Vol. 9: 479–490, 2017 AQUACULTURE ENVIRONMENT INTERACTIONS Published December 5 https://doi.org/10.3354/aei00247 Aquacult Environ Interact OPENPEN ACCESSCCESS Model-based analysis of the energy fluxes and trophic structure of a Portunus trituberculatus polyculture ecosystem Jie Feng1, Xiang-Li Tian1,*, Shuang-Lin Dong1, Rui-Peng He1, Kai Zhang1, Dong-Xu Zhang1, Qing-Qi Zhang2 1The Key Laboratory of Mariculture, Ministry of Education, Fisheries College, Ocean University of China, Qingdao 266003, PR China 2Marine Fishery Technology Guiding Office of Ganyu, Lianyungang 222100, PR China ABSTRACT: We constructed a quantitative Ecopath model of a trophic network to evaluate the energy flow and properties in a polyculture ecosystem containing 4 species (swimming crab Por- tunus trituberculatus, white shrimp Litopenaeus vannamei, short-necked clam Ruditapes philip- pinarum, and redlip mullet Liza haematochila) over a 90 d experimental period. The model con- tained 10 consumers, 4 detritus groups, and 4 primary producers. Ecotrophic efficiency values indicated that the system had high energy utilization efficiency. However, benthic bacteria con- verted the largest amount of energy back to the detritus groups, which had the lowest ecotrophic efficiency (0.01). When aggregating the network to discrete trophic levels (TLs), most of the throughput and biomass of the system were distributed on the first 2 TLs; consequently, there was high energy transfer efficiency between TL I and II (81.98%). The trophic flow of this ecosystem was dominated by energy that originated from the detritus groups (73.77%). Imported artificial food was particularly important for the trophic flow of the total ecosystem, contributing 31.02% to total system consumption. The trophic network of the polyculture ecosystem had a moderate Finn’s cycling index (17.44%), a relatively low connectance index (CI: 26.70%), and a low system omnivory index (SOI: 0.08). Relative ascendancy was estimated as 44.90% in this model. Overall, ecosystem properties (i.e. CI, SOI, and relative ascendancy) showed that the artificial 4-species polyculture system represents a simple and fragile, but also ‘balanced,’ ecosystem. KEY WORDS: Energy flow · Trophic structure · Ecopath · Polyculture · Portunus trituberculatus INTRODUCTION economic benefits over monoculture systems when suitable farming densities are used (K. Zhang et al. The swimming crab Portunus trituberculatus is one 2016). Such benefits include improved food resource of China’s 3 major crab species used in aquaculture utilization, increased aquatic production, and en- (Song et al. 2006) and is widely cultured on the coast hanced water quality (Dong 2015). Among the differ- of China, with production reaching 117 772 t in 2015 ent polyculture modes associated with P. trituber - (FDAMC 2016). Pond culture is the main culture culatus, the inclusion of white shrimp Litopenaeus mode for this species in China (Shi et al. 2010). In the van namei, short-necked clam Ruditapes philip- pond culture of P. trituberculatus, individual crabs pinarum, and redlip mullet Liza haematochila has are often polycultured with other organisms, such as proven highly effective. P. trituberculatus is often shrimp, clams, and fish, due to various ecological and fed with imported feed (blue clam Aloidis laevis), the © The authors 2017. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are unrestricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 480 Aquacult Environ Interact 9: 479–490, 2017 uneaten remains of which are a very good food straightforward construction, mass-balancing, and source for L. vannamei. R. philippinarum inhabits analysis of trophic models in aquatic ecosystems the bottom habitat of ponds, whereas L. haema- (Christensen et al. 2000). The model allows steady- tochila uses the upper part of the water column. Both state trophic interactions to be constructed for the of these species mainly feed on phytoplankton and respective ecosystems, which helps address knowl- detritus particles (Xu et al. 1987, K. Zhang et al. edge gaps of process-oriented models by pinpointing 2016). As a result, the polyculture of these 4 culture the questionable estimates of certain parameters organisms at suitable farming densities could facili- (Christensen & Pauly 1993). To date, the Ecopath tate the effective use of both food and space re - model has been widely employed to investigate vari- sources in this pond ecosystem. However, insuffi- ous types of water bodies globally, including oceans, cient data and in struction are currently available on lakes, and gulfs (Colléter et al. 2015). In contrast, few how to optimize these aquaculture activities. Conse- studies have applied this model to aquaculture pond quently, cultured organisms are often stocked by ecosystems globally or in China. To analyze the farmers empirically, with activities failing to reach energy flow and trophic structure of the P. tritubercu- potential ecological efficiency and economic benefits latus, L. vannamei, R. philippinarum, and L. haema- (Feng et al. 2015). Thus, during the last 5 yr, a series tochila polyculture system at the ecosystem level, we of standardized pond aquaculture modes associated first quantified the characteristics of the system struc- with P. trituberculatus was explored in a collabora- ture. This aim was achieved by obtaining a steady- tion between the Laboratory of Aquaculture Ecology, state, mass-balanced representation of energy flow Ocean Uni versity of China, and related fishery sec- and trophic structure over a 90 d culture period. Sec- tors. Within these modes, the polyculture of P. tritu- ond, we applied this information to evaluate the P. berculatus with L. vannamei, R. philippinarum, and trituberculatus, L. vannamei, R. philippinarum, and L. haematochila represents an optimized mode with L. haematochila polyculture ecosystem. We expected suitable farming density. our results to demonstrate how the Ecopath model The ecological characteristics of P. trituberculatus could be used to advance aquaculture practices aquaculture ponds have been extensively studied in in China, both from a scientific and a management China. These studies include investigations of struc- perspective. tural optimization that intended to improve aquacul- ture production (Zhou et al. 2010, Ban et al. 2015a), energy budgets (Feng et al. 2015), nitrogen and MATERIALS AND METHODS phosphorus budgets (Dong et al. 2013, Zhang et al. 2015a), the organic carbon budget (K. Zhang et al. Pond and enclosures 2016), and ‘emergy’ analysis (emergy analysis is a quantitative analysis technique that determines the The experiment was conducted using the land- values of non-monied and monied resources, serv- based experimental enclosures in a pond located in ices, and commodities in common units of solar Ganyu County, Jiangsu Province, China (34° 58’ N, energy; Ban et al. 2015b). These studies investigated 119° 20’ E). The pond was ~0.02 km2 in size, with a the ecological efficiency of the pond ecosystem. In water depth of 1.6 to 1.7 m. Four land-based enclo- addition, studies of organic carbon storage (D. Zhang sures, representing 4 replicates of the same size et al. 2016) investigated the structure of the ecosys- (length × width × depth = 5 × 5 × 2 m), were estab- tem, while others have investigated the characteris- lished in the pond and were lined with polyethylene tics of the phytoplankton (Fu et al. 2012), zooplank- (water-proof material) and supported with wood ton (Mao et al. 2014), and bacterioplankton commu- poles. At the bottom, the square walls of the enclo- nities (H. Zhang et al. 2008, K. Zhang et al. 2015b). sure were covered with mud from a pond, and sup- However, most studies have focused on the ecologi- ported by posts at 2.5 m intervals. An aeration system cal process of the P. trituberculatus ecosystem. Con- consisting of a blower, PVC tubes, gas tubes, and air sequently, detailed studies are required on trophic stones was used for aeration and water circulation. structure and material flow at the ecosystem scale. Five air stones connected by the gas tube were hung Here we used the Ecopath model to develop an in each enclosure, at about 20 cm from the bottom. ecosystem-based approach to analyze the energy The structure of the enclosures was described in flow and trophic structure of the P. trituberculatus detail by Tian et al. (2001) and Wang et al. (1998). polyculture at the ecosystem level. The Ecopath The entire experiment was carried out for 90 d from model is an ecosystem approach designed for the 13 July to 13 October 2014. Feng et al.: Portunus trituberculatus polyculture ecosystem model 481 Cultured animals and aquaculture management biomass of prey (i); EEi is ecotrophic efficiency (EE); Yi is the biomass that is caught; (Q/B)j is the ratio of Juvenile swimming crabs Portunus trituberculatus food consumption to biomass of predator j; DCji is the were cultured with white shrimp Litopenaeus van- proportion of prey i in the food composition of pre - namei, redlip mullet Liza haematochila, and short- dator j; BAi is the biomass accumulation rate of prey necked clam Ruditapes philippinarum in the en - (i); and Ei is the margin between immigration and closure ecosystems. All animals were purchased from emigration of prey i. Ganyu Jiaxin Aquatic Food Co., Ltd. (Ganyu, Jiangsu, The second equation represents the consumption China). P. trituberculatus, L. vannamei, L. haema- of a model group that is composed of production, tochila, and R. philippinarum were stocked in the 4 respiration, and unassimilated food: enclosures at densities of 6, 45, 3, and 30 ind. m−2, re- BBRU()Q ()P (2) spectively. The initial individual wet weights of P. i ×=×++B iiB ii i trituberculatus, L. vannamei, L. haematochila, and R. where Ri is respiration and Ui is the food that is not philippinarum were (mean ± SD) 0.57 ± 0.13, 0.045 ± assimilated. Ecopath requires that at least 3 of these 0.01, 0.67 ± 0.09, and 0.92 ± 0.11 g, respectively.