Environmental Science and Pollution Research

, Volume 22, Issue 20, pp 15285–15293 | Cite as

Functional response of an adapted subtidal macrobenthic community to an oil spill: macrobenthic structure and bioturbation activity over time throughout an 18-month field experiment

DECAPAGE Project: Hydrocarbon degradation in coastal sediments*


An experimental oil spill was carried out in order to assess in situ responses of a macrobenthic community of shallow subtidal sediments historically exposed to petroleum contamination. Both structural and functional (bioturbation activity) parameters of the community, subjected or not to a pulse acute contamination (25,000 ppm), were studied for 18 months. No difference in the community structure was detected between contaminated and control sediments, from 6 to 18 months of experimentation. Vertical distributions of organisms, however, were affected by the presence of oil contamination leading to a deeper burial of some polychaete species. In the same time, changes in sediment-reworking activity and more especially a deeper particle burying in sediments subjected to acute oil contamination were shown. These results highlight the need to complete the analysis of community structure by assessing functional aspects, such as bioturbation activity, a process integrating various aspects of benthic behaviour (e.g. feeding, locomotion, burrow building) in order to estimate real (structural and functional) and long-term effects of oil contamination on benthic communities.


Subtidal shallow sediments Field experiment Acute oil contamination Macrobenthic community Bioturbation Sediment reworking 

Supplementary material

11356_2014_3906_MOESM1_ESM.pdf (32 kb)
ESM 1(PDF 32 kb)


  1. Aller RC (1994) Bioturbation and remineralization of sedimentary organic matter: effects of redox oscillation. Chem Geol 114:331–345CrossRefGoogle Scholar
  2. Bickman JW, Smolen MJ (1994) Somatic and heritable effects of environmental genotoxins and the emergence of evolutionary toxicology. Environ Health Perspect 102:25–28Google Scholar
  3. Bolam SG (2011) Burial survival of benthic macrofauna following deposition of simulated dredged material. Environ Monitor Assess 181:13–27CrossRefGoogle Scholar
  4. Bray JR, Curtis JT (1957) An ordination of upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349CrossRefGoogle Scholar
  5. Buchanan JB (1964) A comparative study of some features of the biology of Amphiura filiformis and Amphiura chiajei (Ophiuroidea) considered in relation to their distribution. J Mar Biol Assoc UK 44:565–576CrossRefGoogle Scholar
  6. Carman KR, Fleeger JW, Pomarico SM (2000) Does historical exposure to hydrocarbon contamination alter the response of benthic communities to diesel contamination? Mar Environ Res 49:255–278CrossRefGoogle Scholar
  7. Cuny P, Miralles G, Cornet-Barthaux V, Acquaviva M, Stora G, Grossi V, Gilbert F (2007) Influence of bioturbation by the polychaete Nereis diversicolor on the structure of bacterial communities in oil contaminated coastal sediments. Mar Poll Bull 54:452–459CrossRefGoogle Scholar
  8. Cuny P, Cravo-laureau C, Grossi V, Gilbert F, Militon C (2011) Biodegradation of hydrocarbons in bioturbated marine sediments. In: Koukkou AI (ed) Microbial bioremediation of non-metals: current research. Caister Academic Press, pp 55–92Google Scholar
  9. Depledge MH (1996) Genetic ecotoxicology: an overview. J Exp Mar Biol Ecol 200:57–66CrossRefGoogle Scholar
  10. Di Toro DM, Zarba CS, Hansen DJ, Berry WJ, Swartz RD, Cowan CE, Pavlou SP, Allen HE, Thomas NA, Paquin PR (1991) Technical basis for establishing sediment quality criteria for nonionic organic chemicals using equilibrium partitioning. Environ Toxicol Chem 10:1541–1583CrossRefGoogle Scholar
  11. Duport E, Gilbert F, Poggiale JC, Dedieu K, Rabouille C, Stora G (2007) Benthic macrofauna and sediment reworking quantification in contrasted environment in the Thau Lagoon. Estuar Coast Shelf Sci 72:522–533CrossRefGoogle Scholar
  12. Egres AG, Martins CC, Oliveira VM, Lana PC (2012) Effects of an experimental in situ diesel oil spill on the benthic community of unvegetated tidal flats in a subtropical estuary (Paranaguá Bay, Brazil). Mar Poll Bull 64:2681–2691CrossRefGoogle Scholar
  13. Fauchald K, Jumars PA (1979) The diet of worms: a study of polychaete feeding guilds. Oceanogr Mar Biol 17:193–284Google Scholar
  14. Ferrando A, Gonzalez E, Franco M, Commendatore M, Nievas M, Militon C, Stora C, Gilbert F, Esteves JL, Cuny P (2015) Oil spill effects on macrofaunal communities and bioturbation of pristine marine sediments (Caleta Valdés, Patagonia, Argentina): experimental evidence of low resistance capacities of benthic systems without history of pollution. (in this issue)Google Scholar
  15. Fodrie FJ, Herzka SZ, Lucas AJ, Francisco V (2007) Intraspecific density regulates positioning and feeding mode selection of the sand dollar Dendraster excentricus. J Exp Mar Biol Ecol 340:169–183CrossRefGoogle Scholar
  16. François F, Gerino M, Stora G, Durbec JP, Poggiale JC (2002) Functional approach to sediment reworking by gallery-forming macrobenthic organisms: modeling and application with the polychaete Nereis diversicolor. Mar Ecol Progr Ser 229:127–136CrossRefGoogle Scholar
  17. Gandra MS, Bemvenuti CE, Angonesi LG (2006) Experimental study of oil impact and its consequences upon benthic macrofauna in the Estuary of Patos Lagoon (RS-Brazil). J Coast Res, SI ICS 2004 Proc 39:1450–1454Google Scholar
  18. Gilbert F, Rivet L, Bertrand JC (1994) The in vitro influence of the burrowing polychaete Nereis diversicolor on the fate of petroleum hydrocarbons in marine sediments. Chemosphere 29:1–12CrossRefGoogle Scholar
  19. Gilbert F, Stora G, Bertrand JC (1996) In situ bioturbation and hydrocarbon fate in an experimental contaminated Mediterranean coastal ecosystem. Chemosphere 33:1449–1458CrossRefGoogle Scholar
  20. Gilbert F, Stora G, Bonin P, Ledréau Y, Mille G, Bertrand JC (1997) Hydrocarbon influence on denitrification in bioturbated Mediterranean coastal sediments. Hydrobiologia 345:67–77CrossRefGoogle Scholar
  21. Glasby TM, Underwood AJ (1996) Sampling to differentiate between pulse and press perturbations. Environ Monitor Assess 42:241–252CrossRefGoogle Scholar
  22. Gómez Gesteira JL, Dauvin JC (2000) Amphipods are good bioindicators of the impact of oil spills on soft-bottom macrobenthic communities. Mar Poll Bull 40:1017–1027CrossRefGoogle Scholar
  23. Gómez Gesteira JL, Dauvin JC (2005) Impact of the Aegean Sea oil spill on the Rîa of Ares and Betanzos fine sand community (Northwest Spain). Mar Environ Res 60:289–316CrossRefGoogle Scholar
  24. Grossi V, Massias D, Stora G, Bertrand JC (2002) Burial, exportation and degradation of acyclic petroleum hydrocarbons following a simulated oil spill in bioturbated Mediterranean coastal sediments. Chemosphere 48:947–954CrossRefGoogle Scholar
  25. Hale R, Mavrogordato MN, Tolhurst TJ, Solan M (2014) Characterizations of how species mediate ecosystem properties require more comprehensive functional effect descriptors. Sci Rep 4:6463CrossRefGoogle Scholar
  26. Hawkins AJ (1998) Population responses to contaminant exposure in marine animals: infuences of genetic diversity measured as allozyme polymorphism. Arch Tox 20:429–439CrossRefGoogle Scholar
  27. Hinchey EK, Schaffner LC, Hoar CC, Vogt BW, Batte LP (2006) Responses of estuarine benthic invertebrates to sediment burial: the importance of mobility and adaptation. Hydrobiologia 556:85–98CrossRefGoogle Scholar
  28. Je J-G, Belan T, Levings C, Koo BJ (2003) Changes in benthic communities along a presumed pollution gradient in Vancouver Harbour. Mar Environ Res 57:121–135CrossRefGoogle Scholar
  29. Kingston PF (1992) Impact of offshore oil production installations on the benthos of the North Sea. ICES J Mar Sci 49:45–53CrossRefGoogle Scholar
  30. Kristensen E, Penha-Lopes G, Delefosse M, Valdemarsen T, Quintana CO, Banta GT (2012) What is bioturbation? The need for a precise definition for fauna in aquatic sciences. Mar Ecol Prog Series 446:285–302CrossRefGoogle Scholar
  31. Kristensen E, Delefosse M, Quintana CO, Flindt MR, Valdemarsen T (2014) Influence of benthic macrofauna community shifts on ecosystem functioning in shallow estuaries. Front Mar Sci 1:41CrossRefGoogle Scholar
  32. Lindsay SM, Woodin SA (1995) Tissue loss induces switching of feeding mode in spionid polychaetes. Mar Ecol Prog Series 125:159–169CrossRefGoogle Scholar
  33. Lopez GR, Levinton SS (1987) Ecology of deposit-feeding animals in marine sediments. Q Rev Biol 62:235–260CrossRefGoogle Scholar
  34. Maire O, Merchant JN, Bulling M, Teal LR, Gremare A, Duchene JC, Solan M (2010) Indirect effects of non-lethal predation on bivalve activity and sediment reworking. J Exp Mar Biol Ecol 395:30–36CrossRefGoogle Scholar
  35. Mille G, Mulyono M, El Jammal T, Bertrand JC (1988) Effects of oxygen on hydrocarbon degradation studies in vitro in surficial sediments. Estuar Coast Shelf Sci 27:283–295CrossRefGoogle Scholar
  36. Mille G, Asia L, Guiliano M, Malleret L, Doumenq P (2007) Hydrocarbons in coastal sediments from the Mediterranean Sea (Gulf of Fos area, France). Mar Poll Bull 54:566–575CrossRefGoogle Scholar
  37. Miller DC, Muir CL, Hauser OA (2002) Detrimental effects of sedimentation on marine benthos: what can be learned from natural processes and rates? Ecol Engin 19:211–232CrossRefGoogle Scholar
  38. Miralles G, Nérini D, Manté C, Acquaviva M, Doumenq P, Michotey V, Nazaret S, Bertrand JC, Cuny P (2007) Effects of spilled oil on bacterial communities of mediterranean coastal anoxic sediments chronically subjected to oil hydrocarbon contamination. Microb Ecol 54:646–661CrossRefGoogle Scholar
  39. Negrello Filho OA, Underwood AJ, Chapman MG (2006) Recolonization of infauna on a tidal flat: an experimental analysis of modes of dispersal. J Exp Mar Biol Ecol 328:240–250CrossRefGoogle Scholar
  40. Nikitik CCS, Robinson AW (2003) Patterns in benthic populations in the Milford Haven waterway following the ‘Sea Empress’ oil spill with special reference to amphipods. Mar Pollut Bull 46:1125–1141CrossRefGoogle Scholar
  41. Pischedda L, Poggiale JC, Cuny P, Gilbert F (2008) Imaging oxygen distribution in marine sediments. The importance of bioturbation and sediment heterogeneity. Acta Biotheor 56:123–135CrossRefGoogle Scholar
  42. Pischedda L, Cuny P, Poggiale JC, Gilbert F (2012) Spatial oxygen heterogeneity in a Nereis diversicolor irrigated burrow. Hydrobiologia 680:109–124CrossRefGoogle Scholar
  43. Plante-Cuny MR, Salen-Picard C, Grenz C, Plante R, Alliot E, Barranguet C (1993) Experimental field study of the effects of crude oil, drill cuttings and natural biodeposits on microphyto- and macrozoobenthic communities in a Mediterranean area. Mar Biol 117:355–366CrossRefGoogle Scholar
  44. Riisgård HU (1994) Filter-feeding in the polychaete Nereis diversicolor: a review. Neth J Aquat Ecol 28:453–458CrossRefGoogle Scholar
  45. Riisgård HU, Larsen PS (2010) Particle capture mechanisms in marine suspension-feeding invertebrates. Mar Ecol Progr Ser 418:255–293CrossRefGoogle Scholar
  46. Sánchez-Moyano JE, García-Asencio I (2009) Distribution and trophic structure of annelid assemblages in a Caulerpa prolifera bed from southern Spain. Mar Biol Res 5:122–132CrossRefGoogle Scholar
  47. Scaps P (2002) A review of the biology, ecology and potential use of the common ragworm Hediste diversicolor (O.F. Müller) (Annelida: Polychaeta). Hydrobiologia 470:203–218CrossRefGoogle Scholar
  48. Seo JY, Kim M, Lim H-S, Choi J-W (2014) The macrofaunal communities in the shallow subtidal areas for the first 3 years after the Hebei Spirit oil spill. Mar Poll Bull 82:208–220CrossRefGoogle Scholar
  49. Thrush SF, Hewitt JE, Gibbs M, Lundquist C, Norkko A (2006) Functional role of large organisms in intertidal communities: community effects and ecosystem function. Ecosystems 9:1029–1040CrossRefGoogle Scholar
  50. Venturini N, Tommasi LR (2004) Polycyclic aromatic hydrocarbons and changes in the trophic structure of polychaete assemblages in sediments of Todos os Santos Bay, Northeastern, Brazil. Mar Poll Bull 48:97–107CrossRefGoogle Scholar
  51. Venturini N, Muniz P, Bícego MC, Martins CC, Tommasi LR (2008) Petroleum contamination impact on macrobenthic communities under the influence of an oil refinery: Integrating chemical and biological multivariate data. Estuar Coast Shelf Sci 78:457–467CrossRefGoogle Scholar
  52. Zabbey N, Uyi H (2014) Community responses of intertidal soft-bottom macrozoobenthos to oil pollution in a tropical mangrove ecosystem, Niger Delta, Nigeria. Mar Pollut Bull 82:167–174CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.INP, UPS, EcoLab (Laboratoire écologie fonctionnelle et environnement)Université de ToulouseToulouseFrance
  2. 2.CNRS, EcoLabToulouseFrance
  3. 3.Aix-Marseille Université, CNRSUniversité de Toulon, IRD, MIO (Mediterranean Institute of Oceanography) UM 110MarseilleFrance

Personalised recommendations