Journal of Ecology and Environment

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Published online December 15, 2023
https://doi.org/10.5141/jee.23.069

Journal of Ecology and Environment (2023) 47:22

Long-term and multidisciplinary research networks on biodiversity and terrestrial ecosystems: findings and insights from Takayama super-site, central Japan

Hiroyuki Muraoka1,2* , Taku M. Saitoh1 and Shohei Murayama3

1River Basin Research Center, Gifu University, Gifu 501-1193, Japan
2Biodiversity Division, National Institute for Environmental Studies, Tsukuba 305-8506, Japan
3National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8569, Japan

Correspondence to:Hiroyuki Muraoka
E-mail muraoka.hiroyuki.y6@f.gifu-u.ac.jp

Received: October 18, 2023; Revised: November 15, 2023; Accepted: November 15, 2023

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Growing complexity in ecosystem structure and functions, under impacts of climate and land-use changes, requires interdisciplinary understandings of processes and the whole-system, and accurate estimates of the changing functions. In the last three decades, observation networks for biodiversity, ecosystems, and ecosystem functions under climate change, have been developed by interested scientists, research institutions and universities. In this paper we will review (1) the development and on-going activities of those observation networks, (2) some outcomes from forest carbon cycle studies at our super-site “Takayama site” in Japan, and (3) a few ideas how we connect in-situ and satellite observations as well as fill observation gaps in the Asia-Oceania region. There have been many intensive research and networking efforts to promote investigations for ecosystem change and functions (e.g., Long-Term Ecological Research Network), measurements of greenhouse gas, heat, and water fluxes (flux network), and biodiversity from genetic to ecosystem level (Biodiversity Observation Network). Combining those in-situ field research data with modeling analysis and satellite remote sensing allows the research communities to up-scale spatially from local to global, and temporally from the past to future. These observation networks oftern use different methodologies and target different scientific disciplines. However growing needs for comprehensive observations to understand the response of biodiversity and ecosystem functions to climate and societal changes at local, national, regional, and global scales are providing opportunities and expectations to network these networks. Among the challenges to produce and share integrated knowledge on climate, ecosystem functions and biodiversity, filling scale-gaps in space and time among the phenomena is crucial. To showcase such efforts, interdisciplinary research at ‘Takayama super-site’ was reviewed by focusing on studies on forest carbon cycle and phenology. A key approach to respond to multidisciplinary questions is to integrate in-situ field research, ecosystem modeling, and satellite remote sensing by developing crossscale methodologies at long-term observation field sites called “super-sites”. The research approach at ‘Takayama site’ in Japan showcases this response to the needs of multidisciplinary questions and further development of terrestrial ecosystem research to address environmental change issues from local to national, regional and global scales.

Keywords: biodiversity observation network, carbon cycle, ecosystem observation super-site, forest ecosystem, in-situ observation network, long-term ecological research network, phenology, Takayama super-site

Climate change, biodiversity loss and degradation of natural environment and resources due to local, national, regional, and global anthropogenic activities are the urgent issues to be addressed by science and society (Pörtner et al. 2021). Ecosystem integrity is vital for the environmental and societal sustainability, but growing complexity in the ecosystem structure and functions under impacts of climate and land-use changes requires interdisciplinary understandings on their processes and whole-system dynamics (Haase et al. 2018; Mirtl et al. 2018). Ecosystem science to inform a deeper understanding of the current status, mechanisms and future changes of ecosystems, and their ecosystem services, is a challenge to the community of relevant sciences (e.g., Loescher et al. 2022). To tackle these scientific challenges, various Earth observations by satellites, ships, aircrafts, drones, in-situ sensors, and field scientists have been developed in the last decades over the world. Data and knowledge on the short- to long-term responses of ecosystem functions in response to on-going environmental change from short-term to long-term are key for mitigation of and adaptation to climate change (e.g., Dolman et al. 2022; Muraoka 2022).

In-situ field observations in local ecosystems provide us with a deeper understanding of the ecological mechanisms and dynamics of ecosystem functions as they have complicated interactions of biological, physical and biochemical processes over broad spatial and temporal scales (e.g., Muraoka and Koizumi 2009; Muraoka et al. 2012). But further integrative efforts are needed to gain interdisciplinary understanding of the spatial and temporal dynamics of ecosystem structure, function and services and biodiversity in changing environments (Muraoka et al. 2012; Pörtner et al. 2021). In general, these in-situ field observations or investigations are conducted at the ‘plot (site)’ scale, with plots having various sizes depending on the processes or phenomena of interests (e.g., 100 × 100 m for a forest ecological monitoring plot, but sometimes up to a few hectares). Studies at these plots to monitor and detect changes in biodiversity and ecosystem functions, to quantify the atmosphere—ecosystem interactions through CO2 and heat fluxes, and to evaluate impacts of climate and land-use changes on ecosystems, have been conducted by different scientific disciplines using different techniques. Considering the growing demands to the integrated environmental sciences to address challenges of climate change, biodiversity loss and other related issues for seeking sustainability of our environment and society, in this paper we aimed to review 1) the development and on-going activities of those observation networks, 2) some outcomes on forest carbon cycle studies at our super-site “Takayama site” in Japan to illustrate the benefits of integration of data across scales, and 3) a few ideas how we can better connect various observations and modeling analyses, and fill observational gaps in the Asia-Oceania region.

Studies on biological, biochemical, hydrological and physical processes and their interactions is key to understand the mechanisms and functions of our ecosystems in changing environments. Since those processes are largely variable among space and time, cooperative studies including collaborative research, data sharing, and synthesis by networking research initiatives or institutions are invaluable to cover those variations. There are number of such observation or research networks worldwide, such as Long-Term Ecological Research Network (LTER) (Mirtl et al. 2018), Critical Zone Observatories (CZO) (https://www.czen.org/, see also Mirtl et al. 2018), Flux network (FLUXNET and its regional/national networks) (Baldocchi et al. 2001), and Biodiversity Observation Network (BON) (Scholes et al. 2012), and so on. Below we will attempt to give a brief outline of a few networks in which our ‘Takayama’ super-site has been involved.

Long-Term Ecological Research Network

LTER is an approach in ecology to investigate decadal to longer-term changes of ecological and biogeochemical characteristics which determine structure and functions of ecosystems (Mirtl et al. 2018). LTER asks questions to investigate the mechanisms and dynamics of ecosystems, drivers of ecosystem changes, and interactions of ecosystems and societies (i.e., socio-ecological system). The network of LTER sites and researchers enables the community of ecologists to up-scale their data and knowledge from site to landscape, national, regional, and global scales. The international LTER network (ILTER, https://www.ilter.network/), was established in 1993 and currently more than 700 LTER sites from 44 national networks and a few regional/continental groups are cooperating (Mirtl et al. 2018). Detailed information on the LTER sites including ecosystem types, climate, research topics are all documented on DEIMS-SDR (Dynamic Ecological Information Management System-Site and Dataset Registry, https://deims.org/) (Wohner et al. 2019). The network of those LTER sites and research groups enables us to investigate continental or global patterns of ecosystems and their ecological components and functions along the gradient of geographical environments and socio-economic conditions. The East Asia-Pacific regional group of ILTER (ILTER-EAP) was established in 1995, to further enable cooperation among LTER scientists in the region. Currently ILTER- EAP consists of several LTER networks including the Chinese Ecosystem Research Network (CERN), the Japan LTER network (JaLTER), the Korea LTER network (K-LTER), the Taiwan Ecological Research Network (TERN), the Terrestrial Ecosystem Research Network of Australia (TERN- Australia), Malaysia LTER Network (Malaysia LTER), the Thailand LTER Network (Thailand LTER), the Philippines LTER Network (PhiLTERnet), and an associate network in Vietnam. Major research topics of the LTERs in the region include carbon cycle, ecohydrology, biogeochemistry and biodiversity. Many observations and/or research have been focusing on the whole-ecosystem level responses to changing environments as well as the ecological components such as phenology and photosynthesis of leaves and canopy, plant density and growth which structure the ecosystems and their functions. Contributors to ILTER-EAP and its member LTER networks are sharing these questions, and data and knowledge are being delivered to academia and society through publications (Muraoka and Nakaoka 2018), data sharing, and capacity building efforts.

Flux Research Network

Terrestrial ecosystem functions are also investigated by applying micrometeorological techniques which measure fluxes of greenhouse gases (e.g., CO2 and CH4) and water cycle. In general, an observation tower with height of far above the top of those vegetation canopy is installed at a targeted ecosystem (forest, grassland, and cropland), and multiple sensors to measure meteorological components such as radiation, temperature, humidity, wind speed, and trace gases are set-up along the tower. Observation of CO2 flux between the atmosphere and the ecosystem provides data of Net Ecosystem Exchange (NEE) between the systems as a result of photosynthetic CO2 absorption and respiratory CO2 release. Figure 1 illustrates schematic diagram of CO2 and carbon fluxes between the atmosphere and terrestrial ecosystem (forest as an example) and within the ecosystem, as an example of ecosystem structure and function. NEE is nearly equivalent to Net Ecosystem Production (NEP) if the lateral flow of photosynthetic matters is negligible. The long-term and continuous data from observation towers enable us to investigate the dynamics of ecosystem functions such as carbon sequestration and the water cycle, their responses to short-term to long-term meteorological variability, impacts of disturbance on ecosystems, and impacts of climate extreme and global warming (Saigusa et al. 2005; Yamamoto et al. 1999).

Figure 1. Schematic diagram of carbon cycle and budget of a forest ecosystem. Carbon or CO2 fluxes are indicated by arrows. The exchange of CO2 between the atmosphere and the ecosystem can be evaluated as the balance of photosynthetic CO2 absorption (gross primary production) and respiratory CO2 release (ecosystem respiration), and these are the part of the major components of climate—ecosystem interaction. In general net exchange rate of CO2 between the atmosphere and the ecosystem is measured by eddy covariance method. Within the ecosystem, photosynthesis, translocation of photosynthetic matters, and respiration of plants and heterotrophic organisms are the major components of ecological process of carbon cycle and budget. In general, these components are measured by ecological and biogeochemical research.

There are hundreds of such observation sites in the world, and a global, regional, and national networks have formed since 2001, including the global FLUXNET (Baldocchi et al. 2001). Synthesizing data from different observation sites and local or regional networks enable us to investigate the geographical patterns of carbon and water cycles (Pastorello et al. 2020). For example, Kondo et al. (2017) in the Japanese network (JapanFlux) conducted a meta-data analysis on the carbon cycle components of forest ecosystems in the Asian network (AsiaFlux), and clarified dependency of carbon sequestration on mean annual temperature over different climatic zones ranging from Northeast to Southeast Asia. The flux research networks are also utilizing satellite remote sensing data and simulation models to up-scale their plot-level findings to national, continental, and global scales to investigate the long-term changes of distribution of vegetations and their carbon cycles (Ichii et al. 2017), impacts of increasing atmospheric CO2 concentration on photosynthetic productivity at ecosystem level (Ueyama et al. 2020), and future terrestrial carbon cycle projections in different climate scenarios (Sasai et al. 2016).

Biodiversity Observation Network

With the development of human society and economies, particularly through transformation of natural ecosystems such as forests, rivers and coasts into agricultural fields or urban areas, overexploitation of biological resources, environmental pollution and degradation and loss of biodiversity have been accelerated worldwide (Brondízio et al. 2019). In addition to the direct impacts of human activities, climate change is also a driver of such biodiversity loss while they would provide Earth system resilience through ecosystem functions (Pörtner et al. 2021). Biodiversity and ecosystem integrity are vital for sustainable environment and society. Here also, scientists are challenged to urgently provide data and knowledge on the status of biodiversity and possible drivers of changes in biodiversity from local to global scales (Haase et al. 2018). In 2008, the Biodiversity Observation Network in Group on Earth Observations (GEO BON) was launched to promote observations of biodiversity at genetic, species and ecosystem levels and ecosystem services by various techniques including in-situ field survey and remote sensing for effective biodiversity conservation (Scholes et al. 2012). GEO BON’s mission is “to improve the acquisition, coordination and delivery of biodiversity observations and related services to users including decision makers and the scientistic community” (https://geobon.org/). In response to the call to the global community by the founders of GEO BON, the Asia-Pacific Biodiversity Observation Network (APBON) was launched in 2009 to network biodiversity scientists, institutions and practitioners for collaborative observations, capacity building, and fostering biodiversity conservation in the region (Takeuchi et al. 2021). The APBON has been developing its community through inter-governmental symposia (Global Earth Observing System of System [GEOSS] – Asia-Pacific Symposium) that have been hosted by Asia-Oceania GEO (AOGEO, https://aogeo.net/en/). APBON’s collaborative research and knowledge sharing have contributed to the related sciences as well as biodiversity assessment in the region (Karki et al. 2018).

For operational and comprehensive observations and assessment of biodiversity worldwide, GEO BON has developed concept of Essential Biodiversity Variables (EBV) which span scales from genes to species and ecosystems (Navarro et al. 2017; Pereira et al. 2013). EBV is a set of systematic observational components of biodiversity and ecosystems, and designed to support scientific communities in collecting data, monitoring the changes of biodiversity status among different locations and environments, and delivering information on biodiversity status and changes under environmental changes for policy and decision making. Recently GEO BON proposed an interconnected worldwide system named “Global Biodiversity Observing System (GBiOS)” (Gonzalez et al. 2023) which accelerates multidisciplinary biodiversity observations and integrates the data and knowledge to promote biodiversity science and to contribute to the Kunming-Montreal Global Biodiversity Framework adopted at the Conference of the Parties 15 of UN Convention on Biological Diversity in 2022.

Toward an integrated observations: network of networks

While these observation networks have arisen from different scientific disciplines and use different methodologies, the need for comprehensive observations and understanding on biodiversity and ecosystem functions under climate and societal changes at local, national, regional, and global scales are growing to address the on-going environmental issues. Such growing need provide challenges and opportunities to network these networks since those environmental issues involve biological, biochemical, physical, and hydrological interactions under climatic and societal changes (Loescher et al. 2022; Muraoka and Koizumi 2009; Muraoka et al. 2012). These data and knowledge are not only required for scientific studies in academia but should also be used by local and regional stakeholders as indicators progress towards societal goals addressing environmental issues such as Sustainable Developmental Goals (SDGs), biodiversity conservation, sustainable use of natural resources, carbon neutrality, mitigation of and adaptation to climate change.

There are number of key phenomena to be investigated by interdisciplinary approach worldwide such as carbon cycle between the atmosphere and ecosystem as well as its biogeochemical and ecological processes, consequence of biodiversity and ecosystem functions in terrestrial, freshwater, coast and marine areas, spatial and temporal consequences of ecosystem functions and their services to humanity, to name a few. Among the number of components in terrestrial ecosystems, phenology and primary production may be examples of key variables to help bridge ecology, biodiversity and Earth system sciences. This is because they are sensitive to environmental changes through ecophysiological processes, and also they are responsible for the complex climate−ecosystem interactions through carbon cycle as well as biodiversity−ecosystem function interactions (Muraoka and Koizumi 2009; Piao et al. 2019; Tang et al. 2016). Phenological monitoring is conducted worldwide in the sciences of biodiversity and ecosystem functions, ranging in scope from species to vegetation canopy, and in scale from landscape to global, using various methods (e.g, Cleland et al. 2007; Kikuzawa and Lechowicz 2011; Tang et al. 2016). Ecophysiological and ecosystem studies have also been coupled with phenology models to explain the environmental responses from leaf to canopy (Ito et al. 2006; Kuribayashi et al. 2017). Hence, these studies are enabling us to predict the possible influence of short- and long-term climate change on phenology and consequently on ecosystem functions. An existing scientific challenge is to achieve a comprehensive understanding of the biological and biogeochemical interactions related to phenological events by focusing on the processes occurring in plants and soil microbes. This is because that they determine flows of carbon, water, and nutrients in forest ecosystems (e.g., Muraoka and Koizumi 2009; Tang et al. 2016). The increasing needs and development of satellite remote sensing observations on terrestrial vegetation phenology should also be linked with ecological data, and mechanistic understandings on forest ecosystem phenology should be advanced for accurate analysis and interpretation of satellite data for landscape−regional−global scale observations, because they are critical for our accurate detection of ‘signals’ and further prediction of vegetation change (Muraoka and Koizumi 2009; Muraoka et al. 2012).

Ecologically appropriate parameterizations of forest structure and functions are required in models of ecosystem carbon cycle. Knowledge from long-term, multidisciplinary, and cross-scale findings will help the communities working on such models to develop meaningful collaborations and reliable products. The challenges indicated above can be tackled by first clearly viewing our state-of-the-art mechanistic understanding on the components involved in the given ecosystem by long-term observations, open-field experiments, coupled with observations of atmospheric dynamics at in-situ research sites. Comprehensive analysis of the system by pulling together various phenomena and variables would then allow us to identify ‘key ecosystem variables’ that are crucial to follow and compare in future efforts to extend principles to larger scales. These variables will permit truly meaningful interpretation of satellite remote sensing data and the inclusion of new principles into ecosystem models used to evaluate the potential consequences of climate change.

Among the challenges to produce and share integrated knowledge on climate, ecosystem functions and biodiversity, filling scale-gaps in space and time among ecosystem processes is crucial. Some questions this is crucial for include: How does climate change influence plant ecological behavior such as phenology and species composition, and result in ecosystem functions and services? How and to what extent do those ecological changes impact the climatic systems through interactive processes in the biosphere? How do we measure and predict those changes in ecosystem structure and resulting functions and services under the impacts of changing climate and society? What are the key ecological and climatic phenomena that drive dynamic interaction of the biodiversity and ecosystem functions along different spatial and temporal scales? To address these challenges and further our ecosystem science to tackle global environmental change, integration of in-situ multiple observations and research, ecosystem process modeling, and satellite remote sensing should be developed by interdisciplinary research through networking the networks.

Key solutions to respond to these multidisciplinary questions would include integrating in-situ field investigation on biodiversity and ecosystem functions, ecosystem modeling, and satellite remote sensing at long-term observation field sites where multiple observations and research have been conducted. This in-situ ‘site-based’ integration concept is called as ‘super-site’ (Karan et al. 2016; Muraoka and Koizumi 2009; Muraoka et al. 2012) or ‘master-site’ (Mirtl et al. 2018). This concept allows the community of sciences (ecology, hydrology, micrometeorology, etc.) to facilitate collaborative research and to integrate data from different scientific disciplines. These efforts then allow us to foster interdisciplinary methodologies and to up-scale or down-scale the findings over broad space and time for comprehensive understanding of our dynamic natural environments. In the next section, we illustrate the concept of super-site research at the ‘Takayama’ site in central Japan, which was launched in 1993 starting with the observations of atmospheric CO2 concentration and CO2 flux in a cool-temperate deciduous broadleaf forest ecosystem (Fig. 2) (Ito et al. 2015; Muraoka et al. 2015; Murayama et al. 2003; Yamamoto and Koizumi 2005; Yamamoto et al. 1999). Takayama site currently functions as a platform of interdisciplinary science of biodiversity ecosystem research, satellite remote sensing, and model simulations in Earth system science.

Figure 2. Image of super-site concept for observing and studying phenology and carbon cycle in a forest ecosystem. The observation infrastructure is consisting of meteorological sensors, eddy covariance system, automated cameras and spectroradiometer along the observation tower(s). Automated cameras for phenology observations and litter-traps are also located in understory. Measurements of leaf ecophysiological traits (photosynthesis, respiration, stomatal conductance, morphology) and leaf optical properties can be made on the tower. All these observations by different methodologies can be linked with satellite remote sensing and model simulations by up-scaling methods.

Background

In the early 1990’s, in response to the growing concerns of global environmental change associated with rising atmospheric CO2 concentration, scientific needs to elucidate the budgets of carbon, water and other materials between the atmosphere and ecosystems, or the dynamics of those materials within ecosystems as the interactions of physical, chemical, and biological components and processes have been increased. To respond to such needs for studies integrating by micrometeorology, hydrology and ecology, an observation tower and long-term plot was launched in Takayama city, Gifu Prefecture, central Japan in 1993 under the collaboration of National Institute of Advanced Institute of Science and Technology, and Gifu University (Yamamoto and Koizumi 2005). The site is in a cool-temperate deciduous broadleaf forest on a mountainous landscape at approximately 1,400 m a.s.l. In addition, in 2004, another observation tower was installed in an evergreen coniferous forest at 800 m a.s.l. (Muraoka and Koizumi 2009). The deciduous broadleaf forest site is dominated by Quercus crispula, Betula ermanii, B. platyphylla in the canopy, and an evergreen bamboo grass Sasa senanensis in the understory, whereas the evergreen coniferous forest site is a planted forest with Cryptomeria japonica and Chamaecyparis obtuse. According to the AsiaFlux site codes, the former is known as ‘TKY’ site (http://asiaflux.net/index.php?page_id=112) and the latter is known as ‘TKC’ site (http://asiaflux.net/index.php?page_id=111). Both sites are also registered as ‘Takayama’ to JaLTER and ILTER. The atmospheric CO2 concentration data at TKY are also registered in the World Data Centre for Greenhouse Gases (WDCGG, https://gaw.kishou.go.jp/search/station#TKY).

Micrometeorological observations and ecological research on carbon budget and processes

In the last 30 years numerous observations and investigations have been conducted at the Takayama super-site. These include: monitoring of CO2 exchange between the atmosphere and ecosystems (Saigusa et al. 2005; Saitoh et al. 2010; Yamamoto et al. 1999), measurement of tree biomass growth and net primary production (NPP) (Ohtsuka et al. 2009; Yashiro et al. 2010), biotic and abiotic mechanisms of soil respiration (Lee et al. 2005, 2008; Mo et al. 2005; Noh et al. 2016), investigating phenology and leaf ecophysiology responses to environmental changes (Muraoka and Koizumi 2005; Noda et al. 2015), characterizing the phenology of the forest canopy (Motohka et al. 2010; Nagai et al. 2013), analyzing tree ring growth pattern (Hirano et al. 2021; Shen et al. 2022), conducting open-field warming experiments on the branches of canopy trees (Chung et al. 2013; Muraoka 2022) and on soil carbon dynamics (Noh et al. 2016, 2017) have been conducted. These studies covered the atmospheric and ecological processes that are illustrated in Figure 1, and highlighted remarkable changes in the CO2 budget and associated ecological processes (e.g., photosynthesis, phenology, and respiration) throughout the seasons and years under environmental changes such as extreme weather events due to Asia Monsoon, increasing atmospheric CO2 concentration, and global warming.

One noteworthy scientific challenge and finding was to compare the carbon budget data between the biometric-method and eddy-covariance method (Ohtsuka et al. 2009). They investigated interannual variations of NPP, heterotrophic respiration, ecosystem respiration and resulting NEP. Note that NEP was estimated by both biometric method and eddy-covariance method, while NPP could only be measured by biometric method. They found that the interannual variation of NEP, which is generally measured by eddy-covariance method, was primarily led by the variation of NPP of woody parts of the forests, while NPP of foliage and heterotrophic respiration were rather stable. Their finding implied a further research idea on the impacts of short-term environmental changes on leaf photosynthesis and phenology, as these ecophysiological processes are sensitive to microenvironment in the forest ecosystem. This study also gave insights into the importance of ecological studies to understand the processes determining ecosystem-level carbon budget which is now widely measured by meteorological methodology.

Leaf photosynthetic responses to environmental conditions such as photosynthetic photon flux density (PPFD), temperature, humidity and CO2 concentration are fundamental processes regulating ecosystem-scale photosynthetic CO2 absorption. In addition, phenology is identified as a key phenomenon particularly in temperate regions where environmental conditions for plants and other organisms change drastically throughout the seasons in a year. To reveal the phenology of photosynthesis and further to evaluate its impact on forest canopy photosynthesis, Muraoka and Koizumi (2005, 2007), 2007 and Muraoka (2022) measured leaf ecophysiological traits responsible for the photosynthetic capacity of canopy and understory trees in two–three weeks intervals from leaf flushing to leaf fall. These data clearly showed drastic seasonal changes of photosynthetic capacity, stomatal conductance, leaf chlorophyll contents, leaf morphology (leaf mass per area, LMA), and dark respiration. Further Noda et al. (2015) undertook a synthetic analysis of the phenology of leaf ecophysiological traits gained by multi-year observations and developed a phenology model to predict the phenological change from air temperature in the spring-summer phase and the summer-autumn phase. Based on the findings of these long-term observations, an open-field warming experiment on canopy tree branches was combined with in-situ leaf observations during 2011 and 2017 to investigate the impacts of temperature rise on leaf phenology and photosynthetic characteristics (Chung et al. 2013; Muraoka 2022). Over the seven studied years higher monthly air temperature in spring let to earlier leaf development by about 14 days in canopy tree species Quercus crispula and Betula ermanii (Muraoka et al. unpublished work).

Quantifying the amount of soil respiration, which is the process of CO2 efflux from the soil surface (Fig. 1), was one of the central themes of several studies to clarify the dynamics of carbon budget in the deciduous forest ecosystems. Mo et al. (2005) and Lee et al. (2008) demonstrated intensive measurements of soil respiration throughout the year including wintertime, and clarified its dependency on soil temperature and moisture at TKY and TKC sites, respectively. Lee et al. (2005) further studied the contribution of root respiration in soil respiration characterized its seasonal dynamics. Through these studies, the research groups developed and improved the protocols and techniques for measurement of soil and root respirations in an open field under dramatic change of environment on the mountainous landscape. Further, Noh et al. (2016, 2017), 2017 conducted an open-field warming experiment on a soil system by burying heat cables beneath the soil surface and investigated the impacts of rising temperature (~5°C) on soil respiration and carbon dynamics. They found that influence of soil temperature increase also depended on season, with higher sensitivities in spring and in autumn but less in summer.

Data integration using ecosystem process models

By incorporating the in-situ observations described in the previous section, ecological process-based modeling studies were conducted to understand the influence of phenology and environmental change on forest carbon budget. Ito et al. (2006) incorporated the phenology of leaf photosynthetic capacity measured at the site (Muraoka and Koizumi 2005), and clearly demonstrated that leaf phenology has a remarkable influence on the seasonal pattern of carbon budget in a deciduous broadleaf forest. Further, Muraoka et al. (2010) investigated the impacts of interannual variation of phenology of leaf photosynthetic capacity and canopy leaf area index (LAI) on forest canopy and understory gross primary production (GPP). They found that the variation of leaf development and senescence periods as well as the photosynthetic activity in summer caused remarkable interannual variation of GPP in both canopy trees and understory vegetation. Based on these integrated understandings of the ecological mechanisms, model simulation studies on the possible impacts of future global warming and climate change were conducted (Ito 2010; Kuribayashi et al. 2017; Saitoh et al. 2015). In cool-temperate forests rising air temperature is simulated to expand the growing season length by altering leaf phenology and environmental conditions on leaf photosynthesis and result in greater carbon gain. However, the recent change in climate is leading to heat and drought stresses on leaf photosynthesis in summer (Reichstein et al. 2013), and such influence may occur even in the cool-temperate regions (e.g., Yamamoto et al. 2023). Further, a recent model simulation study validated by in-situ observation data at both sites suggested different responses of carbon sequestration to climate change between deciduous broadleaf and evergreen coniferous forests at sub-national scale in Japan (Saitoh et al. 2022). Moreover, climate change is also considered to influence winter weather and snow fall, which impacts photosynthetic activity and disturbance on evergreen coniferous forests (Nagai et al. 2018; Saitoh et al. 2010). To further investigate the impacts of climate change on forest ecosystems combined studies of in-situ observations and modeling analysis must be continued (Ito et al. 2015), and thus gained data and knowledge to be shared with science communities.

Connecting with satellite remote sensing

In addition to pursuing a deeper understanding of the ecophysiological and biogeochemical processes in the ecosystems, connecting in-situ field sciences and satellite remote sensing is a key to scaling up changes observed in terrestrial ecosystems under environmental and societal changes at broader spatial and temporal scales (Muraoka and Koizumi 2009). Satellite remote sensing of terrestrial vegetation provides information on the spatial distribution, and temporal changes in ecosystems over seasonal, annual, and decadal scales. Examples include enabling mapping of ecosystem extent, and detection of seasonal change (phenology) in canopy structure and photosynthetic productivity (Melnikova et al. 2018; Muraoka et al. 2013). While acknowledging the recent rapid development and implementation of such Earth observations by satellites, these data must still be coupled with field-based research and knowledge to build scientific knowledge of the biological processes involved in the ecosystem structure and functions, and information to support Nature-based Solutions through adaptive management of ecosystems under climate change.

In response to the emerging needs of such integrative observations from in-situ ecological research and satellite remote sensing, a set of automated digital cameras (ADFC), spectroradiometer, and sky radiometer were developed and installed in a few research plots including forests and grasslands (Fig. 2). The system was named the ‘Phenological Eyes Network (PEN)’ as a network of those in-situ observations in Japan (Nasahara and Nagai 2015; http://www.pheno-eye.org/). The ADFC captures phenology of tree branches and forest canopy along the forest canopy tower, as well as the seasonality of the landscape (Fig. 3). These images and data are used to validate and understand the spectral data (e.g., Nagai et al. 2013) which are available by satellites such as Terra/Moderate Resolution Imaging Spectroradiometer (MODIS) and Global Change Observation Mission-Climate (GCOM-C). The spectroradiometer captures spectral radiation incoming from the sky and reflected by the forest and enabled the researchers to compare the calculated vegetation indices such as Normalized-Difference Vegetation Index (NDVI) and Enhanced Vegetation Index (EVI) with the forest canopy structure and phenology observed at the same plot. We have coined the term ‘Satellite Ecology’ for this multidisciplinary observation concept (Muraoka and Koizumi 2009).

Figure 3. Sample images from the automated digital camera of Phenological Eyes Network at the Takayama site. The cameras are located on a canopy-access tower with a height of 18 m. The images show seasonal change of branches of Betula ermanii (top), forest canopy taken from the top of the tower (middle), and forest canopy taken from the understory (bottom).

A range of studies have resulted from these integrations of observations from ground to satellite. These include a number of studies to validate the optical signals from the satellites as the indicators of vegetation canopy structure (e.g., Motohka et al. 2010; Potithep et al. 2013), to develop the model to estimate forest canopy photosynthetic capacity from the Vegetation Indices at regional scales (Muraoka et al. 2013; Nagai et al. 2010), and to reveal the cross-scale consequences of ecophysiology and optical properties from single-leaf to landscape (Noda et al. 2021) have been published. Among the spectral signals studied, the Sun-Induced Chlorophyll Fluorescence (SIF) was also found to be sensitive to canopy structure, phenology, and micrometeorological conditions (radiation in particular) by in-situ observations of spectrum and CO2 flux (Morozumi et al. 2023; Nakashima et al. 2021). These studies on forest ecosystem structure are always challenging in our mountainous landscape in Japan due to the complex topography and high humidity of the air under influence of Asia Monsoon climate (e.g., Melnikova et al. 2018). However, the researchers attempted to conduct such multidisciplinary science to develop robust observation methodology to gain trustable data to precisely investigate the structure and functions of terrestrial ecosystems which are sensitive to environmental change but have invaluable functional role in Earth system.

Thus, the long-term and multidisciplinary observations at the Takayama site have enabled the science community to explore the dynamics of ecosystem structure and functions, investigate their ecological and meteorological mechanisms, up-scale the findings in spatial and temporal scales from plot to region, or down-scale to explore detailed mechanisms underlying phenomena at landscape to regional scales, for achieving cross-scale and interdisciplinary understanding of our natural environments under climate change (Fig. 4). This integrative, synthetic research and development will provide data and knowledge for promoting broad and deep ecosystem and Earth system sciences as well as addressing environmental challenges of the societal systems such as mitigation of and adaptation to climate change, and carbon neutrality. The next steps from our activities are to re-visit the pros and cons of the different observation and research methodologies which have varied spatial, temporal and thematic characteristics (Fig. 5), and co-design efficient, effective, and operational observation scheme for forest ecosystems to be implemented in the future and developed further over multiple locations worldwide with different characteristics of biodiversity and ecosystems under different climates.

Figure 4. Conceptual value chain from in-situ observations at a super-site, to integrated analysis on the ecological processes and functions under current and future environmental conditions, spatial and temporal scaling analysis (both up- scaling and down-scaling) with satellite remote sensing data, and then outcomes of the research to address scientific interests and societal challenges. RS: remote sensing.

Figure 5. Image of observation and research methodologies with their temporal resolutions with regard to the ecological and environmental phenomena in a forest ecosystem under environmental changes. Modified from Muraoka (2022).

Integrated Earth observations of climate, biodiversity, and ecosystem structure, functions and services, are increasingly needed to detect environmental changes due to human activity and address environmental crises globally. In-situ observations and analyses of terrestrial and aquatic ecosystems need to be conducted over spatial scales to cover various climatic zones, geographical characteristics, and diversity of ecosystems. However, this still leaves observational gaps in space and in themes due to the technical issues and resource limitations for installing research infrastructures at multiple locations as well as the scientific complexity of ecosystems (e.g., Mori et al. 2023). To address these scientific and technical challenges, networking the different observation platforms and sciences is truly important. As we have seen in the case of Takayama super-site, a number of scientists and students interacted by providing their own scientific curiosity and techniques, which further developed new science and technology to tackle the questions on ecological and environmental sciences. Such an ‘atmosphere’ of cooperation and collaboration enabled us to develop an inclusive and productive community of scientists, and this might be one of the reasons why the Takayama site was developed into a successful super-site that has run for 30 years, since the beginning of ‘global warming’ era.

Based on the long-term and multidisciplinary studies on our ecosystems, the challenge for such scientific communities or networks is to respond to the questions on interactions between humans and the natural environment. Particularly in the Asia and Pacific region we are experiencing drastic changes of natural environment and society. Discussions by the East-Asia and Pacific network of ILTER formulated the following questions as priorities for the Asia-Oceania region (Kim et al. 2018):

1. How does the climate change influence differently on the ecological behaviors of ecosystems in the region?

2. What are the critical aspects of biodiversity and ecosystems in the region that contribute to the sustainability of Earth systems and global society?

3. How does the growing spatial gradient of economic development in the region influence biodiversity, ecosystem functions, and their goods and services, and finally influence the ecosystem resilience to climate change?

4. How do the increasing extreme climatic events and land use change influence ecosystem functions and services?

As the societies face the transition from a world in crisis to pursuing sustainability, it is essential that ecosystem scientists contribute answers to these questions, guided by analyses of Planetary Boundaries (Persson et al. 2022; Rockström et al. 2009; Steffen et al. 2015). Climate change, biodiversity loss, and environmental pollution are among most critical issues in our world (Brondízio et al. 2019) and the community of ecosystem and environmental sciences has an important role to produce knowledge by integrating their long-term and multidisciplinary data and deliver to broad stakeholders (e.g., Gonzalez et al. 2023; Mori et al. 2023). To achieve such vision, 1) long-term and multidisciplinary research for interdisciplinary data and knowledge production, 2) connecting existing data, knowledge, infrastructure, and research networks to each other, and 3) promoting the value chain of observations—integrated analysis—co-producing intelligence and delivery to stakeholders, are truly important to share and cooperate with the community of relevant sciences and stakeholders, and next generations.

We appreciate the National Institute of Ecology, Republic of Korea, and Shin-ichi Nakano (Kyoto University and Ecological Society of Japan) who kindly invited HM to the symposium at the 10th Congress of East-Asia Federation of Ecological Societies (EAFES) held in Jeju in July 2023. This article is based on the paper presented at the symposium. The authors are grateful to the ‘Takayama community’ for their cooperative and open-minded activities since 1993. We also appreciate our colleagues in JaLTER, ILTER, JapanFlux, AsiaFlux, PEN, APBON, and GEO BON. HM thanks Hideaki Shibata (Hokkaido University), Kazuhito Ichii (Chiba University), Hibiki M. Noda (National Institute for Environmental Studies), Tsutom Hiura (The University of Tokyo), Yayoi Takeuchi (National Institute for Environmental Studies), Osamu Ochiai (Japan Aerospace Exploration Agency), Antonio Bombelli (Euro-Mediterranean Centre on Climate Change), John D. Tenhunen (University of Bayreuth) and Yowhan Son (Korea University) for discussing the super-site concept and for their generous supports to work with the research communities. We would like to dedicate this article to the late Mr. Kenji Kurumado, who had devoted his enthusiasm and inclusiveness to the scientists and students studying at the Takayama site.

This work was supported by grants (KAKENHI 19H03301, 21H05312, 21H05316, 22H00564) from the Japan Society for the Promotion of Sciences; the Global Environment Research Coordination System from the Ministry of the Environment, Japan (Grant Number MAFF2254); the Environment Research and Technology Development Fund (JPMEERF20232M01) of the Environmental Restoration and Conservation Agency provided by Ministry of the Environment of Japan.

  1. Baldocchi D, Falge E, Gu L, Olson R, Hollinger D, Running S, et al. FLUXNET: a new tool to study the temporal and spatial variability of ecosystem-scale carbon dioxide, water vapor, and energy flux densities. Bull Am Meteorol Soc. 2001;82(11):2415-34. https://doi.org/10.1175/1520-0477(2001)082%3C2415:FANTTS%3E2.3.CO;2.
    CrossRef
  2. Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD. Shifting plant phenology in response to global change. Trends Ecol Evol. 2007;22(7):357-65. https://doi.org/10.1016/j.tree.2007.04.003.
    Pubmed CrossRef
  3. Chung H, Muraoka H, Nakamura M, Han S, Muller O, Son Y. Experimental warming studies on tree species and forest ecosystems: a literature review. J Plant Res. 2013;126(4):447-60. https://doi.org/10.1007/s10265-013-0565-3.
    Pubmed CrossRef
  4. Dolman H, Kutsch W, Muraoka H, Bombelli A, Saigusa N, Schultz J, et al. The group on earth observations carbon and greenhouse gas initiative. In: Kavvada A, Cripe D, Friedl L, editors. Earth observation applications and global policy frameworks. Hoboken: Wiley; 2022.
    CrossRef
  5. Gonzalez A, Vihervaara P, Balvanera P, Bates AE, Bayraktarov E, Bellingham PJ, et al. A global biodiversity observing system to unite monitoring and guide action. Nat Ecol Evol. 2023;7(12):1947-52. https://doi.org/10.1038/s41559-023-02171-0.
    Pubmed CrossRef
  6. Haase P, Tonkin JD, Stoll S, Burkhard B, Frenzel M, Geijzendorffer IR, et al. The next generation of site-based long-term ecological monitoring: linking essential biodiversity variables and ecosystem integrity. Sci Total Environ 2018;613-614:1376-84. https://doi.org/10.1016/j.scitotenv.2017.08.111.
    Pubmed CrossRef
  7. Hirano Y, Saitoh TM, Fukatsu E, Kobayashi H, Muraoka H, Shen Y, et al. Relationships among radial growth of Cryptomeria japonica, carbon budget of a forest ecosystem, and climate factors in a cool temperate zone. Mokuzai Gakkaishi. 2021;67(3):117-28. https://doi.org/10.2488/jwrs.67.117.
    CrossRef
  8. Ichii K, Ueyama M, Kondo M, Saigusa N, Kim J, Alberto MC, et al. New data-driven estimation of terrestrial CO2 fluxes in Asia using a standardized database of eddy covariance measurements, remote sensing data, and support vector regression. J Geophys Res Biogeosci. 2017;122(4):767-95. https://doi.org/10.1002/2016JG003640.
    CrossRef
  9. Karki M, Senaratna Sellamuttu S, Okayasu S, Suzuk W, Acosta LA, Alhafedh Y, et al. Regional assessment report on biodiversity and ecosystem services for Asia and the Pacific. Bonn: Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services; 2018.
  10. Brondízio ES, Settele J, Díaz S, Ngo HT. Global assessment report of the intergovernmental science-policy platform on biodiversity and ecosystem services. Bonn: Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services; 2019.
  11. Ito A. Changing ecophysiological processes and carbon budget in East Asian ecosystems under near-future changes in climate: implications for long-term monitoring from a process-based model. J Plant Res. 2010;123(4):577-88. https://doi.org/10.1007/s10265-009-0305-x.
    Pubmed CrossRef
  12. Ito A, Saitoh TM, Sasai T. Synergies between observational and modeling studies at the Takayama site: toward a better understanding of processes in terrestrial ecosystems. Ecol Res. 2015;30(2):201-10. https://doi.org/10.1007/s11284-014-1205-7.
    CrossRef
  13. Ito A, Muraoka H, Koizumi H, Saigusa N, Murayama S, Yamamoto S. Seasonal variation in leaf properties and ecosystem carbon budget in a cool-temperate deciduous broad-leaved forest: simulation analysis at Takayama site, Japan. Ecol Res. 2006;21(1):137-49. https://doi.org/10.1007/s11284-005-0100-7.
    CrossRef
  14. Karan M, Liddell M, Prober SM, Arndt S, Beringer J, Boer M, et al. The Australian SuperSite Network: a continental, long-term terrestrial ecosystem observatory. Sci Total Environ. 2016;568:1263-74. https://doi.org/10.1016/j.scitotenv.2016.05.170.
    Pubmed CrossRef
  15. Kikuzawa K, Lechowicz MJ. Ecology of leaf longevity. Tokyo: Springer; 2011. p. 147.
    Pubmed CrossRef
  16. Kim ES, Trisurat Y, Muraoka H, Shibata H, Amoroso V, Boldgiv B, et al. The International Long-Term Ecological Research-East Asia-Pacific Regional Network (ILTER-EAP): history, development, and perspectives. Ecol Res. 2018;33(1):19-34. https://doi.org/10.1007/s11284-017-1523-7.
    CrossRef
  17. Kondo M, Saitoh TM, Sato H, Ichii K. Comprehensive synthesis of spatial variability in carbon flux across monsoon Asian forests. Agric For Meteorol. 2017;232:623-34. https://doi.org/10.1016/j.agrformet.2016.10.020.
    CrossRef
  18. Kuribayashi M, Noh NJ, Saitoh TM, Ito A, Wakazuki Y, Muraoka H. Current and future carbon budget at Takayama site, Japan, evaluated by a regional climate model and a process-based terrestrial ecosystem model. Int J Biometeorol. 2017;61(6):989-1001. https://doi.org/10.1007/s00484-016-1278-9.
    Pubmed CrossRef
  19. Lee M, Nakane K, Nakatsubo T, Koizumi H. The importance of root respiration in annual soil carbon fluxes in a cool-temperate deciduous forest. Agric For Meteorol. 2005;134(1-4):95-101. https://doi.org/10.1016/j.agrformet.2005.08.011.
    CrossRef
  20. Lee MS, Lee JS, Koizumi H. Temporal variation in CO2 efflux from soil and snow surfaces in a Japanese cedar (Cryptomeria japonica) plantation, central Japan. Ecol Res. 2008;23(4):777-85. https://doi.org/10.1007/s11284-007-0439-z.
    CrossRef
  21. Loescher HW, Vargas R, Mirtl M, Morris B, Pauw J, Yu X, et al. Building a global ecosystem research infrastructure to address global grand challenges for macrosystem ecology. Earths Future. 2022;10(5):e2020EF001696. https://doi.org/10.1029/2020EF001696.
    CrossRef
  22. Melnikova I, Awaya Y, Saitoh TM, Muraoka H, Sasai T. Estimation of leaf area index in a mountain forest of central Japan with a 30-m spatial resolution based on landsat operational land imager imagery: an application of a simple model for seasonal monitoring. Remote Sens. 2018;10(2):179. https://doi.org/10.3390/rs10020179.
    CrossRef
  23. Mirtl M, Borer ET, Djukic I, Forsius M, Haubold H, Hugo W, et al. Genesis, goals and achievements of long-term ecological research at the global scale: a critical review of ILTER and future directions. Sci Total Environ. 2018;626:1439-62. https://doi.org/10.1016/j.scitotenv.2017.12.001.
    Pubmed CrossRef
  24. Mo W, Lee MS, Uchida M, Inatomi M, Saigusa N, Mariko S, et al. Seasonal and annual variations in soil respiration in a cool-temperate deciduous broad-leaved forest in Japan. Agric For Meteorol. 2005;134(1-4):81-94. https://doi.org/10.1016/j.agrformet.2005.08.015.
    CrossRef
  25. Mori AS, Suzuki KF, Hori M, Kadoya T, Okano K, Uraguchi A, et al. Perspective: sustainability challenges, opportunities and solutions for long-term ecosystem observations. Philos Trans R Soc Lond B Biol Sci. 2023;378(1881):20220192. https://doi.org/10.1098/rstb.2022.0192.
    Pubmed KoreaMed CrossRef
  26. Morozumi T, Kato T, Kobayashi H, Sakai Y, Nakashima N, Buareal K, et al. Contributions of the understory and midstory to total canopy solar-induced chlorophyll fluorescence in a ground-based study in conjunction with seasonal gross primary productivity in a cool-temperate deciduous broadleaf forest. Remote Sens Environ. 2023;284:113340. https://doi.org/10.1016/j.rse.2022.113340.
    CrossRef
  27. Motohka T, Nasahara KN, Oguma H, Tsuchida S. Applicability of green-red vegetation index for remote sensing of vegetation phenology. Remote Sens. 2010;2(10):2369-87. https://doi.org/10.3390/rs2102369.
    CrossRef
  28. Muraoka H, Ishii R, Nagai S, Suzuki R, Motohka T, Noda HM, et al. Linking remote sensing and in situ ecosystem/biodiversity observations by "Satellite Ecology". In: Nakano S, Yahara T, Nakashizuka T, editors. The biodiversity observation network in the Asia-Pacific region. Tokyo: Springer; 2012. p. 277-308.
    CrossRef
  29. Muraoka H, Koizumi H. Photosynthetic and structural characteristics of canopy and shrub trees in a cool-temperate deciduous broadleaved forest: implication to the ecosystem carbon gain. Agric For Meteorol. 2005;134(1-4):39-59. https://doi.org/10.1016/j.agrformet.2005.08.013.
    CrossRef
  30. Muraoka H, Koizumi H. Leaf and shoot ecophysiological properties and their role in photosynthetic carbon gain of cool-temperate deciduous forest trees. In: Kawahata H, Awaya Y, editors. Elsevier oceanography series. Amsterdam: Elsevier; 2007. p. 417-43.
    CrossRef
  31. Muraoka H, Koizumi H. Satellite Ecology (SATECO)-linking ecology, remote sensing and micrometeorology, from plot to regional scale, for the study of ecosystem structure and function. J Plant Res. 2009;122(1):3-20. https://doi.org/10.1007/s10265-008-0188-2.
    Pubmed CrossRef
  32. Muraoka H, Saigusa N, Nasahara KN, Noda H, Yoshino J, Saitoh TM, et al. Effects of seasonal and interannual variations in leaf photosynthesis and canopy leaf area index on gross primary production of a cool-temperate deciduous broadleaf forest in Takayama, Japan. J Plant Res. 2010;123(4):563-76. https://doi.org/10.1007/s10265-009-0270-4.
    Pubmed CrossRef
  33. Muraoka H, Noda HM, Nagai S, Motohka T, Saitoh TM, Nasahara KN, et al. Spectral vegetation indices as the indicator of canopy photosynthetic productivity in a deciduous broadleaf forest. J Plant Ecol. 2013;6(5):393-407. https://doi.org/10.1093/jpe/rts037.
    CrossRef
  34. Muraoka H, Saitoh TM, Nagai S. Long-term and interdisciplinary research on forest ecosystem functions: challenges at Takayama site since 1993. Ecol Res. 2015;30(2):197-200. https://doi.org/10.1007/s11284-015-1251-9.
    CrossRef
  35. Muraoka H, Nakaoka M. Biodiversity and ecosystems in Asia: studies and activities of International Long-Term Ecological Research Network in East Asia and Pacific. Ecol Res. 2018;33(1):17-8. https://doi.org/10.1007/s11284-017-1548-y.
    CrossRef
  36. Muraoka H. Phenology of photosynthesis in a deciduous broadleaf forest: implications for the carbon cycle in a changing environment. In: Li F, Awaya Y, Kageyama K, Wei Y, editors. River basin environment: evaluation, management and conservation. Singapore: Springer; 2022. p. 3-27.
    CrossRef
  37. Murayama S, Saigusa N, Chan D, Yamamoto S, Kondo H, Eguchi Y. Temporal variations of atmospheric CO2 concentration in a temperate deciduous forest in central Japan. Tellus B Chem Phys Meteorol. 2003;55(2):232-43. https://doi.org/10.3402/tellusb.v55i2.16751.
    CrossRef
  38. Nagai S, Saigusa N, Muraoka H, Nasahara KN. What makes the satellite-based EVI-GPP relationship unclear in a deciduous broad-leaved forest? Ecol Res. 2010;25(2):359-65. https://doi.org/10.1007/s11284-009-0663-9.
    CrossRef
  39. Nagai S, Saitoh TM, Kajiwara K, Yoshitake S, Honda Y. Investigation of the potential of drone observations for detection of forest disturbance caused by heavy snow damage in a Japanese cedar (Cryptomeria japonica) forest. J Agric Meteorol. 2018;74(3):123-7. https://doi.org/10.2480/agrmet.D-17-00038.
    CrossRef
  40. Nagai S, Saitoh TM, Noh NJ, Yoon TK, Kobayashi H, Suzuki R, et al. Utility of information in photographs taken upwards from the floor of closed-canopy deciduous broadleaved and closed-canopy evergreen coniferous forests for continuous observation of canopy phenology. Ecol Inform. 2013;18:10-9. https://doi.org/10.1016/j.ecoinf.2013.05.005.
    CrossRef
  41. Nakashima N, Kato T, Morozumi T, Tsujimoto K, Akitsu TK, Nasahara KN, et al. Area-ratio Fraunhofer line depth (aFLD) method approach to estimate solar-induced chlorophyll fluorescence in low spectral resolution spectra in a cool-temperate deciduous broadleaf forest. J Plant Res. 2021;134(4):713-28. https://doi.org/10.1007/s10265-021-01322-3.
    Pubmed CrossRef
  42. Nasahara KN, Nagai S. Review: Development of an in situ observation network for terrestrial ecological remote sensing: the Phenological Eyes Network (PEN). Ecol Res. 2015;30(2):211-23. https://doi.org/10.1007/s11284-014-1239-x.
    CrossRef
  43. Navarro LM, Fernández N, Guerra C, Guralnick R, Kissling WD, Londoño MC, et al. Monitoring biodiversity change through effective global coordination. Curr Opin Environ Sustain. 2017;29:158-69. https://doi.org/10.1016/j.cosust.2018.02.005.
    CrossRef
  44. Noda HM, Muraoka H, Nasahara KN, Saigusa N, Murayama S, Koizumi H. Phenology of leaf morphological, photosynthetic, and nitrogen use characteristics of canopy trees in a cool-temperate deciduous broadleaf forest at Takayama, central Japan. Ecol Res. 2015;30(2):247-66. https://doi.org/10.1007/s11284-014-1222-6.
    CrossRef
  45. Noda HM, Muraoka H, Nasahara KN. Plant ecophysiological processes in spectral profiles: perspective from a deciduous broadleaf forest. J Plant Res. 2021;134(4):737-51. https://doi.org/10.1007/s10265-021-01302-7.
    Pubmed KoreaMed CrossRef
  46. Noh NJ, Kuribayashi M, Saitoh TM, Nakaji T, Nakamura M, Hiura T, et al. Responses of soil, heterotrophic, and autotrophic respiration to experimental open-field soil warming in a cool-temperate deciduous forest. Ecosystems. 2016;19(3):504-20. https://doi.org/10.1007/s10021-015-9948-8.
    CrossRef
  47. Noh NJ, Kuribayashi M, Saitoh TM, Muraoka H. Different responses of soil, heterotrophic and autotrophic respirations to a 4-year soil warming experiment in a cool-temperate deciduous broadleaved forest in central Japan. Agric For Meteorol. 2017;247:560-70. https://doi.org/10.1016/j.agrformet.2017.09.002.
    CrossRef
  48. Ohtsuka T, Saigusa N, Koizumi H. On linking multiyear biometric measurements of tree growth with eddy covariance-based net ecosystem production. Glob Chang Biol. 2009;15(4):1015-24. https://doi.org/10.1111/j.1365-2486.2008.01800.x.
    CrossRef
  49. Pastorello G, Trotta C, Canfora E, Chu H, Christianson D, Cheah YW, et al. The FLUXNET2015 dataset and the ONEFlux processing pipeline for eddy covariance data. Sci Data. 2020;7(1):225. https://doi.org/10.1038/s41597-020-0534-3.
    Pubmed KoreaMed CrossRef
  50. Pereira HM, Ferrier S, Walters M, Geller GN, Jongman RH, Scholes RJ, et al. Ecology. Essential biodiversity variables. Science. 2013;339(6117):277-8. https://doi.org/10.1126/science.1229931.
    Pubmed CrossRef
  51. Persson L, Carney Almroth BM, Collins CD, Cornell S, de Wit CA, Diamond ML, et al. Outside the safe operating space of the planetary boundary for novel entities. Environ Sci Technol. 2022;56(3):1510-21. https://doi.org/10.1021/acs.est.1c04158.
    Pubmed KoreaMed CrossRef
  52. Piao S, Liu Q, Chen A, Janssens IA, Fu Y, Dai J, et al. Plant phenology and global climate change: current progresses and challenges. Glob Chang Biol. 2019;25(6):1922-40. https://doi.org/10.1111/gcb.14619.
    Pubmed CrossRef
  53. Potithep S, Nagai S, Nasahara KN, Muraoka H, Suzuki R. Two separate periods of the LAI-VIs relationships using in situ measurements in a deciduous broadleaf forest. Agric For Meteorol. 2013;169:148-55. https://doi.org/10.1016/j.agrformet.2012.09.003.
    CrossRef
  54. Pörtner HO, Scholes RJ, Agard J, Archer E, Arneth A, Bai X, et al. Scientific outcome of the IPBES-IPCC co-sponsored workshop on biodiversity and climate change. Bonn: IPBES Secretariat; 2021.
  55. Reichstein M, Bahn M, Ciais P, Frank D, Mahecha MD, Seneviratne SI, et al. Climate extremes and the carbon cycle. Nature. 2013;500(7462):287-95. https://doi.org/10.1038/nature12350.
    Pubmed CrossRef
  56. Rockström J, Steffen W, Noone K, Persson A, Chapin FS 3rd, Lambin EF, et al. A safe operating space for humanity. Nature. 2009;461(7263):472-5. https://doi.org/10.1038/461472a.
    Pubmed CrossRef
  57. Saigusa N, Yamamoto S, Murayama S, Kondo H. Inter-annual variability of carbon budget components in an AsiaFlux forest site estimated by long-term flux measurements. Agric For Meteorol. 2005;134(1-4):4-16. https://doi.org/10.1016/j.agrformet.2005.08.016.
    CrossRef
  58. Saitoh TM, Nagai S, Yoshino J, Kondo H, Tamagawa I, Muraoka H. Effects of canopy phenology on deciduous overstory and evergreen understory carbon budgets in a cool-temperate forest ecosystem under ongoing climate change. Ecol Res. 2015;30(2):267-77. https://doi.org/10.1007/s11284-014-1229-z.
    CrossRef
  59. Saitoh TM, Shin N, Toriyama J, Murayama S, Yasue K. Forest carbon sequestration in mountainous region in Japan under ongoing climate change: implication for future research. In: Li F, Awaya Y, Kageyama K, Wei Y, editors. River basin environment: evaluation, management and conservation. Singapore: Springer; 2022. p. 55-80.
    CrossRef
  60. Saitoh TM, Tamagawa I, Muraoka H, Lee NY, Yashiro Y, Koizumi H. Carbon dioxide exchange in a cool-temperate evergreen coniferous forest over complex topography in Japan during two years with contrasting climates. J Plant Res. 2010;123(4):473-83. https://doi.org/10.1007/s10265-009-0308-7.
    Pubmed CrossRef
  61. Sasai T, Obikawa H, Murakami K, Kato S, Matsunaga T, Nemani RR. Estimation of net ecosystem production in Asia using the diagnostic-type ecosystem model with a 10 km grid-scale resolution. J Geophys Res Biogeosci. 2016;121(6):1484-502. https://doi.org/10.1002/2015JG003157.
    CrossRef
  62. Scholes RJ, Walters M, Turak E, Saarenmaa H, Heip CHR, Tuama ÉÓ, et al. Building a global observing system for biodiversity. Curr Opin Environ Sustain. 2012;4(1):139-46. https://doi.org/10.1016/j.cosust.2011.12.005.
    CrossRef
  63. Shen Y, Takata K, Kudo K, Muraoka H, Saitoh TM, Hirano T, et al. Effects of climate on the tree ring density and weight of Betula ermanii in a cool temperate forest in central Japan. Trees. 2022;36(5):1597-605. https://doi.org/10.1007/s00468-022-02315-y.
    CrossRef
  64. Steffen W, Richardson K, Rockström J, Cornell SE, Fetzer I, Bennett EM, et al. Sustainability. Planetary boundaries: guiding human development on a changing planet. Science. 2015;347(6223):1259855. https://doi.org/10.1126/science.1259855.
    Pubmed CrossRef
  65. Takeuchi Y, Muraoka H, Yamakita T, Kano Y, Nagai S, Bunthang T, et al. The Asia-Pacific Biodiversity Observation Network: 10-year achievements and new strategies to 2030. Ecol Res. 2021;36(2):232-57. https://doi.org/10.1111/1440-1703.12212.
    CrossRef
  66. Tang J, Körner C, Muraoka H, Piao S, Shen M, Thackeray SJ, et al. Emerging opportunities and challenges in phenology: a review. Ecosphere. 2016;7(8):e01436. https://doi.org/10.1002/ecs2.1436.
    CrossRef
  67. Wohner C, Peterseil J, Poursanidis D, Kliment T, Wilson M, Mirtl M, et al. DEIMS-SDR - a web portal to document research sites and their associated data. Ecol Inform. 2019;51:15-24. https://doi.org/10.1016/j.ecoinf.2019.01.005.
    CrossRef
  68. Ueyama M, Ichii K, Kobayashi H, Kumagai T, Beringer J, Merbold L, et al. Inferring CO2 fertilization effect based on global monitoring land-atmosphere exchange with a theoretical model. Environ Res Lett. 2020;15:084009. https://doi.org/10.1088/1748-9326/ab79e5.
    CrossRef
  69. Yamamoto S, Koizumi H. Long-term carbon exchange at Takayama site, a cool-temperature deciduous forest in Japan. Agric For Meteorol. 2005;134(1-4):1-3. https://doi.org/10.1016/j.agrformet.2005.11.006.
    CrossRef
  70. Yamamoto S, Murayama S, Saigusa N, Kondo H. Seasonal and inter-annual variation of CO2 flux between a temperate forest and the atmosphere in Japan. Tellus B Chem Phys Meteorol. 1999;51(2):402-13. https://doi.org/10.3402/tellusb.v51i2.16314.
    CrossRef
  71. Yamamoto Y, Ichii K, Ryu Y, Kang M, Murayama S, Kim SJ, et al. Detection of vegetation drying signals using diurnal variation of land surface temperature: application to the 2018 East Asia heatwave. Remote Sens Environ. 2023;291:113572. https://doi.org/10.1016/j.rse.2023.113572.
    CrossRef
  72. Yashiro Y, Lee NY, Ohtsuka T, Shizu Y, Saitoh TM, Koizumi H. Biometric-based estimation of net ecosystem production in a mature Japanese cedar (Cryptomeria japonica) plantation beneath a flux tower. J Plant Res. 2010;123(4):463-72. https://doi.org/10.1007/s10265-010-0323-8.
    Pubmed CrossRef

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