Taxonomic Sufficiency For A Monitoring Program in a Tropical Continental Shelf, Rio De Janeiro, Brazil

This work aims to determine the taxonomic identification level needed to detect petroleum hydrocarbon environmental impact. The investigation was carried out at the Pargo oil production platform, located on the Campos Basin oil field, in January (austral summer) and July (austral winter) of 1998. The sampling design followed a radial pattern of 11 stations arranged at 250, 500, 1000 and 3000 m off the center of the platform. Three replicate samples were taken at each station using a box-corer device. Species abundance was aggregated into progressively higher taxa matrices (genus, family, class), and data were analyzed using univariate (biological indices) and multivariate (cluster analysis and NMDS ordination) methods. The analysis at the species, genus and family levels showed similar results. The observed pattern did not agree with the putative pollution gradient, and stations were clustered according to the cardinal points, rather than to distance from the platform. Diversity, richness, and evenness values were lower at northern stations, compared to southern ones. The analysis at the class level did not show any apparent structure around the platform. The literature about taxonomic sufficiency has demonstrated that faunal patterns at different taxonomic levels tend to become similar due to increased pollution. Several authors have found a good correspondence of results obtained at species, genus and family levels to those found in this work, suggesting that even in species-rich tropical communities it is possible to adopt a higher taxonomic level monitoring program.

Keywords: taxonomic sufficiency; marine pollution monitoring; hydrocarbons; macrobenthos ; community structure; soft bottom; continental shelf.

INTRODUCTION

The materials discharged from oil and gas production platforms can potentially cause environmental impacts. According to Blumer (1970), due to their hydrophobic character the petroleum organic compounds can adsorb to the particulate matter and accumulate in bottom sediments below the aerobic surface layer, where they can remain unchanged and toxic for long periods.

Pollutants that accumulate in sediments can induce chronic contamination in benthic communities (Giere, 1993 and others). Changes in benthic community structure are widely used in environmental monitoring programs, being an important tool in marine pollution assessment (Warwick, 1993). In these programs, the main goal is often to identify patterns in community structure and to relate them to measured environmental variables, including pollutants (Olsgard et al., 1998).

Traditionally, such benthic environmental impact investigations require taxonomic species-level determination. However, species identification is an expensive and time-consuming task that could constrain benthic surveys. To reduce such costs, several authors have suggested the possible use of a higher level of taxonomic resolution (e.g. Warwick, 1988; Ferraro & Cole, 1990; Drake et al., 1999).

In Maurer 's (2000) point of view, taxonomic resolution sufficiency is a cost-benefit exercise, and money accrued from reduced taxonomic services could be allocated to other elements of a monitoring program. According to him, another argument for taxonomic sufficiency studies is that there is not enough expertise in monitoring program technical staffs that can confidently and correctly identify a broad spectrum of invertebrate taxa. Furthermore, Warwick (1988) showed that identification based on higher taxa might more closely reflect a contamination gradient than analyses based on the species level. Ferraro & Cole (1990) went further and stated that "grouping animals into higher taxa may dampen the natural variability in the proportion of major taxa and other measures of community structure, thus actually improving our ability to assess small pollution impacts".

Taxonomic sufficiency studies search to identify supra-specific taxa (genus, family, order, class, or phylum) which, without loss of statistical vigor, could be used in assessing pollution impacts. Such kind of studies are lacking in rich tropical benthic communities.

The aim of this study was to investigate the taxonomic resolution sufficiency of a benthic community around an offshore hydrocarbon-production platform, located on a tropical continental shelf. This work is part of the Pre-Monitoring Program carried out by the Brazilian Federal Oil Company (PETROBRAS) at Campos Basin in association with the Marine Biology Graduate Program of Universidade Federal Fluminense.

MATERIAL AND METHODS
STUDY AREA

Campos Basin is the largest offshore oil field in Brazil and is responsible for about 83% of the total national oil reserve. The first drilling in the basin was carried out in 1971 and it has been explored since 1974. This basin is situated on the continental shelf and slope off Rio de Janeiro State, between 21o 30' and 23o 30' S. The total oil production from the installed platforms is 1,000,000 thousands barrels.d-1, which represents approximately 80% of the total national production.

The Pargo Platform is situated approximately 60 km away from the coast, at about 100 m water depth. It has been operating since 1989, discharging very large volumes of produced waters.

The oceanographic conditions of Campos Basin are complex, governed by oligotrophic areas associated with tropical waters of the Brazil Current, and mesotrophic areas due to seasonal upwelling of cold, nutrient-rich waters - South Atlantic Central Waters - near Cabo Frio (Emilsson, 1961; Silva, 1971; Valentin et al. 1987). Primary productivity varies between 0.3 to 1.1 gC.m-2 .d-1 (Gaeta et al. 1999). Freshwater input of the main rivers (Doce and Paraíba do Sul) is only in the order of 900 m3.s-1. Broad areas of the shelf are characterised by low organic matter deposition (Jennerjahn & Ittekkot, 1996), with higher concentrations of sediment organic carbon and nitrogen occurring over the slope (Soares-Gomes et al. 1999). A comprehensive study on the morphology and sedimentation of the region is presented by Viana et al. (1998).

According to Soares-Gomes et al. (1999), the mean abundance of the macrobenthos in the area follows an inshore-offshore gradient; the abundance on the continental shelf is an order of magnitude higher than on the slope. Information about meiobenthos was provided by Soares-Gomes et al. (2000) for sediments around Pargo Platform.

SAMPLING DESIGN AND ANALYTICAL TECHNIQUES

Macrobenthos and sediment sampling was conducted in January (summer) and July (winter) 1998, from the RV. Astro Garoupa, following a sampling design with a radial pattern of 11 stations arranged at 250, 500, 1000, and 3000 meters around the center of Pargo Platform.

Sediment grain size was determined by standard dry-sieved and pipette method (Suguio,1973). Mean grain size and other granulometric statistics were calculated using Folk and Ward’s (1957) formula, and sediments were classified according to the Wentworth scale (1922).

The total polyaromatic hydrocarbons (PAHs) content in the sediment samples was determined only on the surface layer (0-2 cm), following UNESCO (1990).

Organic carbon and total nitrogen were determined in a Carlo Erba CHN analizer (model EA1110), after removal of inorganic carbon.

Surface-sediment heavy metal concentrations around Pargo platform were described by Ovalle et al. (2000).

In each station 3 replicate samples were taken with a 30x30x30-cm box-corer, totalling 33 samples. The biological samples were sieved using 0.5, 1 and 2 mm mesh sieves and preserved in 5% formalin. The macrobenthos were sorted in the laboratory under a stereomicroscope for identification to the finest possible level.

Species abundance of macrobenthos in each sample was aggregated to the levels of genus, family and class.

The macrobenthos community structure around the platform was established using univariate measures and multivariate analysis. The following univariate indexes were calculated for the different taxonomic levels: abundance of individuals, specific richness (number of taxa), Pielou evenness (j’) and Shannon diversity (h’). These biological indexes were calculated for each station and the results displayed as mean, minimum, and maximum values for each distance and direction (northern and southern) from the platform. The values of diversity and log2 of abundance were displayed in a DIMO (Diversity Model) graphic, proposed by Qinghong (1995). The non-metric multidimensional scaling (NMDS), based on the square root transformed pooled data with the Bray-Curtis similarity index, was performed using the PRIMER software package (Clarke & Warwick, 1994).

RESULTS

Distribution of grain size was uniform in the area. The mean sediment grain size ranged from 3.37 to 3.49 phi, and the sorting coefficient from 0.41 to 1.11 phi in summer samples. In winter samples the mean grain size ranged from 3.19 to 3.49 phi, and the sorting coefficient from 0.24 to 1.48 phi. These sediments could be classified as fine sand, mostly well sorted.

Sediment organic carbon and total nitrogen content ranged from 0.9 to 2.9 mg g-1 and < 0.1 to 0.4 mg g-1, respectively.

The sediment PAHs measured by UVF in equivalents of crysene ranged from 3.5 to 53.4 g.g-1, with the greatest values occurring at the 250 and 500 m stations.

The biological indexes did not show any expressive difference when analyzed in relation to the distance from the platform, at all taxonomic levels. Nevertheless, some pattern in the macrobenthic community emerged in relation to direction away from the center of the platform (northern and southern). These results were found in both summer and winter surveys.

The Qinghong graphic model showed a geographic gradient of spatial distribution of macrobenthic communities, with the southern station showing higher values of diversity. These results were the same for all taxonomic levels, apart from class level, both in summer and winter surveys. The results of NMDS were similar to the Dimo graphic model. The community proved to be structured at species, genus and family levels, but not at the class level. Also, the same results were found in the summer and in the winter surveys.

DISCUSSION

The range of PAH concentration in sediments around Pargo Platform was from 3.5 to 53.4 g g-1. These sediment concentrations are below the concentrations that could cause biological effects on marine fauna. According to limits cited by Patin (1999), the lowest levels of oil hydrocarbons that cause primary physiological and biochemical response or no effect at all range from 10-3 to 10-2 mg L-1 for seawater, and from 10 to 100 mg kg-1 for bottom sediments.

Besides hydrocarbons, heavy metals are another class of contaminant commonly related to petroleum production platforms (Kennicutt et al., 1996). The concentration of Al, Fe, Ba, Cu, Cr, Zn, Ni, V, Pb, and Cd of surface sediment samples (0-2 cm) around Pargo Platform were determined by Ovalle et al. (2000). According to the Enrichment Factor used by these authors, Cu and Ni increased twice between 250 and 1000 m, and Zn three times in samples 250 m away from the platform. The other metals did not show an enrichment near the platform. In spite of these results, the element concentrations were in the same order of magnitude as other coastal areas in a regional scale, except for Ba (range of variation 70.4-269 g.g-1). In general, the spatial distribution of pollutants was erratic, and did not fit the macrobenthos distribution. These results are similar to the ones obtained on the Gulf of Mexico by Kennicutt et al. (1996), who concluded that contaminant concentrations were below the levels that induce biological responses.

It should be kept in mind, however, that toxicological studies do not give the last say in environmental impact studies. Patin (1999) advanced the possibility of long-term effects caused by low levels of chemical pollution. According to him, "in spite of the difficulties of revealing such responses, more and more studies prove the existence of nonobvious (subtle) long-term consequences of chronic contamination". One such consequence is an increased frequency of mutagenic and carcinogenic effects and diseases among benthic organisms. Thus, long-term and further studies (e.g. genetic diversity) on Campos Basin are necessary to appropriately determine to what degree the local marine fauna is under impact of offshore oil production.

Many studies have demonstrated that, in macrobenthic communities, the effects of pollution are usually detected with multivariate techniques at higher taxonomic levels, even in situations where the effects are so subtle that they cannot be detected by univariate techniques at lower taxonomic levels (species level) (James et. al., 1995). In the present work the results showed that univariate techniques were sensitive enough to detect, even at a higher taxonomic level, a faunal distribution pattern similar to the results of the multivariate analyses.

Usual practice in a monitoring study involves identification of all faunas down to species when practicable (Warwick, 1988). A pilot study could, however, determine the level of taxonomic resolution and sampling design needed. For example, according to Kingston and Riddle (1989), the clear trends in reduced diversity, associated with the discharge of oil-based drilling cuttings around an oil production platform, can be demonstrated almost as precisely using identification down only to the genus or family level. Recent work has focused attention on this area as a major cost-saving alternative. However, extreme caution should be exercised in the adoption of such an approach, as the loss of information could be critical if subtle effects are overlooked.

Ferraro & Cole (1995) found that faunal identification at genus, family, order and phylum levels reduced the cost, respectively, by 25%, 55%, 80% and 95% as compared to the total spent in analyses at the species level. Their study showed that patterns can be consistently identified using different levels of taxonomic resolution. They suggested that, when resources are limited, for consistent patterns to be measured it is more important to collect enough replicates at a range of spatial and/or temporal scales, so that the assemblages are well represented, than to sort the taxa down to a fine taxonomic resolution.

The results of this work evidenced a spatial distribution pattern of benthic communities at the family level for both univariate and multivariate analyses. The analysis of the communities at family level produced similar results to those found at genus and species levels, without loss of important information. The macrobenthos spatial distribution around the platform did not agree with the putative distance gradient; instead, the spatial distribution showed a geographical pattern: the stations placed to the South of Pargo Platform showed higher values of diversity compared to northern ones, suggesting that pollutants could be negatively influencing the macrobenthos, even in lower concentrations.

CONCLUSIONS

The analyses performed at species level showed a geographic gradient of spatial distribution of macrobenthic communities, with the southern station showing higher values of diversity . The same pattern was detected when the data were analysed at genus and family levels. Thus, the analysis of these macrobenthic communities at the family level proved to be satisfactory, without loss of important information, and could therefore be adopted in monitoring programs.

LITERATURE CITED

Blumer, M. (1970) Oil contamination and the living resources of the sea. FAO Tech. Conf. Rome, FIR: MP/70/R-1, 11 p.

Clarke, K.R., Warwick, R.M., 1994. Change in marine communities: an approach to statistical analysis and interpretation. Plymouth Marine Laboratory, Natural Environment Research Council, UK, 144 p.

Drake, P., Baldó, F., Sáenz, V. & Arias, A.M., 1999. Macrobenthic community structure in estuarine pollution assessment on the Gulf of Cádiz (SW Spain): is the phylum-level meta-analysis approach applicable? Mar. Poll. Bull. 38(11):1038-1047.

Emilson, I., 1961. The shelf and coastal waters off Southern Brazil. Bolm. Inst. Oceanogr., S. Paulo, 11(2): 101-112.

Ferraro, S.P. Cole, F.A., 1990. Taxonomic level and samples size sufficient for assessing pollution impacts on the Southern California Bight macrobenthos. Mar. Ecol. Prog. Ser., 67: 251-262.

Ferraro, S.P. Cole, F.A., 1995. Taxonomic level sufficient for assessing pollution impacts on the Southern California bight macrobenthos - Revisited. Environ. Toxicol. and Chem., 14: (6) 1031-1040.

Folk, R.L.; Ward, W.C., 1957. Brazos river bar: a study of the significance of grain size parameters. J. sedim. Petrology, 27: 3-26.

Gaeta, S.A.; Lorenzzetti, J.A.; Miranda, L.B.; Susini-Ribeiro, S.M.M.; Pompeu, M. and Araújo, C.E.S, 1999. The Vitória Eddy and its relation to the phytoplankton biomass and primary productivity during the austral fall of 1995. Arch. Fish. Mar. Res., 47(2/3): 253-270.

Giere, O., 1993. Meiobenthology. The microscopic fauna in aquatic sediments. Springer-Verlag, Berlin, 328 p.

James, R.J., M.P.L. Smith, & P.G. and Farweather, P.G. 1995. Sieve mesh-size and taxonomic resolution needed to describe natural spacial variation on marine macrofauna. Mar. Ecol. Prog. Ser., 118: 187-198.

Jennerjahn, T.C., Ittekkot, V., 1996. Organic matter in sediments in the mangrove areas and adjacent continental margins of Brazil. I. Amino acids and hexosamines. Oceanol. Acta, 20(2): 359-369.

Kennicutt II, M.C.; Boothe, P.N.; Wade, T.L.; Sweet, S.T.; Rezak, R.; Kelly, F.J.; Brooks, J.M.; Presley, B.J. & Wiesenburg, D.A., 1996. Geochemical patterns in sediments near offshore production platforms. Can. J. Fish. Aqutat. Sci., 53: 2554-2566.

Kingston, P. F., Riddle, M. J., 1989. Cost effectiveness of benthic faunal monitoring. Mar. Poll. Bull., 20(10): 490-496.

Maurer, D., 2000. The dark side of Taxonomic Sufficiency (TS). Mar. Poll. Bull. 40 (2): 98-101.

Olsgard, F., P.J. Somerfield & M.R. Carr, 1998. Relationships between taxonomic resolutions, macrobenthic community patterns and disturbance. Mar. Ecol. Prog. Ser. 172: 25-36.

Ovalle, A.R.C.; Carvalho, C.E.V.; Carneiro, M.E.; Lacerda, L.D. and Rezende, C.E., 2000. Distribution of trace, minor and major elements in sediments around the petroleum production platforms, Campos Basin - Rio de Janeiro, Brazil. Proceedings of the International Conference on Heavy Metals in the Environment, Michigan, 6 pp.

Patin, S., 1999. Environmental impact of the offshore oil and gas industry. Ecomonitor Publishing, New York, 425 p.

Qinghong, L., 1995. A model for species diversity monitoring at community level and its applications. Environ. Moni. Assesment 34: 271-287.

Silva, P.C.M., 1971. Upwelling and its biological effects in the Southern Brazil. In: Costlow, J.D. (ed.). The fertility of the sea. New York, Gordon and breach, p. 285-308.

Soares-Gomes, A.; Abreu, C.M.R.C.; Absher, T.M. and Figueiredo, A.G., 1999. Abiotic features and the abundance of macrozoobenthos of continental margin sediments of East Brazil. Arch. Fish. Mar. Res., 47 (2/3): 321-334.

Soares-Gomes, A.; Oliveira, E.B.; Gabardo, I.T.; Carreira, R.S. & Fernandez, G.B. [2000]. Environmental impact associated with offshore hydrocarbon production on benthic meiofauna in Campos Basin, Southeast Brazilian continental shelf. Proceedings of the 5th Congress on Marine Sciences, La Habana, Cuba. CD-ROM Edition, 25 pp.

Suguio, K., 1973. Introdução à Sedimentologia. Edgard Blücher/EDUSP, São Paulo.

UNESCO (1990) The determination of petroleum hydrocarbons in sediments. Intergovernmental Oceanographic Commission. Manual and Guides, 96 p.

Valentin, J.L.; Andre, D.L. and Jacob, S.A., 1987. Hydrobiology in the Cabo Frio (Brazil) upwelling: two-dimensional structure and variability during a wind cycle. Continent. Shelf Res., 7(1): 77-88.

Viana, A.R.; Faugères, J.C.; Kowsmann, R.O; Lima; Caddah, L.F.G. and Rizzo, J.G. 1998. Hydrology, morphology and sedimentology of the Campos continental margin, offshore Brazil. Sedim. Geol., 115: 133-157.

Warwick, R.M., 1988. The level of taxonomic discrimination required to detect pollution effects on marine benthic communities. Mar. Pollut. Bull., 19: 259-268.

Warwick, R.M., 1993. Environmental impact studies on marine communities: Pragmatical considerations. Aust. J. Ecol., 18: 63-80.

Wentworth, C.K., 1922. A scale of grade and class for clastic sediments. J. Geol., 30: 377-392.

ACKOWLEDGEMENTS

The authors are indebted to PETROBRAS for taking the initiative for this work and supporting it financially, technically, and logistically. Special thanks to Dr. Paulo Secchin Young for taxonomic identification of peracaridan crustaceans. The second author also wishes to thank "Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro" (FAPERJ) for its financial support (E-26/171.431/97).
 

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