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Effects of hypoxia on macrobenthos of the inner shelf off Cameron, Louisiana
Estuarine,
Coastal
and Shelf
Science
(1985) 20,603-613
Effects of Hypoxia on Macrobenthos Inner Shelf off Cameron, Louisiana
Gary
R. Gaston
Department University, Received
of the
of Biological Lake Charles, 5 March
and Environmental Louisiana 70609,
1984 and in revisedform
Keywords: hypoxia; macrobenthos; Annelida; Louisiana
Sciences, U.S.A. 33uly
McNeese
State
1984
population composition;
Polychaeta;
The effects of hypoxic bottom water, an annual event, were documented on the inner shelf off Cameron, Louisiana during the summer of 1981. Populations of most species of macrobenthos were dramatically reduced. In an area of fine sediment that was numerically dominated by polychaetous annelids, the most severely affected populations were those of tube-dwelling and surface-feeding species. Burrowing species were less influenced by the hypoxia.
Introduction Interest in the effects of hypoxic bottom waters ( < 2 mg I- ‘) on benthic macrofauna of the northwestern Gulf of Mexico (e.g. Fotheringham & Weissberg, 1979; Harper et al., 1981; Pavela et al., 1983; Boesch, 1983) has led to observations that hypoxia occurs during summer months on the inner continental shelf from the Mississippi River to Texas, in response to discharge from the Mississippi and Atchafalaya rivers. Mass mortalities may occur among macrobenthic communities, and nektonic species may leave the area (Ragan et al., 1978; Bedinger, 1979; Harper et al., 1981), with drastic implications on commercial fisheries, especially those including shrimp, crabs, and demersal fish. The purpose of this paper is to document the effects of hypoxia on inner shelf macrobenthic communities off Cameron, Louisiana, which is among the leading ports in the nation for commercial landings of finfish and shellfish. Data for this investigation were collected from February 1981 to April 1982. Background As early as 1935, low bottom dissolved oxygen values (3.9 mg 1-i) were recorded along the Texas and Louisiana coasts (Richards, 1957). In recent years investigations of the environmental impacts of petroleum production noted oxygen-depleted bottom waters in and around Timbalier Bay (e.g. Farrell, 1979; Fotheringham & Weissberg, 1979; Bedinger, 1979; Bedinger et al., 1981), as did investigations on the inner continental shelf from the Mississippi delta to Atchafalaya Bay (Ragan et al., 1978; Stuntz et al., 603 0272-7714/85/050603
+ 11 $03.00/O
0 1985Academic Press
Inc. (London)
Limited
G. R. Gaston
604
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1. Chart
of the study
area off Cameron,
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93;251
93T30’ Figure
,
J&3------------mio-
___-------
__--
____----
I’
Louisiana,
indicating
1982) and as far west as the Brazos River, Texas (Harper & McKinney,
collection
sites.
1980; Harper et
al., 1981; Pavela et al., 1983).
Several probable causesof hypoxia have been postulated. Most studies attribute hypoxia to the freshwater runoff from the Mississippi and Atchafalaya rivers, which leads to density stratification of the water column, and elimination of oxygen exchange between the surface and bottom (e.g. Fotheringham & Weissberg, 1979; Bedinger et al., 1981). Additionally, decomposition of the water-borne organic debris increases the biological oxygen demand (BOD) of the sedimentsand decreasesthe dissolved oxygen of the near-bottom water (Oetking et al., 1979; Price, 1979; Bedinger et al., 1981; Officer et al., 1984). Farrell (1979) reported high quantities of sediment phaeopigments in hypoxic areas, suggestingthat oxygen depletion off central Louisiana may be linked with production and decomposition of phytoplankton. An associationof hypoxia and primary production would imply that an overabundance of phytoplankton occurs seasonallyoff Louisiana. This is supported by evidence of a dramatic increasein nitrate content of the Mississippi River in recent years (Walsh et al., 1981), a phenomenon which could enhanceoffshore primary production on the Louisiana continental shelf (Boesch, 1983). Materials
and methods
The present study was conducted from February 1981 to April 1982. Seven stations were sampled monthly and an additional four (M6, M15, DN, DS) were included in quarterly sampling (Figure 1) as part of a brine discharge monitoring study (Gaston & Weston, 1983). Sampling sites were located primarily on an east-west transect along the 10-m depth contour near a Department of Energy Strategic Petroleum Reserve Program brine diffuser. The area is approximately 15 km southeast of Cameron, Louisiana.
Effects of hypoxia on macrobenthos
605
All stations were located by LORAN C. At each site observations were made of time, sea state, and weather conditions. A vertical profile of conductivity, temperature, dissolved oxygen and pH was made with a Hydrolab Series 8000 meter at 3 m depth intervals. Six replicate grab sampleswere taken at all stations using a 0.1 m2 stainless steel Smith-McIntyre grab. The contents of each grab were washed through a O-5mm screen. The material retained on the sieve was preserved in 109b buffered formalin containing RoseBengal, to be sorted to macrofaunal specieslater in the laboratory. Dominant specieswere selected by cumulative ranking of numerical dominants. The ten most abundant speciescollected at the seven monthly siteswere ranked according to abundance. The most abundant speciescollected each month received a score of 10 and less abundant species were given successively lower scores. The ranking was then determined by summing the twelve monthly scores. Several indices of community structure were employed in data analysis of the benthic collections. Diversity was measuredusing Shannon’s formula (Pielou, 1966). This index is dependent on both number of speciesin the sampleas well astheir relative dominance. To examine these two parameters independently, speciesrichness (S) and evennesscr> were computed separately using the formulae: S-l S=---
1nN ’
J= H’ 10&S’
where N equals the total number of individuals. These indices, when calculated for a station, are based on the number of speciesand their mean abundances in all replicate grabs taken. In order to present the large data set in an interpretable form, as well as to determine zones of rapid fauna1 change, multivariate analysis techniques were employed. Species which occurred in only a single replicate sample were eliminated. Clustering was performed using the Virginia Institute of Marine Science program COMPAH (Combinatorial Polythetic Agglomerative Hierarchical) program. Log transformation (log X+ 1) and the Bray-Curtis similarity measure (Bray & Curtis, 1957) were employed in the clustering. Results Sediments of the study area were generally silty clays with approximately lo?,, sand, 35O, silt and 55?,0clay. There was a general homogeneity in sediment type, and consequent similarity in fauna1 composition which enhanced the suitability of the sites for comparative observations of hypoxic effects (Gaston & Weston, 1983). The dissolved oxygen concentration of bottom waters exhibited wide variation both spatially and temporally. The most notable temporal changes were the periods of low dissolved oxygen during the summer of 1981, when bottom dissolved oxygen concentrations often dropped below 1 mg 1-r (Figure 2). These periods of hypoxia were noted intermittently from mid-June through mid-September and corresponded to a period of pronounced salinity stratification (Gaston & Weston, 1983). During the latter half of July and early August bottom dissolved oxygen concentrations at the brine diffuser (2.5-3.5 mg 1-l) exceeded that of station Ml8 (0.5-2.0 mg l- ‘). This elevation of dissolved oxygen in the vicinity of the diffuser resulted either from aeration of bottom water by mixing with the oxygenated brine effluent or, more probably, from turbulent
606
G. R. Gaston
Station
Ml8
6-
----
Bottom
-
FMAMJJASONDJFMA
D
? 0
Surface
,
P I
Station
MIOA
FMAMJJASONDJFM 1981
1982
Figure2. Temporalvariationsin dissolvedoxygen(mgl-‘) at fwo sites(Ml8 and MlOA, seeFigure1).
mixing of the water column during brine discharge and the consequent breakdown of stratification. During late August and September, oxygen levels at the diffuser site (station MlOA) dropped below those of other sites. This occurrence corresponded to periods during which brine discharge was suspended’(2P31 August; 3-14 September). During periods of brine discharge the brine plume was barely detectable outside a 2 km radius of the diffuser (Randall, 1983). Data on the other physical parameters of the study area were discussedin Gaston & Weston (1983). Although the sampling sites were generally similar in physical characteristics other than dissolved oxygen (Gaston & Weston, 1983), there were notable variations in benthic communities. A number of stations (e.g. MlO, M6) were more speciose,as evidenced in the species-richnessvalues (Figure 3). Sampling sites to the east of the diffuser (e.g. stations M15, M18, M20) were generally lessrich in speciesthan those to the west (e.g. stations M3, M6). Species-evennessvalues, a measure of how evenly the individuals were distributed among the species,at station M3 were consistently lower than other sitesfrom May to August and were higher than all other sites from October to March. Numerical classification (clustering) was used to delimit consistent patterns of station similarity. All 15 months of sampling were incorporated in the analyses,and each month of collection at a site was treated as a separate entity (Figure 4). Because of the high temporal variability of the benthic community, numerical classification groupings were formed primarily on the basis of month rather than station. Three major groupings, established on the basis of season,were evident: (1) February to April 1981, (2) May to October 1981, including the hypoxic period during the summer months; and (3) November 1981 to April 1982. The fact that the February-April period of 1981 is more similar to May-October 1981 than to the February-April period of 1982 indicates the magnitude of temporal fauna1 change in the study area and the absence of a repeated
Effects
of hypoxia
607
on macrobenthos
Hypoxlc period
/ 1-d’
c /
,“V /
d’
12 II c
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I
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Y
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rJh /? >’ i 1i’ /I ‘1/Y/\\’f / /
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1981
FMA I982
Figure 3. Temporal variations in species diversity, species richness and species evenness at three sites (M3, MlOA, M18, see Figure 1). cycle. Certain collections at stations MlOA and M3 separatedin the cluster. This resulted from the distinct fauna which occurred during these collections. Although the use of diversity indices has fallen in disfavor among many ecologists in recent years, Shannon diversity and its components (species richness and species evenness) were useful here to demonstrate temporal variations in the communities (Figure 3). Based on the numerical classification, three sites (stations M3, MIOA, M18)
annual
were
selected
for comparisons
of these measurements.
There
was a radical
values of all three indices during summer hypoxia. Additionally, values for evenness and Shannon diversity variations in diversity among the stations
varied concurrently, were due primarily
change
in
throughout the year
indicating to changes
that temporal in the relative
abundance of the speciesrather than to differences in the number of speciesinhabiting the sites. This resulted from the numerical dominance of a few species at particular sites. The low value for evenness which occurred at station MlOA in June (Figure 3) was
608
G. R. Gaston
Feb
I
1981 -Mar
1981
I -fzz .E r-
May
1981
Jun
1981
1981
Sep
IQEI-
Nov
1981-Jan
Feb
1982
Feb
1982-Apr
Ott
1981
1982
-Apr
1982
1982
-
Figure 4. Numerical classification sorting, beta= -0.25).
of all collections
off Cameron,
Louisiana.
(Flexible
atypical of the pattern seen at any other station, and represented a sudden eruption in population of a single species(Phoronis sp.). The ten highest-ranked speciesare presented in Table 1. During a three-month period sp. (Phoronida) and Sabellides sp. (February-April 1981) two species, Phoronis (Polychaeta) numerically dominated the macrobenthic communities of the study area. Although the high abundance of Sabellides sp. did not continue into the summer months, Phoronis sp. population numbers did continue, totalling 729, of the total macrobenthos in May. This pattern of domination by Phoronis sp. continued through July. Populations
of hypoxia
Effects
on macrobenthos
TABLE 1. Dominant macrobenthic both dominance during a given (February 1981 to April 1982)
Rank
2 4 5 6 8 9 10 11 12 13 14
609
species off Cameron, month and persistance
Species Magelona cf. phyllisae Paraprionospio pinnata Mediomastus californiensis Cirratulus cf. filiformis Phoronis sp. Sigambra tentaculata Owenia fusiformis Pseudeurythoe paucibranchiat Diopatra cuprea Cossura soyeri Glycinde solitaria Nemertea sp. B Mulinia lateralis Spiochaetopterus oculatus
Louisiana. throughout
Score is based on the study period
Score (max = 120) 107 97 58 58 54 51 47 38 35 35 30 29 18 12
of Phoronis sp. decreased in number through August and September. By October Z’horonissp. was not among the 10 most numerically-dominant species.The population eruption observed in the winter and spring of 1981 wasnot repeated in 1982. The polychaete, Paruprionospio pinnata, increased from 52 individuals mm2 in July to a maximum of 973 individuals m- 2 m September. Populations of this species later decreased in number, and stabilized at approximately 150individuals m- 2 for the remainder of the year. Magelona cf. phyllisae, a burrowing polychaete, was the top-ranked macrobenthic speciesduring the study (Table 1). Although it was seldom the most abundant speciesin monthly collections, it was present at most stations throughout the year. It was among the ten most abundant speciesevery month. The most numerically-dominant speciesfrom January to April 1982was CirratuZus cf. filiformis, a sedentary polychaete. Its populations reached 6400 individuals me2 at site M20 during March 1982. In the study area, numbers of C. cf. jiliformis increased dramatically from October 1981to April 1982. Many of the speciesin the study area are opportunistic specieswhose life histories are adapted to rapid colonization of a habitat. Included among these are the phoronid, Phoronis sp. mentioned above and the polychaetes, Mediomastus californiensis and Owenia fusiformis. M. californiensis was most abundant around the diffuser (station MlOA) in June 1981 and February to April 1982, and least abundant during hypoxic conditions of the summer of 1981. 0. fusiformis was not present in the study area in the first three months (March to April 1981) but became abundant thereafter. Unlike most species it increased in population numbers during hypoxia. It was among the ten numerical dominants every month after August 1981. The susceptibility of amphipod crustaceansto physiological stresswas demonstrated in recent U.S. East Coast investigations (Sanders, 1978). Although amphipods were generally poorly represented in the study area, due in part to the fine texture of the sediments, they were included in this discussion because of noteworthy variations in
610
G. R. Gaston
1981
Figure
5. Temporal
variation
in density
of amphipods.
their populations. The most abundant specieswere Ampelisca abdita and two undescribed species of Corophium. There were 18 species of amphipods collected. Their abundance decreasedafter the onset of hypoxia in July 1981, and very few amphipods were collected subsequently (Figure 5). Population abundances of amphipods in the spring of 1982 were markedly below those of the sameperiod in 1981. Discussion The occurrence of hypoxia in the study area during the summer of 1981 resulted in reduced numbers of macrobenthic speciesand reduced populations of most species.The effects of hypoxia were most dramatically evidenced in population reductions of the numerically-dominant speciesPhoronis sp., Mediomastus californiensis and Cirratulus cf. filiformis. Although M. californiensis and C. cf. filiformis were abundant throughout the year, their lowest population levels occurred during middle and late summer following periodic conditions of hypoxia and anoxia. These population reductions were not believed to be temperature-related, as populations of the same speciesin nonhypoxic estuarine areas just north of the study area were not reduced in summer (Gaston & Weston, 1983). Species richness values dropped markedly during hypoxia, indicating elimination of numerous moderately-abundant and rare species from the area (e.g. Amphipoda, some Polychaeta). Reduction of populations of dominant species by hypoxia was also reflected in values for speciesevenness.Evenness values were elevated during the summer since no species overwhelmingly dominated the communities, increasing the relative abundancesof the other species. As an alternative hypothesis I considered the possibility that increased predation pressure during the summer of 1981 contributed to the demise of the benthic community. I examined data on abundance of species collected in the study area with an otter trawl (Ilg et al., 1983), and basedon recent investigations of the feeding habits of demersalfishes in the area (Matlock & Garcia, 1983; Sheridan & Trimm, 1983), included all speciesof crabs and fishesknown to feed on macrobenthos. Rather than an increasein
Effects of hypoxia on macrobenthos
611
predatory species,as one might expect if predation pressure causedthe reduction of the benthic populations, there was a decreasein abundance of all dominant speciesof crabs and demersal fishesin the study area concurrent with the hypoxia. Based on observations made in recent years it appearsthat hypoxia in the area may be an annual event (Fotheringham & Weissberg, 1979; Harper et al., 1981; Gaston & Weston, 1983) and may be the reason that the study area off Cameron was dominated by macrobenthic communities of young individuals and a rapidly-changing suite of opportunistic species.Where tube-dwelling species(e.g. Phoronis sp., Spiochaetopterus oculatus, and Diopatra cuprea) dominated, the substrate was apparently covered by clumps of tubes. These specieswere in greatest relative abundance during the summer, perhaps becauseof reduced bottom currents and more stable sediment conditions during those months. During most of the year, however, the fine sediments contributed to the generally unstable nature of the environment. This compounded the problem of establishment of assemblagesof speciesto the extent that colonization of the area by benthic specieswas likely limited by both the fine, mobile substrate and what probably was an annual hypoxic event. The result was domination of the area by opportunistic, vermiform species, particularly those adapted to fine sediments and tolerant of periodic hypoxia. These primarily included speciescapable of rapid burial and utilization of an unstable substrate (e.g. Magelona cf. phyllisae, Mediomastus californiensis, and Cirratulus cf.filiformis).
Harper et al. (1981) discussedthe recovery rates of various macrobenthic taxa following hypoxia on the Texas shelf. Most of the speciescommon to both study areas (e.g. Mediomastus californiensis, and Paraprionospio pinnata) were similarly affected by hypoxia. The only notable exception among the dominants was Magelona cf. phyllisae. Those collected off Cameron generally increased in population numbers at most sites during the hypoxic period of 1981, whereaspopulations of those collected at comparable depths off Freeport, Texas, maintained patterns of change or decreased in abundance during the summer hypoxia of 1978 and 1979. Populations at both sitesincreased following hypoxia. This apparent aberration in the susceptibility of Magelona to hypoxia may be related to its burrowing behavior. Unlike many of the speciesin the fine sedimentsof the study area, Magelona inhabited the reduced sediments below the sediment surface. Most of the other numerical dominants either lived at the sediment-water interface or maintained contact with the water column by tube irrigation. Hypoxia may have a long history in the northern Gulf of Mexico. During the periods of summer hypoxia in 1981 shrimpers in Cameron, Louisiana pulled their nets asclose to the beach as possible, probably becausehypoxia forced the shrimp and fish inshore to better-oxygenated waters (as described by Pavela et ul., 1983). Long-time Cameron residents reported that shrimp have concentrated in the shallow inner-shelf waters during summer months for at least forty years (I’. Hebert, pers. comm.), perhaps indicative that hypoxia is not a recent phenomenon. Acknowledgements There are a number of people at McNeese State University whose contributions I gratefully acknowledge. In particular, I am grateful to Don Weston who helped in all phasesof the preparation and execution of the project. I also thank all of the personnel who helped with the field and laboratory work: Flip Rutledge, Margaret Walther, Cynthia Grosze, George Warner, Ella Barbe, Barbara Benson, Mary Grosze, Dorothy
612
G. R.
Gaston
Walther, David Walther, Ann Pallet, Marjorie Klein, and Jan Westfall. I especially thank Patrick Cormier for drafting the figures, Michael Vecchione for reviewing the manuscript, and Anne Arceneaux for typing. This research was supported by the U.S. Department of Energy under contract DE-AC9680P010288 to McNeese State University, Lake Charles, Louisiana. Note added in proof Phoronis
sp. has been identified by Christian C. Emig asP. muelleri
Selys-Longchamps.
References Bedinger, C. A. 1979 Ecological investigations of petroleum production platforms in the central Gulf of Mexico-preliminary findings. 1 lth Annual Offshore Technology Conference, Houston, Texas. Bedinger, C. A., Jr, Childers, R. E., Cooper, J., Kimball, K. T. & Kwok, A. 1981 Background, program organization and study plan. In Ecological Investigations of Petroleum Production Platforms in the Central Gurf of Mexico, vol. 1, part 1, Southwest Research Institute, San Antonio, Texas. Report on Bureau of Land Management Contract AA551-CTS-17. pp. l-53. Boesch, D. F. 1983 Implications of oxygen depletion on the continental shelf of the northern Gulf of Mexico. Coastal Ocean Pollution Assessment News 2(3), 25-28. Bray, J. R. & Curtis, J. T. 1957 An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs 27,325-349. Farrell, D. H. 1979 Ben&c molluscan and crustacean communities in Louisiana. In The Offshore Ecology Investigation. Effects of OilDrilling and Production in a Coastal Environment. Rice University Studies 65 (4-5). pp. 401-436. Fotheringham, N. & Weissberg, G. H. 1979 Some causes, consequences and potential environmental impacts of oxygen depletion in the northern Gulf of Mexico. Offshore Technology Conference Proceedings OT3611. pp. 2205-2207. Gaston, G. R. & Weston, D. P. 1983 Benthos. In West Hackberry Brine Disposal Project. Year 1 PostDischarge Monitoring Report (DeRouen, L. R., Casserly, D. M., Lascara, V. J., Hann, R. W., Jr & Giammona, C., eds), chapter 6. Prepared for the U.S. Department of Energy under contract DE-AC96-80P010288. Harper, D. E., Jr & McKimrey, L. D. 1980 Benthos. In Evaluation of Brine Disposalfrom the Bryan Mound Site of the Strategic Petroleum Reserve Program. Final Report of Predisposal Studies (Hann, R. W., Jr & Randall, R. E., eds), chapter 5. Prepared for the U.S. Department of Energy under contract DE-FC9&79P010114. Harper, D. E., McKinney, L. D., Salzer, R. B. & Case, R. J. 1981 The occurrence of hypoxic bottom water off the upper Texas coast and its effects on the benthic biota. Contributions in Marine Science 24,53-79. Ilg, R. J., Kirby, T. L. & Stacy, G. 1983 Nekton. In West Hackberry Brine Disposal Project. Year 1 PostDischarge Monitoring Report (DeRouen, L. R., Casserly, D. M., Lascara, V. J., Harm, R. W. Jr & Giammona, C., eds), chapter 7. Prepared for the U.S. Department of Energy under contract DE-AC9&80P010288. Matlock, G. C. & Garcia, M. A. 1983 Stomach contents of selected fishes from Texas Bays. Contributzons tn Marine Science 26,95-l 10. Oetking, I’., Back, R., Watson, R. & Merks, C. 1979 Physical studies of the near-shore continental shelf of south central Louisiana: currents and hydrography. In The Offshore Ecology Investigation. Effects of Oil Drilling and Production in a Coastal Environment. Rice University Studies 65(4-5). pp. 119-144. Officer, C. B., Biggs, R. B., Taft, J. L., Cronin, L. E., Tyler, M. A. & Boynton, W. R. 1984 Chesapeake Bay anoxia: origin, development, and significance. Science 223,22-27. Pavela, J. S., Ross, J. L. & Chittenden, M. E., Jr 1983 Sharp reductions in abundance of fishes and benthic macroinvertebrates in the Gulf of Mexico off Texas associated with hypoxia. Northeast Gulf Science 6(2), 167-173. Pielou, E. C. 1966 The measurement of diversity in different types of biological collections. Journaf of Theoretical Biology 13,3?C-383. Price, K. C. 1979 Onshore hydrography of Timbalier Bay, Louisiana. In The Of/shore Ecology Investigation. Effects of Oil Drilling and Production in a Coastal Environment. Rice University Studies 65(4-5). pp. 145-158. Ragan, J. G., Harris, A. H., Green, J. H. 1978 Temperature, salinity and oxygen measurements of surface and bottom waters on the continental shelf off Louisiana during portions of 1975 and 1976. Professional Paper Series (Biology) 3. Nicholls State University, Thibodaux, LA. 29pp.
Effects
of hypoxia
on macrobenthos
61’5
Randall, R. E. 1983 Brine plume measurements. In West Hackberry Brine Disposal Project. Year I PostDischarge Monitoring Report (DeRouen, L. R., Casserly, D. M., Lascara, V. J., Hann, R. W. Jr & Giammona, C., eds). chapter 4. Prepared for the U.S. Department of Energy under contract DE-AC9~80P010288. Richards, F. A. 1957 Oxygen in the ocean. In Treatise on Marine Ecology and Paleoecology (Hedgpeth, J. W., ed.). Geological Society of America, Memoirs 67(l). pp. 185-238. Sanders, H. L. 1978 Florida oil spill impact on the Buzzards Bay benthic fauna: West Falmouth. Journal of the Fisheries Research Board of Canada 35(S), 717-730. Sheridan, P. F. & Trimm, D. L. 1983 Summer foods of Texas coastal fishes relative to age and habitat. Fishery Bulletin 81(3), 643-647. Stuntz, W. E., Sanders, N., Leming, T. D., Baxter, K. N. & Barazotto, R. M. 1982 Area of hypoxic bottom water found in northern Gulf of Mexico. Coastal Oceanography and Climatological News 4,37-38. Walsh, J. J., Rowe, G. T., Iverson, R. L. & McRoy, C. I’. 1981 Biological export of shelf carbon is a sink of the global CO, cycle. Nature 291, 198-201.
Coastal
and Shelf
Science
(1985) 20,603-613
Effects of Hypoxia on Macrobenthos Inner Shelf off Cameron, Louisiana
Gary
R. Gaston
Department University, Received
of the
of Biological Lake Charles, 5 March
and Environmental Louisiana 70609,
1984 and in revisedform
Keywords: hypoxia; macrobenthos; Annelida; Louisiana
Sciences, U.S.A. 33uly
McNeese
State
1984
population composition;
Polychaeta;
The effects of hypoxic bottom water, an annual event, were documented on the inner shelf off Cameron, Louisiana during the summer of 1981. Populations of most species of macrobenthos were dramatically reduced. In an area of fine sediment that was numerically dominated by polychaetous annelids, the most severely affected populations were those of tube-dwelling and surface-feeding species. Burrowing species were less influenced by the hypoxia.
Introduction Interest in the effects of hypoxic bottom waters ( < 2 mg I- ‘) on benthic macrofauna of the northwestern Gulf of Mexico (e.g. Fotheringham & Weissberg, 1979; Harper et al., 1981; Pavela et al., 1983; Boesch, 1983) has led to observations that hypoxia occurs during summer months on the inner continental shelf from the Mississippi River to Texas, in response to discharge from the Mississippi and Atchafalaya rivers. Mass mortalities may occur among macrobenthic communities, and nektonic species may leave the area (Ragan et al., 1978; Bedinger, 1979; Harper et al., 1981), with drastic implications on commercial fisheries, especially those including shrimp, crabs, and demersal fish. The purpose of this paper is to document the effects of hypoxia on inner shelf macrobenthic communities off Cameron, Louisiana, which is among the leading ports in the nation for commercial landings of finfish and shellfish. Data for this investigation were collected from February 1981 to April 1982. Background As early as 1935, low bottom dissolved oxygen values (3.9 mg 1-i) were recorded along the Texas and Louisiana coasts (Richards, 1957). In recent years investigations of the environmental impacts of petroleum production noted oxygen-depleted bottom waters in and around Timbalier Bay (e.g. Farrell, 1979; Fotheringham & Weissberg, 1979; Bedinger, 1979; Bedinger et al., 1981), as did investigations on the inner continental shelf from the Mississippi delta to Atchafalaya Bay (Ragan et al., 1978; Stuntz et al., 603 0272-7714/85/050603
+ 11 $03.00/O
0 1985Academic Press
Inc. (London)
Limited
G. R. Gaston
604
I __----
,’
_----
29O45’
/’
---5m-------
I’
--._ ‘.
‘--._
,’ /‘...
&
_/-5m--
I’
_\ \ \\ \.A
---------
Qd @
I’
__----
_----
--_____
1. Chart
of the study
area off Cameron,
I \?I\ \2J 29O40’ \A\ IO m-f+ ~_ \ \ 93T)20’ \ ,
93;251
93T30’ Figure
,
J&3------------mio-
___-------
__--
____----
I’
Louisiana,
indicating
1982) and as far west as the Brazos River, Texas (Harper & McKinney,
collection
sites.
1980; Harper et
al., 1981; Pavela et al., 1983).
Several probable causesof hypoxia have been postulated. Most studies attribute hypoxia to the freshwater runoff from the Mississippi and Atchafalaya rivers, which leads to density stratification of the water column, and elimination of oxygen exchange between the surface and bottom (e.g. Fotheringham & Weissberg, 1979; Bedinger et al., 1981). Additionally, decomposition of the water-borne organic debris increases the biological oxygen demand (BOD) of the sedimentsand decreasesthe dissolved oxygen of the near-bottom water (Oetking et al., 1979; Price, 1979; Bedinger et al., 1981; Officer et al., 1984). Farrell (1979) reported high quantities of sediment phaeopigments in hypoxic areas, suggestingthat oxygen depletion off central Louisiana may be linked with production and decomposition of phytoplankton. An associationof hypoxia and primary production would imply that an overabundance of phytoplankton occurs seasonallyoff Louisiana. This is supported by evidence of a dramatic increasein nitrate content of the Mississippi River in recent years (Walsh et al., 1981), a phenomenon which could enhanceoffshore primary production on the Louisiana continental shelf (Boesch, 1983). Materials
and methods
The present study was conducted from February 1981 to April 1982. Seven stations were sampled monthly and an additional four (M6, M15, DN, DS) were included in quarterly sampling (Figure 1) as part of a brine discharge monitoring study (Gaston & Weston, 1983). Sampling sites were located primarily on an east-west transect along the 10-m depth contour near a Department of Energy Strategic Petroleum Reserve Program brine diffuser. The area is approximately 15 km southeast of Cameron, Louisiana.
Effects of hypoxia on macrobenthos
605
All stations were located by LORAN C. At each site observations were made of time, sea state, and weather conditions. A vertical profile of conductivity, temperature, dissolved oxygen and pH was made with a Hydrolab Series 8000 meter at 3 m depth intervals. Six replicate grab sampleswere taken at all stations using a 0.1 m2 stainless steel Smith-McIntyre grab. The contents of each grab were washed through a O-5mm screen. The material retained on the sieve was preserved in 109b buffered formalin containing RoseBengal, to be sorted to macrofaunal specieslater in the laboratory. Dominant specieswere selected by cumulative ranking of numerical dominants. The ten most abundant speciescollected at the seven monthly siteswere ranked according to abundance. The most abundant speciescollected each month received a score of 10 and less abundant species were given successively lower scores. The ranking was then determined by summing the twelve monthly scores. Several indices of community structure were employed in data analysis of the benthic collections. Diversity was measuredusing Shannon’s formula (Pielou, 1966). This index is dependent on both number of speciesin the sampleas well astheir relative dominance. To examine these two parameters independently, speciesrichness (S) and evennesscr> were computed separately using the formulae: S-l S=---
1nN ’
J= H’ 10&S’
where N equals the total number of individuals. These indices, when calculated for a station, are based on the number of speciesand their mean abundances in all replicate grabs taken. In order to present the large data set in an interpretable form, as well as to determine zones of rapid fauna1 change, multivariate analysis techniques were employed. Species which occurred in only a single replicate sample were eliminated. Clustering was performed using the Virginia Institute of Marine Science program COMPAH (Combinatorial Polythetic Agglomerative Hierarchical) program. Log transformation (log X+ 1) and the Bray-Curtis similarity measure (Bray & Curtis, 1957) were employed in the clustering. Results Sediments of the study area were generally silty clays with approximately lo?,, sand, 35O, silt and 55?,0clay. There was a general homogeneity in sediment type, and consequent similarity in fauna1 composition which enhanced the suitability of the sites for comparative observations of hypoxic effects (Gaston & Weston, 1983). The dissolved oxygen concentration of bottom waters exhibited wide variation both spatially and temporally. The most notable temporal changes were the periods of low dissolved oxygen during the summer of 1981, when bottom dissolved oxygen concentrations often dropped below 1 mg 1-r (Figure 2). These periods of hypoxia were noted intermittently from mid-June through mid-September and corresponded to a period of pronounced salinity stratification (Gaston & Weston, 1983). During the latter half of July and early August bottom dissolved oxygen concentrations at the brine diffuser (2.5-3.5 mg 1-l) exceeded that of station Ml8 (0.5-2.0 mg l- ‘). This elevation of dissolved oxygen in the vicinity of the diffuser resulted either from aeration of bottom water by mixing with the oxygenated brine effluent or, more probably, from turbulent
606
G. R. Gaston
Station
Ml8
6-
----
Bottom
-
FMAMJJASONDJFMA
D
? 0
Surface
,
P I
Station
MIOA
FMAMJJASONDJFM 1981
1982
Figure2. Temporalvariationsin dissolvedoxygen(mgl-‘) at fwo sites(Ml8 and MlOA, seeFigure1).
mixing of the water column during brine discharge and the consequent breakdown of stratification. During late August and September, oxygen levels at the diffuser site (station MlOA) dropped below those of other sites. This occurrence corresponded to periods during which brine discharge was suspended’(2P31 August; 3-14 September). During periods of brine discharge the brine plume was barely detectable outside a 2 km radius of the diffuser (Randall, 1983). Data on the other physical parameters of the study area were discussedin Gaston & Weston (1983). Although the sampling sites were generally similar in physical characteristics other than dissolved oxygen (Gaston & Weston, 1983), there were notable variations in benthic communities. A number of stations (e.g. MlO, M6) were more speciose,as evidenced in the species-richnessvalues (Figure 3). Sampling sites to the east of the diffuser (e.g. stations M15, M18, M20) were generally lessrich in speciesthan those to the west (e.g. stations M3, M6). Species-evennessvalues, a measure of how evenly the individuals were distributed among the species,at station M3 were consistently lower than other sitesfrom May to August and were higher than all other sites from October to March. Numerical classification (clustering) was used to delimit consistent patterns of station similarity. All 15 months of sampling were incorporated in the analyses,and each month of collection at a site was treated as a separate entity (Figure 4). Because of the high temporal variability of the benthic community, numerical classification groupings were formed primarily on the basis of month rather than station. Three major groupings, established on the basis of season,were evident: (1) February to April 1981, (2) May to October 1981, including the hypoxic period during the summer months; and (3) November 1981 to April 1982. The fact that the February-April period of 1981 is more similar to May-October 1981 than to the February-April period of 1982 indicates the magnitude of temporal fauna1 change in the study area and the absence of a repeated
Effects
of hypoxia
607
on macrobenthos
Hypoxlc period
/ 1-d’
c /
,“V /
d’
12 II c
I
\
.’
I
\ ,\ \ \
/ /
Y
O-8 0 -7 F-
rJh /? >’ i 1i’ /I ‘1/Y/\\’f / /
I/,
J
A
S
ON
0
J
1981
FMA I982
Figure 3. Temporal variations in species diversity, species richness and species evenness at three sites (M3, MlOA, M18, see Figure 1). cycle. Certain collections at stations MlOA and M3 separatedin the cluster. This resulted from the distinct fauna which occurred during these collections. Although the use of diversity indices has fallen in disfavor among many ecologists in recent years, Shannon diversity and its components (species richness and species evenness) were useful here to demonstrate temporal variations in the communities (Figure 3). Based on the numerical classification, three sites (stations M3, MIOA, M18)
annual
were
selected
for comparisons
of these measurements.
There
was a radical
values of all three indices during summer hypoxia. Additionally, values for evenness and Shannon diversity variations in diversity among the stations
varied concurrently, were due primarily
change
in
throughout the year
indicating to changes
that temporal in the relative
abundance of the speciesrather than to differences in the number of speciesinhabiting the sites. This resulted from the numerical dominance of a few species at particular sites. The low value for evenness which occurred at station MlOA in June (Figure 3) was
608
G. R. Gaston
Feb
I
1981 -Mar
1981
I -fzz .E r-
May
1981
Jun
1981
1981
Sep
IQEI-
Nov
1981-Jan
Feb
1982
Feb
1982-Apr
Ott
1981
1982
-Apr
1982
1982
-
Figure 4. Numerical classification sorting, beta= -0.25).
of all collections
off Cameron,
Louisiana.
(Flexible
atypical of the pattern seen at any other station, and represented a sudden eruption in population of a single species(Phoronis sp.). The ten highest-ranked speciesare presented in Table 1. During a three-month period sp. (Phoronida) and Sabellides sp. (February-April 1981) two species, Phoronis (Polychaeta) numerically dominated the macrobenthic communities of the study area. Although the high abundance of Sabellides sp. did not continue into the summer months, Phoronis sp. population numbers did continue, totalling 729, of the total macrobenthos in May. This pattern of domination by Phoronis sp. continued through July. Populations
of hypoxia
Effects
on macrobenthos
TABLE 1. Dominant macrobenthic both dominance during a given (February 1981 to April 1982)
Rank
2 4 5 6 8 9 10 11 12 13 14
609
species off Cameron, month and persistance
Species Magelona cf. phyllisae Paraprionospio pinnata Mediomastus californiensis Cirratulus cf. filiformis Phoronis sp. Sigambra tentaculata Owenia fusiformis Pseudeurythoe paucibranchiat Diopatra cuprea Cossura soyeri Glycinde solitaria Nemertea sp. B Mulinia lateralis Spiochaetopterus oculatus
Louisiana. throughout
Score is based on the study period
Score (max = 120) 107 97 58 58 54 51 47 38 35 35 30 29 18 12
of Phoronis sp. decreased in number through August and September. By October Z’horonissp. was not among the 10 most numerically-dominant species.The population eruption observed in the winter and spring of 1981 wasnot repeated in 1982. The polychaete, Paruprionospio pinnata, increased from 52 individuals mm2 in July to a maximum of 973 individuals m- 2 m September. Populations of this species later decreased in number, and stabilized at approximately 150individuals m- 2 for the remainder of the year. Magelona cf. phyllisae, a burrowing polychaete, was the top-ranked macrobenthic speciesduring the study (Table 1). Although it was seldom the most abundant speciesin monthly collections, it was present at most stations throughout the year. It was among the ten most abundant speciesevery month. The most numerically-dominant speciesfrom January to April 1982was CirratuZus cf. filiformis, a sedentary polychaete. Its populations reached 6400 individuals me2 at site M20 during March 1982. In the study area, numbers of C. cf. jiliformis increased dramatically from October 1981to April 1982. Many of the speciesin the study area are opportunistic specieswhose life histories are adapted to rapid colonization of a habitat. Included among these are the phoronid, Phoronis sp. mentioned above and the polychaetes, Mediomastus californiensis and Owenia fusiformis. M. californiensis was most abundant around the diffuser (station MlOA) in June 1981 and February to April 1982, and least abundant during hypoxic conditions of the summer of 1981. 0. fusiformis was not present in the study area in the first three months (March to April 1981) but became abundant thereafter. Unlike most species it increased in population numbers during hypoxia. It was among the ten numerical dominants every month after August 1981. The susceptibility of amphipod crustaceansto physiological stresswas demonstrated in recent U.S. East Coast investigations (Sanders, 1978). Although amphipods were generally poorly represented in the study area, due in part to the fine texture of the sediments, they were included in this discussion because of noteworthy variations in
610
G. R. Gaston
1981
Figure
5. Temporal
variation
in density
of amphipods.
their populations. The most abundant specieswere Ampelisca abdita and two undescribed species of Corophium. There were 18 species of amphipods collected. Their abundance decreasedafter the onset of hypoxia in July 1981, and very few amphipods were collected subsequently (Figure 5). Population abundances of amphipods in the spring of 1982 were markedly below those of the sameperiod in 1981. Discussion The occurrence of hypoxia in the study area during the summer of 1981 resulted in reduced numbers of macrobenthic speciesand reduced populations of most species.The effects of hypoxia were most dramatically evidenced in population reductions of the numerically-dominant speciesPhoronis sp., Mediomastus californiensis and Cirratulus cf. filiformis. Although M. californiensis and C. cf. filiformis were abundant throughout the year, their lowest population levels occurred during middle and late summer following periodic conditions of hypoxia and anoxia. These population reductions were not believed to be temperature-related, as populations of the same speciesin nonhypoxic estuarine areas just north of the study area were not reduced in summer (Gaston & Weston, 1983). Species richness values dropped markedly during hypoxia, indicating elimination of numerous moderately-abundant and rare species from the area (e.g. Amphipoda, some Polychaeta). Reduction of populations of dominant species by hypoxia was also reflected in values for speciesevenness.Evenness values were elevated during the summer since no species overwhelmingly dominated the communities, increasing the relative abundancesof the other species. As an alternative hypothesis I considered the possibility that increased predation pressure during the summer of 1981 contributed to the demise of the benthic community. I examined data on abundance of species collected in the study area with an otter trawl (Ilg et al., 1983), and basedon recent investigations of the feeding habits of demersalfishes in the area (Matlock & Garcia, 1983; Sheridan & Trimm, 1983), included all speciesof crabs and fishesknown to feed on macrobenthos. Rather than an increasein
Effects of hypoxia on macrobenthos
611
predatory species,as one might expect if predation pressure causedthe reduction of the benthic populations, there was a decreasein abundance of all dominant speciesof crabs and demersal fishesin the study area concurrent with the hypoxia. Based on observations made in recent years it appearsthat hypoxia in the area may be an annual event (Fotheringham & Weissberg, 1979; Harper et al., 1981; Gaston & Weston, 1983) and may be the reason that the study area off Cameron was dominated by macrobenthic communities of young individuals and a rapidly-changing suite of opportunistic species.Where tube-dwelling species(e.g. Phoronis sp., Spiochaetopterus oculatus, and Diopatra cuprea) dominated, the substrate was apparently covered by clumps of tubes. These specieswere in greatest relative abundance during the summer, perhaps becauseof reduced bottom currents and more stable sediment conditions during those months. During most of the year, however, the fine sediments contributed to the generally unstable nature of the environment. This compounded the problem of establishment of assemblagesof speciesto the extent that colonization of the area by benthic specieswas likely limited by both the fine, mobile substrate and what probably was an annual hypoxic event. The result was domination of the area by opportunistic, vermiform species, particularly those adapted to fine sediments and tolerant of periodic hypoxia. These primarily included speciescapable of rapid burial and utilization of an unstable substrate (e.g. Magelona cf. phyllisae, Mediomastus californiensis, and Cirratulus cf.filiformis).
Harper et al. (1981) discussedthe recovery rates of various macrobenthic taxa following hypoxia on the Texas shelf. Most of the speciescommon to both study areas (e.g. Mediomastus californiensis, and Paraprionospio pinnata) were similarly affected by hypoxia. The only notable exception among the dominants was Magelona cf. phyllisae. Those collected off Cameron generally increased in population numbers at most sites during the hypoxic period of 1981, whereaspopulations of those collected at comparable depths off Freeport, Texas, maintained patterns of change or decreased in abundance during the summer hypoxia of 1978 and 1979. Populations at both sitesincreased following hypoxia. This apparent aberration in the susceptibility of Magelona to hypoxia may be related to its burrowing behavior. Unlike many of the speciesin the fine sedimentsof the study area, Magelona inhabited the reduced sediments below the sediment surface. Most of the other numerical dominants either lived at the sediment-water interface or maintained contact with the water column by tube irrigation. Hypoxia may have a long history in the northern Gulf of Mexico. During the periods of summer hypoxia in 1981 shrimpers in Cameron, Louisiana pulled their nets asclose to the beach as possible, probably becausehypoxia forced the shrimp and fish inshore to better-oxygenated waters (as described by Pavela et ul., 1983). Long-time Cameron residents reported that shrimp have concentrated in the shallow inner-shelf waters during summer months for at least forty years (I’. Hebert, pers. comm.), perhaps indicative that hypoxia is not a recent phenomenon. Acknowledgements There are a number of people at McNeese State University whose contributions I gratefully acknowledge. In particular, I am grateful to Don Weston who helped in all phasesof the preparation and execution of the project. I also thank all of the personnel who helped with the field and laboratory work: Flip Rutledge, Margaret Walther, Cynthia Grosze, George Warner, Ella Barbe, Barbara Benson, Mary Grosze, Dorothy
612
G. R.
Gaston
Walther, David Walther, Ann Pallet, Marjorie Klein, and Jan Westfall. I especially thank Patrick Cormier for drafting the figures, Michael Vecchione for reviewing the manuscript, and Anne Arceneaux for typing. This research was supported by the U.S. Department of Energy under contract DE-AC9680P010288 to McNeese State University, Lake Charles, Louisiana. Note added in proof Phoronis
sp. has been identified by Christian C. Emig asP. muelleri
Selys-Longchamps.
References Bedinger, C. A. 1979 Ecological investigations of petroleum production platforms in the central Gulf of Mexico-preliminary findings. 1 lth Annual Offshore Technology Conference, Houston, Texas. Bedinger, C. A., Jr, Childers, R. E., Cooper, J., Kimball, K. T. & Kwok, A. 1981 Background, program organization and study plan. In Ecological Investigations of Petroleum Production Platforms in the Central Gurf of Mexico, vol. 1, part 1, Southwest Research Institute, San Antonio, Texas. Report on Bureau of Land Management Contract AA551-CTS-17. pp. l-53. Boesch, D. F. 1983 Implications of oxygen depletion on the continental shelf of the northern Gulf of Mexico. Coastal Ocean Pollution Assessment News 2(3), 25-28. Bray, J. R. & Curtis, J. T. 1957 An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs 27,325-349. Farrell, D. H. 1979 Ben&c molluscan and crustacean communities in Louisiana. In The Offshore Ecology Investigation. Effects of OilDrilling and Production in a Coastal Environment. Rice University Studies 65 (4-5). pp. 401-436. Fotheringham, N. & Weissberg, G. H. 1979 Some causes, consequences and potential environmental impacts of oxygen depletion in the northern Gulf of Mexico. Offshore Technology Conference Proceedings OT3611. pp. 2205-2207. Gaston, G. R. & Weston, D. P. 1983 Benthos. In West Hackberry Brine Disposal Project. Year 1 PostDischarge Monitoring Report (DeRouen, L. R., Casserly, D. M., Lascara, V. J., Hann, R. W., Jr & Giammona, C., eds), chapter 6. Prepared for the U.S. Department of Energy under contract DE-AC96-80P010288. Harper, D. E., Jr & McKimrey, L. D. 1980 Benthos. In Evaluation of Brine Disposalfrom the Bryan Mound Site of the Strategic Petroleum Reserve Program. Final Report of Predisposal Studies (Hann, R. W., Jr & Randall, R. E., eds), chapter 5. Prepared for the U.S. Department of Energy under contract DE-FC9&79P010114. Harper, D. E., McKinney, L. D., Salzer, R. B. & Case, R. J. 1981 The occurrence of hypoxic bottom water off the upper Texas coast and its effects on the benthic biota. Contributions in Marine Science 24,53-79. Ilg, R. J., Kirby, T. L. & Stacy, G. 1983 Nekton. In West Hackberry Brine Disposal Project. Year 1 PostDischarge Monitoring Report (DeRouen, L. R., Casserly, D. M., Lascara, V. J., Harm, R. W. Jr & Giammona, C., eds), chapter 7. Prepared for the U.S. Department of Energy under contract DE-AC9&80P010288. Matlock, G. C. & Garcia, M. A. 1983 Stomach contents of selected fishes from Texas Bays. Contributzons tn Marine Science 26,95-l 10. Oetking, I’., Back, R., Watson, R. & Merks, C. 1979 Physical studies of the near-shore continental shelf of south central Louisiana: currents and hydrography. In The Offshore Ecology Investigation. Effects of Oil Drilling and Production in a Coastal Environment. Rice University Studies 65(4-5). pp. 119-144. Officer, C. B., Biggs, R. B., Taft, J. L., Cronin, L. E., Tyler, M. A. & Boynton, W. R. 1984 Chesapeake Bay anoxia: origin, development, and significance. Science 223,22-27. Pavela, J. S., Ross, J. L. & Chittenden, M. E., Jr 1983 Sharp reductions in abundance of fishes and benthic macroinvertebrates in the Gulf of Mexico off Texas associated with hypoxia. Northeast Gulf Science 6(2), 167-173. Pielou, E. C. 1966 The measurement of diversity in different types of biological collections. Journaf of Theoretical Biology 13,3?C-383. Price, K. C. 1979 Onshore hydrography of Timbalier Bay, Louisiana. In The Of/shore Ecology Investigation. Effects of Oil Drilling and Production in a Coastal Environment. Rice University Studies 65(4-5). pp. 145-158. Ragan, J. G., Harris, A. H., Green, J. H. 1978 Temperature, salinity and oxygen measurements of surface and bottom waters on the continental shelf off Louisiana during portions of 1975 and 1976. Professional Paper Series (Biology) 3. Nicholls State University, Thibodaux, LA. 29pp.
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on macrobenthos
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Randall, R. E. 1983 Brine plume measurements. In West Hackberry Brine Disposal Project. Year I PostDischarge Monitoring Report (DeRouen, L. R., Casserly, D. M., Lascara, V. J., Hann, R. W. Jr & Giammona, C., eds). chapter 4. Prepared for the U.S. Department of Energy under contract DE-AC9~80P010288. Richards, F. A. 1957 Oxygen in the ocean. In Treatise on Marine Ecology and Paleoecology (Hedgpeth, J. W., ed.). Geological Society of America, Memoirs 67(l). pp. 185-238. Sanders, H. L. 1978 Florida oil spill impact on the Buzzards Bay benthic fauna: West Falmouth. Journal of the Fisheries Research Board of Canada 35(S), 717-730. Sheridan, P. F. & Trimm, D. L. 1983 Summer foods of Texas coastal fishes relative to age and habitat. Fishery Bulletin 81(3), 643-647. Stuntz, W. E., Sanders, N., Leming, T. D., Baxter, K. N. & Barazotto, R. M. 1982 Area of hypoxic bottom water found in northern Gulf of Mexico. Coastal Oceanography and Climatological News 4,37-38. Walsh, J. J., Rowe, G. T., Iverson, R. L. & McRoy, C. I’. 1981 Biological export of shelf carbon is a sink of the global CO, cycle. Nature 291, 198-201.