Journal of Applied Phycology

, Volume 25, Issue 1, pp 97–107 | Cite as

δ15N values of macroalgae as an indicator of the potential presence of waste disposal from land-based marine fish farms

  • Carlos Carballeira
  • Inés G. Viana
  • Alejo Carballeira
Article
First Online:
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Revised:
Accepted:

Abstract

The nitrogen isotope ratio (δ15N) in tissues of native macroalgae was evaluated as a means of indicating the intensity and spatial extent of organic contamination due to disposal of waste from land-based marine fish farms (LBMFFs). Three species of macroalgae from the genus Fucus and the green macroalgae Codium tomentosum were selected for study. The study was carried out at seven flat marine fish farms located in Galicia (NW Spain). Tests were carried out to determine the intra-annual variation in δ15N values and any differences between selected macroalgae. The δ15N values enrichment was observed close to the disposal point, and δ15N values varied more widely throughout the year (±5.57 ‰) at sites affected by the marine fish farm effluent compared to natural conditions (±2 ‰). No significant differences in the isotopic signals were observed in the different species studied (standard major axis). The δ15N values of macroalgae may be an ideal means of detecting the presence of LBMFFs effluents.

Keywords

Fucus Codium tomentosum Pollution Monitoring Bioconcentration Aquaculture Eutrophication 
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Notes

Acknowledgments

The present study was partly financed by the Spanish Government's National Plan for Marine Culture (JACUMAR, 2008): “Selection of indicators, determination of reference values, design of programmes, protocols and measures for environmental studies in aquaculture (INDAQUA)”. Carlos Carballeira is grateful to the University of Cadiz Predoctoral Fellowships Programme (Spain).

References

  1. APROMAR (2011) La acuicultura marina en España. APROMAR. www.apromar.es/Informes/. Accessed 21 November 2011
  2. Burford MA, Costanzo SD, Dennison WC, Jackson CJ, Jones AB, McKinnon AD, Preston NP, Trott LA (2003) A synthesis of dominant ecological processes in intensive shrimp ponds and adjacent coastal environments in NE Australia. Mar Pollut Bull 46:1456–1469PubMedCrossRefGoogle Scholar
  3. Carballeira A, Carral E, Puente X, Villares R (2000) Regional-scale monitoring of coastal contamination. Nutrients and heavy metals in estuarine sediments and organisms on the coast of Galicia (northwest Spain). Int J Environ Pollut 13:534–572CrossRefGoogle Scholar
  4. Carballeira C, Espinosa J, Carballeira A (2011) Linking δ15N and histopathological effects in molluscs exposed in situ to effluents from land-based marine fish farms. Mar Pollut Bull 62:2633–2641PubMedCrossRefGoogle Scholar
  5. Carballeira C, Ramos-Gómez J, Martín-Díaz ML, DelValls TA, Carballeira A (2012) Designing an integrated environmental monitoring plan for land-based marine fish farms located at exposed and hard bottom coastal areas. J Environ Monit. doi: 10.1039/c2em10839a
  6. Cloern JE (2001) Our evolving conceptual model of the coastal eutrophication problem. Mar Ecol Prog Ser 210:223–253CrossRefGoogle Scholar
  7. Cohen RA, Fong P (2005) Experimental evidence supports the use of δ15N content of the opportunistic green macroalga Enteromorpha intestinalis (Chlorophyta) to determine nitrogen sources to estuaries. J Phycol 41:287–293CrossRefGoogle Scholar
  8. Costanzo SD, O'Donohue MJ, Dennison WC, Loneragan NR, Thomas M (2001) A new approach for detecting and mapping sewage impacts. Mar Pollut Bull 42:149–156PubMedCrossRefGoogle Scholar
  9. Costanzo SD, O'Donohue MJ, Dennison WC (2004) Assessing the influence and distribution of shrimp pond effluent in a tidal mangrove creek in north-east Australia. Mar Pollut Bull 48:514–525PubMedCrossRefGoogle Scholar
  10. Dailer ML, Knox RS, Smith JE, Napier M, Smith CM (2010) Using δ15N values in algal tissue to map locations and potential sources of anthropogenic nutrient inputs on the island of Maui, Hawaii, USA. Mar Pollut Bull 60:655–671PubMedCrossRefGoogle Scholar
  11. Dailer ML, Ramey HL, Saephan S, Smith CM (2012) Algal δ15N values detect a wastewater effluent plume in nearshore and offshore surface waters and three-dimensionally model the plume across a coral reef on Maui, Hawaii, USA. Mar Pollut Bull. doi: 10.1016/j.marpolbul.2011.12.004
  12. Dalsgaard T, Krause-Jensen D (2006) Monitoring nutrient release from fish farms with macroalgal and phytoplankton bioassays. Aquaculture 256:302–310CrossRefGoogle Scholar
  13. Deutsch B, Voss M (2006) Anthropogenic nitrogen input traced by means of δ15N values in macroalgae: results from in-situ incubation experiments. Sci Total Environ 366:799–808PubMedCrossRefGoogle Scholar
  14. Dolenec T, Lojen S, Lambasa S, Dolenec M (2006) Effects of fish farm loading on sea grass Posidonia oceanica at Vrgada Island (Central Adriatic): a nitrogen stable isotope study. Isot Environ Health Stud 42:77–85CrossRefGoogle Scholar
  15. Ervik A, Hansen PK, Aure J, Stigebrandt A, Johannessen P, Jahnsen T (1997) Regulating the local environmental impact of intensive marine fish farming I. The concept of the MOM system. Aquaculture 158:85–94CrossRefGoogle Scholar
  16. FAO (2010) The state of world fisheries and aquaculture. Food and Agricultural Organization of the United Nations, RomeGoogle Scholar
  17. Fernandes TF, Eleftheriou A, Ackefors H, Eleftheriou M, Ervik A, Sanchez-Mata A, Scanlon T, White P, Cochrane S, Pearson TH, Read PA (2001) The scientific principles underlying the monitoring of the environmental impacts of aquaculture. J Appl Ichthyol 17:181–193CrossRefGoogle Scholar
  18. Filgueira R, Castro BG (2011) Study of the trophic web of San Simón Bay (Ría de Vigo) by using stable isotopes. Cont Shelf Res 31:476–487CrossRefGoogle Scholar
  19. García-Sanz T, Ruiz-Fernández JM, Ruiz M, García R, González MN, Pérez M (2010) An evaluation of a macroalgal bioassay tool for assessing the spatial extent of nutrient release from offshore fish farms. Mar Environ Res 70:189–200PubMedCrossRefGoogle Scholar
  20. Gartner A, Lavery P, Smit AJ (2002) Use of δ15N signatures of different functional forms of macroalgae and filter-feeders to reveal temporal and spatial patterns in sewage dispersal. Mar Ecol Prog Ser 235:63–73CrossRefGoogle Scholar
  21. Hadas O, Altabet MA, Agnihotri R (2009) Seasonally varying nitrogen isotope biogeochemistry of particulate organic matter in Lake Kinneret, Israel. Limnol Oceanogr 54:75–85CrossRefGoogle Scholar
  22. Heaton THE (1986) Isotopic studies of nitrogen pollution in the hydrosphere and atmosphere: a review. Isot Geosci 59:87–102CrossRefGoogle Scholar
  23. Hoering T (1955) Variations of nitrogen15 abundance in naturally occurring substances. Science 122:1233–1234PubMedCrossRefGoogle Scholar
  24. Jones AB, O'Donohue MJ, Udy J, Dennison WC (2001) Assessing ecological impacts of shrimp and sewage effluent: biological indicators with standard water quality analyses. Estuar Coast Shelf Sci 52:91–109CrossRefGoogle Scholar
  25. Lamb K, Swart PK, Altabet MA (2012) Nitrogen and carbon isotopic systematics of the Florida reef tract. Bull Mar Sci 88:119–146CrossRefGoogle Scholar
  26. Landrum JP, Montoya JP (2009) Organic matter processing by the shrimp Palaemonetes sp.: isotopic and elemental effects. J Exp Mar Biol Ecol 380:20–24CrossRefGoogle Scholar
  27. Lapointe BE, Bedford BJ (2007) Drift rhodophyte blooms emerge in Lee County, Florida, USA: evidence of escalating coastal eutrophication. Harmful Algae 6:421–437CrossRefGoogle Scholar
  28. Lapointe BE, Langton R, Bedford BJ, Potts AC, Day O, Hu C (2010) Land-based nutrient enrichment of the Buccoo Reef Complex and fringing coral reefs of Tobago, West Indies. Mar Pollut Bull 60:334–343PubMedCrossRefGoogle Scholar
  29. Lin DT, Fong P (2008) Macroalgal bioindicators (growth, tissue N, δ15N) detect nutrient enrichment from shrimp farm effluent entering Opunohu Bay, Moorea, French Polynesia. Mar Pollut Bull 56:245–249PubMedCrossRefGoogle Scholar
  30. Lobban CS, Harrison PJ (1994) Seaweed ecology and physiology. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  31. Lojen S, Spanier E, Tsemel A, Katz T, Eden N, Angel D (2005) δ15N as a natural tracer of particulate nitrogen effluents released from marine aquaculture. Mar Biol 148:87–96CrossRefGoogle Scholar
  32. Macko SA, Ostrom NE (1994) Pollution studies using stable isotopes. In: Michener R, Lajtha K (eds) Stable isotopes in ecology and environmental science. Blackwell Scientific, London, pp 42–65Google Scholar
  33. Mattern S, Sebilo M, Vanclooster M (2011) Identification of the nitrate contamination sources of the Brusselian sands groundwater body (Belgium) using a dual-isotope approach. Isot Environ Health Stud 47:297–315CrossRefGoogle Scholar
  34. McClelland JW, Valiela I, Michener RH (1997) Nitrogen-stable isotope signatures in estuarine food webs: a record of increasing urbanization in coastal watersheds. Limnol Oceanogr 42:930–937CrossRefGoogle Scholar
  35. Michener R, Lajtha K (2007) Stable isotopes in ecology and environmental science, 2nd edn. Blackwell Publishing, MaldenCrossRefGoogle Scholar
  36. 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 48:1135–1140CrossRefGoogle Scholar
  37. Miyake Y, Wada E (1967) The abundance ratio of 15N/14N in marine environments. Rec Oceanogr Works Jpn 9:37–53Google Scholar
  38. Naldi M, Wheeler PA (2002) 15N Measurements of ammonium and nitrate uptake by Ulva fenestrata (chlorophyta) and Gracilaria pacifica (rhodophyta): comparison of net nutrient disappearance, release of ammonium and nitrate, and 15N accumulation in algal tissue. J Phycol 38:135–144CrossRefGoogle Scholar
  39. Nier AO (1950) A redetermination of the relative abundances of the isotopes of neon, krypton, rubidium, xenon, and mercury. Phys Rev 79:450–454CrossRefGoogle Scholar
  40. Owens NJP, Blaxter JHS, Southward AJ (1988) Natural variations in 15N in the marine environment. Adv Mar Biol 24:389–451CrossRefGoogle Scholar
  41. Pennock JR, Velinsky DJ, Ludlam JM, Sharp JH, Fogel ML (1996) Isotopic fractionation of ammonium and nitrate during uptake by Skeletonema costatum: implications for δ15N dynamics under bloom conditions. Limnol Oceanogr 41:451–459CrossRefGoogle Scholar
  42. Piñón-Gimate A, Soto-Jimenez MF, Ochoa-Izaguirre M, García-Pages E, Paez-Osuna F (2009) Macroalgae blooms and δ15N in subtropical coastal lagoons from the Southeastern Gulf of California: discrimination among agricultural, shrimp farm and sewage effluents. Mar Pollut Bull 58:1144–1151PubMedCrossRefGoogle Scholar
  43. R Development Core Team (2008) R: a language and environment for statistical computing, vol 1. R Foundation for Statistical Computing, Vienna, p 7Google Scholar
  44. Read P, Fernandes T (2003) Management of environmental impacts of marine aquaculture in Europe. Aquaculture 226:139–163CrossRefGoogle Scholar
  45. Riera P (1998) δ15N of organic matter sources and benthic invertebrates along an estuarine gradient in Marennes-Oleron Bay (France): implications for the study of trophic structure. Mar Ecol Prog Ser 166:143–150CrossRefGoogle Scholar
  46. Riera P, Stal LJ, Nieuwenhuize J (2000) Heavy δ15N in intertidal benthic algae and invertebrates in the Scheldt Estuary (The Netherlands): effect of river nitrogen inputs. Estuar Coast Shelf Sci 51:365–372CrossRefGoogle Scholar
  47. Robinson D (2001) δ15N as an integrator of the nitrogen cycle. Trends Ecol Evol 16:153–162PubMedCrossRefGoogle Scholar
  48. Rogers KM (1999) Effects of sewage contamination on macro-algae and shellfish at Moa Point, New Zealand using stable carbon and nitrogen isotopes. NZ J Mar Freshw Res 33:181–188CrossRefGoogle Scholar
  49. Rogers KM (2003) Stable carbon and nitrogen isotope signatures indicate recovery of marine biota from sewage pollution at Moa Point, New Zealand. Mar Pollut Bull 46:821–827PubMedCrossRefGoogle Scholar
  50. Sarà G, Scilipoti D, Mazzola A, Modica A (2004) Effects of fish farming waste to sedimentary and particulate organic matter in a southern Mediterranean area (Gulf of Castellammare, Sicily): a multiple stable isotope study (δ13C and δ15N). Aquaculture 234:199–213CrossRefGoogle Scholar
  51. Savage C (2005) Tracing the influence of sewage nitrogen in a coastal ecosystem using stable nitrogen isotopes. Ambio 34:145–150PubMedGoogle Scholar
  52. Savage C, Elmgren R (2004) Macroalgal (Fucus vesiculosus) δ15N values trace decrease in sewage influence. Ecol Appl 14:517–526CrossRefGoogle Scholar
  53. Struck U (2012) On the use of stable nitrogen isotopes in present and past anoxic environments anoxia. In: Altenbach AV, Bernhard JM, Seckbach J (eds) Cellular origin, life in extreme habitats and astrobiology, vol 21. Springer, Dordrecht, pp 497–513Google Scholar
  54. Tello A, Corner RA, Telfer TC (2010) How do land-based salmonid farms affect stream ecology? Environ Pollut 158:1147–1158PubMedCrossRefGoogle Scholar
  55. Tett P, Gowen R, Mills D, Fernandes T, Gilpin L, Huxham M, Kennington K, Read P, Service M, Wilkinson M, Malcolm S (2007) Defining and detecting undesirable disturbance in the context of marine eutrophication. Mar Pollut Bull 55:282–297PubMedCrossRefGoogle Scholar
  56. Tucker J, Sheats N, Giblin AE, Hopkinson CS, Montoya JP (1999) Using stable isotopes to trace sewage-derived material through Boston Harbor and Massachusetts Bay. Mar Environ Res 48:353–375Google Scholar
  57. Umezawa Y, Miyajima T, Yamamuro M, Kayanne H, Koike I (2002) Fine-scale mapping of land-derived nitrogen in coral reefs by δ15N in macroalgae. Limnol Oceanogr 47:1405–1416CrossRefGoogle Scholar
  58. Vallyathan V, Castranova V, Shi X (2002) Oxygen/nitrogen radicals: Cell injury and disease, vol 234/235. Kluwer Academic, MassachusettsCrossRefGoogle Scholar
  59. Van Dover CL, Grassle JF, Fry B, Garritt RH, Starczak VR (1992) Stable isotope evidence for entry of sewage-derived organic material into a deep-sea food web. Nature 360:153–156CrossRefGoogle Scholar
  60. Viana IG, Aboal JR, Fernández JA, Real C, Villares R, Carballeira A (2010) Use of macroalgae stored in an Environmental Specimen Bank for application of some European Framework Directives. Water Res 44:1713–1724PubMedCrossRefGoogle Scholar
  61. Viana IG, Fernández JA, Aboal JR, Carballeira A (2011) Measurement of δ15N in macroalgae stored in an environmental specimen bank for regional scale monitoring of eutrophication in coastal areas. Ecol Indic 11:888–895CrossRefGoogle Scholar
  62. Villares R, Carballeira A (2003) Seasonal variation in the concentrations of nutrients in two green macroalgae and nutrient levels in sediments in the Rías Baixas (NW Spain). Estuar Coast Shelf Sci 58:887–900CrossRefGoogle Scholar
  63. Villares R, Carballeira A (2004) Nutrient limitation in macroalgae (Ulva and Enteromorpha) from the Rías Baixas (NW Spain). Mar Ecol 25:225–243CrossRefGoogle Scholar
  64. Villares R, Carballeira A (2006) Trophic categorization in the Rías Baixas (NW Spain): nutrients in water and in macroalgae. Sci Mar 70(1):89–97CrossRefGoogle Scholar
  65. Vizzini S, Mazzola A (2004) Stable isotope evidence for the environmental impact of a land-based fish farm in the western Mediterranean. Mar Pollut Bull 49:61–70PubMedCrossRefGoogle Scholar
  66. Vosz M, Struck U (1997) Stable nitrogen and carbon isotopes as indicator of eutrophication of the Oder River (Baltic Sea). Mar Chem 59:35–49CrossRefGoogle Scholar
  67. Wada E, Hattori A (1976) Natural abundance of 15N in particulate organic matter in the North Pacific Ocean. Geochim Cosmochim Acta 40:249–251CrossRefGoogle Scholar
  68. Wada E, Kadonaga T, Matsuo S (1975) 15N abundance in nitrogen of naturally occurring substances and global assessment of denitrification from isotopic viewpoint. Geochem J 9:139–148CrossRefGoogle Scholar
  69. Warton D, Ormerod J (2007) Smatr: Standardised Major Axis Estimation and Testing Routines. R package, 2.1 edn. http://web.maths.unsw.edu.au/~dwarton
  70. Wolanski E, Spagnol S, Thomas S, Moore K, Alongi DM, Trott L, Davidson A (2000) Modelling and visualizing the fate of shrimp pond effluent in a mangrove-fringed tidal creek. Estuar Coast Shelf Sci 50:85–97CrossRefGoogle Scholar
  71. Yang X, Wu X, Hao H, He Z (2008) Mechanisms and assessment of water eutrophication. J Zhejiang Univ 9(3):197–209CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Carlos Carballeira
    • 1
  • Inés G. Viana
    • 2
  • Alejo Carballeira
    • 3
  1. 1.Marine Ecotoxicology, Área de Química Física, Facultad de Ciencias del MarUniversidad de CádizCadizSpain
  2. 2.Instituto Español de OceanografíaA CoruñaSpain
  3. 3.Ecotoxicología, Área de Ecología, Facultad de BiologíaUniversidad de Santiago de CompostelaSantiago de CompostelaSpain

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