Effects of oil and oil dispersant on an enclosed marine ecosystem

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Environ, Sci. Technol. 1987, 21, 374-382

Effects of Oil and Oil Dispersant on an Enclosed Marine Ecosystem Oiof Lindin" and Arno Rosemarin" Swedish Environmental Research Group, Baltic Sea Laboratory, Utovagen 5, S-371 37 Karlskrona, Sweden

Anne Lindskog and Christina Hoglund Swedish Environmental Research Institute, S- 100 3 1 Stockholm, Sweden

Sit Johansson Ask0 Laboratory, University of Stockholm, S-106 91 Stockholm, Sweden

The effects of a North Sea oil with and without the addition of an oil spill dispersant were studied in a model of the littoral ecosystem of the Baltic Sea. Measured ecosystem parameters included abundance of heterotrophic bacteria, periphyton and phytoplankton photosynthesis, growth of bladderwrack, zooplankton abundance and diversity, physiological responses of certain crustaceans and molluscs, and growth of blue mussels. In addition, net photosynthesis and respiration of the ecosystem were studied. Concentrations of oil in water and blue mussels were monitored. The results of the experiments showed that almost all the measured parameters were affected, although several of the results indicated a stronger response to oil alone than to oil plus dispersant. On the basis of the results of this experiment, it may be concluded that the use of oil dispersants on diverse shallow water communities may produce greater acute effects than if a dispersant is not used. The long-term effects, however, may prove to be less severe than the dispersion of oil by natural processes.

Introduction Over the last 2 decades there has been a debate regarding the environmental implications of the use of chemical oil spill dispersants in the cleanup of oil spills. In a number of laboratory studies, the effects of various oils, either mixed with different dispersants or alone, have been studied on a large set of marine organisms in different developmental stages (for a review, see ref 1). However, the lack of relevance between laboratory-scale experiments and the field situation is well-known. The field studies that can be carried out instead, or in parallel, frequently involve extensive sampling programs and usually lack true reference samples or control sites. For acute spills, such as release of oil under accidental conditions, the logistical problems in addition to the problems with true reference areas are usually even more pronounced. Hence, the need for a bridge between laboratory studies and the field has long been recognized. Therefore, at a number of research stations, test methods have been developed that contain the main components of the natural ecosystem where controlled manipulations can be carried out (for example, the Kiel plankton tower (2),the Oslo fjord basin experiments (3),the MERL tanks (4), and the CEPEX enclosures ( 5 , 6 ) . At the Baltic Sea Laboratory in Karlskrona, Sweden, a test system has been developed that focuses on the littoral community of the Baltic Sea. The experiments, which are carried out in 8-m3pools, were initiated over 10 years ago (7-9). The main biological component of this ecosystem is the bladderwrack (Fucus vesiculosus), which constitutes over 90% of the biomass of the Baltic littoral zone. An important advantage in studying this community, in addition to its function as the ecologically most important subsystem of the Baltic Sea (IO),is the comparatively low diversity. This facilitates the transplanting 374

Environ. Sci. Technol., Vol. 21, No. 4, 1987

of a relatively complete ecosystem into test systems. This investigation was carried out over a 6-month period starting in May 1983.

Methods Test System. The experiment was carried out outside the laboratory building of the Baltic Sea Laboratory in Karlskrona, Sweden. Six circular commerically available pools were used. Each pool had a surface area of 10.25 m2, a height of 1m, and a volume of 8 m3 and was provided with a flow-through of seawater. The seawater was pumped to a reservoir from 7-m depth in the Denmark Bight, a bay of the Baltic Sea at the city of Karlskrona. The constant flow of water into each pool from the reservoir was regulated by head pressure and glass capillaries producing a flux of 2.8 L/min or a 50% replacement of the water in approximately 24 h. A surface paddle wheel with a diameter of 10 cm connected to an electric motor (r = 6O/min) provided a slight wave energy into each pool. The outlet pipe from each pool was situated about 20 cm above the bottom and was covered by a mesh (mesh size 1 X 1 mm) to prevent macrofauna from escaping. The outlet pipe was constructed as a siphon equipped with a gas trap to prevent gas bubbles from blocking the water flow in the pipe. A stream of the incoming and outflowing water from each of the pools was transferred through hoses into a measuring chamber from which it was finally disposed. By flushing the chamber for 3 min, different pools could be automatically monitored in succession with a computer-drivenvalve switch. The chamber was equipped with electrodes for temperature, oxygen, conductivity, and pH measurements. The readings from each pool were automatically stored on a diskette with a microcomputer. In this way it was possible to continuously monitor these parameters during the experiment and to evaluate the net productivity in each pool. Ecosystem. The bottom of each pool was covered with a layer of clean sand. Following this, bladderwracks (Fucus vesiculosus) attached to stones of suitable size (up to a few kilograms) were transferred to the pools and placed so that they covered about one-third of the bottom area in each pool. For the collection of the plants, plastic bags were used. These were carefully folded over the plant and stone to prevent mobile organisms from escaping. The contents of the bag were transferred into a bucket and then immediately taken to the pools where the number of plants and their volumes were determined by volume displacement before being placed into the pools. The quantity of algal material was the same in each pool. In addition to the organisms transplanted this way, some motile species, which could not be obtained by this method, were collected with a dip net and transferred and distributed in equal numbers into the pools. This was done for the crustaceans Neomysis spp, Leander adspersus, and Crangon crangon and for the fish Gasterosteus aculeatus and Platichtys

0013-936X/87/0921-0374$01.50/0

0 1987 American Chemical Society

Table I. Species Composition and Abundance of Macrofauna in the Poolsn

species Turbellaria spp Nemertini Prostoma obscurum Oligochaeta spp Polychaeta Nereis diversicolor Mollusca Theodoxus fluviatilis Hydrobia spp Lymnea peregra Mytilus edulis Cardium spp Macoma baltica Crustacea Balanus improvisus Gammarus spp Zdotea spp Iaera albifrons Leander adspersus Praunus + Neomysis spp Crangon crangon Chironomidae spp Pisces Gasterosteus aceuleatus Platichtys flesus total

estimated tot no. of av no. of individuals individuals per 100 g in one pool of Fucus wet wt f SE 100

0.6 f 0.2

100

0.5 f 0.3

50

0.2 f 0.1

4000 1500 100 3400 6000

25.9 f 3.9 9.7 f 4.8 0.6 f 0.2 22.1 f 3.1 38.9 f 7.4

50b 50

1700 600 150 50b 1500b 50b 100

10.9 f 2.7 3.7 1.3 1.0 f 0.5 0.1 2.3 f 0.7

*

0.7 f 0.3

35b 5b

2x

104

119.1 f 10.7

OThe estimation of the abundance of the Fucus fauna is based on the average counted number of animals per 100 g of Fucus and a rough estimation of the number outside the Fucus part of the pool. The numbers are calculated from 12 samples (two per pool) taken at the beginning of May. Counted number.

flesus. In total, each pool contained approximately 2 X lo4individuals of macrofauna belonging to about 30 species (Table I). The communities in the pools were allowed to stabilize for about 1 month before the start of the experiment. Oil and Dispersant. The oil used in the experiment was a North Sea crude oil from the Forties oil field in the British sector. Two pools were dosed with the same amount Qf oil plus an oil spill dispersant. Two other pools were dosed with oil alone without the dispersant. Two pools were kept as controls. The amount of oil added was calculated so that it would be equivalent to 20 ppm, assuming total mixture into the entire volume of water. The dispersant used was Corexit 9550 (Exxon). Fresh oil and dispersant were mixed in a 1O:l proportion. Hence, 154 mL of oil and 15.4 mL of dispersant were added to 1L of seawater in a 2-L glass bottle. The bottle was vigorously shaken for 1min by hand. After being shaken, the mixture was poured into the pool. The same procedure was followed also for the experiment with oil alone. Abiotic Parameters. In addition to the automated measurements of pH, oxygen, temperature, and conductivity described above (Test System), insolation in pE/ (m2.s)was measured continuously during the experiment. Petroleum hydrocarbons in the water were measured with the IR technique. In addition, the uptake, retention, and release of petroleum hydrocarbons in blue mussels (Mytilus edulis) were monitored by gas chromatography analysis of tissue extracts. The methods for sampling, extraction, and analysis are given as supplementary material. Biotic Parameters. Numbers of heterotrophic bacteria were determined from 2-L water samples from each pool.

The numbers were determined by plate counts on a “nonselective medium” (TGE). Samples were collected 30 h and 4,7,11, 18, and 30 days after the exposure started. In addition, in samples from 30 h and 19 and 73 days the number of Enterobacteriaceae, Aeromonas sp, Vibrio sp, and Alteromonas putrefaciens were counted. Also, the number of organisms growing on a hexadecane medium were counted. Primary productivity of phytoplankton was determined with the standard Steeman Nielsen (13) carbon-14 technique. Results were expressed on a relative scale based on the percent of available 14C that was taken up per volume of water. A similar method was used for periphyton (attached algae), which was composed mostly of filamentous forms. These were first suspended by mixing in a blender at low speed (damage to cells was negligible). Here the results were expressed in relative units based on the percent of available 14Ctaken up per unit of algal dry weight biomass. Primary productivity was determined monthly from June to October for phytoplankton and from June to August for periphyton. Plants of Fucus vesiculosus were marked with a colored plastic band, and individual apical fronds were labeled with small number plates normally used for tagging small fish. At 30-day intervals, apical fronds were photographed on graph paper with a close-up lens and SLR camera. Growth was determined by measuring lengths of the same fronds over time. A useful measure of net productivity in the pools was achieved by comparing the continuously monitored pH of the outgoing water in each treatment relative to the controls. Percent deviation from the control pools was calculated with the hydrogen ion concentration derived from the inverse antilog of pH. A further discussion regarding the relation between pH and net productivity is given below (see Discussion). The zooplankton community was sampled by driving a 15 cm diameter Plexiglass tube through the water column. The tube was closed and the water filtered through a plankton net (mesh size 60 pm). The samples were preserved in formaldehyde-hexamine solution. Counting and species determination were carried out with an inverted microscope (Leitz, lOOX). Three samples were taken in each pool 2,11,19, and 28 days after the exposure started, and sampling was carried out between 1:00 and 2:OO p.m. each time. The organisms in the samples from the different pools were divided into major groups and dominating genera. The number of individuals with obvious oil contamination was also counted. The results from the different pools were compared by use of a normal approximation of a rank-sum test from Lehmann (14). The growth of blue mussels (M. edulis) in terms of total shell length was also measured. Mussels with a length of 15-20 mm were collected in the field before the experiment started. A group of 50-60 mussels was sized (nearest 0.1 mm) and enclosed in a net cage in each pool 1week before the exposure started. New measurements of all mussels in the cages were carried out 28,58,101, and 158 days after the exposure to oil. Furthermore, bioenergetic measurements (0:N ratio) were made for M . edulis and the amphipod Gammarus salinus. Ammonia excretion and respiration rates were measured on G. sdinus, and byssal thread production and spawning behavior were observed in M . edulis. These studies were further reported in Carr and Linden (25).

Results Oil in the Water Column. Maximum concentrations were found immediately after the start of the exposure (1 Envlron. Scl. Technol., Vol. 21, No. 4, 1987

375

CONC. IN UNITS OF AREA RELATiVE PRISTANE Oi5 1;o

Table 11. Hydrocarbons (mg*L-')in Water Samples from the Different Pools Determined by IR"

time, h

oil + dispersant

011

3.88 f 1.09 2.58 f 0.14 1.84 f 0.18 1.13 & 0.27 0.33 f 0.10 0.10 f 0.05 0.11 f 0.01

12-06 14-06

-39-

0

1 6 12 24 63 93 186

11-06

0 MYTILUS 11-06

oil 0.83 f 0.44 0.53 f 0.15 0.64 f 0.35 0.70 f 0.04 0.10 f 0.09 0.03 f 0.00 0.10 f 0.08

"Samples were collected 1-186 h after the start of the experiment. The table shows the mean value (and range) of three to five replicate samples.

d

-9,-

5

0 MYTILUS 18-06 b

-

22- 06

(I-

"-83-29-06 S

-73

-08-07

h

0

b 4

=li

* O M

b

o

CONC. IN UNITS OF AREA RELATIVE PRISTANE Oi5

1.0

11-06 * MYTILUS 12-06 14-06 0

-3,-

0

E=-

-VI-

Flgure 2. Concentrations over time in units of area of n-alkanes and in oil and blue mussel (M. eduls) tissue phytane relative to pristane (0) from a pool exposed to oil plus dispersant.

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