The Pearl River estuary is the second largest estuary in the South China Sea. The species composition and trophic structure of shrimp-trawl catches from this estuary were investigated using stable isotope analyses during the winter of 2012. Crabs dominated the catches, constituting 37% of the total biomass in the inner estuary and 45% in the outer estuary. The δ15N and δ13C values for particulate organic matter gradually changed from the inner to the outer estuary. δ15N of particulate organic matter was more enriched in the inner estuary, while δ13C was more enriched in the outer estuary. Higher δ15N values in the inner estuary suggested a stronger influence from anthropogenic eutrophication. The δ15N and δ13C values of shrimp-trawl catches showed the same trends as the particulate organic matter. Trophic structure and faunal composition of shrimp-trawl catches varied greatly between the inner and outer estuary areas. The trophic niches were clearly distinct among fishery groups in the outer estuary. Community-wide metrics of stable isotope values showed that there was greater diversity of food sources and more complex trophic interactions in the inner estuary, whereas trophic levels were more evenly distributed in the outer estuary.

Introduction

Estuarine ecosystems are very complex because of the high biological diversity and rapidly changing physical and biological processes (Harrison et al., 2008; França et al., 2011). Foodweb structure of estuarine ecosystems usually varies greatly with seasons, particularly in species composition and food chain length (Faye et al., 2011). On the other hand, estuary ecosystems have high primary productivity which provides plenty of food for aquatic organisms, and hence are usually important fishing grounds. However, many estuary ecosystems are threatened by anthropogenic disturbance and pollution (Hadwen and Arthington, 2007; Harrison et al., 2008).

Studies of foodweb structure are useful for detecting the consequences of environmental change through their trophic cascades, and can contribute to sustainable management of estuarine ecosystems (Pasquaud et al., 2008). Foodweb structure is central to understanding the ecological function and dynamics of aquatic systems. The trophic interactions are often complex in estuarine ecosystems as the food resources are derived simultaneously from terrestrial and marine sources (Lin et al., 2007; Faye et al., 2011). Stable carbon and nitrogen isotope ratios have become commonly indicators of trophic level and organic matter source in aquatic ecosystems (Peterson and Fry, 1987; Xu et al., 2011). Stable isotopes signatures represent an integrative record of the food that has been assimilated by a given organism. The δ13C values are usually fixed in different primary producers, and can thus be used as tracers to the original sources of carbon at the base of a food chain (Peterson and Fry, 1987). On the other hand, the δ15N signature of an organism is generally enriched by about 3.4‰ relative to its diet and these values are therefore used to indicate the trophic level of a population (Post, 2002; Gorokhova et al., 2005). This method enables us to improve our structural knowledge by positioning the different taxa in a foodweb according to their δ15N or δ13C signatures (Layman et al., 2007; Pasquaud et al., 2008). The analysis of δ15N and δ13C has become an effective tool that helps to determine the influence of eutrophication and anthropogenic impacts on foodweb structures and aquatic ecosystems (Hadwen et al., 2007; França et al., 2011). Based on the δ13C and δ15N bi-plot of fish assemblages, Layman et al. (2007) proposed six community-wide trophic metrics to estimate the trophic diversity and trophic redundancy of foodwebs. This approach represents a more effective use for stable isotope data in the analysis of consumer's trophic niches (Abrantes et al., 2014).

In this study, the biomass composition and stable isotopic signatures of C and N were examined for the shrimp-trawl catches in the Pearl River estuary (PRE) in the South China Sea. We used community-wide metrics of stable isotopic signatures to assess the trophic structure of shrimp-trawl catches. We focused on comparing the trophic structure of shrimp-trawl catches between the inner and outer estuary. Results from the present study will contribute to a better understanding of the foodweb structure and ecosystem functioning of the PRE.

Materials and methods

The Pearl River is the second largest river in China, located in the south of China and opening into the northern South China Sea. It stretches for 2214 km and drains an area of 452,000 km2 (Zhao, 1990). Its delta region is one of the fastest developing regions in the world and receives high levels of anthropogenic nutrients from agriculture, fish farming and industrial and domestic sewage effluents (Harrison et al., 2008; Hu and Li, 2009). The discharge of the Pearl River has a significant seasonal variation, with higher discharge in the wet season (June to September) and lower discharge in the dry season (October to May). The ecosystem of PRE has been widely studied with respect to species composition of plankton, physical dynamics of water mass and environmental pollution (Harrison et al., 2008; Ke et al., 2012). However, little is known about the trophic foodwebs of its fisheries.

Twenty sampling stations were selected to study the environmental conditions of PRE from 30 November to 2 December 2012 (Figure 1). Shrimp-trawl catches were collected in two zones: inner estuary (S4, S5 and S6) and outer estuary (S18, S19 and S20). Temperature and salinity were measured in situ at each station using an YSI6600 instrument (Yellow Springs Instrument Co., Yellow Springs, OH, USA). Particulate organic matter (POM) was sampled by filtering 0.25 l of surface seawater (0.5 m) on a pre-combusted (450°C, 4 h) Whatman GF/F filters (0.7 μm pore size) with a low pressure vacuum pump. Biological samples were collected using a shrimp-trawl net that was 2 m wide and had a 5 mm stretched mesh size on the cod end. The trawling speed was 3.5 knots and the trawling time was 20 min at each station. After identification, sampled organisms were initially weighed and measured. Muscle samples were then collected, including the dorsal muscle of fish, abdomen muscle of Shrimp, appendage muscle of Crabs and the foot of Snails or Shellfish. Following dissection, all samples were rinsed using distilled water and dried to constant weight in an oven at 60°C. The dried samples were then ground into homogeneous powder and stored in closed vials at −20°C for further analysis. Approximately 0.5 mg of this powder was weighed in tin capsules for stable carbon and nitrogen isotopic analysis. The 13C/12C and 15N/14N ratios were analyzed using a continuous-flow isotope-ratio mass spectrometer (Delta V Advantage, Thermo Fisher Scientific, Whaltham, MA, USA) coupled to an elemental analyzer (Flash EA 1112 Thermo Scientific, Milan, Italy). Isotope ratios were expressed relative to international standards (Pee Dee Belemnite for δ13C and atmospheric N2 for δ15N). δ13C or δ15N = [(Rsample-Rstandard)- 1]×103, where R is 13C/12C or 15N/14N. The analytical precision for the measurement was 0.2‰ for both carbon and nitrogen. No acidification was applied to the samples of trawling catches to avoid altering the isotopic signal (Mateo et al., 2008).

Community-wide metrics based on species' positions in niche space may provide for a novel way to link species richness with measures of ecosystem function (Layman et al., 2007). Six community-wide trophic metrics proposed by Layman et al. (2007) were used to compare the structure and function of the foodweb between the inner and outer PRE. These were: (1) δ13C range (CR); (2) δ15N range (NR); (3) total area (TA), convex hull area encompassed by all species in the δ13C-δ15N bi-plot space; (4) mean distance to centroid (CD), where the centroid is the mean δ13C and δ15N value for all species in the foodweb; (5) mean nearest neighbor distance (MNND) in the bi-plot space; (6) standard deviation of nearest neighbor distance (SDNND). The first four metrics mainly reflect the trophic diversity of the community and the final two metrics reflect relative position of species to each other within niche space and can be used to estimate the extent of trophic redundancy. These metric analyses were performed using the R statistical computing packages (R Development Core Team, 2007). There were 74 sampling data in the inner estuary and 109 sampling data in the outer estuary for calculating the Layman's niche metrics.

Results and discussion

The catch efficiency of the shrimp-trawl net was higher in the inner estuary with 3.62 kg catches compared to 2.87 kg in the outer estuary. Shallow depths (4–8 m) may be one important reason for the higher catch per unit effort in the inner estuary. In total, 42 different taxa were identified from the shrimp-trawl catches in this study, including 20 taxa from the inner estuary and 32 taxa from the outer estuary (Appendix 1 in the online supplementary files). The low number of species registered in this study may be linked to the lower sampling effort of 20 min trawling at each station. Species diversity within catches was greater in the outer estuary than in the inner estuary, particularly for Crabs and Snails. Among the 18 fish species we identified, only three species (Callionymus koreanus, Argyrosomus argentatus and Cynoglossus spp.) were found both in the inner and outer estuary. Most of the Shrimp were found throughout the inner and outer sampling stations, while Penaeus spp., Metapenaeopsis barbata and Solenocera crassicornis were found only in the outer estuary.

In the inner estuary, catches were mainly composed of Crabs (37%), fishes (32%) and Shrimps (30%) (Figure 2). The most abundant species were Charybdis japonica, Metapenaeus spp., Parapenaeopsis spp., Oratosquilla oratoria, Argyrosomus argentatus, Collichthys lucidus and Odontamblyopus rubicundus. These species constituted 89% of the total fisheries biomass in the inner estuary. In the outer estuary, catches were mainly composed of Crab (45%), Shrimp (28%), Snail (18%) and fish (9%). The most abundant species were Charybdis japonica, Brachytoma flavidulus, Oratosquilla oratoris, Solenocera crassicornis, Cynoglossus spp. and Apogon kiensis. These species constituted 86% of the total fisheries biomass in the outer estuary. In general, Crabs were the most dominant species in the shrimp-trawl catches, followed by Shrimp, and fishes. Shrimp-trawl nets are more effective at capturing benthic species (West, 2002), which is why our catches were mainly comprised of Crab and Shrimp in this study.

The δ15N and δ13C values of POM showed significant horizontal variations in the surface waters of PRE (Figure 3). In general, δ15N of POM was more enriched in the inner estuary, while δ13C was more enriched in the outer estuary. Shrimp-trawl catches collected from the inner estuary generally had significantly depleted δ13C signatures compared to those of the outer estuary (Figure 4). The δ13C values of shrimp-trawl catches ranged from -17‰ to -25.1‰ in the inner estuary and from −14.1‰ to −16.5‰ in the outer estuary. These results were consistent with the δ13C distribution of POM in the surface waters of PRE. Terrestrial organic matter usually has a more depleted stable isotope signature in aquatic ecosystems (Vizzini and Mazzola, 2003). This can be explained by the gradual mixture of fluvial or terrestrial (light δ13C) and marine (heavy δ13C) sources of organic matter in estuaries (Fontugne and Jouanneau, 1987). Our results also showed that the δ13C and δ15N of POM was significantly correlated with salinity (p < 0.05), which suggests that stable isotope signatures of POM can be used as reliable indicators for the water mass in estuarine ecosystems. In contrast, the shrimp-trawl catches generally showed enriched δ15N in the inner estuary (Figure 4). For example, the δ15N of Scapharca sp., a filter-feeding Shellfish, was 13.58‰ in the inner estuary and 8.19‰ in the outer estuary. Hadwen and Arthington (2007) indicated that δ15N is usually enriched in the inner estuarine region, since these areas receive greater levels of terrestrial input or sewage effluent. The Pearl River delta is the economic and cultural center of southern China, and as a result PRE receives high levels of nutrient loading from extensive agricultural and urban development (Harrison et al., 2008; Hu and Li, 2009). In the present study, the average concentration of dissolved inorganic N was more than 140 μmol l−1 at the trawling stations within the inner estuary. The higher δ15N in the inner estuary suggests a stronger influence from anthropogenic eutrophication.

Significant variations in δ13C and δ15N occur in different aquatic ecosystems (Vuorio et al., 2006). Moreover, many studies indicate that a measure of the stable isotope baseline is very important in studies of foodweb structure using δ13C and δ15N signatures (Sweeting et al., 2005; Xu et al., 2010). In general, primary consumers can act as baseline organisms to eliminate variation in baseline δ15N and δ13C values. However, it can be difficult to collect the same species in different areas of an estuary. Our results indicated that most fish had lower δ15N values than Shrimp in the inner estuary, however according to the analysis of food habit, it is impossible that these fish have a lower trophic level than Shrimp. Fish generally have stronger movement abilities than Shrimp or Crab. We speculated that these 15N-depleted fish species may have immigrated from the outer estuary shortly prior to being caught by our sampling. It is difficult to evaluate the trophic level of the foodweb using stable isotopic signatures in the inner estuary due to the presence of many interacting factors. In contrast, the plots of δ13C and δ15N signatures showed a clearer niche separation in different catches within the outer estuary. Fish generally dominated the top trophic level, followed by Shrimp, Snails and Crabs in the primary trophic level.

The food sources of aquatic organisms were diverse in the estuary, deriving from marine, fluvial and terrestrial resources. The C and N isotopic ratios usually show great variation in different groups within estuarine ecosystems (Bouillon et al., 2008; Faye et al., 2011). It is thus difficult to precisely identify and quantify the sources of organic matter using the analysis of δ13C isotopic signatures in an environment as complex as an estuary (Winemiller et al., 2007; Pasquaud et al., 2008). In this study, the plots of stable isotope signatures indicated that the trophic structure of shrimp-trawl catches was more complex in the inner estuary than in the outer estuary (Figure 4). The CR of the community can be used as a measure of basal resource diversity in foodwebs, and the CD provides a measure of trophic diversity (Layman et al., 2007). Our results showed that CR and CD of trawling catches were significantly higher in the inner estuary (p < 0.01), suggesting a more diverse food source and more complex trophic interactions (Figure 5). TA can be used as a quantitative measure of a populations total niche width, whereas MNND and SDNND are used to assess the overall similarity of trophic niches among individuals in a population (Layman et al., 2007). In this study, lower TA and SDNND values suggested a narrower trophic-niche width and a more even distribution of trophic niches in the shrimp-trawl catches of the outer estuary.

Conclusions

The δ13C and δ15N of POM and shrimp-trawl catches significantly varied in the different regions of PRE, with more depleted δ13C and more enriched δ15N being found in the inner estuary. The higher δ15N values in the inner estuary suggest a stronger influence from anthropogenic eutrophication in this region. There were also more diverse carbon sources and more complex trophic interactions in the ecosystem of the inner estuary. The separation of trophic niche was clearer between different catches in the outer estuary. Community-wide metrics of stable isotopes showed that the trophic levels of shrimp-trawl catches were more evenly distributed in the outer estuary, suggesting a more stable trophic structure in this region.

Acknowledgements

We wish to extend our appreciation to Dr. Liu Huaxue and Dr. Xu Jun for their kind help in species identification and data analysis. We also thank two anonymous reviewers for their useful comments and suggestions to improve the article.

Funding

This research was supported by the Special Fund for Agro-scientific Research in the Public Interest (201403008), the National Basic Research Program of China (973 Program, 2015CB452904), the Natural Science Foundation of Guangdong Province (2015A030313890) and the Science and Technology Planning Project of Guangdong Province, China (2014B030301064).

Supplemental material

Supplemental data for this article can be accessed on the publisher's website.

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Supplementary data