meiofauna dispersal near natural petroleum seeps in the santa barbara channel: a recolonization...

Oil & Chemical Pollution 4 (1988) 179-189

Meiofauna Dispersal Near Natural Petroleum Seeps in the Santa Barbara Channel: A Recolonization

Experiment

Margaret A. Palmer* Department of Biology, Wabash College, Crawfordsville, Indiana 47933, USA

Paul A. Montagna Marine Science Institute, University of Texas at Austin, Port Aransas, Texas 78373,

USA

Robert B. Spies Environmental Science Division, Lawrence Livermore National Laboratory, L-453,

PO Box 5507, Livermore, California, 94550, USA

&

Dane Hardin

Kinnetic Laboratories, Inc., PO Box 1040, 3050 Paul Sweet Road, Santa Cruz, California 95061, USA

(Accepted 11 August 1987)

ABSTRACT

Studies on the response of fauna to natural disturbances indicate that disturbance events may be important in structuring marine benthic communities. Benthic populations in the Santa Barbara Channel off Isla PTsta, California are regularly subjected to natural disturbances by chronic petroleum seepage in the area. It has been suggested that these populations show enhanced dispersal abilities when compared to populations that are not

*Present address: Department of Zoology, University of Maryland, College Park, MD 20742, USA.

179

Oil & ChemicaI Pollution 0269-8579/88/$03.50 © 1988 Elsevier Applied Science Publishers Ltd, England. Printed in Ireland.

180 Margaret A. Palmer, Paul A. Montagna, Robert B. Spies, Dane Hardin

disturbance-adapted. Our study compared the rate of meiofaunal colonization into azoic sediment trays buried at an oil seep site with a nearby comparison site free of fresh oil. At the comparison site, for all taxa examined, meiofaunal abundances in the colonization trays did not reach ambient (surrounding sediments) levels at any time during the 23-h experiment. At the seep site, meiofaunal abundances in the trays reached ambient levels in 6 to 23 h, depending on taxa. Thus, the rate of meiofaunal colonization was faster at the seep site than at the comparison site. Enhanced susceptibility to passive transport or active water column entry by some species was most likely responsible for the enhanced colonization rate at the seep site.

1 I N T R O D U C T I O N

Studies of the effect of oil on benthic meiofauna communities seem to fall into three categories: those which show a dramatic decline in abundance and diversity after oil exposure (Grassle et al., 1981; McLachlan & Harry, 1982) and those which show no change (Boucher, 1980) or even enhanced abundances (Fleeger & Chandler, 1983). Certainly, differences in the concentration and toxicity of the oil may explain some of these differences. These studies have focussed on the effects of acute petroleum exposure with no attempt to focus on sublethal effects or effects due to long-term exposure. Natural oil seeps in the Santa Barbara Channel provide an ideal setting for the study of chronic oil exposure (Spies et al., 1980). Seeps near Coal Oil Point release 50 to 70 barrels a day in the form of small droplets 3 to 4 m m in diameter (Spies & Davis, 1979). Benthos density and diversity near Coal Oil Point are comparable to nearby areas without seepage (Davis & Spies, 1980; Montagna et al., 1986). Such findings suggest that some fauna are successful in these seep areas.

We view offshore petroleum seeps as natural disturbances because oil seepage at Coal Oil Point has occurred for many years yet the precise locations of oil release within the seep site change frequently and unpredictably. At any one time, active seepage occurs in numerous small areas (0-25-2.0 m 2) where oil droplets and gas bubbles percolate up through the sediments (Spies et al., 1980). Between these areas are larger regions of less active or no seepage. Meiofauna are not likely to survive in the areas where oil actually accumulates on the sediment surface but may survive by moving to nearby patches where the oil is absent or has been dispersed. Marine meiofauna are ideal organisms to use in an investigation of faunal responses to oil disturbance. Meiofauna are intimately associated with the sediments and they are small with rapid development and short generation times. Individuals produce multiple

Meiofauna dispersal near natural petroleum seeps 181

clutches during their life and brooding is the general rule. The most dramatic difference from their macrobenthic counterparts is the absence of pelagic larvae in meiofauna. Previously, this was thought to limit dispersal (Sterrer, 1973) and thus inhibit recovery from large-scale disturbances. We now know that both adult and juvenile meiofauna are dispersed in the water column by both active and passive processes (Palmer & Gust, 1985; Palmer, 1986; Walters & Bell, 1986) and that recolonization into disturbed areas is rapid, usually within hours (Sherman & Coull, 1980; Hockin & Ollason, 1981; Reidenauer & Thistle, 1981; Chandler & Fleeger, 1983).

Alongi et al., (1983) conducted a series of manipulative experiments to examine the rate of meiofaunal recolonization into oiled and untreated azoic sands at a single subtidal site in the lower York River, Virginia. They found colonization began immediately and was complete within 16 days; however, the recruited populations fluctuated more than natural populations. No such study has been conducted on populations which are regularly exposed to natural petroleum-induced disturbances. Such populations may show enhanced recolonization abilities when compared to populations that are not disturbance-adapted. The California oil seeps provide ideal sites for testing such an hypothesis because seepage has occurred in the area for tens of thousands of years (Spies, 1983)

The purpose of the present study was to conduct in-situ experiments to compare the rate ofmeiofaunal colonization in an area near an active oil seep with a nearby comparison area free of oil seepage. If seepage disturbances are important in structuring these communities, then differences in dispersal abilities may occur between the two areas.

2 MATERIALS AND METHODS

The experimental sites were located 300 m offshore of Isla Vista, California, USA on fine-sand bottoms at approximately 19 m depth. The comparison site had a median grain size of 163/~m and was located 1-4 km to the east of the Isla Vista Seep (see Spies et al., 1980 for a complete description of the two areas and composition of seep oil). The seep site had a median grain size of 156/.tm. Throughout the study, a long- shore current of 0.5-1-0 knots (0-925-1.85 km/h) flowed westward from the comparison site toward the seep site. Sand was collected from each site two weeks prior to the experiments and made azoic by repeated freezing and thawing. Four, open-topped recolonization trays (24 cm × 33 cm, 15 cm deep) per site were filled with azoic sediment from that site and soaked with fresh seawater. The sides of each tray had sections cut out


(approximately 2/3 of each side) which were covered with 2 mm-mesh. Prior to filling with sand, these mesh-covered sides were l ined with plastic wrap so that the trays could be deployed without losing sand. The trays were covered and carried to the bottom by divers.

The divers excavated an area the size of each tray and the trays were placed into the sand so that their surfaces were flush with the natural bottom. At each site, trays were deployed on 30 July 1985 so that they were oriented in an East-West direction, and their positions were offset from one another to minimize the possibility of downstream tray contami- nation when divers sampled (Fig. 1). After deployment, the trays were left with top covers and side linings in place for 24 h to allow sediments, which were suspended by the deployment process, to resettle. On 31 July at 10.00 h, the divers removed the plastic linings and uncovered the tops of each of the trays. Sand within each tray had settled and so additional azoic sand was added to the top of each tray (1-2 cm) to bring the tray sand up flush with the surrounding sediment. After all trays were uncovered and leveled, Time 0 samples were collected. During every sampling, the divers were careful to minimize disturbing the bottom and always sampled downstream areas first. At each site and at each sampling time, divers collected one, 2.6-cm dia-sediment core to a depth of 4 cm from within each tray (tray samples) and one core from the area just outside of each tray (outside samples) (Fig. 1). All cores collected inside the trays were taken from the centermost area of each tray to minimize effects due to distance from the edge of the tray. The exact

FLOW

~ olonization tray i _ ~ ~ r a y samples

I ~:'1 := outside samples

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Fig. 1. A schematic illustration of the arrangement of colonization trays and the locations in which cores were taken inside trays and outside of trays.


coring position within each tray was selected prior to each sampling and this position was not resampled during the study. Sample core holes were refilled with azoic sediment from the site.

Samples were collected at 0, 2.5, 6 and 23 h after trays were uncovered. Sediment samples were preserved in Rose Bengal-Formalin and stored for later analysis. Meiofauna were extracted by the decantation technique and counted to major taxa. During three of the sampling times, two cores were collected from trays a n d two from outside areas for determination of biological grain size (after Buchanin & Kain, 1971). During two of the sampling times, two replicate water samples were collected 1 m off the bottom, at each site, for measurement of total suspended solids (after McCave, 1979).

Data were analyzed using SAS software (SAS Institute, Inc., 1985). The number of meiofauna in a core could vary as a function of site (seep, comparison), treatment (tray, outside), time (0, 2.5, 6, 23 h), and area (8 specific sampling areas: trays 1-4 and outside 1-4). Since area is unique within a given site and treatment, area is a nested variable. Thus, the meiofauna data were analyzed using a partially hierarchial design (Kirk, 1982; p. 270) with area nested within site by treatment. The statistical model is

Yijklm = ~j -[- ~k -[- ~/1 "[- O'm(jk) nt" G~/~jk "t- a~ j 1 -[- ]~]/kl "[- aj~Yjkl -[" Ei(jklm)

where the variation of each measurement of meiofaunal abundance, Yijklm, is a function of site a j, treatment ilk, time ?'l, area amOk) (a nested effect), and interaction terms. The statistical effects of primary interest for this study were the interaction terms: time × treatment (flYkl) and site × treatment (afljk). Significant effects for these interactions would indicate that, first, the difference in meiofaunal abundances in a tray vs outside depended on time (i.e., colonization occurred) and, second, that the difference in meiofaunal abundance in a tray vs outside differed between the comparison and seep sites (i.e., a difference in colonization rates between the two sites).

3 RESULTS

At the comparison site, for all taxa examined, meiofaunal abundances in the trays did not reach control levels (outside areas) at any time during the experiment, whereas at the seep site meiofaunal abundance in the trays reached levels similar to outside areas by the end of the experiment (Fig. 2). Foraminiferans, copepods and nauplii recolonized azoic trays in the seep site more quickly than did nematodes (Fig. 3).

From the statistical analysis, the time × treatment interaction was


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significant for copepods (P = 0.07), nematodes (P = 0.04), foraminiferans (P -- 0.04) and total me iofauna (P = 0.05). This indicates that the difference in the n u m b e r of meiofauna in trays and outside of trays at bo th sites depended on time. In general, this difference decreased over t ime (Figs 2, 3) as meiofauna colonized the trays.

Coloniza t ion rates were found to be greater at the seep site. For all four major taxa and total meiofauna, the site × t reatment interact ion was statistically significant at the 0.001 level. This indicates that the difference in the n u m b e r of meiofauna in trays and outside of trays varied between the seep and compar i son sites. Averaged over all times, this difference was greater at the compar i son site. In other words, regardless of time, the n u m b e r of meiofauna colonizing trays was greater at the seep site.

The concentra t ion of suspended sediments in the water was highly variable (17.1-126.9 mg/1 at the compar i son site; 17.9-69.3 mg/1 at the seep site) and there was no statistically significant difference between the two sites or over t ime (ANOVA, P > 0.10). The med ian grain size measured at the seep vs compar i son sites (outside areas) were not


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significantly different (seep = 156pm, comparison = 163pm), yet both had a significantly smaller median grain than found inside of trays (seep = 179 pm, comparison = 186 pro) at each site (ANOVA, P < 0.10).

4 DISCUSSION

Studies on the response of meiofauna to both natural and artificial disturbances have shown that meiofauna are able to rapidly recolonize disturbed areas (e.g., Sherman & Coull, 1980; Reidenauer & Thistle, 1981). Apparently, meiofauna are often highly tolerant to disturbances, even exposure to hydrocarbons (Fleeger & Chandler, 1983). Meiofauna may survive oil spills and, for some species of meiofauna, colonization of oiled sediments may occur at rates comparable to the colonization of untreated azoic and natural sediments (Mongi et al., 1983; Decker & Fleeger, 1984). To date, ours is the only study of the recolonization of azoic sediment by meiofauna which compares populations naturally exposed to fresh oil with populations in areas without fresh oil. We found that the meiofauna of naturally oiled sites did colonize azoic sediment rapidly. The seep foraminiferans, adult copepods and copepod nauplii colonized azoic trays in less than 6 h; the colonization rate of the seep nematodes was slower. In contrast to the seep site, colonization at the comparison site was not complete by 23 h for any of the taxa examined.

The experimental trays used in this study allowed for active colonization via infaunal immigration through the sediments or water and for passive colonization via water column transport. Our experiments were not designed to allow us to distinguish between these modes of dispersal. Chandler & Fleeger (1983) have previously shown that copepods and nauplii colonize azoic areas primarily via the water column and that complete colonization via lateral sediment migration over these distances would require more than 48 h. In the present study, we also attribute meiofaunal colonization to passive transport processes. It is unlikely that any of the animals were able to migrate laterally the distances required to explain colonization in 2. 5 h. For example, recent unpublished work using time-lapse cinemaphotography (K. Wetmore, Smithsonian Institution), has shown that benthic foraminiferans can migrate through sediments at rates of approximately 4 mm/h. Given this rate, foraminiferans could only have reached the sampling areas in our experimental trays (a minimum travel distance from the surrounding sediments of approximately 150 mm) by water column transport. Foraminiferans, like other meiofauna, are known to be transported in


large numbers in the water (Palmer & Gust, 1985; Palmer, 1986). Colonization was faster at the seep site, yet no differences were found

in the concentration of suspended sediments at the two sites and suspended sediments are known to be correlated with passive transport of meiofauna (Palmer & Gust, 1985). Furthermore, flow levels were not consistently higher at the seep site (T. Goddard, pets. comm.), yet elevated flow levels are associated with increases in suspended meiofauna (Palmer & Gust, 1985). Furthermore, although we have not measured critical erosion velocities of the sediments (u,-c~t), we expect U,-cnt is greater at the seep site (even though median grain size is the same at both sites) due to an oil-associated increase in sediment cohesion. If U,-crit is greater at the seep site, then dispersal of meiofauna via passive transport of sediments should be reduced (Palmer, 1986). We suggest that the faster recolonization rate at the seep site may be the result of the shallower redox potential discontinuity depth at the seep site (1.5 cm) vs the comparison site (6-5 cm). This would limit seep meiofauna to a smaller oxygenated zone near the surface where susceptibility of nonbound particles (meiofauna) to passive transport would be enhanced. We further suggest that differences in meiofaunal behavior between the two sites exist such that vertical migrations up to the sediment surface and active water column entry, with subsequent passive transport, is more common at the seep site than at the comparison site. An examination of species differences between the two sites is needed to evaluate this suggestion.

In conclusion, the colonization rate of the meiofauna was greater at the seep site than at the comparison site. The primary mode of colonization at both sites was most likely passive transport. Enhanced susceptibility to water column transport, along with behavioral differences between species, were likely responsible for the faster colonization rate of the seep fauna.

ACKNOWLEDGEMENTS

This research was supported by the Byron K. Trippet Fund of Wabash College, a grant from the National Science Foundation to M. Palmer (OCE 8509904), and the US Department of Interior, Pacific Outer Continental Shelf Office, under contract 14-12-0001-30159, to Kinnetic Laboratories, Inc. Special thanks goes to Shane Anderson and Jim McCollough of the University of California - Santa Barbara for field assistance.


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Spies, R. B., Davis, P. H., & Stuermer, D. H. (1980). Ecology of a submarine petroleum seep off the California coast. In: R. A. Geyer (Ed.), Mar. Environ. Poll. 1. Hydrocarbons. Elsevier Science Publishers, Amsterdam.

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meiofauna dispersal near natural petroleum seeps in the santa barbara channel: a recolonization...

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