Variability in responses to nutrients and trace elements, and transmission of stressor effects through an estuarine food web

Aquatic systems are increasingly exposed to multiple stressors from anthropogenic sources. These stressors can vary in the consistency and magnitude of responses they elicit in biota and in how the presence of additional stressors modifies their effects. Understanding how the biological environment and temporal dynamics influence responses to stressors, and how stressors interact, is important to predicting their effects in the natural environment. We examined temporal variability in responses of an experimental estuarine food web to elevated trace elements and nutrients, as well as non‐additive effects of the combination of these two stressors. Experiments were conducted four times during spring through autumn 1996 in 20 l‐m3 mesocosms. We measured a range of system‐, population‐, and individual‐level parameters to quantify responses of phytoplankton, bacterioplankton, heterotrophic nanoflagellates, copepods, fish, and benthic invertebrates to trace element and nutrient additions. The response to trace element additions was more variable both temporally and among phytoplankton and higher trophic level taxa than was the response to nutrient additions. Most taxa increased, either significantly or showed a trend toward increasing, in response to nutrient additions in all four mesocosm runs. In contrast, the direction as well as the magnitude of responses to trace element additions varied considerably among taxa and experimental runs. Two distinct types of nutrient3trace element interactions were important. First, temporal dynamics of nutrient ratios appeared to affect the temporal pattern of toxicity of trace elements to phytoplankton. Second, in the June mesocosm run when trace element additions reduced production, abundance, or growth of many organisms, these reductions were often proportionately greater in nutrient addition tanks than where no nutrients were added. Our results suggest that considerable temporal and taxonomic variation in responses to trace element loadings are likely to be seen in field settings even under constant loadings to the system and that trace elements may mask the magnitude of the response to high nutrient loadings in eutrophic systems. More generally, the presence of multiple stressors may either increase or dampen the temporal and spatial variability seen in aquatic systems, depending on the interactions among stressors and the influence of background environmental conditions and sensitive species on the expression of stressor effects.

[1]  W. Pearsall,et al.  Phytoplankton of the English Lakes. , 1925 .

[2]  W. Pearsall Phytoplankton in the English Lakes: II. The Composition of the Phytoplankton in Relation to Dissolved Substances , 1932 .

[3]  H. Utermöhl Zur Vervollkommnung der quantitativen Phytoplankton-Methodik , 1958 .

[4]  J. Blum Phosphate Uptake by Phosphate-Starved Euglena , 1966, The Journal of general physiology.

[5]  D. R. Heinle Production of a calanoid copepod,Acartia tonsa, in the Patuxent River estuary , 1966 .

[6]  T. Parsons,et al.  A practical handbook of seawater analysis , 1968 .

[7]  D. Menzel,et al.  Marine Phytoplankton Vary in Their Response to Chlorinated Hydrocarbons , 1970, Science.

[8]  E. Stoermer,et al.  Eutrophication, Silica Depletion, and Predicted Changes in Algal Quality in Lake Michigan , 1971, Science.

[9]  J. Ryther,et al.  Nitrogen, Phosphorus, and Eutrophication in the Coastal Marine Environment , 1971, Science.

[10]  J. Strickland A practical hand-book of seawater analysis , 1972 .

[11]  J. C. Goldman,et al.  Inorganic Nitrogen Removal from Wastewater: Effect on Phytoplankton Growth in Coastal Marine Waters , 1973, Science.

[12]  J. C. Goldman,et al.  Relative growth of different species of marine algae in wasterwater-seawater mixtures , 1974 .

[13]  D. R. Heinle,et al.  Carbon requirements of a population of the estuarine copepod Eurytemora affinis , 1975 .

[14]  M. Gilbert THE BEHAVIOUR AND FUNCTIONAL MORPHOLOGY OF DEPOSIT FEEDING IN MACOMA BALTHICA (LINNE, 1758), IN NEW ENGLAND , 1977 .

[15]  D. Tilman Resource Competition between Plankton Algae: An Experimental and Theoretical Approach , 1977 .

[16]  D. Planas,et al.  EFFECTS OF ARSENATE ON GROWTH AND PHOSPHORUS METABOLISM OF PHYTOPLANKTON 1, 2 , 1978 .

[17]  P. Harrison,et al.  An experimental simulation of changes in diatom and flagellate blooms , 1978 .

[18]  Paul J. Harrison,et al.  Limiting nutrient patchiness and its rôle in phytoplankton ecology , 1979 .

[19]  Professor Dr. Ulrich Förstner,et al.  Metal Pollution in the Aquatic Environment , 1979, Springer Berlin Heidelberg.

[20]  K. Bruland,et al.  Sampling and analytical methods for the determination of copper, cadmium, zinc, and nickel at the nanogram per liter level in sea water , 1979 .

[21]  J. B. Kenworthy,et al.  Metal Pollution in the Aquatic Environment , 1980, Springer Berlin Heidelberg.

[22]  W. Boynton,et al.  A COMPARATIVE ANALYSIS OF NUTRIENTS AND OTHER FACTORS INFLUENCING ESTUARINE PHYTOPLANKTON PRODUCTION , 1982 .

[23]  E. Paasche,et al.  On marine eutrophication , 1984 .

[24]  Timothy R. Parsons,et al.  A manual of chemical and biological methods for seawater analysis , 1984 .

[25]  R. S. Fulton Predation, production and the organization of an estuarine copepod community , 1984 .

[26]  S. Seitzinger,et al.  Eutrophication of a Coastal Marine Ecosystem — An Experimental Study Using the Merl Microcosms , 1984 .

[27]  R. Harvey,et al.  The role of bacterial exopolymer and suspended bacteria in the nutrition of the deposit-feeding clam, Macoma balthica , 1984 .

[28]  J. G. Sanders,et al.  Adaptive behavior of euryhaline phytoplankton communities to arsenic stress , 1985 .

[29]  R. Hodson,et al.  Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems , 1985, Applied and environmental microbiology.

[30]  Condenser replacement in a coastal power plant: Copper uptake and incorporation in the American oyster, Crassostrea virginica , 1986 .

[31]  R. Guillard,et al.  Reduction of marine phytoplankton reproduction rates by copper and cadmium , 1986 .

[32]  W. Boynton,et al.  Nutrient Enrichment Studies in a Coastal Plain Estuary: Phytoplankton Growth in Large-Scale, Continuous Cultures , 1986 .

[33]  R. Kneib The Role of Fundulus heteroclitus in Salt Marsh Trophic Dynamics , 1986 .

[34]  C. Oviatt,et al.  A comparison of system (02 and C02) and C-14 measurements of metabolism in estuarine mesocosms , 1986 .

[35]  E. Ólafsson DENSITY DEPENDENCE IN SUSPENSION-FEEDING AND DEPOSIT-FEEDING POPULATIONS OF THE BIVALVE MACOMA BALTHICA: A FIELD EXPERIMENT , 1986 .

[36]  W. Boynton,et al.  Nutrient Enrichment Studies in a Coastal Plain Estuary: Changes in Phytoplankton Species Composition , 1987 .

[37]  W. Broecker,et al.  Gas exchange on Mono Lake and Crowley Lake, California , 1987 .

[38]  B. Hansen,et al.  Food size spectra, ingestion and growth of the copepodAcartia tonsa during development: Implications for determination of copepod production , 1988 .

[39]  L. Ward,et al.  Phytoplankton, nutrients, and turbidity in the Chesapeake, Delaware, and Hudson estuaries , 1988 .

[40]  R. Howarth Nutrient Limitation of Net Primary Production in Marine Ecosystems , 1988 .

[41]  P. Jumars,et al.  Cross-phyletic patterns of particle selection by deposit feeders , 1988 .

[42]  R. Hecky,et al.  Nutrient limitation of phytoplankton in freshwater and marine environments: A review of recent evidence on the effects of enrichment1 , 1988 .

[43]  E. Ólafsson Contrasting influences of suspension-feeding and deposit-feeding populations of Macoma balthica on infaunal recruitment , 1989 .

[44]  C. Oviatt,et al.  Phytoplankton species and abundance in response to eutrophication in coastal marine mesocosms , 1989 .

[45]  C. Langdon,et al.  Comparative utilization of detritus and bacteria as food sources by two bivalve suspension-feeders, the Crassostrea virginica and the mussel, Geukensia demissa , 1989 .

[46]  M. Søndergaard,et al.  Carbon budgets of the microbial food web in estuarine enclosures , 1990 .

[47]  Hans Blanck,et al.  Arsenate sensitivity in marine periphyton communities established under various nutrient regimes , 1990 .

[48]  S. Williams,et al.  Coasts in crisis , 1990 .

[49]  M. P. Crosby,et al.  Bacterial mediation in the utilization of carbon and nitrogen from detrital complexes by Crassostrea virginica , 1990 .

[50]  J. Fuhrman,et al.  Mesoscale and seasonal variability of heterotrophic nanoflagellate abundance in an estuarine outflow plume , 1990 .

[51]  B. K. Sullivan,et al.  Food limitation and benthic regulation of populations of the copepod Acartia hudsonica Pinhey in nutrient‐limited and nutrient‐enriched systems , 1990 .

[52]  B. K. Sullivan,et al.  Growth of juvenile Atlantic menhaden, Brevoortia tyrannus (Pisces: Clupeidae) in MERL mesocosms: Effects of eutrophication , 1990 .

[53]  R. Newell,et al.  Omnivorous feeding by planktotrophic arvae of the eastern oyster Crassostrea virginica , 1991 .

[54]  C. Gallegos,et al.  Trophic coupling of rotifers, microflagellates, and bacteria during fall months in the Rhode River Estuary , 1991 .

[55]  T. Fisher Nutrient limitation of phytoplankton in Chesapeake Bay , 1992 .

[56]  Derek A. Roff,et al.  DISTRIBUTION-FREE AND ROBUST STATISTICAL METHODS: VIABLE ALTERNATIVES TO PARAMETRIC STATISTICS? , 1993 .

[57]  G. Riedel The annual cycle of arsenic in a temperate estuary , 1993 .

[58]  P. Doering,et al.  Net system production in coastal waters as a function of eutrophication, seasonality and benthic macrofaunal abundance , 1993 .

[59]  J. D. Jong,et al.  Sampling and Analytical Methods for the Determination of Trace Metals in Surface Seawater , 1994 .

[60]  A. Hines,et al.  Effects of suspended food availability on the feeding mode and burial depth of the Baltic clam, Macoma balthica , 1994 .

[61]  J. G. Baretta-Bekker,et al.  Testing the microbial loop concept by comparing mesocosm data with results from a dynamical simulation model , 1994 .

[62]  Robert M. Summers,et al.  Inputs, transformations, and transport of nitrogen and phosphorus in Chesapeake Bay and selected tributaries , 1995 .

[63]  R. Rosenberg,et al.  Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna , 1995 .

[64]  S. Carpenter,et al.  Species Compensation and Complementarity in Ecosystem Function , 1995 .

[65]  R. Riegman Nutrient-related selection mechanisms in marine phytoplankton communities and the impact of eutrophication on the planktonic food web , 1995 .

[66]  D. Hinrichsen,et al.  Coasts in Crisis , 1996 .

[67]  G. Bennett Arsenic in the environment — Part I: Cycling and characterization , 1996 .

[68]  D. Conley,et al.  Scales of nutrient-limited phytoplankton productivity in Chesapeake Bay , 1996 .

[69]  J. Cloern PHYTOPLANKTON BLOOM DYNAMICS IN COASTAL ECOSYSTEMS' A REVIEW WITH SOME GENERAL LESSONS FROM SUSTAINED INVESTIGATION OF SAN FRANCISCO , 1996 .

[70]  V. Kennedy,et al.  The Eastern Oyster: Crassostrea Virginica , 1996 .

[71]  D. Breitburg,et al.  VARYING EFFECTS OF LOW DISSOLVED OXYGEN ON TROPHIC INTERACTIONS IN AN ESTUARINE FOOD WEB , 1997 .

[72]  S. Gasparini,et al.  Autotrophic and heterotrophic nanoplankton in the diet of the estuarine copepods Eurytemora affinis and Acartia bifilosa , 1997 .

[73]  S. F. Umani,et al.  The paradox of diatom-copepod interactions* , 1997 .

[74]  J. G. Sanders,et al.  Metal accumulation and impacts in phytoplankton , 1998 .

[75]  Charles H. Peterson,et al.  The influence of multiple environmental stressors on susceptibility to parasites: An experimental determination with oysters , 1999 .

[76]  M. Moore,et al.  Synergism and antagonism among multiple stressors , 1999 .