To quantify the historical ecosystem changes in the Bohai Sea, the Ecopath models (EWE 6.2) were developed in three time periods (1982–1983, 1992–1993 and 1998–1999), where measured data was available. The trends in the structure, maturity and keystone of the Bohai Sea ecosystem from 1982 to 1999 were assessed and planning and management measures were proposed. Numerical results indicated that (1) the ecosystem size of the Bohai Sea in terms of flow is becoming small; (2) the Bohai Sea has experienced a decline in maturity ascribed to the anthropogenic and natural factors; (3) the Bohai Sea ecosystem is in the developing state. In addition, organisms of the highest trophic level (trophic level ≥3.34), such as Squid, exert significant influences on the Bohai Sea ecosystem, but their biomass is declining. To alleviate and prevent further decline in the ecosystem size in terms of flow and maturity of the Bohai Sea, ecosystem-based management and abundance of organisms of the highest trophic level need to be considered in future conservation planning and management.
The Bohai Sea is traditionally known as a ‘fish storehouse’, a ‘Salt storehouse’ and an ‘oil storehouse’. The region around the sea contributes to one tenth of China's gross national product (Zhang et al., 2009), but the Bohai Sea ecosystem has been degraded due to pollution, overfishing, eutrophication, climate change, etc. (Sündermann and Feng, 2004; Jin, 2004; Lin et al., 2001). It is necessary to understand the status of the ecosystem in order to guide the conservation planning and management actions for improving the Sea's capacity to provide services.
The Ecopath model was proposed by Polovina (1984) to describe the coral reef ecosystem. It was further developed by Christensen and Pauly (1992). This model has been successfully applied to study the structures and functions of the ecosystems ranging from ponds, rivers, and lakes to estuaries, coral reefs, shelves and open sea (Pauly et al., 2000), such as applications in Great South Bay (Nuttall et al., 2011), Bengal bay (Ullah et al., 2012), Lake Awassa of Ethiopia (Fetahi and Mengistou, 2007), and the shallow coastal ecosystem of Sri Lanka (Haputhantri et al., 2008).
This model was also used to assess the previous status of the Bohai Sea. Using fisheries resources data collected during April 1982 to May 1983, Tong et al. (2000) constructed an Ecopath model for the Bohai Sea. With the fishery resource and environment data from 1982 and 1992, Lin et al. (2009) used Ecopath to analyze the changes of the Bohai Sea ecosystem structure and fishery resources between those years. But they described the maturity roughly and did not analyze the species keystoneness index. Xu et al. (2011) examined the ecosystem changes in the Bohai Sea for over last 50 years by using the Ecopath. However, they only focused on the impact of fishing on the ecosystem changes and fisheries resource. The biomass of functional groups in 1959 and 1998 was estimated and the ecosystem maturity and species keystoneness indices were not analyzed in detail. To improve the Bohai Sea's capacity to provide services, it is necessary to know the status of ecosystem. Therefore, the mass-balanced Ecopath (EWE 6.2) models were constructed for three periods (1982–1983, 1992–1993 and 1998–1999) to study the status of ecosystem. Trends in structure, maturity and keystoneness indices from 1982 to 1999 were obtained and the measures were proposed in this study.
Materials and methods
The Bohai Sea (37°07′–41°00′N; 117°35′-122°15′E) is a nearly closed in inland sea, surrounded by land except on the sea side (Figure 1). It is enclosed by Liaodong and Shandong peninsulas and connected with northern Yellow Sea. The area is 77,000 km2 and the average depth is 18.7 m. It is located in the north of temperate zone. The annual average temperature and precipitation are 10.7°C and 500–600 mm, respectively. The salinity is 30%.
After input of all the initial parameters estimates, the Ecopath model needs to be tuned for ensuring the balance of input and output. The balanced model must meet two basic conditions:
The value of EE is between 0 and 1;
Respiration of each functional group is positive, which implies that the assimilation is greater than the production for each functional group.
Assessment of ecosystem status
A number of ecosystem metrics (Table 2) have been used to assess the basically structural properties of the Great South Bay (Nuttall et al., 2011), which sites at a similar latitude to the Bohai Sea. The same metrics were used to evaluate the ecosystem structure of the Bohai Sea as well. Among the metrics, Total System Throughput (TST) was used as the “size of the entire system in terms of flow” (Ulanowicz, 1986). The remaining metrics were described in Nuttall et al. (2011).
Odum (1969) presented an intuitive concept of ecosystem maturity and suggested that ecosystems evolve in succession toward maturity, such as from a grass field to a young forest and, then, to a “mature” forest. Odum (1969) presented 24 attributes to characterize the maturity of ecosystem. Ulanowicz (1986) augmented this list with his work. Herendeen (1989) investigated the variation of energy intensity, exergy and ascendency and analyzed their sensitivities over time with the dynamic model of ecosystem. Combined with various measures of exergy (Mejer and Jorgensen, 1979) and ascendency (Ulanowicz, 1986), Christensen (1995) quantitatively investigated and explained the power of Odum's attributes. Nuttall et al. (2011) utilized the methods of Odum (1969), Ulanowicz (1986), Herendeen (1989) and Christensen (1995) to assess the maturity of the Great South Bay with 24 attributes (Table 3). Because the Great South Bay and the Bohai Sea have a similar latitude, the above 24 attributes were also adopted to assess the maturity of the Bohai Sea. The detailed explanation of the 24 attributes was found in Odum (1969), Ulanowicz (1986), Herendeen (1989) and Christensen (1995).
Keystone species are defined as relatively low biomass species with a structuring role in their food webs. Keystoneness can be used to identify the keystone species in a given ecosystem (Libralato et al., 2006). The Keystoneness Index is a way of identifying keystone species, as it has the property of attributing high values of keystoneness to the functional groups that have both low biomass proportion and high overall effect (Libralato et al., 2006). It is very important to preserve the keystone species and thereby avoid the adverse impacts on the ecosystem.
The input and output for each Ecopath model during the above three time periods are shown in Table 1. The variation in metrics of the ecosystem structural properties for the three periods is shown in Table 2. The trends of ∑P, PP, P, TST and B suggest that the ecosystem size of the Bohai Sea declines in terms of flow from 1982 to 1999. The trends of FD and EXP indicate that the flow into detritus and out of the system decreases. The decrease of P indicates the increase of system utilization and supports the increase of system consumer identified by ∑Q and RESP. Tendency of C and C/PP demonstrates that the catch and the flow utilization descend in the Bohai Sea from 1982 to 1999.
The result of 13 out of 24 maturity indices (C, SOI, DD, FCI, PCI, PL, SPL, Oex, O, A, Red, EX and EXst) indicates that the maturity of ecosystem declines in the Bohai Sea. But the other 11 maturity indices (PP/R, PP/B, B/TST, B/(PP + R), PP − R, B/P, FCI - PCI, B/(R + EXP), R/B, I, A/C) behaved inversely (Table 3). Overall, the maturity of the Bohai Sea ecosystem declines during 1982–1999.
The proportion of ϵ at trophic level (TL) in functional groups has been nearly unchanged for 2.00 ≤ TL ≤ 3.00 since 1982 (Figure 2) and the “ϵ” represents the impact of functional group on the entire ecosystem. The proportion of ϵ at trophic level of Polychaetes increases slightly and that of other crustacean decreases slightly. The functional groups in 3.00 ≤ TL ≤ 3.34 are still controlled by Oratosquilla oratoria, whose proportion of ϵ at trophic level is the largest. In addition, the proportion of ϵ at trophic level in other demersal fishes and Engraulis japonicas decreases. The functional groups in 3.34 ≤ TL are increasingly controlled by Scomberomorus niphonius. Additionally, their cumulative impact of the entire trophic level on the ecosystem (ϵTL/ϵTotal) is always the largest during 1982–1999. This indicates that the highest trophic level species play an important part on the Bohai Sea ecosystem.
A Keystoneness Index of about 33.3% functional groups (4 of 12) is changed by more than six positions during 1982–1999 (Figure 3). The high value of total impact and keystoneness index represents the large influence of the group on the ecosystem. During 1982–1983 and 1992–1993, the Bohai Sea is heavily affected by Oratosquilla oratoria and Squid. The top keystone functional groups are changed to Scomberomorus niphonius and Squid during 1998–1999. Squid always influences the ecosystem strongly.
Our results showed that TST of the Bohai Sea is very small (3259.1355–5369.4956 t.km−2.y−1) compared to TST (486690.70–489083.00 t.km−2.y−1) of the Great South Bay (Nuttall et al., 2011), TST (43016 t.km−2.y−1) of the Delaware Bay (39°03′N; 75°08′W) and TST (45415 t.km−2.y−1) of the Chesapeake Bay (37°14′N; 76°07′W) (Monaco and Ulanowicz, 1997; Su et al., 2002). This means the Bohai Sea ecosystem is minor in terms of flow. In addition, TST of the Bohai Sea declines from 1982 to 1999, which indicates that the ecosystem size of the Bohai Sea is becoming small in terms of flow.
The results also showed that the Bohai Sea ecosystem has experienced declining in maturity, which can be attributed to the anthropogenic and natural factors. From an anthropogenic perspective, the pollution, overfishing, and eutrophication contribute to the maturity decline. Jin (2004) showed that the pollution and overfishing cause the degradation of the Bohai Sea ecosystem, which also contributes to the maturity decline. The Bohai Sea is a main water-receiving body of industrial and agriculture sewage from the surrounding provinces and cities (Zhang et al., 2009). About wastewater of 2.8 × 109 t and other pollutants of 7 × 105 t are discharged into the Bohai Sea from the river runoff each year (approximately 50% of China's total maritime discharge of pollutants) (Zhou et al., 2012). Furthermore, over the past half century, the fishing effort has been increased about 40 fold in the northern part of China (Jin, 2000). Eutrophication increases the frequency of harmful algae blooms (HABs). Only 10 HABs incidents occurred from 1952 to 1990, but the number of HABs increases to 27 between 1991 and 1998 (Zhang et al., 2006). The increase of incident numbers has many adverse environmental effects on the Bohai Sea ecosystem. From a natural perspective, the sea surface salinity (SSS), air temperature (AT) and sea surface temperature (SST) have influences on the ecosystem partly. The increase rate of the annual mean SSS, AT and SST in the Bohai Sea are 0.074 psu.y−1, 0.024°C.y−1 and 0.011°C.y−1, respectively, which have adverse effects on the Bohai Sea ecosystem (Lin et al., 2001).
Odum (1969) suggested that ecosystems can evolve from developmental to mature stage. Our results showed that the Bohai Sea ecosystem is in the developing state by several maturity metrics during 1982–1999. For mature ecosystems, PP/R is expected to be approaching one (Odum, 1969). However, PP/R of the above three study periods is high (10.2659, 10.0319, 6.7279) compared to PP/R (1.3) of the Delaware Bay and PP/R (0.5) of the Chesapeake Bay (Monaco and Ulanowicz, 1997). Low PP/B is expected for ecosystems in mature stage (Odum, 1969). PP/B of the above three study periods (181.0291, 152.6177, 146.8672) is higher than 56.04–58.52 estimated for the Great South Bay (Nuttall et al., 2011), 0.035 for the Delaware Bay and 0.033 for the Chesapeake Bay (Monaco and Ulanowicz, 1997). Finn's Cycling Index (FCI) is used as proportion of throughput cycled within the ecosystems and large FCI value is expected for mature ecosystems (Finn, 1976; Odum, 1969). However, a small proportion of throughput (FCI = 0.85–1.51%) is recycled in the Bohai Sea compared with 1.0–4.0% for the Great South Bay, 37.3% for the Delaware Bay and 24.1% for the Chesapeake Bay (Monaco and Ulanowicz, 1997).
In the Bohai Sea, the ecosystem size in terms of flow becomes small. Maturity declines and the ecosystem were in the developing state between 1982 and 1999, indicating the degradation of the Bohai Sea ecosystem. Because the anthropogenic factor exerts significant impacts on the degradation of ecosystem (Ning et al., 2010), the anthropogenic activities should be considered for protecting the ecosystem. Recently, ecosystem-based management has been paid much attention. It emphasizes human dependence on ecosystems, humility, and precaution in how we interact with and use the environment (Kai et al., 2009). Especially, it emphasizes the importance of ecosystem structures and functions which provide a range of services (Curtin and Prellezo, 2010). The idea has been applied to the effective protection of marine environment in many places, such as Canada's East and West coasts (O’Boyle and Jamieson, 2006), Puget Sound, Washington (Kai et al., 2009), and the Southern Cone of South America (Gelcich et al., 2009). Consequently, ecosystem-based management should be considered and employed to alleviate or prevent the decline of ecosystem size in terms of flow and maturity to improve the services provided by the Bohai Sea's capacity.
The species of the highest trophic level, such as Squid, have important influences on the Bohai Sea ecosystem between 1982 and 1999. However, their biomass decreases during 1982–1999, for instance, the biomass of Squid falls from 0.38 t.km−2 in 1982–1983 to 0.008 t.km−2 in 1998–1999. Depletion of top consumers leads to the trophic-level dysfunction and increases the instability of ecosystem (Steneck et al., 2004). In addition, the consumers of the highest trophic levels, especially predators, suffer more from the exploitation compared to those of low trophic levels (Sandin and Sala, 2012). Consequently, the efforts should be taken to increase or to maintain the biomass of the species of the highest trophic level. The control of activities affecting the species of high trophic levels (such as fishing) has significant impacts on the community dynamics (Halpern et al., 2006). Therefore, the activities affecting the species of the highest trophic level (such as fishing) should be given importance in the future of conservation planning and management actions.
Analysis of the Ecopath models indicated that the ecosystem size of the Bohai Sea in terms of flow and maturity has declined during 1982–1999. This result means that the structures and functions of the Bohai Sea ecosystem can't provide services well and reflects the degradation of ecosystem. To alleviate and prevent further decline in ecosystem size in terms of flow and maturity, ecosystem-based management should be taken into account in the future of conservation planning and management. In addition, the species of the highest trophic level, such as Squid, play an important role in the Bohai Sea ecosystem and their biomass has been decreased. Therefore, their low abundance should be paid attention to in the future of conservation planning and management.
This study was supported by the Tianjin Oceanic Administration through the marine promotion project with science and technology (KJXH2011–15).