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Spatial dietary shift in bivalves from embayment with river discharge and mariculture activities to outer seagrass beds in northwestern Philippines

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Abstract

To investigate the spatial variation in bivalve food sources along a pollution gradient and assess bivalve contribution to biogeochemical cycles in tropical coastal ecosystems, the δ13C and δ15N values of bivalves and their potential food sources were studied in northwestern Philippines. In a semi-enclosed embayment affected by river discharge and mariculture activities, bivalves depended primarily on 13C-depleted suspended particulate organic matter such as phytoplankton and/or fish feeds. However, toward the relatively oligotrophic seagrass beds, the bivalve food source gradually shifted to more 13C-enriched resuspended and/or settled particles. Furthermore, in the outer seagrass beds exposed to the open ocean, bivalves mainly relied on similar food sources, such as detritus of microalgae, regardless of the distance from the embayment. These trends appear to reflect the ready availability of the food sources. Especially in the outer seagrass beds, a semi-closed material cycle within the vicinity of the sea bottom likely emerged between bivalves and algae, but not between the phytoplankton in the overlying water column. This resulted in a relatively weak benthic-pelagic coupling for bivalves. These cycles would need to be taken into account when estimating the biogeochemical cycles in eutrophicated coastal areas.

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References

  • Allen HL (1969) Chemo-organotrophic utilization of dissolved organic compounds by planktonic algae and bacteria in a pond. Int Rev Ges Hydrobiol 54:1–33

    Article  CAS  Google Scholar 

  • Allen HL (1971) Primary productivity, chemo-organotrophy, and nutritional interactions of epiphytic algae and bacteria on macrophytes in the littoral of a lake. Ecol Monogr 41:97–127

    Article  Google Scholar 

  • Asmus RM, Asmus H (1991) Mussel beds: limiting or promoting phytoplankton? J Exp Mar Biol Ecol 148:215–232

    Article  Google Scholar 

  • Azanza RV, Fukuyo Y, Yap LG, Takayama H (2005) Prorocentrum minimum bloom and its possible link to a massive fish kill in Bolinao, Pangasinan, Northern Philippines. Harmful Algae 4:519–524

    Article  Google Scholar 

  • Bayne BL, Hawkins AJS (1992) Ecological and physiological aspects of herbivory in benthic suspension-feeding molluscs. In: John DM, Hawkins SJ, Price JH (eds) Plant–animal interactions in the marine benthos. Clarendon Press, Oxford, pp 265–288

    Google Scholar 

  • Bayne BL, Newell RC (1983) Physiological energetics of marine molluscs. In: Saleudin ASM, Wilburg KM (eds) The Mollusca, vol 4. Academic Press, New York, pp 407–515

    Google Scholar 

  • Bertness MD (1984) Ribbed mussels and Spartina alterniflora production in a New England salt marsh. Ecology 65:1794–1807

    Article  Google Scholar 

  • Cebrián J (1999) Patterns in the fate of production in plant communities. Am Nat 154:449–468

    Article  Google Scholar 

  • Cifuentes LA, Sharp JH, Fogel ML (1988) Stable carbon and nitrogen isotope biogeochemistry in the Delaware estuary. Limnol Oceanogr 33(5):1102–1115

    Article  CAS  Google Scholar 

  • Dame RF (2011) Ecology of marine bivalves: an ecosystem approach. CRC Press, Florida

    Book  Google Scholar 

  • David LT, Pastor-Rengel D, Talaue-McManus L, Magdaong E, Salalila-Aruelo R, Bangi HG, San Diego-McGlone ML, Villanoy C, Cordero-Bailey K (2014) The saga of community learning: Mariculture and the Bolinao experience. Aquat Ecosyst Health Manag 17(2):196–204

    Google Scholar 

  • DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506

    Article  CAS  Google Scholar 

  • Dreier A, Loh W, Blumenberg M, Thiel V, Hause-Reitner D, Hoppert M (2014) The isotopic biosignatures of photo- vs. thiotrophic bivalves: are they preserved in fossil shells? Geobiology 12:406–423

    Article  CAS  Google Scholar 

  • Duarte CM, Chiscano CL (1999) Seagrass biomass and production: a reassessment. Aquat Bot 65:159–174

    Article  Google Scholar 

  • Dubois S, Blin JL, Bouchaud B, Lefebvre S (2007) Isotope trophic-step fractionation of suspension-feeding species: implications for food partitioning in coastal ecosystems. J Exp Mar Biol Ecol 351:121–128

    Article  Google Scholar 

  • Eklöf JS, de la Torre-Castro M, Gullstrom M, Uku J, Muthiga N, Lyimo T, Bandeira SO (2008) Sea urchin overgrazing of seagrasses: A review of current knowledge on causes, consequences, and management. Estuar Coast Shelf Sci 79:569–580

    Article  Google Scholar 

  • Ferrera CM, Watanabe A, Miyajima T, San Diego-McGlone ML, Morimoto N, Umezawa Y, Herrera E, Tsuchiya T, Yoshikai M, Nadaoka K (2016) Phosphorus as a driver of nitrogen limitation and sustained eutrophic conditions in Bolinao and Anda, Philippines, a mariculture-impacted tropical coastal area. Mar Pollut Bull 105:237–248

    Article  CAS  Google Scholar 

  • Fortes MD, Go GA, Bolisay K, Nakaoka M, Uy WH, Lopez MR, Leopardas V, Leriorato J, Pantallano A, Paciencia FJ, Watai M, Honda K, Edralin M (2012) Seagrass response to mariculture-induced physico-chemical gradients in Bolinao, northwestern Philippines. Proc 12th Int Coral Reef Symp 9–13

  • Franco-Nava MA, Blancheton JP, Deviller G, Le-Gall JY (2004) Particulate matter dynamics and transformations in a recirculating aquaculture system: application of stable isotope tracers in seabass rearing. Aquac Eng 31:135–155

    Article  Google Scholar 

  • Fry B (1984) 13C/12C ratios and the trophic importance of algae in Florida Syringodium filiforme seagrass meadows. Mar Biol 79:11–19

    Article  CAS  Google Scholar 

  • Gabbott PA (1975) Storage cycles in marine bivalve molluscs: a hypothesis concerning the relationship between glycogen metabolism and gametogenesis. In: Barnes H (ed) Proc 9th Europ Mar Biol Symp. Aberdeen Univ Press, Aberdeen, pp 191–211

  • Gacia E, Duarte CM (2001) Sediment retention by a Mediterranean Posidonia oceanica meadow: The balance between deposition and resuspension. Estuar Coast Shelf Sci 52:505–514

    Article  Google Scholar 

  • Gao QF, Shin PKS, Lin GH, Chen SP, Cheung SG (2006) Stable isotope and fatty acid evidence for uptake of organic waste by green-lipped mussels Perna viridis in a polyculture fish farm system. Mar Ecol Prog Ser 317:273–283

    Article  CAS  Google Scholar 

  • Gosling E (2015) Marine Bivalve Molluscs, 2nd edn. Wiley, UK

    Book  Google Scholar 

  • Harlin MM (1973) Transfer of products between epiphytic marine algae and host plants. J Phycol 9:243–248

    CAS  Google Scholar 

  • Harrison PG (1982) Control of microbial growth and of amphipod grazing by water soluble compounds from leaves of Zostera marina. Mar Biol 67:225–230

    Article  Google Scholar 

  • Haven DS, Morales-Alamo R (1966) Aspects of biodeposition by oysters and other invertebrate filter feeders. Limnol Oceanogr 11:487–498

    Article  Google Scholar 

  • Hawkins AJS, Salkeld PN, Bayne BL, Gnaiger E, Lowe DM (1985) Feeding and resource allocation in the mussel Mytilus edulis: evidence for time-averaged optimization. Mar Ecol Prog Ser 20:273–287

    Article  Google Scholar 

  • Hummel H (1985) Food intake of Macoma balthica (Mollusca) in relation to seasonal changes in its potential food on a tidal flat in the Dutch Wadden Sea. Neth J Sea Res 19:52–76

    Article  Google Scholar 

  • Jaschinski S, Brepohl DC, Sommer U (2008) Carbon sources and trophic structure in an eelgrass Zostera marina bed, based on stable isotope and fatty acid analyses. Mar Ecol Prog Ser 358:103–114

    Article  Google Scholar 

  • Kanaya G, Takagi S, Kikuchi E (2008) Spatial dietary variations in Laternula marilina (Bivalva) and Hediste spp. (Polychaeta) along environmental gradients in two brackish lagoons. Mar Ecol Prog Ser 359:133–144

    Article  CAS  Google Scholar 

  • Kasai A, Horie H, Sakamoto W (2004) Selection of food sources by Ruditapes philippinarum and Mactra veneriformis (Bivalva: Mollusca) determined from stable isotope analysis. Fish Sci 70:11–20

    Article  CAS  Google Scholar 

  • Kautsky N, Evans S (1987) Role of biodeposition by Mytilus edulis in the circulation of matter and nutrients in a Baltic coastal ecosystem. Mar Ecol Prog Ser 38:201–212

    Article  Google Scholar 

  • Kennedy H, Gacia E, Kennedy DP, Papadimitriou S, Duarte CM (2004) Organic carbon sources to SE Asian coastal sediments. Estuar Coast Shelf Sci 60:59–68

    Article  CAS  Google Scholar 

  • Kharlamenko VI, Kiyashko SI, Imbs AB, Vyshkvartzev DI (2001) Identification of food sources of invertebrates from the seagrass Zostera marina community using carbon and sulfur stable isotope ratio and fatty acid analyses. Mar Ecol Prog Ser 220:103–117

    Article  CAS  Google Scholar 

  • Larkum A, Orth RJ, Duarte CM (2006) Seagrasses: biology, ecology and conservation. Springer, The Netherlands

    Google Scholar 

  • Lebreton B, Richard P, Galois R, Radenac G, Pfleger C, Guillou G, Mornet F, Blanchard GF (2011) Trophic importance of diatoms in an intertidal Zostera noltii seagrass bed: Evidence from stable isotope and fatty acid analyses. Estuar Coast Shelf Sci 92:140–153

    Article  CAS  Google Scholar 

  • Lefebvre S, Barill L, Clerc M (2000) Pacific oyster (Crassostrea gigas) feeding responses to a fish-farm effluent. Aquaculture 187:185–198

    Article  Google Scholar 

  • Lehmann MF, Bernasconi SM, Barbieri A, McKenzie JA (2002) Preservation of organic matter and alteration of its carbon and nitrogen isotope composition during simulated and in situ early sedimentary diagenesis. Geochim Cosmochim Acta 66:3573–3584

    Article  CAS  Google Scholar 

  • Leopardas V, Honda K, Go GA, Bolisay K, Pantallano AD, Uy W, Fortes M, Nakaoka M (2016) Variation in macrofaunal communities of sea grass beds along a pollution gradient in Bolinao, northwestern Philippines. Mar Pollut Bull 105:310–318

    Article  CAS  Google Scholar 

  • Lepoint G, Nyssen F, Gobert S, Dauby P, Bouquegneau JM (2000) Relative impact of a seagrass bed and its adjacent epilithic algal community in consumer diets. Mar Biol 136:513–518

    Article  CAS  Google Scholar 

  • Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG (2004) Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305:997–1000

    Article  CAS  Google Scholar 

  • MacDonald BA, Robinson SMC, Barrington KA (2011) Feeding activity of mussels (Mytilus edulis) held in the field at an integrated multi-trophic aquaculture (IMTA) site (Salmo salar) and exposed to fish food in the laboratory. Aquaculture 314:244–251

    Article  Google Scholar 

  • McClanahan TR, Nugues M, Mwachireya S (1994) Fish and sea urchin herbivory and competition in Kenyancoral reef lagoons: the role of reef management. J Exp Mar Biol Ecol 184:237–254

    Article  Google Scholar 

  • McGlathery KJ (2008) Seagrass habitats. In:Capone DG, Bronk DA, Mulholland MR, Carpenter EJ (eds) Nitrogen in the marine environment, 2nd edn. Elsevier, Amsterdam, pp 1037–1061

    Chapter  Google Scholar 

  • Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: Further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140

    Article  CAS  Google Scholar 

  • Miyajima T, Hori M, Hamaguchi M, Shimabukuro H, Adachi H, Yamano H, Nakaoka M (2015) Geographic variability in organic carbon stock and accumulation rate in sediments of East and Southeast Asian seagrass meadows. Glob Biogeochem Cycle 29:397–415

    Article  CAS  Google Scholar 

  • Moncreiff CA, Sullivan MJ (2001) Trophic importance of epiphytic algae in subtropical seagrass beds: evidence from multiple stable isotope analyses. Mar Ecol Prog Ser 215:93–106

    Article  CAS  Google Scholar 

  • Newell RIE (2004) Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. J Shellfish Res 23(1):51–61

    Google Scholar 

  • Ólafsson EB (1986) Density dependence in suspension-feeding and deposit-feeding populations of the bivalve Macoma balthica: a field experiment. J Anim Ecol 55:517–526

    Article  Google Scholar 

  • Owens NJP, Law CS (1989) Natural variations in 15N content of riverine and estuarine sediments. Estuar Coast Shelf Sci 28:407–416

    Article  CAS  Google Scholar 

  • Parsons TR, Takahashi M, Hargrave B (1984) Biological oceanographic processes, 3rd edn. Pergamon Press, UK

    Google Scholar 

  • Peterson BJ, Heck KL Jr (1999) The potential for suspension feeding bivalves to increase seagrass productivity. J Exp Mar Biol Ecol 240:37–52

    Article  Google Scholar 

  • Peterson BJ, Heck KL Jr (2001) Positive interactions between suspension-feeding bivalves and seagrass – a facultative mutualism. Mar Ecol Prog Ser 213:143–155

    Article  Google Scholar 

  • Reusch TBH, Chapman ARO, Gröger JP (1994) Blue mussels Mytilus edulis do not interfere with eelgrass Zostera marina but fertilize shoot growth through biodeposition. Mar Ecol Prog Ser 108:265–282

    Article  Google Scholar 

  • Riera P, Richard P (1997) Temporal variation of δ13C in particulate organic matter and oyster Crassostrea gigas in Marennes-Oleron Bay (France): effect of freshwater inflow. Mar Ecol Prog Ser 147:105–115

    Article  Google Scholar 

  • Rossi F, Baeta A, Marques JC (2015) Stable isotopes reveal habitat-related diet shifts in facultative deposit-feeders. J Sea Res 95:172–179

    Article  Google Scholar 

  • San Diego-McGlone ML, Azanza RV, Villanoy CL, Jacinto GS (2008) Eutrophic waters, algal bloom and fish kill in fish farming areas in Bolinao, Pangasinan, Philippines. Mar Pollut Bull 57:295–301

    Article  CAS  Google Scholar 

  • Scheffer M, Carpenter SR, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in ecosystems. Nature 413:591–596

    Article  CAS  Google Scholar 

  • Tamondong AM, Blanco AC, Fortes MD, Nadaoka K (2013) Mapping of seagrass and other benthic habitats in Bolinao, Pangasinan using Worldview-2 satellite image. Proc IEEE IGARSS, 1579–1582

  • Tanaka Y, Miyajima T, Yamada K, Hori M, Hasegawa N, Umezawa Y, Koike I (2008) Specific growth rate as a determinant of the carbon isotopic composition of a temperate seagrass Zostera marina. Aquat Bot 89:331–336

    Article  CAS  Google Scholar 

  • Tanaka Y, Go GA, Watanabe A, Miyajima T, Nakaoka M, Uy WH, Nadaoka K, Watanabe S, Fortes MD (2014) 17-year change in species composition of mixed seagrass beds around Santiago Island, Bolinao, the northwestern Philippines. Mar Pollut Bull 88:81–85

    Article  CAS  Google Scholar 

  • Thayer GW, Parker PL, LaCroix MW, Fry B (1978) The stable carbon isotope ratio of some components of an eelgrass, Zostera marina, bed. Oecologia 35:1–12

    Article  Google Scholar 

  • van der Heide T, Govers LL, de Fouw J, Olff H, van der Geest M, van Katwijk MM, Piersma T, van de Koppel J, Silliman BR, Smolders AJP, van Gils JA (2012) A three-stage symbiosis forms the foundation of seagrass ecosystems. Science 336:1432–1434

    Article  Google Scholar 

  • Vander Zanden MJ, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: Implication for aquatic food web studies. Limnol Oceanogr 46(8):2061–2066

    Article  CAS  Google Scholar 

  • Villanueva RD, Yap HT, Montaño MNE (2006) Intensive fish farming in the Philippines is detrimental to the reef-building coral Pocillopora damicornis. Mar Ecol Prog Ser 316:165–174

    Article  Google Scholar 

  • Wada E (1980) Nitrogen isotope fractionation and its significance in biogeoehemical processes occurring in marine environments. In: Goldberg ED, Horibe Y, Saruhashi K (eds) Isotope Marine Chemistry. Uchida Rokkakuho, Tokyo, pp 375–398

  • Ward JE, Shumway SE (2004) Separating the grain from the chaff: particle selection in suspension- and deposit-feeding bivalves. J Exp Mar Biol Ecol 300:83–130

    Article  Google Scholar 

  • Ward LG, Kemp WM, Boyton WR (1984) The influence of waves and seagrass communities on suspended particulates in an estuarine embayment. Mar Geol 59:85–103

    Article  Google Scholar 

  • Watai M, Nakamura Y, Honda K, Bolisay KO, Miyajima T, Nakaoka M, Fortes MD (2015) Diet, growth, and abundance of two seagrass bed fishes along a pollution gradient caused by milkfish farming in Bolinao, northwestern Philippines. Fish Sci 81:43–51

    Article  CAS  Google Scholar 

  • White PG (2009) EIA and monitoring for clusters of small-scale cage farms in Bolinao Bay: a case study. In FAO Environmental impact assessment and monitoring of aquaculture. FAO Fisheries and Aquaculture Technical Paper, No. 527. FAO, Rome, pp 537–552

    Google Scholar 

  • Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MYM, Jørgensen BB (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70

    Article  CAS  Google Scholar 

  • WoRMS Editorial Board (2016) World Register of Marine Species. Available from http://www.marinespecies.org at VLIZ. Accessed 21 Jan 2016

  • Yokoyama H, Higano J, Adachi K, Ishihi Y, Yamada Y, Pichitkul P (2002) Evaluation of shrimp polyculture system in Thailand based on stable carbon and nitrogen isotope ratios. Fish Sci 68:745–750

    Article  CAS  Google Scholar 

  • Yokoyama H, Tamaki A, Harada K, Shimoda K, Koyama K, Ishihi Y (2005) Variability of diet–tissue isotopic fractionation in estuarine macrobenthos. Mar Ecol Prog Ser 296:115–128

    Article  CAS  Google Scholar 

  • Yokoyama H, Abo K, Ishihi Y (2006) Quantifying aquaculture-derived organic matter in the sediment in and around a coastal fish farm using stable carbon and nitrogen isotope ratios. Aquaculture 254:411–425

    Article  CAS  Google Scholar 

  • Yoshikai M (2016) Analysis of environmental impacts of intensive mariculture activities on hypoxic water formation and seagrass bed degradation in Bolinao and Anda, Philippines. Master thesis, Tokyo Institute of Technology

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Acknowledgements

We thank K. Nadaoka and M.D. Fortes for leading this project. We are also grateful to C.M. Ferrera, T. Tsuchiya, E.C. Herrera, J.C. Rengel, M. Atrigenio, D.L. Mancenido, T. Yamamoto, L. Bernardo, A.S.J. Wyatt and staff of University of the Philippines (UP), and UP Marine Science Institute Bolinao Marine Laboratory (BML) for supporting field work. We are also sincerely thankful to the JICA Philippines office and to Y. Nagahama, Y. Geroleo, and the CECAM coordinating office for all logistic arrangements.

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  1. Yoshiyuki Tanaka

    Present address: Center for Liberal Arts and Sciences, Hachinohe Institute of Technology, Ohbiraki 88-1 Myo, Hachinohe, Aomori, 031-8501, Japan

Authors and Affiliations

  1. Marine Biogeochemistry Group, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwanoha 5-1-5, Kashiwa, Chiba, 277-8564, Japan

    Naoko Morimoto & Toshihiro Miyajima

  2. Faculty of Fisheries, Nagasaki University, 1-14 Bunkyo, Nagasaki, 852-8521, Japan

    Yu Umezawa

  3. Marine Science Institute, University of the Philippines, Diliman, Quezon City, 1101, Philippines

    Maria Lourdes San Diego-McGlone, Fernando P. Siringan & Genevieve L. Regino

  4. Department of Transdisciplinary Science and Engineering, School of Environment and Society, Tokyo Institute of Technology, O-okayama 2-12-1 W8-13, Meguro, Tokyo, 152-8552, Japan

    Atsushi Watanabe

  5. Mutsu Institute for Oceanography, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 690 Kitasekine, Mutsu, Aomori, 035-0022, Japan

    Yoshiyuki Tanaka

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  1. Naoko Morimoto
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Correspondence to Naoko Morimoto.

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The present study was supported by the Japan International Cooperation Agency (JICA) and Japan Science and Technology Agency (JST) through the Science and Technology Research Partnership for Sustainable Development Program (SATREPS) under the project “Integrated Coastal Ecosystem Conservation and Adaptive Management under Local and Global Environmental Impacts in the Philippines (CECAM)”, and by JSPS Grant-in-aid for Overseas Scientific Research Grant Number 23405002 (Granted to T.M.).

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Morimoto, N., Umezawa, Y., San Diego-McGlone, M.L. et al. Spatial dietary shift in bivalves from embayment with river discharge and mariculture activities to outer seagrass beds in northwestern Philippines. Mar Biol 164, 84 (2017). https://doi.org/10.1007/s00227-016-3063-z

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