(Groton, CT, October 2002)
Published 2004, pages
return to main site
EUTROPHICATION OF LONG ISLAND SOUND
AS TRACED BY BENTHIC FORAMINIFERA
Thomas1, E., Abramson1, 2, I., Varekamp1, J. C., and Buchholtz ten Brink2, M. R.
1 Department of Earth and Environmental Sciences, Wesleyan University, 265 Church Street, Middletown, CT 06459; 2
2Center for Coastal and Marine Geology, U.S. Geological Survey, 384 Woods Hole Road, Woods Hole, MA 02543
Benthic foraminifera are marine, unicellular eukaryotes which secrete a shell (test) of calcium carbonate or agglutinate mineral grains in an organic matrix. Benthic foraminiferal assemblages in grab samples taken from Long Island Sound (LIS) in the early 1960s were described extensively (Buzas, 1965). These faunas were low-diversity and dominated by 1-3 species, as expected for marginally marine assemblages. At water depths of less than 10-15 m the dominant species was Elphidium excavatum, which consumes living diatoms (Murray, 1991; Bernhard and Bowser, 1999). In deeper areas Buccella frigida and Eggerella advena, which use more refractory organic carbon (Murray, 1991), were common. In the mid-1990s assemblages in grab samples had changed considerably, and in western LIS, which has suffered summer hypoxia since the early 1970s (Parker and O'Reilly, 1991), the species Ammonia beccarii had become common to dominant (Thomas et al., 2000).
In order to document ecosystem changes since the European settlement in the mid-1600s and to constrain the timing of the change from Elphidium- to Ammonia-dominated faunas, we collected benthic foraminiferal assemblage data in samples from 9 cores on depth transects in Long Island Sound (LIS) (Figure 1; Buchholtz ten Brink et al., 2000). Preliminary ages of core samples were determined using 137Cs, 210Pb and metal pollution data (Varekamp et al., 2000, 2003).
In most cores, foraminifera increased in absolute abundance (number of foraminifera per gram of dry bulk sediment) in the early through middle 1800s, coeval with an increase in relative abundance of E. excavatum (Figures 2a, b). These faunal changes coincided with an increase in metal contamination in the sediment (Varekamp et al., 2000, 2003), an increase in the concentration of the bacterial spore and sewage indicator Clostridium perfringens (Buchholtz ten Brink et al., 2000), and in the concentration of organic carbon in the sediments (Lugolobi et al., this volume) as well as in the accumulation rate of organic carbon (Varekamp et al., this volume).
Additional and more profound changes in LIS benthic foraminiferal assemblages occurred after the late 1960s. In cores in western LIS and close to the mouth of the Connecticut River, overall foraminiferal abundance decreased (Figure 2), while the species Ammonia beccarii became common or dominant (Figure 3). The increase in A. beccarii was most extreme in western LIS where episodes of summer hypoxia/anoxia are most common and most severe (Parker and O'Reilly, 1991). This profound faunal change started in the 1960s-1970s in western LIS and outside the mouth of the Connecticut River, then extended further into the Central Basin in the 1990s.
Increased nutrient influx in the middle of the 19th century may have led to increasing biological productivity, as documented by increasing concentrations of organic carbon and nitrogen in the sediments and increasing accumulation rates of organic carbon, especially in western Long Island Sound and the Narrows (Lugolobi et al., this volume; Varekamp et al., this volume). We suggest that this increasing productivity included an increase in productivity of planktic diatoms, the main food source of E. excavatum, as was also documented in Chesapeake Bay (Cooper and Brush, 1993). An increase in productivity of diatoms in response to increased anthropogenic nutrient input may well have caused the changes in benthic foraminiferal faunas in the mid 19th century: increasing percentages of the diatom-consuming E. excavatum and increasing overall foraminiferal abundance.
Less clear is the cause of the increase in relative abundance of A. beccarii and the coeval decrease in overall abundance of foraminifera. Both Elphidium and Ammonia species are adapted to marginally marine conditions and survive in highly polluted waters (e.g., Alve, 1995). A replacement of Elphidium-dominated by Ammonia-dominated assemblages in the Gulf of Mexico (Sen Gupta et al., 1996; Platon and Sen Gupta, 2001) and Chesapeake Bay (Karlsen et al., 2000) has been argued to have been caused by declining oxygen levels. This explanation, however, is problematic because both taxa easily survive low-oxygen conditions in both natural (e.g. Alve, 1995) and laboratory settings (Moodley and Hess, 1992).
A factor that could have caused the increase in relative abundance of A. beccarii is the recent increase in water temperature in LIS, which could have given the competitive advantage to Ammonia over Elphidium. A. beccarii reproduces successfully in the laboratory only if temperatures exceed 20oC for at least several weeks (Bradshaw, 1957; Schnitker, 1974), whereas Elphidium excavatum is abundant in assemblages as far North as the Arctic Ocean (e.g., Polyak et al., 2002). One can thus argue that increasing temperatures may have played a role in the faunal changes in LIS, but this was probably not so in the Gulf of Mexico or even in Chesapeake Bay, where temperatures have not been in the limiting range for A. beccarii in the past.
We speculate that the main cause for the replacement of Elphidium-dominated assemblages by Ammonia-dominated assemblages in LIS may have been the influx of N-rich effluent from waste water treatment plants, which has led to an increase in N/Si values. High N/Si values strongly influence phytoplankton composition (Rabalais and Turner, 2001; Dortch et al., 2001), because they give the competitive advantage to organic-walled primary producers, including cyanobacteria and dinoflagellates, over diatoms which form a siliceous frustule (Escaravage and Prins, 2002). Many organisms that are higher in the food chain, however, strongly prefer or require diatoms rather than organic-walled phytoplankton as their food source, and changes in phytoplankton assemblages thus reverberate through the food chain (e.g., Rabalais and Turner, 2001).
Phytoplankton in western LIS shows a recent shift from being diatom-dominated to being dominated by organic-walled phytoplankton (Capriulo et al., 2002). E. excavatum preferentially consumes diatoms, and such a change in primary producers would thus give the competitive advantage to other species of foraminifera. The total foraminiferal abundance is expected to decline when primary producers are dominated by flagellates because many foraminiferal species do not use these as food (Murray, 1991). The changes in composition of the phytoplankton resulting from high N-concentrations would be expected to be most severe in the regions with most severe eutrophication, in which areas we also see the most severe hypoxia, explaining the correlation between the increasing relative abundance of Ammonia and low-oxygen conditions.
Benthic foraminifera are very common in LIS sediment cores and we used their tests to reconstruct historical changes in the LIS ecosystem. The foraminiferal assemblages indicate that the biota started to react to eutrophication in the middle of the 19th century. Profound ecosystem changes occurred from the late 1960s-early 1970s on, particularly in western LIS. These changes may have been caused by increasing N/Si ratios, which would cause major changes in the primary producers in LIS by giving the advantage to organic walled photosynthesizing algae over diatoms. This change then reverberated throughout the entire ecosystem, including the benthic microfauna.
Funding for this research was received from Connecticut Sea Grant, the EPA Long Island Sound Office and the State of Connecticut Department of Environmental Protection Lobster Research Funds.
Alve, E., 1995. Benthic foraminiferal responses to estuarine pollution: An overview. Journal of Foraminiferal Research 25, 190-203.
Bernhard, J. M., and Bowser, S. S., 1999. Benthic foraminifera of dysoxic sediments: chloroplast sequestration and functional morphology. Earth-Science Reviews 46, 149-165
Buchholtz ten Brink, M. R., Mecray, E. L., and Galvin, E. L., 2000. Clostridium perfringens in Long Island Sound sediments: An urban sedimentary record: Journal of Coastal Research 16, 591-612.
Buzas, M. A., 1965, The distribution and abundance of Foraminifera in Long Island Sound. Smithsonian Institution Miscellaneous Collection 149, 1-88.
Capriulo, G. M., Smith, G., Troy, R., Wikfors, G. H., Pellet, J., and Yarish, C., 2002. The planktonic food web structure of a temperate zone estuary, and its alteration due to eutrophication. Hydrobiologia 475/476, 263-333.
Cooper, S. and Brush, G. S., 1993. A 2,500-year history of anoxia and eutrophication in Chesapeake Bay. Estuaries 38, 617-626.
Dortch, Q., Rabalais, N. N., Turner, R. E., and Qureshi, N. A., 2001. Impacts of changing Si/N ratios and phytoplankton species composition. In: Rabalais, N. N. and Turner, R. E., eds., Coastal Hypoxia: consequences for living resources and ecosystems. American Geophysical Union, Washington D.C., 37-48.
Escaravage, V., and Prins, T. C., 2002. Silicate availability, vertical mixing and grazing control of phytoplankton blooms in mesocosms. Hydrobiologia 484, 33-38.
Karlsen, A. W., Cronin, T. M., Ishman, S. E., Willard, D. A., Holmes, C. W., Marot, M., and Kerhin, R., 2000. Historical trends in Chesapeake Bay dissolved oxygen based on benthic foraminifera from sediment cores. Estuaries 23, 488-508.
Moodley, L. and Hess, C., 1992. Tolerance of infaunal benthic foraminifera for low and high oxygen concentrations. Biological Bulletin 183, 94-98.
Murray, J. W., 1991, Ecology and Palaeoecology of Benthic Foraminifera, Longman Scientific and Technical (John Wiley), 365 pp.
Parker, C. A. and O'Reilly, J. E., 1991. Oxygen depletion in Long Island Sound: a historical perspective. Estuaries 14, 248-264.
Platon, E., and Sen Gupta, B. K., 2001. Benthic foraminiferal communities in oxygen-depleted environments of the Louisiana continental shelf. In: Rabalais, N. N. and Turner, R. E., eds., Coastal Hypoxia: consequences for living resources and ecosystems. American Geophysical Union, Washington D.C., 147-163.
Polyak, L., Korsun, S., Febo, L.A., Stanovoy, V., Khusid, T., Hald, M., Paulsen, B.E. and Lubinski, D.A., 2002. Benthic foraminiferal assemblages from the southern Kara Sea, a river-influenced arctic marine environment, Journal of Foraminiferal Research 32, 252-273
Rabalais, N. N. and Turner, R. E., 2001. Hypoxia in the Northern Gulf of Mexico: description, causes and consequences. In: Rabalais, N. N. and Turner, R. E., eds., Coastal Hypoxia: consequences for living resources and ecosystems. American Geophysical Union, Washington D.C., 1-36.
Sen Gupta, B. K., Turner, E. R. and Rabalais, N. N., 1996. Seasonal oxygen depletion in continental shelf waters of Louisiana: historical record of benthic foraminifers. Geology 24, 227-230.
Thomas, E., Gapotchenko, T., Varekamp, J. C., Mecray, E. L., and Buchholtz ten Brink, M. R., 2000. Benthic foraminifera and environmental changes in Long Island Sound: Journal of Coastal Research 16, 641-655.
Varekamp, J. C., Buchholtz ten Brink, M. R., Mecray, E. L., and Kreulen, B., 2000. Mercury in Long Island Sound Sediments. Journal of Coastal Research 16, 613-626.
Varekamp, J. C., Kreulen, B., Buchholtz ten Brink, M. R., and Mecray, E. L., 2003. Mercury contamination chronologies from Connecticut wetlands and Long Island Sound sediments. Environmental Geology 43, 268-282, DOI: 10.1007/s00254-002-0624-x