JEP  Vol.3 No.4 , April 2012
The Response of Benthic Foraminiferal Assemblages to Copper Exposure: A Pilot Mesocosm Investigation
Abstract: Controlled experiments, including mesocosms and laboratory cultures, are used to identify a potential speci?c cause- effect relationship that has been previously inferred in field studies. In this study, a series of mesocosm experiments are carried out to assess the impact of different concentrations of copper on benthic foraminiferal assemblages over time. This pilot investigation documents that Cu contamination has a detrimental effect on foraminifera when compared to original and control samples. In particular, increased concentrations of Cu (normally higher than 120 μg/l) lead to a lowering of foraminiferal density and diversity and an increased occurrence of abnormalities. This study thus supports that the use of an experimental approach is suitable for investigating the response of benthic foraminifera to stress including pollution. Moreover, the application of mesocosms represents an innovative tool to be placed alongside field studies and culture experiments.
Cite this paper: F. Fabrizio and C. Rodolfo, "The Response of Benthic Foraminiferal Assemblages to Copper Exposure: A Pilot Mesocosm Investigation," Journal of Environmental Protection, Vol. 3 No. 4, 2012, pp. 342-352. doi: 10.4236/jep.2012.34044.

[1]   J. W. Murray, “Ecology and Paleoecology of Benthic Foraminifera,” Longman, Harlow, 1991.

[2]   E. Alve, “Benthic Foraminifera Response to Estuarine Pollution: A Review,” Journal of Foraminiferal Research, Vol. 25, No. 3, 1995, pp. 190-203. doi:10.2113/gsjfr.25.3.190

[3]   V. Yanko, A. J. Arnold and W. C. Parker, “Effects of Marine Pollution on Benthic Foraminifera,” In: B. K. Sen Gupta, Ed., Modern Foraminifera, Kluwer Academic Publisher, Dordrecht, 1999, pp. 217-235.

[4]   R. Coccioni, “Benthic Foraminifera as Bioindicators of Heavy Metal Pollution—A Case Study from the Goro Lagoon (Italy),” In: R. E. Martin, Ed., Environmental Micropaleontology: The Application of Microfossils to Environmental Geology, Kluwer Academic/Plenum Pub- lishers, New York, 2000, pp. 71-103.

[5]   E. Armynot du Chatelet and J.P. Debenay, “Anthropo- genic Impact on the Western French Coast as Revealed by Foraminifera: A Review,” Revue de Micropaléontolo- gie, Vol. 53, No. 3, 2010, pp. 129-137. doi:10.1016/j.revmic.2009.11.002

[6]   F. Frontalini and R. Coccioni, R., “Benthic Foraminifera as Bioindicators of Pollution: A Review of Italian Re- search over the Last Three Decades,” Revue de Micro- paléontologie, Vol. 54, No. 2, 2011, pp. 115-127. doi:10.1016/j.revmic.2011.03.001

[7]   F. Frontalini, C. Buosi, S. Da Pelo, R. Coccioni, A. Cherchi and C. Bucci, “Benthic Foraminifera as Bio-Indicators of Trace Element Pollution in the Heavily Contaminated Santa Gilla Lagoon (Cagliari, Italy),” Marine Pollution Bulletin, Vol. 58, No. 6, 2009, pp. 858-877. doi:10.1016/j.marpolbul.2009.01.015

[8]   E. Geslin, J. P. Debenay and M. Lesourd, “Abnormal Wall Textures and Test Deformation in Ammonia (Hya- line Foraminifer),” Journal of Foraminiferal Research, Vol. 28, No. 2, 1998, pp. 148-156.

[9]   J. W. Murray, “Ecology and Applications of Benthic Foraminifera”, Cambridge University Press, Cambridge, 2006.

[10]   R. Nigam, R. Saraswat and R. Panchang, “Application of Foraminifers in Ecotoxicology: Retrospect, Perspect and Prospect,” Environmental International, Vol. 32, No. 2, 2006, pp. 273-283. doi:10.1016/j.envint.2005.08.024

[11]   O. Gross, “Influence of Temperature, Oxygen and Food Availabilityon the Migrational Activity of Bathyal Ben- thic Foraminifera: Evidence of Microcosm Experiments,” Hydrobiologia, Vol. 426, No. 1, 2000, pp. 123-137. doi:10.1023/A:1003930831220

[12]   M. Gustafsson, I. Dahllof, H. Blanck, P. Hall, S. Mo- -lander and K. Nordberg, “Benthic Foraminiferal Toler- ance to Tri-n-Butyltin (TBT) Pollution in an Experimen- tal Mesocosm,” Marine Pollution Bulletin, Vol. 40, No. 12, 2000, pp. 1072-1075. doi:10.1016/S0025-326X(00)00048-5

[13]   P. Heinz, H. Kitazato, G. Schmiedl and C. Hemleben, “Response of Deep-Sea Benthic Foraminifera from the Mediterranean Sea to Simulated Phytoplankton Pulses un- der Laboratory Conditions,” Journal of Foraminiferal Re- search, Vol. 31, No. 3, 2001, pp. 210-227. doi:10.2113/31.3.210

[14]   P. Heinz, C. Hemleben and H. Kitazato, “Time-Response of Cultured Deep-Sea Benthic Foraminifera to Different Algal Diets,” Deep Sea Research I, Vol. 49, No. 3, 2002, pp. 517-537. doi:10.1016/S0967-0637(01)00070-X

[15]   I. A. P. Duijnstee, S. R. Ernst and G. J. Van der Zwaan, “The Effect of Anoxia on the Vertical Migration of Ben- thic Foraminifera,” Marine Ecology Progress Series, Vol. 246, 2003, pp. 85-94. doi:10.3354/meps246085

[16]   S. R. Ernst, I. A. P. Duijnstee and G. J. Van der Zwaan, “The Dynamics of the Benthic Foraminiferal Microhabi- tat: Recovery after Experimental Disturbance,” Marine Micropaleontology, Vol. 46, No. 3-4, 2002, pp. 343-361. doi:10.1016/S0377-8398(02)00080-4

[17]   S. R. Ernst, R. Bours, I. A. P. Duijnstee and G. J. Van der Zwaan, “Experimental Effects of an Organic Matter Pulse and Oxygen Depletion on a Benthic Foraminiferal Shelf Community,” Journal of Foraminiferal Research, Vol. 35, No. 3, 2005, pp. 177-197. doi:10.2113/35.3.177

[18]   S. R. Ernst, J. Morvan, E. Geslin, A. Le Bihan and F. J. Jorissen, “Benthic Foraminiferal Response to Experi- mentally Induced Erika Oil Pollution,” Marine Micro- paleontology, Vol. 61, No. 1-3, 2006, pp. 76-93. doi:10.1016/j.marmicro.2006.05.005

[19]   J. N. Topping, J. W. Murray and D. W. Pond, “Sewage Effects on the Food Sources and Diet of Benthic Fo- raminifera Living in Oxic Experiment: A Microcosm Ex- periment,” Journal of Experimental Marine Biology and Ecology, Vol. 329, No. 2, 2006, pp. 239-250. doi:10.1016/j.jembe.2005.09.013

[20]   E. Alve and F. Olsgard, “Benthic Foraminiferal Coloniza- tion in Experiments with Copper-Contaminated Sedi- ments,” Journal of Foraminiferal Research, Vol. 29, No. 3, 1999, pp. 186-195.

[21]   M. J. Kennish, “Ecology of Estuaries: Anthropogenic Ef- fects,” CRC Press Inc., Boca Raton, 1992.

[22]   M. C. Austen and P. J. Somerfield, “A Community Level Sediment Bioassay Applied to an Estuarine Heavy Metal Gradient,” Marine Environmental Research, Vol. 43, No. 4, 1997, pp. 315-328. doi:10.1016/S0141-1136(96)00094-3

[23]   G. W. Bryan and W. J. Langston, “Bioavailability, Accumulation and Effects of Heavy Metals in Sediments with Special Reference to United Kingdom Estuaries—A Review,” Environmental Pollution, Vol. 76, No. 2, 1992, pp. 89-131. doi:10.1016/0269-7491(92)90099-V

[24]   E. R. Long, D. D. MacDonald, S. L. Smith and F. D. Calder, “Incidence of Adverse Biological Effects within Ranges of Chemical Concentrations in Marine and Estua- rine Sediments,” Environmental Management, Vol. 19, No. 1, 1995, pp. 81-97. doi:10.1007/BF02472006

[25]   F. Frontalini and R. Coccioni, “Benthic Foraminifera for Heavy Metal Pollution Monitoring: A Case Study from the Central Adriatic Sea Coast of Italy,” Estuarine Coastal and Shelf Science, Vol. 76, No. 20, 2008, pp. 404-417. doi:10.1016/j.ecss.2007.07.024

[26]   F. Frontalini, F. Semprucci, R. Coccioni, M. Balsamo, P. Bittoni and A. Covazzi-Harriage, “On the Quantitative Distribution and Community Structure of the Meio and Macrofaunal Communities in the Coastal Area of the Central Adriatic Sea (Italy),” Environmental Monitoring Assessment, Vol. 180, No. 1-4, 2011, pp. 325-344. doi:10.1007/s10661-010-1791-y

[27]   Activation Laboratories Ltd., Ontario, Canada,

[28]   S. R. Ernst and B. van der Zwaan, “Effects of Experi- mentally Induced Raised Levels of Organic Flux and Oxygen Depletion on a Continental Slope Benthic Fo- raminiferal Community,” Deep Sea Research I, Vol. 51, No. 11, 2004, pp. 1709-1739. doi:10.1016/j.dsr.2004.06.003

[29]   W. R. Walton, “Techniques for Recognition of Living Foraminifera,” Contribution of Cushman. Foundation Fo- raminiferal Research, Vol. 3, 1952, pp. 56-60.

[30]   H. C. De Stigter, F. J. Jorissen and G. J. Van der Zwaan, “Bathymetric Distribution and Microhabitat Partitioning of live (Rose Bengal Stained) Benthic Foraminifera along a Shelf to Deep Sea Transect in the Southern Adriatic Sea,” Journal of Foraminiferal Research, Vol. 28, No. 1, 1998, pp. 40-65.

[31]   F. Cimerman and M. R. Langer, “Mediterranean Fo- raminifera,” Slovenska Akademija Znanosti in Umetnosti, Ljubljana, 1991.

[32]   A. R. Loeblich Jr. and H Tappan, “Foraminiferal Genera and Their Classification,” Van Reinhold Company, New York, 1987.

[33]   R. Coccioni, F. Frontalini, A. Marsili and D. Mana, “Benthic Foraminifera and Trace Element Distribution: A Case-Study from the Heavily Polluted Lagoon of Venice (Italy),” Marine Pollution Bulletin, Vol. 59, No. 8-12, 2009, pp. 257-267. doi:10.1016/j.marpolbul.2009.08.009

[34]   G. A. Seiglie “Foraminifers of Guayanilla Bay and Their Use as Environmental Indicators,” Revista Espanola de Micropaleontologia, Vol. 7, No. 3, 1975, pp. 453-487.

[35]   F. J. Jorissen, “Benthic Foraminifera from the Adriatic Sea: Principles of Phenotypic Variation,” Utrecht Micro- paleontological Bulletin, Vol. 37, 1988, pp. 1-174.

[36]   V. Stouff, E. Geslin, J. P. Debenay and M. Lesourd, “Origin of Morphological Abnormalities in Ammonia (Foraminifera): Studies in Laboratory and Natural Envi- ronments,” Journal of Foraminiferal Research, Vol. 29, No. 2, 1999, 152-170.

[37]   J. Morvan, J., V. Le Cadre, F. J. Jorissen and J. P. De- benay, “Foraminifera as Potential Bio-Indicators of the ‘Erika’ Oil Spill in the Bay of Bourgneuf: Field and Ex- perimental Studies,” Aquatic Living Resources, Vol. 17, No. 3, 2004, pp. 317-322. doi:10.1051/alr:2004034

[38]   E. Armynot du Chatelet, J. P. Debenay and R. Soulard, “Foraminiferal Proxies for Pollution Monitoring in Mod- erately Polluted Harbours,” Environmental Pollution, Vol. 127, No. 1, 2004, pp. 27-40. doi:10.1016/S0269-7491(03)00256-2

[39]   V. Yanko, J. Kronfeld and A. Flexer, “Response of Ben- thic Foraminifera to Various Pollution Sources: Implica- tions for Pollution Monitoring,” Journal of Foraminiferal Research, Vol. 24, No. 1, 1994, 1-17. doi:10.2113/gsjfr.24.1.1

[40]   A. V. Fursenko, “Introduction to the Study of Foraminif- era” in Russian, Nauka, Novosibirsk, 1978.

[41]   V. Le Cadre and J. P. Debenay, “Morphological and Cy- tological Responses of Ammonia (foraminifera) to Copper Contamination: Implication for the Use of Foraminifera as Bioindicators of Pollution,” Environmental Pollution, Vol. 143, No. 2, 2006, pp. 304-317. doi:10.1016/j.envpol.2005.11.033

[42]   A. R. Sharifi, I. W. Crondace and R. L. Austin, “Benthic Foraminiferids as Pollution Indicators in Southampton Water, Southern England, UK,” Journal of Micropaleon- tology, Vol. 10, No. 1, 1991, pp. 109-113. doi:10.1144/jm.10.1.109

[43]   D. Munsel, U. Kramar, D. Dissard, G. Nehrke, Z. Berner, J. Bijma, G.-J. Reichart and T. Neumann, “Heavy Metal Uptake in Foraminiferal Calcite: Results of Multi-Element Culture Experiments,” Biogeosciences Discussion, Vol. 7, No. 1, 2010, pp. 953-977. doi:10.5194/bgd-7-953-2010

[44]   L. J. de Nooijer, G. J. Reichart, A. Duenas-Bohòrquez, M. Wolthers, S. R., Ernst, P. R. D. Mason and G. J. van der Zwaan, “Copper Incorporation in Foraminiferal Calcite: Results from Culturing Experiments,” Biogeosciences, Vol. 4, No. 4, 2007, pp. 493-504. doi:10.5194/bg-4-493-2007

[45]   R. Saraswat, S. R. Kurtarkar, A. Mazumder and N. Ni- gam, “Foraminifers as Indicators of Marine Pollution: A Culture Experiment with Rosalina leei,” Marine Pollution Bulletin, Vol. 48, No. 1-2, 2004, pp. 91-96. doi:10.1016/S0025-326X(03)00330-8

[46]   N. Nigam, V. N. Linshy, S. R. Kurtarkar and R. Saraswat, “Effects of Sudden Stress due to Heavy Metal Mercury on Benthic Foraminifer Rosalina leei: Laboratory Culture Experiment,” Marine Pollution Bulletin, Vol. 59, No. 8- 12, 2009, pp. 362-368. doi:10.1016/j.marpolbul.2009.08.014

[47]   B. J. McCloskey, “Foraminiferal Responses to Arsenic in a Shallow-Water Hydrothermal System in Papua New Guinea and in the Laboratory,” Ph.D. Thesis, University of South Florida, Tampa, 2009.

[48]   M. R. Lee and J. A. Correa, “An Assessment of the Im- pact of Copper Mine Tailings Disposal on Meiofaunal Assemblages Using Microcosm Bioassays,” Marine En- vironmental Research, Vol. 64, No. 1, 2007, pp. 1-20. doi:10.1016/j.marenvres.2006.11.001

[49]   E. His, I. Heyvang, O. Geffard and X. De Montaudouin, “A Comparison between Oyster (Crassostrea gigas) and Sea Urchin (Paracentrotus lividus) Larval Bioassays for Toxicological Studies,” Water Research, Vol. 33, No. 7, 1999, pp. 1706-1718. doi:10.1016/S0043-1354(98)00381-9

[50]   E. Alve, A. Lepland, J. Magnusson and K. Backer-Owe, “Monitoring Strategies for Re-Establishment of Ecologi- cal Reference Conditions: Possibilities and Limitations,” Marine Pollution Bulletin, Vol. 59, No. 8-12, 2009, pp. 297-310. doi:10.1016/j.marpolbul.2009.08.011