Assessment of Ecosystem Service Value of the Liaohe Estuarine Wetland

The functions and services of wetland ecosystems to human society have been generally recognized. Currently, most evaluations of wetlands are a comprehensive evaluation of their ultimate value. It is rare to discuss for energy and matter lost and transferred. In this study, emergy theory was used to assess the ultimate and intermediate service values of the Liaohe estuarine wetland ecosystem. Results show that its ultimate service value was $28.2 million, and its intermediate service value was $35,614.03 million. The 1263 time difference between intermediate and ultimate value shows that much server value was dissipated in the form of energy. In the ultimate service value, the value of adjusting the atmosphere was $8.02 million, accounting for 28.45% of the total value, and flood diversion and storage value was $6.98 million, accounting for 24.75%. These results illustrate that the most important service value of the Liaohe estuarine wetland ecosystem is to adjust the atmosphere and divert and store floods. In intermediate service value, maintaining-biodiversity value was $34,182 million, accounting for 95.98% of total value, showing that the Liaohe estuarine wetland plays an important role in species resources and regional seed banks.


Introduction
Wetland ecosystems are known as the kidneys of Earth [1] and provide a variety of services to humanity. Understanding these services and their "value" to humans can provide necessary information for resource managers and policy makers to make informed decisions. Understanding and evaluating wetland services needs a system approach that considers all variables influencing and driving the system [2]. In addition, as services are extracted, and ecosystems are used by humans, the flows of ecosystem services may change, thus introducing a dynamic aspect that also needs to be considered.
In the last decade or so, the issue of computing the value of ecosystem services has become an important area of research based on the service function of the ecosystem. Its service functions can be global area for leopard seal and red-crowned-crane reproduction. Therefore, it becomes an important transit point and destination for East Asia-Australia migratory birds. In this wetland, reed wetland is irrigated and harvested by mainly artificial covers, and Suaeda heteroptera with regional characteristic form a vermelha landscape, creating one of the most famous and representative regions of biodiversity conservation in the world. In this study, the emergy method was adopted to evaluate the intermediate and ultimate ecosystem service values of the Liaohe estuarine wetland, drawing more attention to the service process of the wetland system and providing the theoretical basis for the protection and rational utilization of Liaohe estuarine wetland resources.

Study Site
The Liaohe estuarine wetland is located in Panjin City, Liaoning Province, China, the southernmost tip of the Liaohe delta, covering the range of 121 • 30 ~122 • 00 E, 40 • 41 ~41 • 10 N, with a total area of about 577.69 km 2 and a coastline of 118 km. It is the largest wetland nature reserve in China ( Figure 1). It is mainly composed of reed marshes, intertidal mudflats, and waters. In this wetland, animal resources are mainly the wild-animal population of migratory waterfowl. In recent years, this wetland has suffered different degrees of destruction due to oil exploration, tourism development, and population growth. The Liaohe estuarine wetland belongs to the northern temperate zone continental semihumid monsoon climate, with four distinctive seasons, including a hot rainy season. Mean annual temperature is 8.4 • C, and mean annual rainfall is 625.6 mm. Rainfall is mainly concentrated in the summer, making up for 63% of total annual precipitation. Rainfall in winter is minimal, making up for 2.2% of total annual precipitation. Mean annual evaporation is greater than mean annual precipitation. Annual average evaporation is 1548 mm, 2.5 times the annual rainfall.

Emergy-Analysis Method
Emergy can be defined as the available energy (exergy) of one form used up directly and indirectly to produce a service or product; its units are solar-emergy joules (sej) [18]. This conception can measure and compare the actual energy values in different forms and hierarchies by using the unified standard. Its calculation method is that flows of energy, materials, or services in a system are transformed into the common unit of solar emergy by multiplying units of energy or mass by the corresponding unit emergy values (UEV). UEV is defined as the form of available energy (usually solar) that is required to produce a unit of another form of energy [18]. If the produced units are in joules of available energy, then the UEVs are called transformity. If the produced units are expressed in mass, the UEVs are called specific emergy. The units of each are as follows: transformity = sej/J, and specific emergy = sej/g. A third type of UEV is emergy per unit of currency, such as dollars, in which case, units are sej/$.
In practice, UEVs are computed from real processes that have been in operation for a sufficient amount of time that makes them likely to be operating at close-to-optimal performance. Ideally, UEVs are computed for each analysis; however, time and resource constraints make this ideal difficult to achieve. Instead, most emergy analyses rely on UEVs computed by others. Odum, Brown, Tillery, and Bastianoniet have computed UEVs for a variety of products and services [18,[21][22][23]. Two databases, the National Environmental Accounting Database and the Emergy Data Base, provide comprehensive lists of UEVs previously computed by others [24,25]. UEVs used in this study were obtained from these sources.

System Diagram
Not only are there the material and energy flows in the Liaohe estuarine wetland ecosystem, but also the social economic monetary and information flows. In order to describe the flowing energy process and make the emergy-calculation process of a wetland ecosystem convenient, the flowchart of the wetland ecosystem was drawn based on the design of the Odum energy language [26], shown in Table 1. This chart reflects the whole process of energy input and output. For the Liaohe estuarine wetland, the system energy-flow diagram, including the relationship between ecological-system components as well as that of the system energy, is shown in Figure 2. This figure was drawn based on determining the energy sources of the Liaohe estuarine wetland ecosystem and its components. Table 1. Symbol explanations of an emergy system.

Symbols Explanations
System frame: A rectangular box drawn to represent the boundaries of the selected system.
Pathway line: a flow of energy, often with a flow of materials.
Source: outside source of energy; a forcing function.
Storage: a compartment of energy storage within the system storing quantity as a balance of inflows and outflows.
Interaction: process that combines different types of energy flows or material flows to produce an outflow in proportion to an inflow function.

Symbols Explanations
Producer: unit that collects and transforms low-quality energy under the control interactions of higher quality flows.
Consumer: unit that transforms energy quality, stores it, and autocatalytically feeds it back to improve inflow.
Transaction: a unit that indicates the sale of goods or services (solid line) in exchange for payment of money (dashed line).

Calculation Method of Wetland-Ecosystem Value
The assessment of wetland ecosystem service value should be performed from maintaining the normal system operation and providing service and impact on the surrounding environment. Based on this, we classified wetland ecosystem service values as either ultimate service value or intermediate service value. Ultimate service value refers to a service being directly used for well-being. Intermediate service value is to keep the ecosystem itself running, and it is continuously converting into ultimate service value. This service value cannot be directly used by humans, but it is part of the necessary conditions for converting it into ultimate service value. In Figure 2, the outflows of material production, flood diversion, and storage, water-quality purification, gas and soil regulation, leisure entertainment, and scientific research and education were classified as ultimate service values. The inside flows of supplementing groundwater, water conservation, and nutrient recycling, and maintaining biodiversity in a system are part of the intermediate service values, based on existing results and studies on the Liao estuarine wetland [14][15][16][17].
The material-production value of the Liaohe estuarine wetland mainly includes the plant-resource value and the value of aquatic products. The key plant resource in this wetland is mainly reed, occupying the majority of the wetland's plant species. Reed yield and aquatic-product output can be obtained from the local yearbook.
(2) Flood Diversion and Storage Value The storage capacity of this wetland and the reservoir, and the annual average runoff in this wetland were used to calculate the total storage capacity of the Liaohe estuarine wetland. This information was from the local yearbook from 2006 to 2015. The calculated total storage capacity was the value of flood diversion and storage of the Liaohe estuarine wetland.

(3) Water-Quality Purification Value
There is a large number of paper mills upstream of the Liaohe estuarine wetland. The value of water-quality purification is the purification capacity of this wetland for paper-making wastewater. The content difference of nitrogen, phosphorus, and heavy-metal ions between upstream and downstream of this wetland was used to indicate purification capacity. Our experimental results from 2006 to 2015 can support the evaluation of water-quality purification.
(4) Gas-Regulation Value Gas regulation of the wetland ecosystem is the amount of carbon dioxide (CO 2 ) that can be aborted and stored, and of oxygen (O 2 ) that can be released, regulating the components of atmosphere and controlling global warming. This value was calculated by using the area of the wetland and the reed yield.

(5) Soil-Conservation Value
Soil conservation of the Liaohe estuarine wetland is the runoff energy that can be consumed by the wetland ecosystem, and the sand carried by the runoff that can be stored in the soil reservoir by turning into a form of emergy. Soil-reservoir emergy was used to calculate the emergy of organic carbon, total nitrogen (TN), and total phosphorus (TP).

(6) Leisure-Entertainment Value
The leisure entertainment of the Liaohe estuarine wetland is ecological tourism activities, such as fishing and bird-watching, which can be implemented. The emergy of tourism activities is from the chorography of Panjin. Tourism revenues from 2013 to 2015 were used.

(7) Scientific Research and Education Value
The value of scientific research and education was calculated by using the number of scientific-research publications. Based on the results of Meillaud [27], the average number of annual papers published in the last three years was considered as the newest research achievement. In this study, papers with Liao estuarine wetland and Panjin wetland keywords were searched in the database of Chinese periodical literature from 2013 to 2015, and the number of published papers was counted.

Intermediate Service Value (1) Groundwater Supplementation Value
In the process of determining the value of supplementing groundwater, only the value supplemented by reed wetland to the groundwater was considered. River infiltration, canal-system leakage, irrigation-water leakage, and underground lateral runoff were not calculated. In this wetland, the reed is submerged by water for six months, from May to October each year. When the infiltration amount of surface water into the groundwater was calculated, the surface-water infiltration coefficient was determined by the reed-wetland infiltration coefficient [27], determining groundwater emergy.
(2) Water-Conservation Value The value of water conservation was determined by measuring the rainfall intercepted by reeds aboveground and calculating the reed area of the Liaohe estuarine wetland based on the method of water conservation of forest ecological systems. The rainfall intercepted by reeds aboveground was obtained from a field survey.

(3) Nutrient-Recycling Value
There are two methods of determining the value of nutrient recycling: maintaining nutrients in the bio bank, and maintaining nutrients in the soil reservoir. This method aims to determine the ratio between net primary productivity and the amount of nutrients. In this study, the method of maintaining nutrients in the bio bank was adopted. N/P content in the net primary productivity of reeds was used to calculate the value of nutrient recycling.

(4) Biodiversity Value
At present, there are 253 species of birds living in the Liaohe estuarine wetland. The value of providing the habitat of this island for birds was used to evaluate the biodiversity value because maintaining bird-population quantity and quality, especially endangered birds, is the most important value of the Liaohe estuarine wetland.
From the above, the total amount of ecosystem services (g) was converted into energy (J), then converted into emergy through emergy transformity (sej/J or sej/g) to calculate each emergy of all wetland server values. Finally, emergy was converted into monetary value through the emergy currency-conversion rate. In this study, the related published survey reports and papers were referred [27][28][29][30], and the indices of all emergy referred to the research results by Liu [31]. The emergy currency -onversion rate was 1.21 × 10 13 sej/$ [32].

Data Sources
The data involved in the evaluation process were mainly from a field survey, sampling, and experimental analysis from 2011 to 2015. The basic information was from the Panjin statistical yearbook and field investigations in 2015.

Material-Production Value
The reed yield in this wetland was 150 million kg in 2015. Aquatic products mainly include crabs, shrimp, freshwater fish, and sea cucumbers. Their productions were 1 million, 250,000, 50,000, and 2.5 million kg, respectively.

Flood Diversion and Storage Value
The average storage capacity of this wetland and reservoir was 1481 million m 3

Gas-Regulation Value
The average reed yield was 1.5 × 10 11 g, the content of absorbed CO 2 in this wetland was 2.23 ×10 11 g, and the released O 2 content was 1.71 × 10 11 g.

Soil-Conservation Value
The area of the Liaohe estuarine wetland was 577.69 km 2 , the average product of reed was 473.12 g/m 2 , and the total nitrogen and phosphorus fixed was 1.84 × 10 8 g, organic carbon was 2.59 × 10 8 g.

Leisure-Entertainment Value
The annual average income was $2.63 × 10 6 from 2013 to 2015 based on local chronicles.

Scientific Research and Education Value
The total papers searched for from 2013 to 2015 were 65, and the average number of published papers was 22. The average number of pages of each paper was 6, and the total number of paper pages was 132 each year.

Intermediate Service Value Groundwater Supplementation Value
The area of the Liaohe estuarine wetland is 547.69 km 2 , the period of the wetland covered with water was six months each year, the soil-infiltration coefficient of the Liaohe estuarine wetland was 2.01 × 10 −6 m/s, and the supplemented groundwater was 1.84 × 10 10 m 3 .

Water-Conservation Value
The water-holding capacity of vegetation was 1389 g/m 2 by field experiment, the area of the Liaohe estuarine wetland was 577.69 × 10 6 m 2 , the areas covered by reeds occupied 97.5%, and the annual volume of water conservation was 4.43 × 10 8 m 3 .

Nutrient-Recycling Value
Reed biomass was 1.50 × 10 11 g each year, and the average contents of TN and TP were 3.245 mg/kg and 1.66 g/kg, respectively. The total weight of absorbed TN was 4.87 × 10 8 g, and TP was 2.49 × 10 8 g.

Biodiversity Value
There are 253 species of birds in this wetland according to the statistical yearbook of the Liaohe estuarine wetland, including eight species of national first-level protected animals. In this study, the value of protecting birds was calculated by using eight species of national first-level protected birds, and the value of protecting normal birds by using 100,000, the sum of two values that are the biodiversity value of the Liaohe estuarine wetland. Table 2 shows that there are 1.538 × 10 11 g of material resources produced by the Liaohe estuarine wetland each year, creating a value of $2.68 million. The regulated surface runoff was 2.48 × 10 10 m 3 , playing the role of flood diversion and storage and creating a value of $6.98 million. The total weight of nitrogen, phosphorus, and heavy metals was 7.49 × 10 8 g, purifying the water and creating a value of $1.05 million. This wetland absorbed 2.34 × 10 11 g of CO 2 and released 1.71 × 10 11 g of O 2 , playing a role in purifying air and acting as a carbon sink, creating value of $8.02 million. Tourism income in this wetland was $2.63 million, and the value of scientific research and education was $3.70 million. In addition, this wetland provided habitat for 253 bird species, maintaining biodiversity and creating value of $34181.82 million. It also supplemented 1.01 × 10 10 m 3 of groundwater, creating a value of $1431.63 million. Water conservancy of 4.4 × 10 11 m 3 in this wetland created a value of $ 0.03 million. The plants of this wetland absorbed 7.36 × 10 5 kg of N and P, creating $0.55 million.

Analysis and Evaluation of Wetland Ecosystem Service Value
The value of the Liaohe estuarine wetland ecosystem service was analyzed in terms of ultimate and intermediate service values, and the results were listed in Table 3. For ultimate service value, the value of adjusting the atmosphere was 28.45% of the ultimate service value of the Liaohe estuarine ecosystem, and flood diversion and storage 24.75%, which suggests that the Liaohe estuarine wetland ecosystem plays a positive role on regional gas regulation and flood control. The values of gas regulation, and flood diversion and storage were more than half of the total value, illustrating they are the main service value of the Liaohe estuarine wetland ecosystem. The value of material production occupied 9.50% of the ultimate service value, in which the value of aquatic products (crabs, shrimp, freshwater fish, sea cucumber) was higher, and reed value was lower. The crab product is one of the main economic sources, which can cause an obvious effect on the income of local residents. The value of scientific research and education was 13.12% and leisure-entertainment value 9.33%, which indicates that the Liaohe estuarine wetland has an important regional status. The values of water-quality purification was 3.72% of the total value, which is less for this wetland. For intermediate service values, the value of biodiversity was 95.98% of the total, the value of supplementing groundwater 4.02%, the value of nutrient recycling 0.34%, and the value of water conservation 0.00004%, which illustrates that the main intermediate value of the Liaohe estuarine wetland is maintaining biodiversity. Comparing the values of ultimate and intermediate services of the Liaohe estuarine wetland in 2015, there is a difference of $1650.1 million. This suggests energy loss occurring during the process of providing human-value services in the wetland.

Discussion
In this study, our findings adequately emphasize that the significance of the Liaohe estuarine wetland ecosystem is in maintaining biodiversity. We identified that its value was $34,181.82 million, accounting for 95.98% of the total intermediate value ($ 35,614.03 million), this being around 1263 times more than the ultimate value ($28.20 million) of the Liaohe estuarine wetland ecosystem, which explains why a lot of the server values were dissipated during the service process.
In other studies, quantifying the service value of a wetland ecosystem usually adopts econometric methods, but the quantifying results remove the richness of estuarine wetland ecosystem [39]. For each econometric method, with both its advantages and disadvantages, the evaluation index and method are also different due to the evaluation objectives and purpose. This causes large differences between evaluation results, leading even to low comparability [40]. In addition, ecosystem evaluation based on classifying the ecosystem services into noninterrelation types can cause double calculation of services owing to their actual relations [17]. In this study, we distinguished between ultimate and intermediate service valuse by defining the inflow and outflow of energy, materials, or services into common units according to the system diagram of the Liaohe estuarine wetland ecosystem, avoiding the double calculation of service values, and achieving comparability between different types of energy and material. Comparing all values of the UEV in this ecosystem, the UEV of bird protection was the maximum (5.17 × 10 22 ). Although there are only eight species of protected birds in this wetland ecosystem, its biodiversity value was also the maximum. This finding illustrates that every protected bird successfully survives in this wetland ecosystem, resulting from a large amount of energy and material in the ecosystem. This is adequate to explain why we especially need to protect these bird species.
This evaluation result based on emergy theory can provide high comparability between different services, especially the intermediate service values of the Liaohe estuarine wetland ecosystem, and can draw more attention to the service process of an ecosystem from decision makers and managers. This evaluation and classification method of ecosystem services in not only suitable for the Liaohe estuarine wetland ecosystem, but can be applied to other ecosystems, such as forest and grassland ecosystems.

Conclusions
This study evaluated the ecosystem service value of the Liaohe estuarine wetland by adopting the emergy analysis method. The ecosystem service values of the Liaohe estuarine wetland were classified as either ultimate or intermediate service values based on emergy flow, which avoided double counting in ecosystem service values, and increased the accuracy of the evaluation result. We concluded that the ultimate service value of this wetland ecosystem was mainly embodied in flood diversion and storage, and atmospheric adjustment services, and the intermediate service value was in maintaining biodiversity. This study can more explicitly explain the ecosystem service value of the Liaohe estuarine wetland for managers, promoting protection policies and actions in total storage capacity, reed areas, and bird populations in this wetland ecosystem.
We also noticed limitations of this emergy analysis method. First, data acquisition was difficult in the region due to a lack of an ecosystem-monitoring system. It is easy for deviations from the actual results to appear with our estimation method to obtain the data. Second, the selection of the emergy value units (transformity and specific emergy) directly affected the credibility of the evaluation result. In this paper, the emergy value unit was mainly based on the research results of Odum and Brown, which are mostly conclusions on a global scale. Although the local emergy unit value was difficult to obtain, it was more adaptable for emergy calculation in the local region. Finally, the continuous evaluation of some ecosystems should be implemented based on continuous monitoring of data to recognize ecosystem-service trends, which can assist decision makers in developing better ecological-protection planning and measurement of management.
Based on this study case, the calculation method of ultimate and intermediate service values of a wetland ecosystem based on emergy theory can be applied to other wetland systems. The calculation results would also provide a more appropriate reference to decision makers, and draw more attention to the service process of wetland systems, promoting the simultaneous sustainable development of human society and the natural environment.