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Sources of primary production supporting food webs in an arid coastal embayment

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Abstract

Penaeid shrimp can be useful ecological indicators of linkages between shallow tropical coastal habitats, acting as integrators of carbon and nitrogen sources due to their generalist feeding habits and their mobility between habitats and with tidal cycles. In the current study, the contribution of mangrove, seagrass and microbial mat to the nutrition of two penaeid shrimp species, Penaeus semisulcatus and Metapeneus ensis, in a shallow arid embayment in the Arabian Gulf was assessed through a combination of analysis of stomach contents and dual carbon and nitrogen stable isotope signatures. Shrimp tissue stable isotope signatures identified seagrass as a major source of carbon and nitrogen for both species, contributing 21–38 % (1–99 ‰). Microbial mat was also detected as a significant nutritional source for early-stage Metapenaeus affinis postlarvae (1–27 %). However, mangroves were not identified as a significant source, with the range of results including the possibility of a zero contribution. Moreover, the greatest possible contribution of mangroves as source of carbon was less than for the other primary producers. This may be due the high salinity and wide temperature range limiting mangrove productivity as well as the low export of dissolved and particulate organic material out of the mangroves due to low rainfall.

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References

  • Abreu PC, Ballester ELC, Odebrecht C, Wasielesky W, Cavalli RO, Graneli W, Anesio AM (2007) Importance of biofilm as food source for shrimp (Farfantepenaeus paulensis) evaluated by stable isotopes (delta C-13 and delta N-15). J Exp Mar Biol Ecol 347:88–96

    Article  CAS  Google Scholar 

  • Al-Khayat JA, Jones DA (1999) A comparison of the macrofauna of natural and replanted mangroves in Qatar. Estuar Coast Shelf Sci 49:55–63

    Article  Google Scholar 

  • Al-Maslamani I (2006) Feeding and nutrition in the marine shrimp Penaeus semisulcatus. Ph.D. thesis, Bangor University, UK

  • Al-Maslamani I, Le Vay L, Kennedy H, Jones DA (2007) Feeding ecology of the grooved tiger shrimp Penaeus semisulcatus De Haan (Decapoda: Penaeidae) in inshore waters of Qatar, Arabian Gulf. Mar Biol 150:627–637

    Article  Google Scholar 

  • Al-Maslamani I, Le Vay L, Kennedy H (2009) Feeding on intertidal microbial mats by postlarval tiger shrimp, Penaeus semisulcatus De Haan. Mar Biol 156:2001–2009

    Article  Google Scholar 

  • Al-Zaidan ASY, Kennedy H, Jones DA, Al-Mohanna SY (2006) Role of microbial mats in Sulaibikhat Bay (Kuwait) mudflat food webs: evidence from delta C-13 analysis. Mar Ecol Prog Ser 308:27–36

    Article  CAS  Google Scholar 

  • Barghoorn ES, Knoll AH, Dembicki H, Meinschein WG (1977) Variation in stable carbon isotopes in organic matter from the Gunflint Iron Formation. Geochim Cosmochim Acta 41:425–430

    Article  CAS  Google Scholar 

  • Bishop JM, Khan MH (1999) Use of intertidal and adjacent mudflats by juvenile penaeid shrimps during 24-h tidal cycles. J Exp Mar Biol Ecol 232:39–60

    Article  Google Scholar 

  • Bouillon S, Raman AV, Dauby P, Dehairs F (2002) Carbon and nitrogen stable isotope ratios of subtidal benthic invertebrates in an estuarine mangrove ecosystem (Andhra Pradesh, India). Estuar Coast Shelf Sci 54:901–913

    Article  CAS  Google Scholar 

  • Camacho AS, Bagarinao T (1987) The impact of fish pond development on the mangrove ecosystem in the Philippines. In: Mangroves of Asia and the Pacific: status and management. Technical report of the UNDP/UNESCO research and technical pilot programme on mangrove ecosystems in Asia and Pacific, pp 395–405

  • Chong VC, Sasekumar A (1981) Food and feeding habits of the white prawn Penaeus merguiensis. Mar Ecol Prog Ser 5:185–191

    Article  Google Scholar 

  • Chong VC, Sasekumar A, Leh MUC, Dcruz R (1990) The fish and prawn communities of a Malaysian coastal mangrove system, with comparisons to adjacent mudflats and inshore waters. Estuar Coast Shelf Sci 31:703–722

    Article  Google Scholar 

  • Chong VC, Low CB, Ichikawa T (2001) Contribution of mangrove detritus to juvenile prawn nutrition: a dual stable isotope study in a Malaysian mangrove forest. Mar Biol 138:77–86

    Article  CAS  Google Scholar 

  • Clayton DA, Halwagy R, Clayton D, Behbehani M (1986) Ecology of mudflats with particular reference to those of the northern Arabian Gulf. Marine Environment and Pollution. In: Proceedings of the first Arabian gulf conference on environment and pollution, Kuwait, 7–9 February 1982, pp 83–96

  • Crona BI, Ronnback P (2005) Use of replanted mangroves as nursery grounds by shrimp communities in Gazi Bay, Kenya. Estuar Coast Shelf Sci 65:535–544

    Article  Google Scholar 

  • de Freitas AJ (1986) Selection of nursery areas by six Southeast African penaeidae. Estuar Coast Shelf Sci 23:901–908

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351

    Article  CAS  Google Scholar 

  • France RL, Peters RH (1997) Ecosystem differences in the trophic enrichment of C-13 in aquatic food webs. Can J Fish Aquat Sci 54:1255–1258

    Article  Google Scholar 

  • Fry B, Ewel KC (2003) Using stable isotopes in mangrove fisheries research—a review and outlook. Isot Environ Health Stud 39:191–196

    Article  CAS  Google Scholar 

  • Fry B, Smith TJ (2002) Stable isotope studies of red mangroves and filter feeders from the Shark River Estuary, Florida. Bull Mar Sci 70:871–890

    Google Scholar 

  • Gamboa-Delgado J, Le Vay L (2009) Natural stable isotopes as indicators of the relative contribution of soy protein and fish meal to tissue growth in Pacific white shrimp (Litopenaeus vannamei) fed compound diets. Aquaculture 291:115–123

    Article  CAS  Google Scholar 

  • Hammerschlag N, Serafy JE (2010) Nocturnal fish utilization of a subtropical mangrove-seagrass ecotone. Marine Ecology 31:364–374

    Article  Google Scholar 

  • Haywood MDE, Vance DJ, Loneragan NR (1995) Seagrass and algal beds as nursery habitats for tiger prawns (Penaeus semisulcatus and P. esculentus) in a tropical Australian estuary. Mar Biol 122:213–223

    Google Scholar 

  • Hemminga MA, Mateo MA (1996) Stable carbon isotopes in seagrasses: variability in ratios and use in ecological studies. Mar Ecol Prog Ser 140:285–298

    Article  Google Scholar 

  • Hunter J, Feller RJ (1987) Immunological dietary analysis of two penaeid shrimp species from a South Carolina tidal creek. J Exp Mar Biol Ecol 107:61–70

    Article  Google Scholar 

  • Hyndes GA, Lavery PS (2005) Does transported seagrass provide an important trophic link in unvegetated, nearshore areas? Estuar Coast Shelf Sci 63:633–643

    Article  CAS  Google Scholar 

  • Jones DA, Price ARG., Al-Yamani F, Al-Zaidan A (2002) Coastal and marine ecology. In: Kahn NY, Munawar M, Price ARG (eds) The gulf ecosystem health and sustainability. Ecovision World Monograph Series, Bakhuys, Leiden, pp 65–103

  • 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 

  • Kennedy P, Kennedy H, Papadimitriou S (2005) The effect of acidification on the determination of organic carbon, total nitrogen and their stable isotopic composition in algae and marine sediment. Rapid Commun Mass Spectrom 19:1063–1068

    Article  CAS  Google Scholar 

  • Kennedy H, Beggins J, Duarte CM, Fourqurean JW, Holmer M, Marba N, Middelburg JJ (2010) Seagrass sediments as a global carbon sink: isotopic constraints. Global Biogeochemical Cycles 24

  • Koch MS, Schopmeyer SA, Kyhn-Hansen C, Madden CJ, Peters JS (2007) Tropical seagrass species tolerance to hypersalinity stress. Aquat Bot 86:14–24

    Article  CAS  Google Scholar 

  • Levine S (1980) Several measures of trophic structure applicable to complex food webs. J Theor Biol 83:195–207

    Article  Google Scholar 

  • Loneragan NR, Kenyon RA, Haywood MDE, Staples DJ (1994) Population-dynamics of juvenile tiger prawns (Penaeus esculentus and P. semisulcatus) in seagrass habitats if the Western Gulf of Carpentaria, Australia. Mar Biol 119:133–143

    Article  Google Scholar 

  • Loneragan NR, Bunn SE, Kellaway DM (1997) Are mangroves and seagrasses sources of organic carbon for penaeid prawns in a tropical Australian estuary? A multiple stable-isotope study. Mar Biol 130:289–300

    Article  Google Scholar 

  • Loneragan NR, Kenyon RA, Staples DJ, Poiner IR, Conacher CA (1998) The influence of seagrass type on the distribution and abundance of postlarval and juvenile tiger prawns (Penaeus esculentus and P. semisulcatus) in the western Gulf of Carpentaria, Australia. J Exp Mar Biol Ecol 228:175–195

    Article  Google Scholar 

  • Macnae W (1968) A general account of fauna and flora of mangrove swamps and forests in Indo-West-Pacific Region. Adv Mar Biol 6:73–270

    Article  Google Scholar 

  • Martinez del Rio C, Wolf N, Carleton SA, Gannes LZ (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84:91–111

    Article  Google Scholar 

  • Mayer MA (1985) Ecology of juvenile white shrimp, Penaeus setiferus Linnaeus, in the salt marsh habitat. Masters thesis. Georgia Institute of Technology, Atlanta, Georgia

  • McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390

    Article  CAS  Google Scholar 

  • Newell RIE, Marshall N, Sasekumar A, Chong VC (1995) Relative importance of benthic microalgae, phytoplankton, and mangroves as sources of nutrition for penaeid prawns and other coastal invertebrates from Malaysia. Mar Biol 123:595–606

    Article  Google Scholar 

  • Odum WE (1971) Pathways of energy flow in a south Florida estuary. University of Miami, Sea Grant Program (Living Resources), Miami, Florida. Sea Grant Tech Bull 7:161

    Google Scholar 

  • Odum EP, de la Cruz AA (1963) Detritus as a major component of ecosystems. Bioscience 13:39–40

    Google Scholar 

  • Odum WE, Heald EJ (1975) The detritus based food web of an estuarine mangrove community. Academic Press, New York, Myrtle Beach, SC, USA, Oct. 1973. In: 2nd international conference, estuarine research, vol 1, Chemistry, Biology and the Estuarine System, pp 265–286

  • Oh C-W, Hartnoll RG, Nash RDM (2001) Feeding ecology of the common shrimp Crangon crangon in Port Erin Bay, Isle of Man, Irish Sea. Mar Ecol Prog Ser 214:211–223

    Article  Google Scholar 

  • Papadimitriou S, Kennedy H, Kennedy DP, Duarte CM, Marba N (2005) Sources of organic matter in seagrass-colonized sediments: a stable isotope study of the silt and clay fraction from Posidonia oceanica meadows in the western Mediterranean. Org Geochem 36:949–961

    Article  CAS  Google Scholar 

  • Parida AK, Jha B (2010) Salt tolerance mechanisms in mangroves: a review. Trees Struct Funct 24:199–217

    Article  Google Scholar 

  • Parker PL, Anderson RK, Lawrence A (1989) A [delta]13C and [delta]15 N tracer study of nutrition in aquaculture: Penaeus vannamei in a pond growout system. Ecol Stud 68:288–307

    Article  Google Scholar 

  • Patel NT, Gupta A, Pandey AN (2010) Salinity tolerance of Avicennia marina (Forssk.) Vierh. from Gujarat coasts of India. Aquat Bot 93:9–16

    Article  CAS  Google Scholar 

  • Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320

    Article  Google Scholar 

  • Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136:261–269

    Article  Google Scholar 

  • Primavera JH (1996) Stable carbon and nitrogen isotope ratios of penaeid juveniles and primary producers in a riverine mangrove in Guimaras, Philippines. Bull Mar Sci 58:675–683

    Google Scholar 

  • Primavera JH (1998) Mangroves as nurseries: shrimp populations in mangrove and non-mangrove habitats. Estuar Coast Shelf Sci 46:457–464

    Article  Google Scholar 

  • Rajendran N, Kathiresan K (2004) How to increase juvenile shrimps in mangrove waters? Wetl Ecol Manag 12:179–188

    Article  Google Scholar 

  • Robertson AI (1988) Decomposition of mangrove leaf litter in tropical Australia. J Exp Mar Biol Ecol 116:235–247

    Article  Google Scholar 

  • Robertson AI, Duke NC (1987) Mangroves as nursery sites—comparisons of the abundance and species composition of fish and crustaceans in mangroves and other nearshore habitats in tropical Australia. Mar Biol 96:193–205

    Article  Google Scholar 

  • Rodelli MR, Gearing JN, Gearing PJ, Marshall N, Sasekumar A (1984) Stable isotope ratio as a tracer of mangrove carbon in Malaysian ecosystems. Oecologia 61:326–333

    Article  Google Scholar 

  • Sasekumar A, Chong VC, Leh MU, Dcruz R (1992) Mangroves as a habitat for fish and prawns. Hydrobiologia 247:195–207

    Article  Google Scholar 

  • Schidlowski M, Matzigkeit U, Mook WG, Krumbein WE (1985) Carbon isotope geochemistry and carbon-14 ages of microbial mats from the Gavish Sabkha and the Solar Lake. In: Friedman GM, Krumbein WE (eds) Ecological studies: analysis and synthesis, vol 53. Hypersaline ecosystems: the Gavish Sabkha. X+484p. Springer, Berlin, pp 381–406

  • Schwamborn R, Bonecker ACT (1996) Seasonal changes in the transport and distribution of meroplankton into a Brazilian estuary with emphasis on the importance of floating mangrove leaves. Arquivos De Biologia E Tecnologia 39:451–462

    Google Scholar 

  • Schwamborn R, Criales MM (2000) Feeding strategy and daily ration of juvenile pink shrimp (Farfantepenaeus duorarum) in a South Florida seagrass bed. Mar Biol 137:139–147

    Article  Google Scholar 

  • Schwamborn R, Ekau W, Voss M, Saint-Paul U (2002) How important are mangroves as a carbon source for decapod crustacean larvae in a tropical estuary? Mar Ecol Prog Ser 229:195–205

    Article  CAS  Google Scholar 

  • Sheaves M, Abrantes K, Johnston R (2007) Nursery ground value of an endangered wetland to juvenile shrimps. Wetl Ecol Manag 15:311–327

    Article  Google Scholar 

  • Sheppard C, Price A, Roberts C (1992) Marine ecology of the Arabian region. Pattern and processes in extreme tropical environment. Academic Press, London, p 159

    Google Scholar 

  • Stoner AW, Zimmerman RJ (1988) Food pathways associated with penaeid shrimps in a mangrove-fringed estuary. US Fish Wildl Serv Fish Bull 6:543–551

    Google Scholar 

  • Su MS, Liao IC (1984) Preliminary studies on the distribution and the stomach contents of some common prawns from the coast of Tungkang, Taiwan, Tungkang Marine Laboratory, Taiwan. In: Proceedings of the ROC-Japan symposium on mariculture TML. Conf. Proc. 1, pp 57–71

  • Sumitra-Vijayaraghavan VR, Krishna Kumari L, Royan JP (1980) Biochemical changes and energy content of the mangrove, Rhizophora mucronata, leaves during decomposition. Indian J Mar Sci 9:120–123

    CAS  Google Scholar 

  • Touchette BW (2007) Seagrass-salinity interactions: physiological mechanisms used by submersed marine angiosperms for a life at sea. J Exp Mar Biol Ecol 350:194–215

    Article  Google Scholar 

  • Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet delta N-15 enrichment: a meta-analysis. Oecologia 136:169–182

    Article  Google Scholar 

  • Vizzini S (2009) Analysis of the trophic role of Mediterranean seagrasses in marine coastal ecosystems: a review. Bot Mar 52:383–393

    Article  Google Scholar 

  • Wassenberg TJ, Hill BJ (1987) Natural diet of the tiger prawns Penaeus esculentus and Penaeus semisulcatus. Aust J Mar Freshw Res 38:169–182

    Article  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 

  • Zieman JC, Macko SA, Mills AL (1984) Role of seagrasses and mangroves in estuarine food webs: temporal and spatial changes in stable isotope composition and amino-acid content during decomposition. Bull Mar Sci 35:380–392

    Google Scholar 

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Acknowledgments

This research was supported by the Qatar National Research Foundation, National Priorities Research Programme research grant 09-129-018.

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Correspondence to L. Le Vay.

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Communicated by S. Connell.

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Al-Maslamani, I., Walton, M.E.M., Kennedy, H. et al. Sources of primary production supporting food webs in an arid coastal embayment. Mar Biol 159, 1753–1762 (2012). https://doi.org/10.1007/s00227-012-1963-0

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