of 5 cm in proximity to the chambers using a handheld temperature probe (CT419WP, Custom Corp., Tokyo, Japan) after setting pots containing dried soda lime into the chambers at approximately noon. Annual (1 January–31 December) Ts at a depth of 5 cm was also monitored continuously by the weather tower in the study plot.
To determine the SWC, soil samples from a depth of 0–5 cm were collected at 100 places near the chambers using a small soil core sampler, with a 5-cm diameter and a height of 5 cm, between August and October 2011 and subsequently weighed. Dried soils were re-weighed after oven drying to a constant weight at 105 C for more than 48 h. SWC values were then determined according to the soil sample weights. The annual SWC at a depth of 5 cm was also monitored by the weather tower in the study plot. Total C and nitrogen (N) concentrations were determined in soil mineral samples that were collected at a depth of 0–5 cm at 100 locations near the chambers in June 2012. These soils were air-dried (35 C), and stones, roots, and coarse litter were removed. Sieved (2mm mesh) soils were ground finely using a blender, and the total soil C and N contents (g C or g N g1 sieved soil) were measured with a NC-analyzer (Sumigraph NC-900, Sumika Chemical Analysis Service Ltd., Tokyo, Japan) using ca. 20-mg soil samples. The DBH of all tree stems (DBH ‡5 cm) in the study plot were measured in each subplot during September 2012. Stem numbers of dwarf bamboo were counted in 2 · 2 m2 plot at each corner of each subplot in November 2011. The sampling of root biomass was conducted with a soil core sampler, a stainless steel tube with a 5-cm diameter and a height of 30 cm. Fifteen samples were collected at a depth of 0–15 cm at six locations (three gap and three canopy areas) on 16–17 June 2014. The samples were washed with tap water on a 0.5-mm mesh sieve. The roots were divided into live (biomass) and dead fractions by visual estimation. Live roots were intact, tough, and flexible, while dead roots were brittle and fractured easily (Bauhus and Bartsch 1996). Live roots were separated into groups of £ 2-mm diameter (ø) (fine roots) and ‡2-mm ø. All live roots were oven-dried at 70 C to a constant weight. Root biomass was calculated as the average dry weight in the gap and canopy areas. Statistical analyses Crown projection diagrams of the study plot (cf. Fig. 4 a) were used to record the specific locations of chambers in the gap and canopy areas. Ground areas under canopy openings (‡5 m2 in area) that were caused by canopy tree deaths were defined as a ‘‘gap’’ (Runkle 1981), and areas under canopy trees were defined as a ‘‘canopy’’. In the study plot, the gap size ranged from 120 to 680 m2, and the average gap size was 350 m2. Differences in Rs and Ts between the gap and canopy areas in each month were analyzed using two-way analysis of variance (ANOVA) and T-tests with a Bonferroni correction for post hoc comparisons. Differences in SWC, total C, total N, C:N ratios, and root biomass between gap and canopy areas were identified using T-tests, and coefficients of variation (CV) of Rs and all environmental factors were calculated as ratios of the standard deviations and mean values.
871
Fig. 4 Crown projection diagram of canopy trees (a), basal area in the sub-tree layer (b), and stem density of dwarf bamboo (c) in the 1-ha study plot. Basal areas of sub-trees (DBH
