Alteration and release of aliphatic compounds by the polychaete Nereis virens (Sars) experimentally fed with hydrocarbons

https://doi.org/10.1016/S0022-0981(00)00317-8Get rights and content

Abstract

In the laboratory, marine worms were fed with a mixture of algae and several aliphatic hydrocarbons for 15 days. After ingestion by the worms, 34.9% of hydrocarbons are found in the faeces and only 3.1% accumulated in the gut. The comparison between the initial mixture and the faeces shows that the worm’s digestive process lead to changes in the distribution of the n-alkane mixture. These changes are different from those only due to physical processes in the experimental conditions. In our experiment, no variation in the distribution of hydrocarbons in faeces with time and no microbial hydrocarbon biodegradation were evidenced. Our results suggest that marine worm feeding can substantially affect the fate of hydrocarbons in the sedimentary marine ecosystem by predominantly stimulating dissolution processes.

Introduction

The activity of benthic organisms modifies the physical and chemical nature of marine sediments (Aller, 1982). In the case of petroleum pollution, if the changes in the chemical environment can affect the sedimentary biota, all the biological processes included under the term ‘bioturbation’ play an important role with regard to the fate of hydrocarbon pollutants (Lee and Swartz, 1980).

Previous works dealing with the role of bioturbation in the fate of hydrocarbons have more particularly taken into account their overall weathering related to the biological distribution and transfers of pollutants adsorbed onto the sediment (Gardner et al., 1979, Karickhoff and Morris, 1985, Reynoldson, 1987, Gilbert et al., 1994, Gilbert et al., 1996, Kure and Forbes, 1997). During the mixing of sediments, bioturbating macrofauna stimulates hydrocarbon desorption for particles (Koerting-Walker and Buck, 1989), and then greatly favours their bioavailability (Mihelcic and Luthy, 1991, Madsen et al., 1997) and resulting bacterial biodegradation (Gordon et al., 1978, Bauer et al., 1988, McElroy et al., 1990). In areas of intensive reworking, where the benthic macrofauna ingests the surface sediment several times a year (Myers, 1977), the digestive activity of macro-organisms, and more especially worms, may represent a non-negligible part of the hydrocarbon handling thus exposed to microbiological transformations (Plante and Jumars, 1992) and to a chemical environment controlled by the digestive chemistry of the organism (Mayer et al., 1997, Gilbert et al., 1998). More especially, passage of hydrocarbons through the worm gut may also result in metabolisation and accumulation (Lee and Singer, 1980, McElroy and Sisson, 1989, Forbes et al., 1996, Fergusson and Chandler, 1998, Sheedy et al., 1998). Moreover, recent works have demonstrated the high hydrocarbon solubilising potential of extracted gut digestive fluids (Mayer et al., 1996, Weston and Mayer, 1998a, Weston and Mayer, 1998b).

The aim of our work was to provide more information on the direct role of macrofauna during its digestive activity with regard to the fate of hydrocarbons in marine sediments. To this end, a laboratory experiment has been carried out with the aim of monitoring the uptake, release and alteration of a mixture of aliphatic hydrocarbons ingested by the marine polychaete Nereis virens. The Nereidae, due to their wide distribution and easy laboratory maintenance and acclimation, are the most suitable genus to test the fate of persistent pollutants in marine animals (Goerke, 1984). In the Saint Lawrence estuary, N. virens is one of the most important mudflat species because of its high density (Desrosiers et al., 1994). This worm builds U-shaped burrows in the sediment layer with extension, for adults, up to 30–50 cm below the sediment surface (Goerke, 1976, Kristensen et al., 1985, Miron et al., 1991a). This species inhabits extensive soft substrates in littoral and sub-littoral zones on the coasts of NE North America and NW Europe. Due to urban and industrial activity, this type of environment is highly exposed to the impact of many types of pollutants, particularly hydrocarbons.

Section snippets

Experimental setup and hydrocarbon tracer preparation

In November 1996, 20 adult polychaetes Nereis virens (wet weight: 3.16±0.29 g; mean±S.D.) were randomly collected in the tidal zone of l’Anse à l’Orignal (Bic, Québec, Canada) and placed in four experimental containers (50×25×5 cm). In the five individual sections of each container, a worm was placed in a transparent horizontal glass tube (length: 19 cm; I.D.: 0.7 cm) which perfectly substitutes for the natural habitat burrows (Goerke, 1984). Each section was filled with filtered (2 μm)

Feeding ethology

Faeces weights collected in experimental containers with time are given in Fig. 2. The first 2 days (FD1 and FD2), the mean weights of collected faeces (five polychaete individuals in each of the four containers) were 15.7±5.57 and 11.9±3.42 mg (mean±S.D.; n=4), respectively. Then, from the third day (FD3), Enteromorpha sp. leaf fragments appeared in the faecal material resulting in the increase of faeces mean weight that varied from 35.8±11.45 to 107.9±26.61 mg (mean±S.D.; n=4) during the

Discussion

In this type of laboratory experiment, it is important to choose a good diet procedure to be quite sure that animals take the entire contaminated ration. In 1984, Goerke showed that using oral dosing through the foods occurs presented a very high uptake efficiency. This procedure is particularly useful if the test compounds are highly volatile or have extremely low water-solubility such as polychlorinated biphenyl. For this reason we chose this method for our study on the release of

Acknowledgements

Authors thank the anonymous reviewers for constructive comments. This work was carried out as part of the G.R.E.C. (Groupe de Recherche en Environnement Côtier, UQAR, Québec, Canada) and the G.D.R. 1123 ‘HYCAR’ (CNRS — Universities — Société Elf Aquitaine, France) and was supported by a grant from the Société de Secours des Amis des Sciences to Franck Gilbert and by grants from the Natural Sciences and Engineering Research Council of Canada (CRSNG) to Gaston Desrosiers and Jean-Pierre Gagné.

References (42)

  • R.C. Aller

    The effects of macrobenthos on chemical properties of marine sediment and overlying water

  • R.M. Atlas

    Microbial degradation of petroleum hydrocarbons: an environmental perspective

    Microbiol. Rev.

    (1981)
  • J.E. Bauer et al.

    Stimulation of microbial activities on polycyclic aromatic hydrocarbon degradation in marine sediments inhabited by Capitella capitata

    Mar. Environ. Res.

    (1988)
  • M.J. Bock et al.

    Digestive plasticity of the marine benthic omnivore Nereis virens

    J. Exp. Mar. Biol. Ecol.

    (1999)
  • M. Blumer et al.

    The environmental fate of stranded crude oil

    Deep Sea Res.

    (1973)
  • G. Desrosiers et al.

    Cycle de développement du pluchète (Sars) dans la zone intertidale de l’Estuaire maritime du Saint-Laurent

    Oceanol. Acta

    (1994)
  • L. Eastcott et al.

    Environmentally relevant physical–chemical properties of hydrocarbons: a review of data and development of simple correlations

    Oil Chem. Pollut.

    (1988)
  • W. Ernst et al.

    Fate of 14C-labelled di-, tri- and pentochlorbiphenyl in the marine annelid. II. Degradation and faecal elimination

    Chemosphere

    (1977)
  • P.L. Fergusson et al.

    A laboratory and field comparison of sediment polycyclic aromatic hydrocarbon accumulation by the cosmopolitan estuarine polychaete Streblospio benedicti (Webster)

    Mar. Environ. Res.

    (1998)
  • V.E. Forbes et al.

    Inducible metabolism of fluoranthene by the opportunistic polychete Capitella sp. I

    Mar. Ecol. Prog. Ser.

    (1996)
  • W.S. Gardner et al.

    Degradation of selected polycyclic aromatic hydrocarbons in coastal sediments: importance of microbes and polychaete worms

    Water Air Soil Pollut.

    (1979)
  • F. Gilbert et al.

    The in vitro influence of the burrowing polychaete Nereis diversicolor on the fate of petroleum hydrocarbons in marine sediments

    Chemosphere

    (1994)
  • F. Gilbert et al.

    In situ bioturbation and hydrocarbon fate in an experimental contaminated Mediterranean coastal ecosystem

    Chemosphere

    (1996)
  • F. Gilbert et al.

    Changes in aliphatic hydrocarbon tracer composition during the marine worm Nereis virens digestive process. Preliminary results

    Chemosphere

    (1998)
  • H. Goerke

    Testing the fate of xenobiotics in Polychaeta

  • D.C. Gordon et al.

    Importance of sediment working by the deposit-feeding polychaete Arenicola marina on the weathering rate of sediment-bound oil

    J. Fish. Res. Board Can.

    (1978)
  • S.W. Karickhoff et al.

    Impact of tubificid oligochaetes on pollutant transport in bottom sediments

    Environ. Sci. Technol.

    (1985)
  • C. Koerting-Walker et al.

    The effect of bacteria and bioturbation by Clymenella torquata on oil removal from sediment

    Water Air Soil Pollut.

    (1989)
  • E. Kristensen et al.

    The impact of polychaete (Nereis virens Sars) burrows on nitrification and nitrate reduction in estuarine sediments

    J. Exp. Mar. Biol. Ecol.

    (1985)
  • L.K. Kure et al.

    Impact of bioturbation by Arenicola marina on the fate of particle-bound fluoranthene

    Mar. Ecol. Prog. Ser.

    (1997)
  • Cited by (15)

    • Response of sediment bacterial community to triclosan in subtropical freshwater benthic microcosms

      2019, Environmental Pollution
      Citation Excerpt :

      This may be associated with the difference in TCS bioavailability due to the disturbance of the water-sediment interface caused by the presence of benthic macroinvertebrates (Cuny et al., 2007; Selck et al., 2005). Due to their feeding strategy which includes ingestion of sediment particles, L. hoffmeisteri can be exposed to sediment-associated TCS from the gut, which may result in TCS dissolution and solubilisation in the worm gut (Gilbert et al., 2001; Cuny et al., 2007). Therefore, in addition to potentially increasing bioaccumulation of TCS from the gut into worm tissue, the TCS passage through the worm gut may stimulate the TCS bioavailability to sediment bacterial communities (both in the gut and in the defecated fecal matter).

    • Redox oscillation and benthic nitrogen mineralization within burrowed sediments: An experimental simulation at low frequency

      2016, Journal of Experimental Marine Biology and Ecology
      Citation Excerpt :

      Bioturbation (sensu Kristensen et al., 2012) plays a major role in the early diagenesis of sedimentary organic matter (OM) (Gilbert et al., 1996; Mayer et al., 1996; Aller and Aller, 1998; Sun et al., 1999; Reise, 2002). Particle reworking by benthos directly affects the distribution and fate of particulate organic substrates and adsorbed OM (Boudreau et al., 1998; Gérino et al., 1998; Widdows et al., 1998; Smallwood et al., 1999; Gilbert et al., 2001). Bioirrigation of sediments due to burrow or feeding-pocket ventilation promotes solute exchange across the sediment-water interface, enhances the removal of metabolites from pore water and supplies respiratory reactants such as O2 and SO42 − (Jørgensen and Revsbech, 1985; Forster et al., 1999; Timmermann et al., 2006; Behrens et al., 2007).

    View all citing articles on Scopus
    View full text