Inferring chemical effects on carbon flows in aquatic food webs: methodology and case study.

The majority of ecotoxicological enclosure experiments monitor species abundances at different chemical concentrations. Here, we present a new modelling approach that estimates changes in food web flows from such data and show that population- and food web level effects are revealed that are not apparent from abundance data alone. For the case of cypermethrin in freshwater enclosures, photosynthesis and excretion (d(-1)) of phytoplankton at 3.643 microg L(-1) cypermethrin were 30% lower and 100% higher than in the control, respectively. The ingestion rate of mesozooplankton (d(-1)) was 6 times higher in the treated enclosures than in the control as food concentration increased with insecticide exposure. With increasing cypermethrin concentrations, nanoflagellates progressively relied on phytoplankton as their main food source, which rendered the food web less stable. We conclude that this tool has excellent potential to analyse the wealth of enclosure data as it only needs species abundance and general constraints.

[1]  Wen-Xiong Wang,et al.  Stoichiometric regulation of carbon and phosphorus in P‐deficient Daphnia magna , 2008 .

[2]  M. R. Droop,et al.  The nutrient status of algal cells in continuous culture , 1974, Journal of the Marine Biological Association of the United Kingdom.

[3]  G. Bratbak,et al.  Viral lysis of Phaeocystis pouchetii and bacterial secondary production , 1998 .

[4]  I. R. Hill Effects on non-target organisms in terrestrial and aquatic environments , 1985 .

[5]  A. Heiskanen,et al.  Carbon flow patterns in the planktonic food web of the Gulf of Riga, the Baltic Sea: a reconstruction by the inverse method , 1999 .

[6]  Ulrich Sommer,et al.  The PEG-model of seasonal succession of planktonic events in fresh waters , 1986, Archiv für Hydrobiologie.

[7]  K. Tjessem,et al.  Effects of Ekofisk crude oil on an enclosed planktonic ecosystem , 1983 .

[8]  L. Wendt-Rasch,et al.  Effects of the pyrethroid insecticide cypermethrin on a freshwater community studied under field conditions. II. Direct and indirect effects on the species composition. , 2003, Aquatic toxicology.

[9]  Weichun Yang,et al.  Effects of dissolved organic matter on permethrin bioavailability to Daphnia species. , 2006, Journal of agricultural and food chemistry.

[10]  J. Salminen,et al.  Interaction modification among decomposers impairs ecosystem processes in lead‐polluted soil , 2002, Environmental toxicology and chemistry.

[11]  M. DeLorenzo,et al.  Toxicity of pesticides to aquatic microorganisms: A review , 2001, Environmental toxicology and chemistry.

[12]  Karline Soetaert,et al.  Package limSolve , solving linear inverse models in R , 2009 .

[13]  O. Klepper,et al.  The use of mass balances to test and improve the estimates of carbon fluxes in an ecosystem , 1987 .

[14]  E. Odum Fundamentals of ecology , 1972 .

[15]  K. Porter,et al.  Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community , 1989 .

[16]  Donald S. Cherry,et al.  The influence of copper exposure on predator-prey interactions in aquatic insect communities , 1989 .

[17]  I. R. Hill Aquatic organisms and pyrethroids , 1989 .

[18]  O. Lindén,et al.  Bioenergetic responses of Gammarus salinus and Mytilus edulis to oil and oil dispersants in a model ecosystem , 1984 .

[19]  C. Karman,et al.  The variation in slope of concentration-effect relationships. , 2001, Ecotoxicology and environmental safety.

[20]  Robert W. Sterner,et al.  Elemental Stoichiometry of Species in Ecosystems , 1995 .

[21]  D. Baird,et al.  Effects of cypermethrin on marine plankton communities: a simulated field study using mesocosms. , 2004, Ecotoxicology and environmental safety.

[22]  D. O. Hessen,et al.  Allocation strategies in crustacean stoichiometry: the potential role of phosphorus in the limitation of reproduction , 2003 .

[23]  J. Finn,et al.  Measures of ecosystem structure and function derived from analysis of flows. , 1976, Journal of theoretical biology.

[24]  Thomas R Anderson,et al.  Metabolic Stoichiometry and the Fate of Excess Carbon and Nutrients in Consumers , 2004, The American Naturalist.

[25]  Karline Soetaert,et al.  Are network indices robust indicators of food web functioning? A Monte Carlo approach , 2009 .

[26]  P. Vanrolleghem,et al.  Validation of an ecosystem modelling approach as a tool for ecological effect assessments. , 2008, Chemosphere.

[27]  P. Vanrolleghem,et al.  Is ecosystem structure the target of concern in ecological effect assessments? , 2008, Water research.

[28]  D. Kirchman Microbial ecology of the oceans , 2008 .

[29]  T. Lauridsen,et al.  A comparison of feeding efficiency and swimming ability of Daphnia magna exposed to cypermethrin. , 2005, Aquatic toxicology.

[30]  B. Riemann,et al.  The carbon and chlorophyll content of phytoplankton from various nutrient regimes , 1989 .

[31]  T. R. Anderson,et al.  Does excess carbon affect respiration of the rotifer Brachionus calyciflorus Pallas , 2006 .

[32]  A. Fliedner,et al.  Effects of lindane on the planktonic community in freshwater microcosms. , 1996, Ecotoxicology and environmental safety.

[33]  P. Vanrolleghem,et al.  An ecosystem modelling approach for deriving water quality criteria. , 2007, Water science and technology : a journal of the International Association on Water Pollution Research.

[34]  Weichun Yang,et al.  Inhibition of aquatic toxicity of pyrethroid insecticides by suspended sediment , 2006, Environmental toxicology and chemistry.

[35]  Robert E. ULANOWlCZ,et al.  Symmetrical overhead in flow networks , 1990 .

[36]  T. Platt,et al.  Food web dynamics in the ocean. I. Best-estimates of flow networks using inverse methods , 1988 .

[37]  L. Wendt-Rasch,et al.  Effects of the pyrethroid insecticide, cypermethrin, on a freshwater community studied under field conditions. I. Direct and indirect effects on abundance measures of organisms at different trophic levels. , 2003, Aquatic toxicology.

[38]  Theo P Traas,et al.  A freshwater food web model for the combined effects of nutrients and insecticide stress and subsequent recovery , 2004, Environmental toxicology and chemistry.

[39]  K. Solomon,et al.  Impact of Fenvalerate on Enclosed Freshwater Planktonic Communities and on in situ Rates of Filtration of Zooplankton , 1987 .

[40]  R. Relyea,et al.  Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. , 2006, Ecology letters.

[41]  D. Baird,et al.  Age- and Sex-Related Variation in Sensitivity to the Pyrethroid Cypermethrin in the Marine Copepod Acartia tonsa Dana , 2002, Archives of environmental contamination and toxicology.

[42]  Stefano Allesina,et al.  Cycling in ecological networks: Finn's index revisited , 2004, Comput. Biol. Chem..

[43]  R. Roijackers,et al.  Effects of nutrient loading and insecticide application on the ecology of Elodea-dominated freshwater microcosms. II. Responses of macrophytes, periphyton and macroinvertebrate grazers. , 1995 .

[44]  C. Heip,et al.  Carbon‐nitrogen coupling and algal‐bacterial interactions during an experimental bloom: Modeling a 13C tracer experiment , 2004 .

[45]  B. Finlay,et al.  Freshwater protozoa: biodiversity and ecological function , 1998, Biodiversity & Conservation.

[46]  K. Solomon,et al.  Probabilistic risk assessment of cotton pyrethroids: I. Distributional analyses of laboratory aquatic toxicity data , 2001, Environmental toxicology and chemistry.

[47]  E. Sherr,et al.  Bacterivory and herbivory: Key roles of phagotrophic protists in pelagic food webs , 1994, Microbial Ecology.

[48]  P. K. Bjørnsen Automatic Determination of Bacterioplankton Biomass by Image Analysis , 1986, Applied and environmental microbiology.

[49]  J. Rasmussen,et al.  A Trophic Position Model of Pelagic Food Webs: Impact on Contaminant Bioaccumulation in Lake Trout , 1996 .

[50]  D. Baird,et al.  Determining Demographic Effects of Cypermethrin in the Marine Copepod Acartia tonsa: Stage-Specific Short Tests Versus Life-Table Tests , 2002, Archives of environmental contamination and toxicology.

[51]  N. Kautsky,et al.  Does cadmium pollution change trophic interactions in rockpool food webs? , 1997 .

[52]  Wataru Naito,et al.  Evaluation of an ecosystem model in ecological risk assessment of chemicals. , 2003, Chemosphere.

[53]  Michel Loreau,et al.  Food-web constraints on biodiversity–ecosystem functioning relationships , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[54]  D. Oevelen,et al.  Modeling food web interactions in benthic deep-sea ecosystems. A practical guide , 2009 .

[55]  Karline Soetaert,et al.  xsample(): An R Function for Sampling Linear Inverse Problems , 2009 .

[56]  M. Kawachi,et al.  Effect of the water-soluble fraction of diesel oil on bacterial and primary production and the trophic transfer to mesozooplankton through a microbial food web in Yangtze estuary, China , 2007 .

[57]  M. Perry,et al.  Closing the microbial loop: dissolved carbon pathway to heterotrophic bacteria from incomplete ingestion, digestion and absorption in animals , 1989 .

[58]  T. Nagata Production mechanisms of dissolved organic matter , 2000 .

[59]  J. Lawton,et al.  Linking Species and Ecosystems. , 1997 .

[60]  M. Søndergaard,et al.  Potential role of fish predation and natural populations of zooplankton in structuring a plankton community in eutrophic lake water , 1993 .

[61]  P. K. Bjørnsen,et al.  Zooplankton grazing and growth: Scaling within the 2‐2,‐μm body size range , 1997 .

[62]  Carlo H. R. Heip,et al.  Carbon flows through a benthic food web: Integrating biomass, isotope and tracer data , 2006 .

[63]  K. Solomon,et al.  Impact of Permethrin on Zooplankton Communities in Limnocorrals , 1985 .

[64]  M. J. Barry,et al.  The use of temporary pond microcosms for aquatic toxicity testing: direct and indirect effects of endosulfan on community structure , 1998 .

[65]  U. Sommer,et al.  Zooplankton interactions in an enclosure experiment: insights from stable isotope analyses , 2004 .

[66]  G. Jackson,et al.  Food web analysis of a planktonic system off Southern California , 1992 .

[67]  Karline Soetaert,et al.  Incorporating ecological data and associated uncertainty in bioaccumulation modeling: methodology development and case study. , 2009, Environmental science & technology.

[68]  Colin R. Janssen,et al.  Comparing ecotoxicological effect concentrations of chemicals established in multi-species vs. single-species toxicity test systems. , 2009, Ecotoxicology and environmental safety.

[69]  J. Svensson,et al.  Effects of the pesticides captan, deltamethrin, isoproturon, and pirimicarb on the microbial community of a freshwater sediment , 2004, Environmental toxicology and chemistry.

[70]  A. Lindskog,et al.  Effects of oil and oil dispersant on an enclosed marine ecosystem. , 1987, Environmental science & technology.

[71]  A. Sih,et al.  Community ecology as a framework for predicting contaminant effects. , 2006, Trends in ecology & evolution.

[72]  R. Wetzel Gradient-dominated ecosystems: sources and regulatory functions of dissolved organic matter in freshwater ecosystems , 1992 .

[73]  B. Finlay,et al.  Protozoan control of bacterial abundances in freshwater. , 1991 .

[74]  Connie Wagner,et al.  Estimation of ecotoxicological protection levels from NOEC toxicity data , 1991 .

[75]  J. Leahey The pyrethroid insecticides. , 1985 .

[76]  Theo Vermeire,et al.  Risk assessment of chemicals : an introduction , 2007 .

[77]  Carl J. Walters,et al.  Ecopath, Ecosim, and Ecospace as tools for evaluating ecosystem impact of fisheries , 2000 .