States, Trends, and Future of Aquaponics Research

: As an environmentally-friendly aquaculture and planting system, aquaponics has attracted attention in various ﬁelds, such as ﬁsheries, agriculture, and ecology. The existing review qualitatively described the development and challenges of aquaponics but lacked data support. This study selected 513 related documents (2000–2019) in the Web of Science database (WOS) to mine and quantitatively analyze its text data. The keyword co-occurrence network shows that the current aquaponics research mainly focuses on the system components, wastewater treatment, nutrient management, and system production. Research areas reﬂect obvious regional characteristics. China, the United States and Europe are dedicated to the application of new technologies, the optimization of system production, and the exploration of multiple roles. At present, the aquaponics development is facing many pressures from management and market. Future research requires more in-depth research in the system construction, nutrient management, and microbial community structure to provide a theoretical basis. Moreover, the identity construction within the conceptual framework of green infrastructure is a research direction worth exploring to solve low social recognition for aquaponics.


Introduction
In order to meet human demand for aquatic products, total global aquatic production increased by 27.5% in 2010-2018, during which aquaculture and capture output increased by 29.8% and 10.4%, respectively (FAO, 2018). Currently, capture has severely damaged species diversity [1,2], and traditional aquaculture also causes a series of problems. First, traditional aquaculture is characterized by crude management based on the natural environment [3], where weather changes and exogenous pollutants increase the risk of aquaculture disease. For instance, continuous rain will prevent the photosynthesis of phytoplankton from proceeding normally, causing water hypoxia. Secondly, the aquaculture area discharges a considerable amount of wastewater containing nitrogen, phosphorus [4], antibiotics [5], and other pollutants [6]. In addition, large-scale aquaculture of commodity fish reduces the habitat of other species [7] and disrupts the balance of the ecosystem. Therefore, it is imperative to develop a new environmentally-friendly aquaculture form.
Aquaponics is an integrated system of aquaculture and hydroponic cultivation [8]. Water circulates between the components of the system (fish tank, biofilter, hydroponic system), during which the feces of the fish become fertilizers for the plants [9], and the nitrifying bacteria in the biofilter convert the nitrogen form from ammonia to nitrate, which is absorbed by the plants [10]. The cycle of water and

Cluster Analysis
This study selected the six most creative countries related to aquaponics research and compared the research areas (identified by WOS database) of these countries. In order to facilitate comparison, the number of publications in different countries is normalized using z-score method, and cluster analysis is conducted for the research areas of these countries.

The Publication Growth Trend Analysis
In total, 513 publications (include articles, reviews, patents, and books) with "aquaponics" during 2000-2019 were refined from WOS database, and the annual change of publications containing highfrequency keywords with different average published time, publications of most creative countries, and common research areas were analyzed to show the growth trend of aquaponics research.

Data Processing and Visualization
Co-occurrence networks analysis of keywords and research institutes were performed using Vos viewer software. The analysis and visualization of the country's cooperation relationship were completed through the online analysis platform (bibliometric.com). The heat map was implemented using "pheatmap" package through R 4.0.1. Other diagrams were drawn using origin 2017.

Hot Issue and Research Area of Aquaponics
The keyword co-occurrence network reflects the research hotspot of aquaponics ( Figure 1). Among selected keywords, "aquaponics" has the highest frequency in publications as the center of the co-occurrence network. Followed by keywords such as "aquaculture", "hydroponic", "growth", "water", and "nitrogen" closely related to the "aquaponics". The publications of other keywords are relatively low. The overall network is radial, and the number of publications of keywords decreases with its increasing distance from the center.  According to the degree of association between keywords, the entire co-occurrence network is divided into four clusters with different colors. Cluster 1 (green) takes "aquaponics" as the hub, mainly focusing on the research of various parts of aquaponics (such as hydroponic). Since water is the carrier of nutrient circulation in system, hydroponic types is an important basis for distinguishing Sustainability 2020, 12, 7783 4 of 14 the aquaponics type, tilapia and lettuce are the most common fish and plants in aquaponics research, so keywords "water", "hydroponic", "Tilapia", and "lettuce" are most closely related to "aquaponics". Cluster 2 (red) takes "aquaculture" and "wastewater" as the hubs. An in-depth study was processed on the water management of aquaponics wastewater, for which "nitrification" and "denitrification" are the main regulation mechanism. Cluster 3 (yellow) mainly focuses on the study of nutrient circulation and distribution. Currently, nitrogen is the most studied nutrient element, and pH is the key factor affecting nutrient circulation. "growth" is the hub of cluster 4 (blue) which mainly discusses aquaponics production [22][23][24]. A series of requirements for system output were proposed, such as growth, yield, quality, and sustainability. In addition, compared with fish, plants are the main object of research in the cluster.
Aquaponics has attracted wide attention. Survey of the literature related to aquaponics in WOS database shows highest publications and citations in fishery-and agriculture-related research areas (MARINE FRESHWATER BIOLOGY, FISHERIES; AGRICULTURE, PLANT SCIENCES), indicating the greatest concern for aquaponics production. In addition, the hot issue of aquaponics also involved research areas including ENVIRONMENTAL SCIENCES ECOLOGY, BUSINESS ECONOMICS, ENGINEERING, etc. Feasibility of aquaponics was analyzed from the perspective of environmental and market benefits, and system optimization was completed through the design of devices and the application of new technologies. As mentioned in the introduction, aquaponics can treat aquaculture wastewater and improve water use efficiency. Therefore, WATER RESOURCES is also a hot research area for aquaponics (Table 1).  (Table 2). Zurich University is the most influential institute, which carried out a series of studies on the factors affecting plant growth in aquaponics. It was found that the lack of potassium inhibited the growth of plants [25], and different treatments of aquaponics wastewater also had a significant effect on the growth of plants due to different products [26]. However, the hydroponic type has no significant effect on plant growth [27]. In addition, the agency also involved the model construction of decoupled aquaponics to simulate the dynamic changes of water, nitrogen, phosphorus, sludge, fish, and plants in the system [28]. Further, the microbial diversity of each component of the system was also explored [29]. Wageningen University is the most productive institute in aquaponics research. Compared with the Zurich University, Wageningen University's participation in research is more biased towards the commercialization and promotion of aquaponics. Optimization of system management was performed by constructing several models for different aquaponics type. The promotion of commercial aquaponics was performed through the system definition, market research, and economic feasibility analysis [30][31][32][33][34]. In addition, Shandong University and the University of Hawaii participated in a series of studies on the dynamic changes and distribution of nitrogen forms in aquaponics, and conducted an in-depth exploration of the influencing factors, such as pH [35], season [36], and plant species [37].
Selecting 30 high-frequency keywords from the publications of high-influence institutes for co-occurrence network analysis (Figure 2), the results show that the research of selected institutes mainly involved the growth of fish and plants (yellow), aquaculture (blue), and other related research areas (green). Similar to the previous keyword analysis result, the research on the growth of fish and plants in aquaponics includes several keywords, such as "yield", "quality", and "sustainability". For aquaculture, these institutes mainly focused on nitrogen transition and sewage treatment. In addition, these institutes also conducted research on hydroponic systems, involving keywords, such as "nitrogen", "water", and "agriculture", but showed no clear research direction.  Wageningen University is the most productive institute in aquaponics research. Compared with the Zurich University, Wageningen University's participation in research is more biased towards the commercialization and promotion of aquaponics. Optimization of system management was performed by constructing several models for different aquaponics type. The promotion of commercial aquaponics was performed through the system definition, market research, and economic feasibility analysis [30][31][32][33][34]. In addition, Shandong University and the University of Hawaii participated in a series of studies on the dynamic changes and distribution of nitrogen forms in aquaponics, and conducted an in-depth exploration of the influencing factors, such as pH [35], season [36], and plant species [37].
Selecting 30 high-frequency keywords from the publications of high-influence institutes for cooccurrence network analysis (Figure 2), the results show that the research of selected institutes mainly involved the growth of fish and plants (yellow), aquaculture (blue), and other related research areas (green). Similar to the previous keyword analysis result, the research on the growth of fish and plants in aquaponics includes several keywords, such as "yield", "quality", and "sustainability". For aquaculture, these institutes mainly focused on nitrogen transition and sewage treatment. In addition, these institutes also conducted research on hydroponic systems, involving keywords, such as "nitrogen", "water", and "agriculture", but showed no clear research direction.  In general, the current research on aquaponics involves many fields such as fisheries, agriculture, environment, and economy. These studies mainly focused on the system itself, wastewater treatment, nutrient cycling, and crop growth. Less focus on crop growth was found in research, and the word frequency analysis also shows that the identity of aquaponics is biased toward aquaculture systems. However, "fish" and "plant" have the same word frequency. The reason for this phenomenon may be because the functions of fish and plants in the system are different. Fish in the system are mainly regarded as products or nutrients providers for plants, and plants in the system can play roles in treating farming wastewater, providing a microorganism growth environment and promoting nutrient circulation. Due to the critical role of plants in the operation of the system, the fact that plants are also system products was ignored by researchers. Even more, aquaculture management is more difficult in aquaponics operation, and hydroponic technology is basically mature. As a result, scholars prefer to regard aquaponics as an aquaculture form.

Overview for the Research of Top 10 Influential Literature
As shown in Table 3, the highly cited literature was published in 2008-2016 (the period of rapid development of aquaponics research). These reports mainly discussed the role of various factors (pH, plant species, etc.) and the N 2 O emissions during the nutrient cycle in aquaponics, which aims to improve the system production efficiency and reduce costs in order to maximize the benefits. Commercialization, sustainability, and challenges of aquaponics were also illustrated and analyzed. The most cited literature mainly summarized the challenges and solutions of fishery development. The survey introduced aquaponics as a new aquaculture system, compared with systems providing similar services, such as the recirculating aquaculture system (RAS). It was suggested that the existing aquaponics cannot provide the best growth conditions for fish, plants, and microorganisms at the same time, nor does it construct a model to adapt to the large-scale production [38].
Word frequency analysis was performed on the high-cited literature abstracts and 15 high-frequency keywords were selected (Table 4). Unlike the results of the co-occurrence network, high-frequency keywords involved aquaponics components, wastewater treatment, and nutrient circulation, but not growth-related research. Among them, "aquaculture" appears more frequently than "hydroponics", and "agriculture" does not appear in the selected high-frequency words, indicating that aquaponics is more frequently described as an aquaculture system than hydroponic system or agricultural system. "Fish" and "plant" appear at the same frequency, indicating that although the identity of the system is biased towards aquaculture, however, both fish and plants are important research objects for aquaponics.

Regional Differences of Research Direction
Institute co-occurrence network is linear (Figure 3a), and a low-degree connection between countries was revealed (Figure 3b). The collaboration relationship reflected obvious geographic relevance, pointing that independent research and local regional cooperation are the main forms of organization for aquaponics research. The research on aquaponics carried out by relevant institutions in Europe and China was later than that in the United States. Different development of aquaponics research may be due to the different attitudes towards the aquaponics system. According to surveys of relevant practitioners in USA [16] and Europe [42], compared with USA, practitioners in Europe had better educational background, the proportion of practitioners with a post-graduate degree was 91.7%, which was only 24% in USA. However, the proportion of commercial production was lower, which was 19.1% in Europe and 32% in USA. In the Different development of aquaponics research may be due to the different attitudes towards the aquaponics system.
According to surveys of relevant practitioners in USA [16] and Europe [42], compared with USA, practitioners in Europe had better educational background, the proportion of practitioners with a post-graduate degree was 91.7%, which was only 24% in USA. However, the proportion of commercial production was lower, which was 19.1% in Europe and 32% in USA. In the survey, 42.6% of participating organizations in Europe were universities. Most practitioners in Europe tended to regard the aquaponic system as a studying tool, not a production tool.

The Hot Issue Transition of Aquaponics Research
The average published year of keywords indicated the development trend of aquaponics ( Figure 4). Some new keywords have appeared in research related to aquaponics production and wastewater treatment. For aquaponics production, more demand for system output is emerging, such as "yield", "sustainability", and "quality". For wastewater treatment, the removal efficiency of denitrification and nitrification in aquaponics are being further studied [43]. Generally, the entire network is radial, and shows obvious transition from internal components (fish, water, nitrogen, etc) to external characteristics (yield, quality, sustainability).
Sustainability 2020, 12, x FOR PEER REVIEW 9 of 14 monitored the TDS value in the aquaponics system through IoT technology in order to determine the feeding strategy [48].

Annual Changes in Publications
The growth trend of aquaponics research was described through annual changes in publications. There is a significant literature gap regarding aquaponic systems in terms of aquaculture and hydroponic (Figure 5a). To a certain extent, this confirms the view that the system positioning is biased towards aquaculture. Non-linear fitting and simple prediction were performed for the growth Besides keywords in the co-occurrence network, currently, some new topics have been suggested, such as feasibility of aquaponic system. Researchers compared the input and output of aquaponics products: the energy cost of tilapia production was twice higher than that of plants [11]. Maucieri built a micro-aquaponic system (1.5 m 2 ) using recycled material and tested its feasibility through life cycle assessment (LCA) analysis [44]. Ghamkhar performed a LCA analysis for the aquaponic system in a cold climate to evaluate the impact of fish food, equipment, electricity, and heat on several environmental issues [45]. In addition to product properties, the educational function of aquaponics is also receiving increasing attention as a teaching tool for environmental science [46].
New technologies began to be applied in aquaponics. For instance, Kyaw designed a temperature sensor to control tank water temperature through an android application [47]. Wibowo monitored the TDS value in the aquaponics system through IoT technology in order to determine the feeding strategy [48].

Annual Changes in Publications
The growth trend of aquaponics research was described through annual changes in publications. There is a significant literature gap regarding aquaponic systems in terms of aquaculture and hydroponic (Figure 5a). To a certain extent, this confirms the view that the system positioning is biased towards aquaculture. Non-linear fitting and simple prediction were performed for the growth trend using the Logistic model (Levenberg-Marquardt algorithm), the fitted curve roughly matches the trend (R 2 = 0.9912). The growth trend of publications was in line with the characteristics of the second stage of the sigmoid growth curve. The growth rate of aquaponics research increased sharply since 2010 and slowed down slightly after 2018.A similar situation appeared in publications with "aquaculture" and "hydroponics". The forecast of growth trend shows that the related publications will continue to grow in the future, but there is a possibility that the growth rate will decline, or even enter the third stage of the Sigmoid growth curve in the next few years. Except "growth", both the growth trend of other selected keywords related publications slowed down after 2017 (Figure 5b). A similar situation also occurs in the publication growth trend of selected countries (Figure 5c) and research areas (Figure 5d). The results supported this possibility to some extent. The slowdown in the growth trend of publications The forecast of growth trend shows that the related publications will continue to grow in the future, but there is a possibility that the growth rate will decline, or even enter the third stage of the Sigmoid growth curve in the next few years. Except "growth", both the growth trend of other selected keywords related publications slowed down after 2017 (Figure 5b). A similar situation also occurs in the publication growth trend of selected countries (Figure 5c) and research areas (Figure 5d). The results supported this possibility to some extent. The slowdown in the growth trend of publications indicates that the research and development of aquaponics are facing a strong challenge.

Future of Aquaponics Research
Several researchers summarized the challenge of aquaponics development, there are two major issues need to be solved urgently: (1) The operation and maintenance of aquaponics need more strategy [39] because insecticides and antibiotics cannot be used in aquaponics, it is difficult to prevent fish and plants from disease and pests [14]. In addition, plants have different requirements for nutrients at different growth stages [49], and it has not been resolved how to integrate the hydroponic subsystems with the aquaculture one to maximize nutrient utilization efficiency, so more culture strategies are urgently needed [23]. (2) Low social recognition: for aquaponics commercialization, high investment [34] causes high price of aquaponics products, and there is currently no policy to subsidize the initial investment in the construction of aquaponics. There are also problems, such as lack of understanding of the new method, uncertainty about its benefits, and concerns about health risks for consumers [50,51]. Without market and policy support, farmers cannot afford the cost of large-scale production, which limits the development of aquaponics.
More theoretical support is required for aquaponics culture strategy. Completed culture strategy consists of system construction and nutrient management. For system construction, the effects of influencing factors are not standardized under different aquaponics conditions (fish and plants species, hydroponics types, growth medium, etc.). Research on more effective biological methods is essential for possible risks of disease and pest. For nutrient management, the main studied element is nitrogen. Research on other elements (such as phosphorus, potassium, and sulfur) distribution in the system is needed for more comprehensive nutrient management. Current research mainly focuses on the morphological distribution and overall utilization of elements in aquaponics components. It is urgent to study the temporal dynamic changes of elements in order to coordinate fish and plants growth for finer nutrient management. In addition, microbial community drives element (such as nitrogen) circulation in aquaponics and plays a key role in nutrient management and wastewater treatment. Research on the microbial communities has been processed but far from enough [52,53].
Improving market recognition needs to start with clarifying identity. As mentioned above, several studies on multi-role of aquaponics have been conducted, however, aquaponics positioning in future production and life is still unclear. As a result, related research has been involved in various disciplines, but not in-depth. There is an urgent requirement to combine the development of aquaponics with urban construction in a new conceptual framework. Green infrastructure is a type of interconnected green space network that is planned and managed for its natural resource values, and for the associated benefits, it confers to human populations [54], which has practical significance for urban planning and construction [55]. Aquaponics has functions of production, protection of biodiversity, water saving, and etc. It is a good combination of natural resources and human well-being, in line with the purpose of green infrastructure [56]. Incorporating aquaponics into the category of green infrastructure can help clarify the role in urban construction and provide the direction for aquaponics research. In addition, green infrastructure construction has been widely processed [57,58]. Identity building under the framework of green infrastructure can provide a development environment and policy support for aquaponics.

Conclusions
At present, aquaponics research mainly focuses on the system components, wastewater treatment, nutrient management, and system production. USA, Europe, and China are the most creative regions with significantly different research directions. The aquaponics research spread from USA to Europe, research issues are expanding from internal components to external characteristics, and aquaponics identity shifted from production to multi-roles. The aquaponics development has great potential, but faces challenges of management and market. For management, more research on influencing factor, nutrient and microbial community in aquaponics are required. For market, completing the identity construction within the framework of green infrastructure provides research directions, development environment, and policy support for aquaponics. Aquaponics identity in urban production and life needs clarifying within the new conceptual framework to gain market recognition. Incorporating aquaponics into the category of green infrastructure can provide it with research directions, development environment, and policy support.