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An Adaptive Management Scheme for Wetland Restoration Incorporating Participatory Monitoring into Scientific Predictions Using Dragonflies as an Indicator Taxon Taku KADOYA* and Izumi WASHITANI Institute of Agriculture and Life Science, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan e-mail: [email protected] *corresponding author

Abstract Here we propose an adaptive management scheme for wetland restoration using data collected by citizens to make scientific predictions. We assessed the potential advantages of such a scheme using a wetland restoration project conducted in a small floodplain area along the Matsu-ura River in Kyushu, Japan. For the case study, we compiled data provided by amateur naturalists on distribution patterns of dragonflies on the eco-regional scale, as well as ecological characteristics such as behavior and habitat preferences. Based on this information, we predicted a species recovery trajectory at the wetland restoration site. By monitoring species recovery to test our prediction, we demonstrated that colonization by dragonfly species at the restored site could be predicted using species prevalence on the regional scale based on the nestedness rule. The data collected by the amateur naturalists were critical in making this prediction, which highlights the importance of citizen participation in the proposed scheme. Key words: agricultural ecosystem, assembly rule, immigration potential, Odonata, participation, satoyama

1. An Adaptive Framework for Restoration Programs Rapid biodiversity loss is occurring on global, regional and local scales, and biodiversity conservation is an urgent international issue. For example, the 2002 World Summit on Sustainable Development (WSSD) endorsed the Hague Ministerial Declaration of the 6th Conference of the Parties to the Convention of Biological Diversity (CBD) in its Plan of Implementation. Specifically, its mandate was “to achieve by 2010 a significant reduction of the current rate of biodiversity loss at the global, regional and national levels as a contribution to poverty alleviation and to the benefit of all life on earth” (United Nations, 2002). In addition, the 3rd National Biodiversity Strategy of Japan, which was approved in 2007 based on the CBD’s provisions, aims to “reinforce the protected-area system, expand the designation of protected areas, improve conservation and management activities based on scientific data” and “promote the restoration of nature by having human beings assist with natural restoration processes through launching of nature restoration projects” to prevent speGlobal Environmental Research 11: 179-185 (2007) printed in Japan

cies extinction and conserve biodiversity (Ministry of the Environment of Japan, 2007). Ecological restoration, defined as the process of assisting the recovery and management of ecological integrity (Society for Ecological Restoration International, 2004), is a fundamental and effective approach to preventing the loss of biodiversity and to achieving progress toward the CBD’s objective, especially for ecosystems that have been severely damaged. The early establishment of a guiding image based on an understanding of the dynamic nature of ecosystems is thought to be the most critical aspect of successful ecological restoration projects (Gillilan et al., 2005; Palmer et al., 2005). The guiding image, which must be shared by all project participants, should stand on sound scientific predictions (Halle & Fattorini, 2004). This will help with the quantitative and/or qualitative evaluation of the results of restoration actions to create an ongoing feedback loop, which will ultimately improve the understanding of ecosystems and subsequent predictions. This process, called “adaptive management,” assumes that scientific knowledge is provisional, and focuses on management as a learning process or continuous experiment that incorporates the results of actions, thereby allowing ©2007 AIRIES

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managers to remain flexible and adapt to uncertainty (Grumbine, 1994). In the face of limited funding, knowledge and time, predictions often rely on shortcuts, or indicators, for the creation of biodiversity maintenance plans. Indicators are measurable surrogates for environmental endpoints such as biodiversity conservation that are assumed to be of value to the public (Niemi & McDonald, 2004). Selecting appropriate indicator species that satisfy scientific (ecological) needs as well as public interests (e.g., charismatic species) is important for facilitating citizen participation in restoration programs and for stimulating meaningful interactions between scientists and citizens. An enormous amount of ecological data with related mechanistic understanding is needed to make reliable predictions. To predict species colonization potential, for example, which is fundamental for designing restoration plans (Keddy, 1999; Campbell et al., 2003; Srivastava, 2005), data concerning species distribution, abundance, and ecological characteristics including dispersal ability, tolerance and habitat preference are required. Ecological data for various popular species are often available in developed countries such as Japan, which has many active amateur naturalists. However, this information is often random or inconsistent with respect to temporal and spatial scales.

many restoration projects in Japan aim to restore the aquatic habitats that were once maintained in the traditional agricultural landscape and floodplain wetlands (Washitani, 2003a; Yoshimura et al., 2005). Dragonflies (Odonata) are one of the major taxa that inhabit aquatic ecosystems. They have been used as indicators of the ecological quality of land-water ecotones, aquatic habitat heterogeneity (e.g., bank morphology and aquatic vegetation), and the hydrological dynamics of water bodies (e.g., Clark & Samways, 1996; Chovanec & Waringer, 2001; D’Amico et al., 2004). In Japan, dragonflies constitute one of the major taxa inhabiting the aquatic habitat networks maintained in the satoyama landscape (Sugimura et al., 1999). In addition, the Japanese people are particularly fond of this insect group (Primack et al., 2000). The distribution patterns and ecological characteristics such as behavior and habitat preferences of approximately 200 resident dragonfly species have been well described by a number of professional and amateur dragonfly enthusiasts (e.g., Sugimura et al., 1999). Therefore, dragonflies exhibit the ideal features of an indicator taxon for aquatic ecosystems in the satoyama landscape of Japan.

2. Dragonflies as an Indicator Taxon for Traditional Agricultural Ecosystems in Japan

An adaptive scheme for ecological restoration consists of three stages: (1) data collection, (2) prediction, and (3) examination and feedback (Fig. 1). Public participation plays an important role at the data collection stage. Stimulating relationships between scientists and citizens should be encouraged for the cyclic prediction and monitoring processes of an adaptive management plan. A rational approach to any of the stages in the scheme depends on the outcome of other activities and, in practice, a stage may have to be repeated if feedback from other stages indicates that changes are needed.

The satoyama, a traditional rural agricultural ecosystem that was common before the rapid development and modernization of Japanese communities, consisted of a mosaic of patches of forests, grasslands, paddies, ponds, and creeks supplying various resources to support traditional agriculture and village life (Washitani, 2001; Kobori & Primack, 2003). In the satoyama, the landscape mosaic maintained by human disturbance for agricultural purposes provided a variety of habitats for wild animals and plants, and contributed to high inter-habitat diversity (Washitani, 2003b). In particular, the aquatic habitat complex consisting of a network of paddy fields, ponds, and creeks connected to adjacent rivers or streams provided various habitats for a number of aquatic organisms including plants, invertebrates, fish and amphibians (e.g., Mukai et al., 2005; Takeda et al., 2006). The abandonment of satoyama ecosystems, which lost their instrumental value as a result of the fuel revolution and the popularization of chemical fertilizers, and their destruction due to regional development projects during periods of rapid growth and the “bubble economy,” resulted in the loss of various habitat types constituting traditional rural landscapes (Fukamachi et al., 2001). This caused serious threats to many aquatic organisms including those that were among the most familiar to people several decades ago (Washitani, 2001; Ministry of the Environment of Japan, 2007). As a result,

3. Scientific Processes and Participation with Respect to Indicator Species

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Fig. 1 Structure of a scheme for restoration projects using the cooperation of volunteers. The framework is a set of linked activities carried out by scientists and citizens consisting of three stages: (1) data collection, (2) prediction, and (3) examination and feedback.

Adaptive Scheme for Wetland Restoration

3.1 Defining the guiding image with indicator species in scientific terms For ecological restoration to be successful, the guiding image of a restoration project should be defined primarily based on the scientific predictions of the colonizing potential of indicator species (Keddy, 1999; Campbell et al., 2003; Srivastava, 2005). Although the colonization by a species is the outcome of complex interactions among spatio-temporal processes, we can quantify the colonizing potential of a species to predict: (1) how likely the species is to reach the restored site from the regional species pool (i.e., the immigration potential of the species), and (2) whether the species will be able to establish itself at the site by interacting with other species (i.e., the establishment potential of the species). However, some dispersal-limited species including plants may require physical introduction to the restored site to facilitate the immigration process and the recovery of their populations, and thus of the target ecosystem. On the other hand, in the case of species with greater dispersal abilities, a project should be planned to take advantage of their natural immigration from the existing species pool to restore self-sustaining populations. 3.2 Evaluation of the regional sources of immigrating species A species’ potential to reach the restoration site involves spatial processes, and to predict the immigration potential of a species, we must understand how different spatial levels, such as the regional species pool and the assemblage at the local restored site, are connected by the dispersal of the species. In general, the immigration potential of a given species is defined as its expected ease of immigration to a habitat. This can be predicted from landscape connectivity, which is defined as “the degree to which the landscape facilitates or impedes movement among resource patches” (Taylor et al., 1993), as well as the source size at the meta-level (i.e., the regional species pool). Landscape connectivity can be assessed using the data regarding the landscape structure around the restored site including the spatial configuration of habitats, dispersal ability, and behavior of the species (Taylor et al., 2006). In addition, data archived in distributional databases of wildlife records collected by amateur naturalists at eco-regional scales can be used to evaluate the source size of the regional species pool of some major species, including dragonflies in Japan. 3.3 Evaluating species selection through environmental filters Once a species has reached the restored site, whether it can become established at the site depends on the concerted operation of biotic and abiotic environmental filters, as well as a list of species traits that determine whether the species can persist through the filters (Temperton & Hobbs, 2004). Specification of the assembly rules, namely, the identification of the fundamental

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filters and species traits interacting to govern the target community, is thus one of the most important tasks of the predictions in the establishment stage (Keddy, 1999). The life history data for species archived by amateur naturalists can be of great help for this purpose. Most assembly models assume a static species pool from which potential colonizers are drawn (Aviron et al., 2005). All members of this pool have equal access to the community in the sense that they all attempt to invade an approximately equal number of times and are seeded into the community at the same initial population densities. Therefore, as described above, consideration of both immigration potential and assembly rules is fundamental at the scientific prediction stage. 3.4 Data compilation and updates through monitoring In the adaptive approach to ecological restoration, predictions based on data collected at the appropriate spatial scales should be tested through the implementation of the restoration projects. This would create feedback to the prediction stage and would therefore provide powerful tests of the ecological models used for the predictions. This would ultimately provide information as to whether the model assumptions were correct and how far the scientists have come in the understanding of nature. The outcome of the monitoring would also directly and/or indirectly provide feedback on the amateur naturalist data. Therefore, the information collected should be used to update the data, so that the outcome of the monitoring could encourage improvements to the data collection methods used by volunteer citizens. In particular, given the need to estimate the source size of a species accurately, the establishment of a citizen-driven systematic data collecting system may be useful or even required in order to archive more precise distributional records of the target species on the eco-regional scale. These processes will benefit researchers as well as citizens participating in ecological restoration projects because their activities are tightly linked to a socially relevant task, namely conserving biodiversity. In addition, the citizens participating in the project will enjoy a sense of satisfaction brought about by the restored biodiversity, and may therefore improve their quality of life through such activities. The formation of stimulating interactions between citizens and researchers will facilitate further data accumulation for scientific predictions in subsequent restoration projects and the establishment of long-term monitoring, which is otherwise often difficult to carry out.

4. A Case Study: Azame Wetland Restoration Project in Japan We assessed the potential advantages of a scheme combining data collected by citizens and scientific predictions in an adaptive framework using a wetland restoration project conducted in a small part of the

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floodplains of the Matsu-ura River in Kyushu, Japan, as a case study (Kadoya et al., in press). Specifically, we compiled data on the distributional patterns of dragonfly species on the eco-regional scale as well as ecological characteristics such as behavior and habitat use. These data were provided by amateur naturalists, and based on this information, we predicted the species recovery trajectory at the wetland restoration site. We then tested our prediction by monitoring species recovery at the restoration site. The Matsu-ura River is one of the largest rivers on Kyushu Island, with a catchment area of approximately 446 km2 and an annual average discharge of about 12.46 m3/s. The Azame restoration area (33º20’N, 129º59’E; 6 ha) is located in the old floodplain in the middle reaches of the Matsu-ura River, approximately 15.8 km from the mouth of the river, and was farmed as rice paddies until 2001. Prior to the restoration, the ground level of the Azame area was approximately 5 m above the normal water level of the river because of the deeply incised main channel, the aggraded floodplain, and regulation of the river’s flow path by embankments. Consequently, the connectivity and ecotones between the habitats of aquatic organisms had been entirely lost. Therefore, the restoration project prioritized solutions that would eliminate this lack of connectivity and create ecotones from the river to the study site by lowering the

aggraded site and partially removing the embankments (Fig. 2). As a second step, restoration of agricultural aquatic habitats maintained by traditional forms of agriculture, including paddy fields, marshes, ponds and creeks connected to the river, was started in 2005. The project required frequent meetings of the planning group and continuous monitoring of the effects of the restoration. Active participation of the local people and a nongovernmental organization through discussions held every month with a governmental office (Takeo Office of Rivers, Ministry of Land, Infrastructure and Transport of Japan) played an important role in the planning. 4.1 Data compilation and evaluation of the source size on the eco-regional scale Dragonflies are an insect group with relatively high dispersal capabilities that enable them to colonize even newly restored aquatic environments. Therefore, we started with an evaluation of the source size of dragonfly species on the eco-regional scale to predict the species immigration potential based on the collected data. Specifically, data on the distributional pattern of dragonfly species in northern Kyushu were obtained from the national database on wildlife distribution archived by amateur naturalists (Environment Agency of Japan, 2000). The database included records of the occurrence

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Fig. 2 Habitat types at the Azame restoration site (1a-c) and in nearby habitats (3a-c). At the restoration site, colonizer species such as Crocothemis servilia mariannae (2a), Orthetrum albistylum speciosum (2b), and Ischnura senegalensis (2c), all of which prefer temporary pools, were frequently observed. In the nearby habitats, we observed species that require abundant aquatic vegetation in their habitat, such as Libellula quadrimaculata asahinai (4a) and Platycnemis foliacea sasakii (4b), and species that inhabit open marshes, such as Sarasaeschna pryeri (4c).

Adaptive Scheme for Wetland Restoration

of every species on a grid with a cell size of 5’ latitude by 7’30’’longitude (about 10 km × 10 km) that covers all of Japan. We used the species occurrence data from 320 grid cells in northern Kyushu, which covers one of the eco-regions of dragonflies in Japan (Sugimura et al., 1999). Based on the database, we calculated the order of prevalence on the regional scale for each species as an index of source size on the regional scale (for details see Kadoya et al., in press). 4.2 Specification of assembly rules of dragonfly species Previous studies (Sahlen & Ekestybbe, 2001; Kadoya et al., 2004) as well as existing natural history knowledge have indicated that the distribution of dragonfly species within a community is strongly “nested;” that is, prevalent species are found everywhere, whereas rare species tend to occur only at the richest sites (Patterson & Atmar, 1986). Therefore, we assumed that immigration by dragonflies to the restored site would be governed mainly by the nestedness rule. We tested the nestedness of the distributional pattern of dragonfly species using the species database. Among the 320 grid cells, 154 grid cells contained at least one species, and the presence of 91 species had been recorded in the database. As expected, the presence–absence matrix for the 91 species recorded in northern Kyushu represented a significantly nested distribution (T = 12.4°, p < 0.0001; Fig. 3). The nested distribution of dragonfly species indicated a positive correlation between immigration potential and habitat tolerance. That is, prevalent species with G1

higher immigration potential tended to exhibit a wider habitat preference whereas rare species with lower immigration potential tended to have narrower habitat preferences. We therefore expected that the colonization of dragonflies to a restored site could be predicted simply from the source size (i.e., prevalence) on the regional scale. Testing this prediction required monitoring of the colonization by dragonfly species at the restoration site and analyzing the relationships between the species prevalence on the regional scale and species occurrence at the site. 4.3 Prediction testing by monitoring We conducted a census of adult dragonflies from 2003 to 2005 at the restoration site. The restoration site was rather new for the assessment of the colonization by a species. To compensate for this, we also conducted a census of species occurrences in nearby habitats (Fig. 2). We recorded 17 and 52 species at the restoration site and in the nearby habitats, respectively. All of these species had been previously recorded in the regional database. We excluded some non-target species from the analysis (for details see Kadoya et al., in press). Consequently, we analyzed 15 and 50 species observed at the restoration site and in the nearby habitats, respectively. An analysis using logistic regression revealed that the probability of occurrence of restoration-site species decreased significantly with decreasing species prevalence (Fig. 4b). A similar relationship was detected in the nearby habitats (Fig. 4a). These data support the prediction that colonization of the restored site by dragonfly species can be predicted from their prevalence on the regional scale.

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Species Fig. 3 Nested distribution of 91 dragonfly species in 154 grid cells in northern Kyushu. Each shaded square represents the presence of a species in a grid cell. The 91 species were ordered to maximize the nestedness of the matrix on the basis of the algorithm proposed by RodriguezGirones and Santamaria (2006). The degree of nestedness in the matrix was examined using a randomization test (n = 5,000, Monte Carlo simulations) with the binary matrix nestedness temperature calculator of Rodriguez-Girones and Santamaria (2006), and significant nestedness (T=12.4°, p < 0.0001) was detected (modified from Kadoya et al., in press).

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Rank order of prevalence Fig. 4 Probability of occurrence of dragonfly species (a) observed in nearby habitats and (b) at the restoration site based on logistic regression models using the rank order of prevalence of the species as an explanatory variable. Binary numbers were assigned to each species based on presence/ absence, and the number was plotted with a line representing the occurrence probabilities estimated by the logistic regression (nearby habitats: likelihood ratio test, p < 0.0001; restoration site: likelihood ratio test, p < 0.001); modified from Kadoya et al., in press).

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5. Scientific Predictions Combined with Participatory Monitoring Our case study demonstrated that species colonization could be predicted using species prevalence on a regional scale based on the nestedness rule. Although long-term monitoring at the local restoration site is a remaining task for the project, the study showed that data archived by amateur naturalists are critical in the prediction of species colonization, and thus highlights the importance of the proposed scheme that incorporates data collected by citizens into an adaptive framework of ecological restoration. Once species colonization becomes predictable, we can specify the recovery trajectory of a given species and can adaptively improve the project design for the subsequent microhabitat restoration of species that are expected to colonize a site. A credible prediction of species colonization also enables us to quantitatively assess the success of restoration by monitoring the extent of colonization at the site in order of prevalence on the eco-regional scale. Cultivated systems (areas where at least 30% of the landscape are croplands or are used for shifting cultivation, livestock production or freshwater aquaculture) now cover one-quarter of the Earth’s terrestrial surface (Millennium Ecosystem Assessment, 2004). The loss of semi-natural habitats due to agricultural intensification and marginalization of traditional agricultural systems, both of which have led to the abandonment of traditional land uses, is one of the main threats to biodiversity in agricultural ecosystems (Krebs et al., 1999; Ormerod et al., 2003). Citizen participation would play a particularly important role in the restoration of semi-natural habitats in agricultural ecosystems given that the heterogeneous habitats of the agricultural landscape had been maintained by various human activities concerning agricultural production (Washitani, 2001), and that reinstating such activities would be fundamental to restoring the habitats. In this situation, the proposed scheme is also useful for stimulating interactions between citizens and researchers through the cyclic process of predictions and monitoring in an adaptive framework. This would ultimately help to establish a system of citizen participation in restoration projects.

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(Received 9 October 2007, Accepted 13 December 2007)