Bioavailability of Petroleum Hydrocarbons from Water, Sediments, and Detritus to the Marine Annelid, Neanthes Arenaceodentata
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BIOAVAILABILITY OF PETROLEUM HYDROCARBONS FROM WATER, SEDIMENTS, AND DETRITUS TO THE MARINE ANNELID, NEANTHES ARENACEODENTATA Steven S. Rossi Marine Biology Research Division Scripps Institution of Oceanography Downloaded from http://meridian.allenpress.com/iosc/article-pdf/1977/1/621/2349813/2169-3358-1977-1-621.pdf by guest on 29 September 2021 La Jolla, California 92093 ABSTRACT Methods Uptake, retention, metabolism, and depuration of diaromatic hydrocar- All experiments were performed with immature young adult polychaetes bons by the polychaete, Neanthes arenaceodentata, were examined in from a laboratory population of Neanthes arenaceodentata which was experiments utilizing seawater solutions and sediments contaminated with originally cultured by D. J. Reish, California State University, Long Beach. either No. 2 fuel oil water-soluble fractions or radio-labelled naphthalenes. Equal numbers of males and females were used, and all work was conducted Polychaetes rapidly accumulate 14C'-naphthalene (magnification factor at 21 ±2°C, with artificial seawater (Instant Ocean), adjusted to a salinity of = 40X) from solution during short-term exposure (24 hr). Worms slowly 32 ppt (7oo). released hydrocarbons accumulated during acute exposure down to unde- In experiments on the uptake, release, and metabolism of PHCs in tectable levels (<0.05ppm) within 300 hours after return to clean seawater. solution, male-female pairs were exposed for 24 hours to seawater contain- x 4 14C-naphthalene accumulated from solution was metabolized by ing 0.15 ppm C-naphthalene (specific activity = 1.72 mCi/mM) in air-free polychaetes, and associated microflora apparently play no role in uptake, containers. Following exposure, worms were transferred to hydrocarbon release, or metabolism. Analyses of worms held for 28 days in clay-silt (radioactivity) free seawater in aerated 1 liter bowls. At selected intervals sediments artificially contaminated with No. 2 fuel oil (9 ßg total during the latter period (depuration), pairs of worms were placed in air-free naphthalenes Ig wet sediment) indicate that naphthalenes were not accumu- containers for 24 hours to monitor the release of radioactivity from exposed lated by worms at tissue concentrations above 0.1 ppm. Polychaetes animals into seawater. Tissue samples were taken periodically throughout likewise failed to accumulate ^C-methylnaphthalene from ingestion of exposure and depuration for analysis of hydrocarbon content. Tissue and contaminated detritus (10-15 μ-g ^^C-methylnaphthalenelg dry detritus) for seawater samples were extracted with a known volume of high grade 16 consecutive days. These data suggest that petroleum hydrocarbons hexane, and radioactivity in the hexane and water extracts was determined in bound to sediment particles or paniculate organic matter are less available Aquasol-2 (New England Nuclear) on a Packard Tricarb liquid scintillation to marine worms than those in solution. spectrometer. Radioactivity extracted by hexane was assumed to be 14C- naphthalene, while that remaining in aqueous phases presumably rep- resented 14C-naphthalene-polar derivatives (metabolites). All data were corrected for background interference and quenching. The above experi- ments were performed both in the presence and absence of antibiotic agents (300 mg Penicillin G + 200 mg streptomycin sulphate + 50 mg Chloram- INTRODUCTION phenicol per liter of seawater). This mixture of antibiotic agents completely inhibits bacterial and fungal metabolism,4 permitting an assessment of the Members of several marine phyla concentrate petroleum hydrocarbons role which symbiotic microbes might play in the accumulation, metabolism, (PHCs) in their tissues when acutely exposed to seawater contaminated with and release of naphthalene by Neanthes. oil or specific hydrocarbons.3'27 In most cases, a majority of the accumulated PHC transfer from sediments to infauna (Neanthes) was studied by compounds are rapidly released when exposed animals are returned to clean exposing worms to sediment which had been previously contaminated seawater. Molluscs appear to be an exception to this trend, since depuration (artificially) by No. 2 fuel oil water-soluble fraction, prepared as described of PHCs from mussels and oysters occurs somewhat more slowly than in by Anderson et al.2 At selected times during exposure, worms and sediment other marine species.10'31 Some marine crustaceans8'1217 and fish19'23 can were analyzed for diaromatic hydrocarbons (naphthalenes) by ultraviolet biochemically alter (metabolize) accumulated PHCs, which may play a role spectrophotometry.22 Polychaetes were exposed in 1-liter culture dishes in their depuration from, and possibly detoxification with, body tissues. containing 600 ml flowing (15 ml/min) seawater and 80 g contaminated 918 Molluscs apparently lack the ability to metabolize PHCs. Dynamics of sediment (3 parts clay-silt mud: 1 part powdered alfalfa) for 28 days. soluble PHC uptake and release by polychaetous annelids, which are ecolog- Neanthes burrowed within and actively ingested sediment throughout the ically important in most bottom communities, have not been studied. In exposure period. The initial concentration of naphthalenes in sediments was addition, the role of PHC metabolism in members of this important marine approximately 9 ppm (9 μ-g total naphthalenes/ g fresh weight sediment). 16 phylum has only recently been investigated. To examine the feasibility of PHC contamination from ingestion of Crustacean zooplankters1115 andbenthic decapods1217 accumulate, depu- contaminated detritus (particulate organic matter), young adult Neanthes rate, and metabolize a broad variety of PHCs originally introduced through were offered detritus (powdered alfalfa) previously contaminated with 10-15 the diet. Studies on the bioavailability of PHCs in the diet of other important ppm * 4C-2-methylnaphthalene (specific activity = 7.98 mCi/mM), for 16 marine organisms have not been made. While some work has concerned days in succession. Worms were offered 5 mg of contaminated alfalfa daily itself with the transfer of pesticides in sediments to benthic (bottom- in individual culture dishes containing 50 ml seawater. After each 24-hour dwelling) species,21'25 no such work has been performed using PHCs. Thus, feeding period, some worms were transferred to clean feeding chambers for an examination of dynamics describing PHC contamination of marine or- continued feeding, others were sacrificed for analysis of hydrocarbon con- ganisms from food or sediments, particularly among burrowing species (e.g. tent (radioactivity), while others were fed powdered Tetramin for 24 hours polychaetes), merited further attention. before analysis of hydrocarbon content. After feeding on Tetramin for 24 621 622 1977 OIL SPILL CONFERENCE hours, worms had voided their guts of all alfalfa detritus, as determined by Table 1. Radioactivity in seawater containing pairs of polychaetes visual examination. Culture dish seawater, fecal pellets, and alfalfa were for selected 24 hour intervals during depuration, following acute ex- also monitored for radioactivity, both before and after daily feeding. posure to seawater solutions of l^C-naphthalene; total radioactivity Radioactivity was extracted with hexane, and determined as described equals that amount extracted by hexane and aqueous radioactivity earlier. not ex tractable with hexane (metabolized radioactivity); mean values for 8 samples are given; standard deviations were generally ± 20 cpm/ml Results Metabolized 14 Total radioactivity Kinetics of C-naphthalene uptake and release by both control and Depuration interval radioactivity released released treated (with antibiotic mixture—ABM) Neanthes are seen in Figure 1. Both (hours) groups accumulated and released 14C-naphthalene in nearly identical fash- (cpm/ml) (% of total) ion, and the quantitative role of metabolism appeared similar in both groups. Control ABM Control ABM 14 Downloaded from http://meridian.allenpress.com/iosc/article-pdf/1977/1/621/2349813/2169-3358-1977-1-621.pdf by guest on 29 September 2021 Uptake from solution was rapid, with close to maximal (i.e., 6 /xg C- 2 2 naphthalene/g tissue) accumulation observed after only three hours of expo- 0-24 6 X 10 4.8 X 10 60 69 sure. There was no trend toward a net decrease in tissue concentrations 24-48 5.5 X 102 4 X 102 78 71 during the latter stages of exposure, as has been observed in work with other 1 1 marine organisms.3 Neanthes did not metabolize significant quantities of 72-96 2 X 10 1.5 X 10 80 82 14 C-naphthalene during exposure. 168-192 40 25 100 100 When returned to clean seawater, both groups slowly released accumu- lated 14C-naphthalene, and depuration of native x 4C-naphthalene was com- plete (<0.05 ppm in tissues) within 300 hours. Polychaetes treated with ABM depurated 14C-naphthalene in much the same manner as did untreated (control) worms. Thus, bacteria or fungi do not appear to play any part in the uptake, metabolism, and depuration of 14C-naphthalene by Neanthes. Data from the analysis of radioactivity released by worms during depuration are presented in Table 1. Both groups released radioactivity in the un- metabolized (native), as well as metabolized, form. Approximately one- / third of the radioactivity released by both groups during their first 24 hours in SEDIMENTS clean seawater was in the native form. The relative percentages of radioac- tivity released during depuration closely paralleled those which simulta- neously occurred within tissues.