WFL Publisher Science and Technology
Meri-Rastilantie 3 B, FI-00980 Journal of Food, Agriculture & Environment Vol.9 (3&4): 649-654. 2011 www.world-food.net Helsinki, Finland e-mail: [email protected]
Study on the feeding habits of fishery organisms in the Yangtze River estuary and the southern Yellow Sea in spring with δ13C method
Zhongyi Li, Zhimeng Zhuang, Fangqun Dai and Xianshi Jin* Key Laboratory for Sustainable Utilization of Marine Fisheries Resource, Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Science, 106 Nanjing Road, Qingdao 266071, China. *e-mail: [email protected]
Received 18 June 2011, accepted 10 October 2011.
Abstract The Yangtze River estuary and the southern Yellow Sea are the natural habitats for numerous marine organisms. These systems are influenced both by oceanic water and the runoff. The main objectives of this study were to compare the feeding habits of organisms from these two areas using stable isotopes to calculate the percent reliance on benthic prey and to compare the results of stomach content analysis from the previous researches the carbon stable isotope technique. The ratios of carbon stable isotopes (δ13C) of 19 fish species and 12 invertebrates in the Yangtze River estuary, and 14 fish species and 10 invertebrates in the southern Yellow Sea in spring, 2005, were examined. The results showed that there were 10 fishery species that had the same feeding habits in the Yangtze River estuary and the southern Yellow Sea. The percent reliance on benthic prey of organisms in the southern Yellow Sea was mostly higher than those of organisms in the Yangtze River estuary. If the feeding habits types of the two methods were identified using only pelagic feeding, benthic feeding and mixed feeding habit three categories, there were 20 out of 23 organism species that had the same feeding habits. The study showed that the feeding habits of fishery organisms had spatial variations, and the carbon stable isotope technology can be used to calculate the feeding habits of organism practically.
Key words: Feeding habit, fishery organism, China, Shanghai, Yangtze River estuary, the southern Yellow Sea, spring, δ13C.
Introduction Aquatic organism feeding behaviour is a complicated course, isotope ratios of organisms can also reflect the coupling of the affected by many biological and abiotic factors, such as organism’s benthic and pelagic environment, the organisms living in the middle habitat, nutritional condition, seasonal change, geographic area water layer having the ratios between those of benthic and pelagic and alternative foods. Aquatic organisms mainly feed some certain organisms. Therefore, the different carbon stable isotope ratios species, sometimes alter their feeding strategies for adapting to of organisms in different water layers can be helpful in studying their new habitats. The study of feeding habits of marine organisms their feeding habits. A few researchers have used stable isotopes could provide useful information on the trophic class of fishery to distinguish the feeding habit of similar species or the feeding organism in food web and management strategy options in multi habit of different developmental stages of the same species, and species fishery 1. to study the influences of feeding habits of species on environment A few methods have been developed to evaluate the feeding and other species. However, most of these researchers mainly habits of organisms, such as stomach content analysis, fatty acid focus on continent species 8-10, only a few studied marine species, analysis and stable isotope analysis. Stable isotopes are for example, Vander Zanden and Vadeboncoeur 11 and Sherwood increasingly used as natural indicators, particularly in aquatic and Rose 12 have calculated the feeding habits of marine organisms organism studies. An organism’s δ13C and nitrogen isotope δ15N using δ13C signature. ratios are integration of the isotopic signatures of prey items that In this study, the feeding habits of fishery organisms in the have been assimilated, and the ratios vary with food and living Yangtze River estuary and the southern Yellow Sea were compared conditions. The rate at which an organism will realize isotopic using stable isotope techniques following Vander Zanden and equilibrium within its diet depends on growth and tissue Vadeboncoeur 11 and Sherwood and Rose 12. The feeding habits conversion rates 2, 3. of fishery organisms were analyzed by calculating the proportion In aquatic ecosystem, δ13C of organisms varies with their of planktonic and benthic invertebrates in diet. These results were environment. Davenport and Bax 4 found that the carbon stable compared with the previous results obtained by using stomach isotope ratios of plankton were lighter (more negative delta) than content analysis method. The Yangtze River estuary and the those of benthos. Pinnegar and Polunin 5 also discovered that Southern Yellow Sea are the natural habitats for numerous marine organisms with enriched δ13C values were usually related to the organisms. These systems are influenced both by oceanic water benthic food web, and organisms with depleted carbon stable and the runoff. It is helpful in studying the difference of the isotope ratios were usually influenced by the pelagic food web. ecosystem structure of the two areas and protecting them by Hobson et al. 6 and Chandra et al. 7 found that the carbon stable comparing the feeding habits of fishery organisms from them.
Journal of Food, Agriculture & Environment, Vol.9 (3&4), July-October 2011 649 Materials and Methods Stable isotope analysis: All samples were thawed and rinsed with Study sites: The feeding habits of the organisms in the Yangtze distilled water. The tissues of different fishery organisms were River estuary and the adjacent southern Yellow Sea were studied. selected as follows: white back muscle for fish, abdominal muscles The boundary between the southern Yellow Sea and the Yangtze for shrimp, and leg muscle for crab. Zooplankton were acidified River estuary was marked according to Xu et al. 13. The two adjacent with 1 M HCl to remove carbonates, and rinsed in distilled water areas have different physical, chemical and biological to neutral. All samples were freeze-dried at -80°C 19, 20, then all characteristics, and are impacted by the runoff of the Yangtze freeze-dried samples were ground into powder using quartz mortars, River. The Yangtze River is the longest (6300 km) river in Asia and and the powder of the same species were mixed together. the fifth largest river in the world. On average, 9.24×1011 m3 fresh Isotopic analysis was completed in the Stable Isotope water is transported into the sea annually, including 8.9×105 tons Laboratory, College of Resources and Environmental Sciences, 4 6 14 TIN, 1.4×10 tons PO4-P and 2.0×10 tons SiO3-Si . The Yangtze China Agricultural University. A Delta XL, continuous flow-isotope River estuary is known as feeding and spawning grounds for ratio mass spectrometer was connected to a Carlo Erba Elemental many important commercial species, such as largehead hairtail Analyzer. In order to ensure the accuracy of the results, a standard (Trichiurus haumela), Japanese anchovy (Engraulis japonicus) sample was analyzed 2 or 3 times after each group of five samples, and crabs 15. The adjacent Yellow Sea is a semi-enclosed sea, to keep equipment in good working order. The carbon stable surrounded by the west coast of the Korean peninsula and the isotopic composition of a sample was quantified relative to an east coast of China. It is shallow, with depth ranging from 90 m in international standard reference material (Pee Dee Belemnite the central trough to less than 20 m within 50 km off the coast. The limestone). The ratio of 13C/12C (δ13C) is expressed as the relative deepest water is confined to the north-south trough which runs per mil differences between the sample and conventional gas from the northern boundary of the Yellow Sea to the continental standards 21. shelf break southwest of Cheju Island. Another feature of the R bottom topography is the east-west asymmetry of the bathymetric 13 ª R sample s tan dard º 3 G C= « R » u10 gradients. Generally, the bathymetric gradients are relatively smaller ¬ s tan dard ¼ on the Chinese side than those on the Korean side 16. where, R = 13C/12C, the accuracy of δ13C is ± 0.5 × 10-3. Sample collection and pretreatment: Samples were collected from the Yangtze River estuary and the adjacent southern Yellow Sea Feeding habit analysis: Pelagic, mixed and benthic feeding types (30.5° to 33.5° N, 122° to 125° E) onboard R/V “Beidou” in April were defined based on the percent reliance on benthic prey, as and May, 2005. Twenty-seven stations in total were sampled, indicated by carbon stable isotope measurements. The feeding including 10 stations in the southern Yellow Sea and 17 stations habit was calculated as: in the Yangtze River estuary, respectively (Fig. 1). Samples were randomly collected (all specimens were collected when their Percent reliance on benthic prey (Bp)= 13 13 13 13 G CC G C P G CBˉG CP u100 number was less than 5, at least 5 specimens were collected for δ13 δ13 δ13 δ13 the other species). Zooplankton size larger than 900 µm and where, Cc, Cp and CB is the mean C of a consumer, pelagic benthic crustacean invertebrates were selected as pelagic and invertebrate, and benthic invertebrate, respectively 8-10. Note that benthic food web base prey. They were collected with a standard the mixing model assumes 0.6‰ trophic fractionation for δ13C, the medium- and large-sized zooplankton net from bottom to surface value originated from the research of Cai et al. 22, based on the in each station. The zooplankton were transferred to the filtrated results of indoor feeding experiment of Japanese anchovy. seawater and preserved for 24 h at 4°C in refrigerator until their Zooplankton larger than 900 µm were selected as the pelagic stomach emptied, and then stored at -20°C 17, 18. Total of 36 species invertebrate. According to the research of Cheng and Zhu 23, the were analyzed, including 31 species in the Yangtze River estuary benthic invertebrates include Parapenaeus dalei, Palaemon and 24 species in the southern Yellow Sea. There were 19 fishes, 8 gravieri, Solenocera crassicornis, Oratosquilla oratoria, crustaceans and 4 cephalopods in the Yangtze River estuary and Trachypenaeus curvirostris and Crangon affinis. 4 fishes, 8 crustaceans and 2 cephalopods in the southern Yellow The estimation criteria of feeding habit were: Bp <25% benthic Sea. reliance is pelagic, Bp = 0 or Bp <0% means complete pelagic; 25%
Statistical analysis: The carbon stable isotope ratios results are Southern Yellow Sea 34 expressed as means±SD. F-test was used to compare the carbon stable isotope variances among specimens in the Yangtze River
32 estuary and the southern Yellow Sea, and Student’s test was used Yangtze River estuary to compare carbon stable isotope differences among specimens. The limit of statistical significance was set at P<0.05 3, 24. Statistical 30 analyses were performed using the SPSS 16.0.
28 118 120 122 124 126 128 130 Figure 1. Sampling station.
650 Journal of Food, Agriculture & Environment, Vol.9 (3&4), July-October 2011 Results species. Among them, the Agrammus agrammus larva was complete The carbon stable isotope ratios of zooplankton selected as pelagic pelagic feeding fish, with Bp 0%. Odontamblyopus rubicundus, food web base prey in the Yangtze River estuary and the southern Nibea albiflora and Miichthys miiuy were complete benthic Yellow Sea were -20.60‰ and -21.54‰, respectively. Those of feeding fish, their Bp were higher than 100%. There were 2 complete benthic food web base prey in the Yangtze River estuary and the pelagic feeding species, 3 mixed feeding species and 5 benthic southern Yellow Sea were -17.74‰ and -18.28‰, respectively feeding species in 10 invertebrate species. Among them, (Table 1). The carbon stable isotope ratios of organism in the Leptochela gracilis was complete pelagic feeding species, with Yangtze River estuary were from -21.12‰ to -16.46‰, and those Bp less than 0%, Metapenaeopsis dalei and Solenocera in the southern Yellow Sea ranged from -21.97‰ to -19.46‰. crassicornis were complete benthic feeding species, with Bp In the Yangtze River estuary, the percent reliance on benthic higher than 100%. prey (Bp) of organisms showed that there were 8 pelagic feeding There were 20 same organism species besides >900 µm plankton species, 7 mixed feeding species and 5 benthic feeding species in in the Yangtze River estuary and the southern Yellow Sea, and 20 fish species (Table 1). Among them, Benthosema pterotum, there were only 18 organism species whose carbon stable isotope Setipinna taty, Pampus argenteus and Erisphex pottii were ratios meet statistical requirements. Between the Yangtze River complete pelagic feeding fish (Bp<0%), while Ariosoma anagoides estuary and the southern Yellow Sea, to the base prey species and Dysomma anguillare were complete benthic feeding fish among the 18 organism species, there was significant differences (Bp>100%). There were 2 complete pelagic feeding species, 5 mixed (P<0.01) between the carbon stable isotopes of zooplanktons feeding species and 4 benthic feeding species in 11 invertebrate larger than 900 µm, no significant differences (P>0.05) between species. Among them, Sepiola birostrat and Todarodes pacificus the carbon stable isotopes of the 4 base benthic invertebrate prey were complete pelagic feeding species (Bp<0%), and Oratosquilla species. While to the remaining 13 organism species of the same oratoria was complete benthic feeding species (Bp>100%). species from the Yangtze River estuary and the southern Yellow In the southern Yellow Sea, there were 3 pelagic feeding species, Sea, there were significant differences (P<0.01) between the carbon 7 mixed feeding species and 4 benthic feeding species in 13 fish stable isotopes of Setipinna taty, Amblychaeturichthys hexanema and Leptochela gracilis, and differences (P<0.05) δ13 Table 1. Carbon stable isotope ratio ( C), percent reliance on benthic prey between the carbon stable isotopes of Engraulis (Bp) of organisms in Yangtze River estuary and southern Yellow Sea. japonicus and Erisphex pottii, no differences between Sea area Yangtze River estuary Southern Yellow Sea the carbon stable isotopes of the others. Species (number) į13C (number) Bp į13C (number) Bp >900µm plankton -21.20±0.36 (15) -22.13±0.12(4) Discussion Fishes Among the 20 same organism species, there were 10 Setipinna taty -20.84±0.11 (7) -0.25 -19.56±0.24 (19) 0.52 Pampus argenteus -20.47±0.16 (10) -0.12 -20.46±0.30 (5) 0.3 organism species with the same feeding habits in the Erisphex pottii -20.21±0.12 (15) -0.04 -20.79±0.17 (8) 0.23 Yangtze River estuary and the southern Yellow Sea, Engraulis japonicus -19.98±0.14 (5) 0.04 -19.31±0.13 (22) 0.57 and the organisms selected as benthic invertebrates in Thryssa kammalensis -19.94±0.19 (3) 0.05 -20.30±0.08 (46) 0.34 Eupleurogrammus muticus -19.32±0.24 (12) 0.27 -20.00±0.25 (10) 0.41 the present study were also categorized as benthic Harpadon nehereus -19.18±0.26 (20) 0.31 -18.58±0.55 (4) 0.75 species by Cheng and Zhu 23 based on stomach content Larimichthys polyactis -18.14±0.29 (6) 0.66 -17.53±0.13 (6) 0.99 analysis. Amblychaeturichthys hexanema -17.87±0.11 (20) 0.75 -19.22±0.28 (9) 0.6 Odontamblyopus rubicundus -17.41±0.55 (3) 0.91 -17.46±0.22 (3) 1.01 In addition to Amblychaeturichthys hexanema and Agrammus agrammus -21.75±0.17 (2) 0 Oratosquilla oratoria, the percent reliance on benthic Collichthys niveatus -21.62 (1) 0.03 prey (Bp) of organisms in the southern Yellow Sea were Nibea albiflora -17.45 (1) 1.01 mostly higher than those of organisms in the Yangtze Miichthys miiuy -16.91 (1) 1.14 River estuary. There were 5 pelagic feeding habit Benthosema pterotum -21.02±0.21 (8) -0.31 Champsodon capensis -19.97±0.15 (10) 0.05 organism species in the Yangtze River estuary, while Argyrosomus argentatus -19.72 (1) 0.13 these species were mixed feeding habits in the southern Coilia mystus -19.26±0.39 (8) 0.28 Yellow Sea, and there were 3 mixed feeding habit Apogon lineatus -18.51±0.10 (22) 0.54 Saurida elongata -17.73±0.45 (5) 0.8 organism species in the Yangtze River estuary, while Ctenotrypauchen chinensis -17.47±0.09 (2) 0.89 these species were benthic feeding habits in the Ariosoma anagoides -16.92±0.09 (2) 1.08 southern Yellow Sea, which is probably due to the Dysomma anguillare -16.74±0.47 (2) 1.14 Crustaceans specific location of the Yangtze River estuary. Every Leptochela gracilis -20.01±0.20 (13) 0.03 -21.97±0.04 (3) -0.1 year the Yangtze River estuary receives high nutrient Crangon affinis -18.59±0.12 (14) 0.51 -18.74±0.22 (8) 0.71 loads from the Yangtze River, which makes the Yangtze Trachypenaeus curvirostris -18.30±0.08 (3) 0.61 -18.53 (1) 0.76 Palaemon gravieri -17.84±0.12 (13) 0.77 -18.13±0.16 (10) 0.85 River estuary become the feeding and spawning Metapenaeopsis dalei -17.40±0.20 (6) 0.91 -17.20±0.50 (2) 1.07 grounds for many fishery resources and forms the Solenocera crassicornis -17.24±0.28 (7) 0.97 -17.18±0.10 (6) 1.07 fishery communities with high biodiversity. This could Oratosquilla oratoria -16.46±0.20 (3) 1.23 -18.56 (1) 0.75 Charybdis bimaculata -18.37±0.39 (5) 0.58 -18.33 (1) 0.8 be speculated from the food composition of Japanese Cephalopods anchovy from the Yangtze River estuary, which has Todarodes pacificus -20.33±0.12 (6) -0.08 -19.80±0.33 (3) 0.46 the largest biomass in the Eastern Sea and the Yellow Sepiola birostrat -21.12±0.47 (7) -0.34 -21.16±0.31 (19) 0.14 Sea and plays an important role in the nutrient and Loligo beka -19.04±0.19 (4) 0.36 Loligo japonica -19.08±0.20 (5) 0.34 energy connection between zooplankton and fish in the two marine ecosystems 25. Its food is mostly
Journal of Food, Agriculture & Environment, Vol.9 (3&4), July-October 2011 651 composed of zooplankton species, dominated by Calanus sinicus advantages in evaluating feeding habit, such as detailed and and Euphausia pacifica, also including the larvae of benthic distinct results. However, stomach content analysis provides only species, such as Decapoda, Amphipoda and Megalopa a snapshot of diet components, and a large sample size is needed occasionally 26. Because there are abundant food resources in the for the relatively accurate estimation of the importance of a Yangtze River estuary, Engraulis japonicus primarily preys on particular diet item. Even with a large sample size, stomach analysis zooplankton 15. may has predicaments due to differing digestion rates of different The feeding habits difference were not consistent with the prey items. To stable isotope technique used in feeding habit significant difference of carbon stable isotopes between organism studies, its analysis only needs a relatively small size of sample, species from the Yangtze River estuary and the southern Yellow and the stable isotope of a predator integrates the stable isotope Sea. The significant spatial difference of carbon stable isotopes information of their diets. of >900 µm plankton did not result in the significant spatial Researchers have studied the feeding habits of some organisms difference of pelagic feeding habits of organism. Among 8 in the Yangtze River estuary and the southern Yellow Sea with the organism species with different feeding habits between the stomach content analysis 1, 11, 15, 23. The feeding habit types defined Yangtze River estuary and the southern Yellow Sea, only Engraulis based on stomach content analysis were more than those of stable japonicus simultaneously had the feeding habits difference and isotope technique. However, if we identify the feeding types of significant carbon stable isotopes difference between the two the two methods using only three categories, that is, all feeding areas. types except for pelagic feeding and benthic feeding are simplified Most previous studies on feeding habits were based upon into the mixed feeding habit, we would find that there were 20 in 23 stomach content analysis, and the feeding habit criterion was organism species that had the same feeding habits, calculated determined according to the number or weight percentage of diets. respectively by stomach content analysis and stable isotope However, there was no demarcation criterion of feeding habits 27, technique, between the two areas, except for Coilia nasus, Apogon 28. The “majority” principle is widely accepted in feeding habit lineatus and Crangon affinis. The feeding habits of the three studies by most researchers, namely, 60% being the demarcation organisms in the two areas did not change from pelagic to benthic criterion of feeding habits. If the percentage of a diet item to a dramatically. Instead, they all changed between mixed feeding predator is beyond 60%, the habitat type of the diet item is the habit and pelagic feeding habit or benthic feeding habit gradually. feeding habit of the predator. If a predator has two or more diet Table 2 shows comparison of feeding habits of species in different items, and the percentages of all preys are less than 60%, the areas with different methods. habitat types of all diet items are the feeding habit of the predator. As described above, the feeding habits not only had According to that, the feeding habits of organisms would generally methodological and spatial difference, but also temporal difference. be divided into 5 categories, including pelagic feeding, pelagic Zhang and Tang 1 found that the feeding habit of M. miiuy and benthic feeding, benthic feeding, nektonic feeding and mixture calculated using stomach content analysis during 1985-1986 in feeding. The stomach content analysis method has many the Yellow Sea showed a mixture of benthic and pelagic prey, with
Table 2. Comparison of feeding habits of species in different areas with different methods. Stable isotope technique Stomach content analysis (Cited references) Species Yangtze River estuary Southern Yellow Sea Yangtze River estuary Southern Yellow Sea Fishes 1)Benthonic 1, 28 E. pottii Completely pelagic Pelagic 2)Pelagic 1 P. argenteus Completely pelagic Mixed Pelagic 28 S. taty Completely pelagic Mixed Nektonic 15 E. japonicus Pelagic Mixed Nektonic 15 Pelagic 1, 28 H. nehereus Mixed Mixed Nektonic 15 Nektonic 1, 28 (1)Nektonic 1 E. muticus Mixed Mixed (2)Pelagic 1 (3)Benthonic, pelagic 28 L. polyactis Mixed Benthonic Mixed 1, 28 A. hexanema Benthonic Mixed Benthonic 28 T. kammalensis Pelagic Mixed Nektonic 15 Pelagic 1, 28 A. argentatus Pelagic Benthonic, nektonic 15, 28 A. lineatus Mixed Benthonic 15 Benthonic 28 C. mystus Mixed Nektonic 15 Pelagic 28 S. elongata Benthonic Nektonic 15 Benthonic 28 A. anagoides Completely benthonic Benthonic 29 D. anguillare Completely benthonic Benthonic 29 1)Benthonic, nektonic 1, 28 M. miiuy Benthonic (2)Benthonic 1 N. albiflora Benthonic Benthonic, nektonic 15 Benthonic, nektonic 28 Crustaceas C. affinis Mixed Mixed Benthonic 1, 23 C. bimaculata Mixed Benthonic Benthonic 1, 23 M. dalei Benthonic Completely benthonic Benthonic, pelagic 23 (1)Benthonic, nektonic 1 P. gravieri Benthonic Benthonic (2)Benthonic, pelagic 23 O. oratoria Completely benthonic Mixed Benthonic, pelagic 23 Cephalopods T. pacificus Completely pelagic Mixed Nektonic 23
652 Journal of Food, Agriculture & Environment, Vol.9 (3&4), July-October 2011 the percentages of them being 55.0% and 45.0% respectively, did not have lipid extraction on all samples. If the feeding habits during 2000-2001, M. miiuy was benthic feeding habit with the of organisms are studied in one area, we should consider effect of percentage of benthic preys 100%. For E. muticus, its feeding the sample preparation to the results. habit was also different in different years. Zhang and Tang 1 found that the feeding habit of E. muticus during 1985-1986 and 2000- Acknowledgements 2001 in the Yellow Sea was nektonic and pelagic, respectively, We thank the captain and crew of the RV “Bei Dou” for their while Jiang and Wei 28 found that the feeding habit of E. muticus cooperation during the sampling operation. We thank the staffs during 1985-1986 in Yellow Sea was mixed, mixture of benthic and in the Stable Isotope Laboratory in College of Resources and nektonic preys. For E. pottii in the Yellow Sea, Zhang and Tang 1 Environmental Sciences at China Agricultural University. This and Jiang and Wei 28 found that its feeding habit calculated using project is sponsored by National Basic Research Program of China stomach content analysis was benthic during 1985-1986, but its (No. 2006CB400608), National High-tech Research and feeding habit was pelagic during 2000-2001. For the three fish Development Scheme (No. 2009AA09Z401), National Natural species, E. muticus is feeding throughout the year. E. pottii just Science Foundation (40606037). Doctoral Start-up Fund of Yellow does not feed during winter, while M. miiuy does not feed during Sea Fisheries Research Institute (No. 61200603), and State-level winter and its spawning period. Therefore, the feeding habits of Public Basic Investigation Fund for Scientific Research Institute organisms have spatial, temporal and geographical differences as (No, 2007-gy-01). 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