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Blackwell Science, LtdOxford, UKFISFisheries Science0919-92682005 Blackwell Science Asia Pty LtdFebruary 2005711151158Original ArticleUse of terrestrial matter by corbiculaA Kasai and A Nakata

FISHERIES SCIENCE 2005; 71: 151–158

Utilization of terrestrial organic matter by the bivalve Corbicula japonica estimated from stable isotope analysis

Akihide KASAI* AND Akiko NAKATA

Graduate school of Agriculture, University, Oiwake, Kitashirakawa, Sakyo, Kyoto 606-8502,

ABSTRACT: Carbon and nitrogen isotopic ratios in tissue of the bivalve corbicula (Corbicula japon- ica) and particulate organic matter (POM) were measured along a salinity gradient in the Kushida Estuary, Japan. The bivalve exhibited a gradual isotopic enrichment from the uppermost estuarine site (d13C = -24.8‰ and d15N = 8.6‰) to the marine site (d13C = -16.1‰ and d15N = 11.8‰). Using the concentration-weighted mixing model, the bivalves’ food source is estimated from the isotope values for the bivalves and POM from terrestrial plants, marine phytoplankton and benthic microalgae. The results indicated that the contributions of benthic micro algae and phytoplankton were small, while terrestrial particulate matter is significantly important for the corbicula diet, although the contribution varies among sampling sites.

KEY WORDS: bivalve, Corbicula japonica, ecosystem, food source, particulate organic matter, stable isotope.

INTRODUCTION tration by holding its inhalant siphon above the sediment surface. It is important to know the food The infaunal suspension-feeding bivalve corbicula sources for not only the management of the corbi- (Corbicula japonica) inhabits brackish waters. This cula resources but also the elucidation of carbon species is broadly distributed from , in and nitrogen cycling in the estuarine ecosystem. In which water freezes in winter, to warm Kyushu in general, bivalves are assumed to be herbivores and Japan. It often dominates in estuaries and brackish phytoplankton is considered to be the major pri- lakes and is thus, an important fisheries resource. mary source of nutrition.5 However, phytoplankton The Japanese corbicula fishery was developed in abundance may be insufficient to maintain bivalve the 1950s and its landing was at a high level of more growth and reproduction because of the spatial than 50 000 tons in the 1960s. However, it has and temporal variations in production.6 Various started to decline since 1980 and has become potential food sources are available to benthic sus- one-third of the largest landing in recent years. pension feeders in the seston of estuarine environ- From the biological and commercial interests, ments.7 It is difficult to assess the relative the ecology of corbicula, such as temperature and contribution of each food source to their growth salinity preference and tolerance for low oxygen and secondary production because direct observa- concentration and sulfide, has been intensively tion of feeding behavior is unfeasible over long investigated (reviewed in M Nakamura; M Yama- periods in the field. Indirect methods, such as gut muro).1,2 It is also pointed out that corbicula plays content analyses, are also not satisfactory since an important role in nutrient cycling in estuaries.3,4 they give only snapshot information on food items Despite extensive knowledge on the ecology of the that have been ingested and not what is assimi- corbicula, its feeding classification, which is one of lated over long periods. the most basic information, still remains uncer- Recently, stable isotope analyses have attracted tain. The only information on the feeding of attention as it can provide answers to this ques- C. japonica is that it obtains particles through fil- tion.8 The 13C/12C and 15N/14N ratios of an animal directly reflect the composition of food sources assimilated and incorporated over a period of 9 *Corresponding author: Tel. 81-75-753-6314. time. Stable isotope analyses have been used suc- Fax: 81-75-753-6468. Email: [email protected] cessfully in many studies of spatial and temporal Received 22 April 2004. Accepted 14 September 2004. variations of isotopic composition in invertebrates

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and their potential diets in various estuarine and oyster Crassostrea gigas, which also inhabits brack- saltmarsh food webs.8 ish waters.12 However, the importance of terrestrial In our previous paper, we measured carbon and matter as a source of nutrition for C. japonica has nitrogen isotopic ratios in the body of the bivalves never been tested. The purpose of this study, there- Ruditapes philippinarum and Mactra veneriformis, fore, is to quantify the relative contribution of both of which are common infauna in Japanese terrestrial matter to the food source of C. japonica coastal areas.10 Comparing the bivalves’ isotopic using nitrogen and carbon stable isotope analysis. signatures with those obtained from particulate organic matter (POM) in the middle reach of the river, in the estuary and off the estuary, the relative MATERIALS AND METHODS contributions of terrestrial organic matter was esti- mated to the bivalves’ diet. The results indicated Sampling was carried out in the Kushida Estuary that both bivalves select marine POM from the (Fig. 1). The empties into , organic matter available in their habitat, although which is a gulf-type bay connected to the Pacific most of the POM in the estuary originated from ter- Ocean at its southern end. The Kushida River restrial organic material. The stable isotope analy- contributes an average discharge of ~7 m3 s-1. The sis was also applied to identify the sources of riversides are fringed by emergent plants such as nutrition for the bivalve Theora lubrica in the common reeds Phragmites australis and mugworts Gokasho Estuary, Japan.11 The isotopic composi- Artemisia indica in places, but are managed with- tion of T. lubrica and POM showed that their dom- out any natural vegetation of marsh plants in inant food sources are benthic microalgae and others. There are tidal flats in and around the river coastal phytoplankton. Both studies showed that mouth. The sampling points are in the lower reach the bivalves utilize little terrestrial organic matter of the Kushida River and dominated by sandy or carried by the river inflow. muddy sediments (Fig. 1c). Most of the mudflats in Compared to R. philippinarum, M. veneriformis which the bivalves were collected were bare and and T. lubrica, the corbicula inhabits upper estuar- seaweed was rarely observed. In contrast, seagrass ies where salinity is low and the terrestrial matter is Zostera marina was abundant out of the river abundant. Therefore, the corbicula could induce a mouth. differential use of food resources and assimilate Live bivalves were collected by hand at nine much terrestrial matter. It was indicated from the points on 25 April and 24 July 2002. The details of stable isotope analysis that the terrestrial organic the sampling are listed in Table 1. A total of 51 indi- matter would be one of the food sources for the viduals of C. japonica were collected. Their shell

130 140 E (a) (c) Kushida Estuary

N 40 M 1 km Ise Bay L

Japan

K Pacific Ocean J 30 N I H (b) Ise Bay G F 20km E D C Kushida Fig. 1 Sampling sites, Kushida Estuary T B Estuary, Japan. Sts. A–N are estu- A ary stations, Sta. S is a terrestrial station and Sta. T is a marine S Kushida R. station. The data at Sta. T are from Kasai et al.10

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Table 1 Details of sampling Location Date Material C, D, E, G, K 24 and 25 July 2002 C. japonica H, J 25 April 2002 C. japonica B 24 July 2002 C. leana, A. indica N 26 April 2002 R. philippinarum, M. veneriformis N 25 July 2002 Z. marina G 24 July 2002 P. australis A, B, C, G, I, K, L 24 July 2002 POM F, H, M, S 25 April 2002 POM T 23 April to 25 July 2001 POM

POM, particulate organic matter.

lengths were 9.7–33.9 mm. For comparison, 12 Subsequently, they were freeze-dried and ground and 13 individuals of R. philippinarum and to powder by a grinder. M. veneriformis were collected from Sta. N, respec- Stable isotope ratios of carbon and nitrogen were tively. R. philippinarum and M. veneriformis measured by a continuous-flow isotope-ratio mass inhabit rather salty tidal flats. In addition, five indi- spectrometry with an elemental analyzer (Carlo viduals of Corbicula leana were collected from Sta. Erba, Lakewood, USA) connected to a mass spec- B. C. leana inhabits fresh water areas such as lakes trometer (Finnigan MAT, Bremen, Germany). The and the middle reach of rivers. In fact, the observed concentration of organic carbon and nitrogen were salinity was zero at Sta. B. Bivalve samples were measured simultaneously. Isotope ratios, d13C and stored at -40∞C until analysis. The foot muscle for d15N, are expressed by the standard d unit notation each sample was excised, dried in an oven at 60∞C, as follows: and ground to a fine powder with a mortar and dX = [(R /R ) - 1] ¥ 103, (1) pestle. sample standard To differentiate between terrestrial and marine where X is 13C and 15N, and R is 13C/12C for carbon organic sources, the isotopes for particulate and 15N/14N for nitrogen. Pee dee belemnite (PDB) organic matter (POM) were also measured. For and atmospheric nitrogen were used as the isotope sampling the estuarine particulate organic matter standards for carbon and nitrogen, respectively. (EPOM), 1 L of water was collected from stations spanning the estuarine salinity gradient (see Table 1 and Fig. 1c for details). The freshwater at RESULTS the middle reach of the Kushida River (Sta. S) was also sampled to provide data on terrestrial partic- The results are summarized in Table 2. Isotope ulate organic matter (TPOM) which is transported ratios for TPOM (d13C = -26.3‰ and d15N = 5.5‰) to the estuary. The POM was defined as the parti- were significantly lower than that for mean MPOM cles collected on a precombusted Whatman GF/F (d13C = -18.9 ± 2.08‰ and d15N = 9.0 ± 0.89‰). This glass microfibre filter (Whatman, Kent, UK). The large difference confirms convenience of the stable filter samples were put in a desiccator with HCl isotope analysis for estimates of bivalves’ potential 13 15 13 fumes for the first 24 h to eliminate any CaCO3, diets. d C and d N for EPOM (d C = -25.5 ± then put with NaOH fumes for the next 24 h to neu- 1.89‰ and d15N = 6.3 ± 0.71‰) were between tralize the acid, and then freeze dried. In addition, TPOM and MPOM, showing a mixture of material as representatives of marine produced organic originating from terrigenous and marine sources. matter (MPOM), the data shown in Kasai et al.10 However, a considerable shift in the isotope ratios were used. In their study, the water was collected at for EPOM to those for TPOM from MPOM indicates the center of Ise Bay (Sta. T; Fig. 1b) in the summer a higher contribution of TPOM to EPOM. of 2001. C/N ratios for POM provide an indication of the To estimate the food source for the bivalves from quality of organic matter. The C/N ratio for MPOM seagrass and seaweed, live leaves of Z. marina were was 6.0 ± 0.36 (Table 2). Since this value is com- collected out of the river mouth (Sta. N), and parable to that for phytoplankton estimated from A. indica and P. australis at the riversides (Sts. B the Redfield ratio (= 6.6), the main component of and G). The samples were cleaned of their epi- MPOM is regarded as phytoplankton or its detritus. bionts by hand and rinsed with distilled water. In contrast, the C/N ratio for TPOM was high

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154 FISHERIES SCIENCE A Kasai and A Nakata

Table 2 Carbon and nitrogen stable isotope ratios (%0) and C/N ratios for the bivalves, seagrass, plants and particulate organic matter

13 15 Species n d C (%0) d N (%0) C/N ratio C. japonica 51 -21.2 ± 2.16 10.3 ± 0.67 4.0 ± 0.27 C. leana 5 -24.6 ± 0.25 8.9 ± 0.37 4.6 ± 0.13 R. philippinarum 12 -14.8 ± 0.49 10.4 ± 0.56 3.7 ± 0.22 M. veneriformis 13 -14.4 ± 0.72 11.0 ± 0.24 3.7 ± 0.27 Z. marina 1 -11.8 6.7 4.1 P. australis 1 -27.7 6.8 4.3 A. indica 1 -29.2 5.7 18.2 TPOM 1 -26.3 5.5 13.2 EPOM 10 -25.5 ± 1.89 6.3 ± 0.71 9.1 ± 1.25 MPOM 7 -18.9 ± 2.08 9.0 ± 0.89 6.0 ± 0.36

Values are mean ± 1SD. n, number of samples analyzed; TPOM, terrestrial particulate organic matter; EPOM, estuarine particulate organic matter; MPOM, marine particulate organic matter.

15

C. japonica C. leana R. philippinarum 10 M. veneriformis TPOM EPOM

N (‰) MPOM 15 d Benthic diatom Fig. 2 d13C and d15N plot of 5 Z. marina bivalves and their potential food P. australis sources. The data for benthic A. indica diatom are from previous studies.10,11,24–28 Bars indicate standard deviations except for 0 benthic diatom, and the maxi- -30 -25 -20 -15 -10 mum and minimum isotope d13C (‰) values for benthic diatom.

(= 13.2), indicating the source of TPOM is terres- In contrast, at the most landward site (Sta. B), trial plants. EPOM showed intermediate C/N ratios C. leana showed the most depleted value of d13C (9.1 ± 1.25), consistent with the indication of the (-24.6‰), which is close to terrestrial values. This mixture of TPOM and MPOM from the isotope indicates C. leana prefers the terrestrial matter as a values. food source. The difference among species was The stable isotope composition of muscle tis- greater in d13C than in d15N. sues of the bivalves is plotted on the d13C–d15N map Muscle tissues of C. japonica displayed a wide (Fig. 2) which provides useful information about range of d13C and d15N values, while those for the the transport pathways of organic matter. There other bivalves were rather constant. Figure 3 shows were significant differences in d13C and d15N values carbon and nitrogen isotope ratios for C. japonica among the species (ANOVA, P < 0.01) indicating dif- at each sampling site. As shown in the difference by ferences in each food preference. The tissues of the species, the isotopic composition of C. japonica bivalves collected at lower (higher) reaches showed collected along longitudinal transects showed a more enriched (depleted) isotope composition. At systematic landward decrease of d13C. A similar the most seaward site (Sta. N), the d13C values for trend was also shown in the d15N variation, but the R. philippinarum and M. veneriformis showed ca. difference in d15N by the sampling position was 13 -15%0 which is similar to typical marine values, smaller than that in d C. The variations in each indicating the food dependence on marine matter. station were small for both d13C and d15N. This fis_942.fm Page 155 Thursday, January 6, 2005 12:55 PM

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K J HG E D C However, phytoplankton production in Japanese –15 rivers is usually small because water retention time is short due to the steep slope.18 Therefore, the freshwater phytoplankton would not be the

C major contributor to EPOM in our study area. C/N

13 –20

d ratios of EPOM (7.0–9.9) were lower than that of terrestrial plants (> 10). It is reported that the wastewater treatment plant had very low C/N 16 –25 ratios (~7). Since the lower catchment basin of the 012Kushida River is studded with residential areas, the wastewater could lead the observed low C/N ratios Distance (km) in the estuary, although its contribution should be trivial. K J HG E D C 15 Besides terrestrial organic matter and phy- toplankton, benthic microalgae has recently been recognized as the other important food source for secondary producers by their high palatability. N 10 19 20

15 Cahoon and Cooke and Jahnke et al. measured d production in continental shelf regions and pointed out that benthic primary production is comparable or larger than that by phytoplankton. 5 Yokoyama and Ishihi11 investigated isotope values 012for benthic diatoms in Gokasho Bay, which is close Distance (km) to our study area, and compared with those for T. lubrica. Their results showed that benthic algae, 13 15 Fig. 3 d C (upper panel) and d N (lower panel) values as well as phytoplankton, is a dominant food for Corbicula japonica in the Kushida Estuary, Japan. source for the bivalve. Therefore, in addition to ter- Alphabets on the upper axis indicate station number. restrial matter (TPOM) and marine phytoplankton (MPOM), benthic microalgae is hereinafter consid- ered as the potential food sources for the corbicula. denotes that the variety of isotope ratios for In order to estimate carbon and nitrogen flow C. japonica shown in Fig. 2 depends on the differ- from the diet to animals based on the stable iso- ence in the collected position. tope ratios, it is necessary to determine the trophic P. australis and A. indica showed isotope ratios shifts in d13C and d15N. It has been presumed that close to TPOM and EPOM, indicating that they d13C and d15N of an animal tissue are ca. 1‰ and could be one of the components of EPOM. In con- 3‰ heavier, respectively, than those of the diet.8,21 trast, the carbon isotope ratio for Z. marina However, it is also well known that these shifts recorded the highest value (-11.8‰). Since the vary to some degree according to the animal. The ratio was significantly larger than those for EPOM trophic shifts have never been reported for and C. japonica, Z. marina cannot contribute C. japonica, but it is possible to estimate the shifts EPOM and would be an unsuitable food source for for C. leana from the present results. C. leana the bivalve. inhabits fresh water areas so that it cannot intake marine matter, but terrestrial matter only. The d13C and d15N values for TPOM were -26.3‰ and 5.5‰, DISCUSSION while those for C. leana were -24.6‰ and 8.9‰, respectively. Assuming that C. leana only ingests The d13C and d15N values for TPOM were -26.3‰ the TPOM, its trophic shifts are estimated at 1.7‰ and 5.5‰, respectively. They are comparable to for d13C and 3.4‰ for d15N. These values are in the those for terrestial organic matter, ranging from range of the previous studies.8,21 Considering the -30 to -23‰ of d13C and -5 to 5‰ of d15N.11,13–15 ecology of C. japonica and C. leana are similar to This indicates that TPOM consisted mainly of ter- each other, it can be assumed in the following dis- rigenous C3 plants in the upper catchment basin of cussion that the trophic shifts for C. japonica are the river. In contrast, Figure 2 shows EPOM is the same as those for C. leana. apparently a mixture of TPOM and tidally-advected In this study, the relative contribution of each MPOM. In estuaries that are not vigorously flushed component to the bivalves’ food source is esti- by fresh water, autochthonously-produced organic mated using the concentration-weighted mixing matter might be an important supply for EPOM.16,17 model,22 because carbon and nitrogen concentra- fis_942.fm Page 156 Thursday, January 6, 2005 12:55 PM

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tions in the terrestrial and marine matter are dif- B-fraction ferent from each other. In the model, it is assumed 1.0 that for each element (C and N), the contribution of a food source is proportional to the included 0.8 mass times the elemental concentration in that TPOM source. Based on the aforementioned estimates 0.6 BA that d13C and d15N for corbicula increases 1.7‰ and MPOM 3.4‰ from the diet, respectively, mass balance 0.4 equations can be written as

13 13 13 13 Relative Contribution 0.2 Ê ()ddCCCTBTMBM- ¢¢[] () d C- d CC[] 15 15 15 15 Á()ddNNNN- ¢¢[]() d- d NN[ Á TBTMBM 0.0 Ë 11 CDEGHJ K Station 13 13 ()ddCCCABA- ¢ []ˆÊ fTB, ˆ Ê0ˆ 15 15 Fig. 4 Fractions of assimilated biomass of terrestrial ()ddNNNABA- ¢ []˜Á f MB, ˜ = Á0˜ (2) ˜Á ˜ Á ˜ particulate organic matter (TPOM), marine produced 1 ¯Ë f AAB, ¯ Ë1¯ organic matter (MPOM), and benthic microalgae (BM) 13 13 by C. japonica, estimated from the concentration- d CB¢ = d CB - 1.7 (3) weighted mixing model. 15 15 d NB¢ = d NB - 3.4 (4)

13 13 13 13 15 15 15 where d CT, d CM, d CA, d CB, d NT, d NM d NA the uppermost estuary, the relative contribution of 15 and d NB represent the C and N isotopic signatures TPOM is over 90% (Fig. 4). The relative dependence for TPOM, MPOM, benthic microalgae and the of each source varies by the sampling position.

bivalves, [CT], [CM], [CA], [NT], [NM] and [NA] are the MPOM is important in the lower estuary, and its C and N concentrations in sources TPOM, MPOM contribution is larger than that of TPOM at the

and benthic microalgae, and fT,B, fM,B and fA,B are the most marine site (Sta. K). The large contribution of fractions of assimilated biomass of TPOM, MPOM TPOM to the diet for the corbicula is consistent and benthic microalgae by the bivalves, respec- with the results that EPOM consists chiefly of tively. C and N concentrations for P. australis were TPOM. The corbicula might unselectively 44.1% and 2.6%, and those for A. indica were 44.8% assimilate POM in its habitat. and 2.5%, respectively. The values were similar to In the previous studies on the corbicula, it has typical terrestrial plants (44% for carbon and 1% been supposed that they use phytoplankton or for nitrogen).22 The values of 44.5% and 2.5% are, detritus as food sources.1,2 Diatoms were often therefore, used for C and N concentrations for observed in the guts of corbicula, although the TPOM in this study. In contrast, it is reported that main component was undefined detritus (K Itoh, the C concentration for phytoplankton is 45%.23 pers. comm., 2004). However, the origin of the Using the Redfield ratio, the N concentration detritus cannot be detected and thus, the previous is estimated at 7%. No observations on benthic hypothesis on the food source was unconvincing. microalgae were conducted in this study. From the In contrast, it is quantitatively clarified in this study previous studies, the d13C values for benthic diatom that the terrestrial organic matter is one of the lie between -17.6‰ and -12.1‰, and the d15N val- major food sources for the corbicula rather than ues between 3.8‰ and 6.6‰ (Fig. 2).10,11,24–28 The marine organic matter. In addition, the relative medians of these values (-14.9‰ for d13C and importance is different by site along the estuarine 5.2‰ for d15N) are used for d13C and d15N of benthic gradient. This food habit is similar to that of microalgae. It is assumed that C and N concentra- C. gigas,12 but different from those of tions for the benthic microalgae are the same as R. philippinarum and M. veneriformis, which those for MPOM. select marine matter from the organic matter Substituting the C and N concentrations for the available in their habitat.10 potential food sources and the isotope values in Littoral or sublittoral areas have recently been Equations 2–4, the fractions are calculated. The recognized as playing an important role in the eco- results are presented in Fig. 4. Overall, the contri- system, linking fresh and marine environments. A bution of TPOM is large, while that of benthic dia- key role in the retention and removal of organic toms is small. The lesser contribution of benthic and inorganic matter in water is generally attrib- diatoms is understandable from Fig. 2 that shows uted to benthic filter-feeders.29 Amongst various isotope values for benthic diatoms are significantly benthic organisms, bivalves have attracted atten- different from those for the corbicula. Especially at tion because of their large biomass. They are fis_942.fm Page 157 Thursday, January 6, 2005 12:55 PM

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believed to purify the water, removing organic 6. Asmus H, Asmus RM, Reise K. Exchange processes in a material that flows into the sea through rivers from intertidal mussel bed: a Sylt-flume study in the Wadden Sea. the land and those formed in the sea, so that they Berichte Biologie Helgolander 1990; 6: 1–79. are supposed to function as sewage disposal facil- 7. Dame RF. Ecology of Marine Bivalves – An Ecosystem ities.30 Although hypothesized to be important, it Approach. CRC Press, Florida. 1996. 8. Fry B, Sherr EB. d13C measurements as indicators of carbon has been difficult to quantify the ability of benthos flow in marine and freshwater ecosystem. Contrib. Mar. Sci. by conventional methods, because organic matter 1984; 27: 13–47. in estuaries contain various matter, which have dif- 9. DeNiro MJ, Epstein S. Influence of diet on the distribution ferent origins. In contrast, in this study, it is con- of carbon isotopes in animals. 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