Skip to main content
SpringerLink
Log in

Metal biomonitoring in a Patagonian salt marsh

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

Patagonian salt marshes are not affected by pollution, but historical mining wastes are a continuous source of metals to salt marsh in San Antonio Bay. The present study evaluated the concentration of metals in sediments and used the halophyte Spartina spp. and the crab N. granulata as biomonitors. The levels of metals in sediment and organisms in SAB remained at levels corresponding to a slight enrichment or contamination. The highest levels corresponded to innermost sites of the Encerrado channel and close to the mining wastes. Spartina is a phytostabilizer so its aboveground tissues do not reflect the concentrations in the sediment; although, it retains the metals in its belowground tissues and in the rhizosediment. N. granulata showed to be a useful biomonitor for Pb, but not for the other metals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Almeida, C. M. R., Mucha, A. P., & Vasconcelos, M. T. (2011). Role of different salt marsh plants on metal retention in an urban estuary (Lima estuary, NW Portugal). Estuarine, Coastal and Shelf Science, 91, 243–249.

    Article  CAS  Google Scholar 

  • AOAC. (1995). Official methods of analyses of Association of Analytical Chemist (16th ed.). DC: Washington.

    Google Scholar 

  • Barron, M.G. (2002) Chapter 32: Bioaccumulation and bioconcentration in aquatic organisms. In: Hoffman DJ et al. (Eds.), Handbook of ecotoxicology 2nd ed. Boca Raton London New York Washington, D.C.

  • Beltrame, M. O., De Marco, S. G., & Marcovecchio, E. J. (2011). The burrowing crab Neohelice granulata as potential bioindicator of heavy metals in estuarine systems of the Atlantic coast of Argentina. Environmental Monitoring and Assessment, 172, 379–389.

    Article  CAS  Google Scholar 

  • BOE. (1991). Normas microbiológicas, límites de contenido en metales pesados y métodos analíticos para su determinación en los productos de la pesca y acuicultura con destino al consumo humano. Boletín Oficial del Estado, España, 195, 5937–5941.

    Google Scholar 

  • Bonanno, G., & Lo Giudice, R. (2010). Heavy metal bioaccumulation by the organs of Phragmites australis (common reed) and their potential use as contamination indicators. Ecological Indicators, 10, 639–645.

    Article  CAS  Google Scholar 

  • Brown, C. E., Pezeshki, S. R., & De Laune, R. D. (2006). The effects of salinity and soil drying on nutrient uptake and growth of Spartina alterniflora in a simulated tidal system. Environmental and Experimental Botany, 58, 140–148.

    Article  CAS  Google Scholar 

  • Burke, D. J., Weis, J. S., & Weis, P. (2000). Release of metals by the leaves of the salt marsh grasses Spartina alterniflora and Phragmites australis. Estuarine, coastal and Shelf Science, 51, 153–159.

    Article  CAS  Google Scholar 

  • Byers, S. C., Mills, E. L., & Stewart, P. L. (1978). A comparison of methods of determining organic carbon in marine sediments, with suggestions for a standard method. Hydrobiologia, 58(1), 43–47.

    Article  CAS  Google Scholar 

  • Cambrollé, J., Redondo-Gómez, S., Mateos-Naranjo, E., & Figueroa, M. E. (2008). Comparison of the role of two Spartina species in terms of phytostabilization and bioaccumulation of metals in the estuarine sediment. Marine Pollution Bulletin, 56, 2037–2042.

    Article  Google Scholar 

  • Cambrollé, J., Mateos-Naranjo, E., Redondo-Gómez, S., Luque, T., & Figueroa, M. E. (2011). The role of two Spartina species in phytostabilization and bioaccumulation of Co, Cr, and Ni in the Tinto-Odiel estuary (SW Spain). Hydrobiologia, 671, 95–103.

    Article  Google Scholar 

  • CCME (2001a). Canadian Council of Ministers of the Environment. Canadian sediment quality guidelines for the protection of aquatic life: Introduction. Updated. In: Canadian environmental quality guidelines, 1999, Canadian Council of Ministers of the Environment, Winnipeg.

  • CCME (2001b). Canadian Council of ministers of the Environment [online] http://www.ccme.ca/en/resources/canadian_environmental_quality_guidelines. Access Feb 2017.

  • Conover, W. J. (1999). Practical nonparametric statistics. New York: John Wiley y Sons.

    Google Scholar 

  • Di Rienzo, J. A., Casanoves, F., Balzarini, M. G., Gonzalez, L., Tablada, M., & Robledo, C. W. (2008). InfoStat, versión 2008. Grupo InfoStat: FCA, Universidad Nacional de Córdoba, Argentina.

    Google Scholar 

  • Duarte, B., Almeida, P. R., & Caçador, I. (2009). Spartina maritima (cordgrass) rhizosediment extracellular enzymatic activity and its role in organic matter decomposition processes and metal speciation. Marine Ecology, 30(1), 65–73.

    Article  Google Scholar 

  • Duarte, B., Caetano, M., Almeida, P. R., Vale, C., & Caçador, I. (2010). Accumulation and biological cycling of heavy metal in four salt marsh species, from Tagus estuary (Portugal). Environmental Pollution, 158, 1661–1668.

    Article  CAS  Google Scholar 

  • Escofet, A. M., Orensanz, J. M., Olivier, S., & Scarabino, V. (1978). Biocenología bentónica del golfo San Matías (Río Negro, Argentina): metodología, experiencias y resultados del estudio ecológico de un gran espacio geográfico en América Latina. An Inst Cienc Mar Limnol Univ Autón Méx, 5, 59–82.

    Google Scholar 

  • Feng, H., Qian, Y., Kirk Cochran, J., Zhu, Q., Hu, W., Yan, H., et al. (2017). Nanoscale measurement of trace element distributions in Spartina alterniflora root tissue during dormancy. Scientific Reports, 7, 40420.

    Article  CAS  Google Scholar 

  • Ferrer, L. (2001). Tesis Doctoral: Estudio de diversos metales pesados en sedimentos del estuario de Bahía Blanca y sus efectos tóxicos sobre el cangrejo Chasmagnathus granulata. Universidad Nacional del Sur 212 pp.

  • Ferrer, L., Andrade, S., Asteasuain, R., & Marcovecchio, J. (2006). Acute toxicities of four metals on the early life stages of the crab Chasmagnathus granulata from Bahía Blanca estuary, Argentina. Ecotoxicology and Environmental Safety, 65, 209–217.

    Article  CAS  Google Scholar 

  • Fucks, E. E., Scalise, A. H., & Schnack, E. J. (2011). Evaluación de alternativas para la conservación y manejo del frente costero en Las Grutas, Río Negro. Informe Final. Provincia de Rio Negro y Consejo Federal de Inversiones. Pp 15–26.

  • Giarratano, E., Gil, M. N., Marinho, C. H., & Malanga, G. (2016). Metal from mine waste as potential cause of oxidative stress in burrowing crab Neohelice granulata from San Antonio bay. Ecotoxicology and Environmental Safety, 132, 68–76.

    Article  CAS  Google Scholar 

  • Gibbons, R. D., & Coleman, D. E. (2001). Statistical methods for detection and quantification of environmental contamination (p. 139). New York: John Willey & Sons.

    Google Scholar 

  • Gil, M. N., Torres, A., Harvey, M., & Esteves, J. L. (2006). Metales pesados en organismos marinos de la zona costera de la Patagonia Argentina Continental. Revista de Biología Marina y Oceanografía, 41(2), 167–176.

    Article  Google Scholar 

  • Hänsch, R., & Mendel, R. R. (2009). Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Current Opinion in Plant Biology, 12, 259–266.

    Article  Google Scholar 

  • Hempel, M., Botté, S. E., Negrin, V. L., Chiarello, M. N., & Marcovecchio, J. E. (2008). The role of the smooth cordgrass Spartina alterniflora and associated sediments in the heavy metal biogeochemical cycle within Bahía Blanca estuary salt marshes. Journal of Soils and Sediments, 8, 289–297.

    Article  CAS  Google Scholar 

  • Henry, R. P., Lucu, C., Onken, H., & Weihrauch, D. (2012). Multiple functions of the crustacean gill: osmotic/ionic regulation, acid-base balance, ammonia excretion, and bioaccumulation of toxic metals. Frontiers in Physiology, 3, 431.

    Article  CAS  Google Scholar 

  • Idaszkin, Y. L., Bouza, P. J., Marinho, C. H., & Gil, M. N. (2014). Trace metal concentrations in Spartina densiflora and associated soil from a Patagonian salt marsh. Marine Pollution Bulletin, 89, 444–450.

    Article  CAS  Google Scholar 

  • Idaszkin, Y. L., Lancelotti, J. L., Bouza, P. J., & Marcovecchio, J. E. (2015). Accumulation and distribution of trace metals within soils and the austral cordgrass Spartina densiflora in a Patagonian salt marsh. Marine Pollution Bulletin, 101(1), 457–465.

    Article  CAS  Google Scholar 

  • Idaszkin, Y. L., Lancelotti, J. L., Pollicelli, M. P., Marcovecchio, J., & Bouza, P. (2017). Comparison of phytoremediation potential capacity of Spartina densiflora and Sarcocornia perennis for metal polluted soils. Marine Pollution Bulletin, 118, 297–306.

    Article  CAS  Google Scholar 

  • Isacch, J. P., Costa, C. S. B., Rodríguez-Gallego, L., Conde, D., Escapa, M., Gagliardini, D. A., & Iribarne, O. O. (2006). Distribution of saltmarsh plant communities associated with environmental factors along a latitudinal gradient on the south-west Atlantic coast. Journal of Biogeography, 33, 888–900.

    Article  Google Scholar 

  • ISO International Organization for Standardization. (1995). Soil quality, extraction of trace elements soluble in aqua Regia. ISO, 11466, 1–6.

    Google Scholar 

  • Ituarte, R., Spivak, E., & Luppi, T. (2004). Female reproductive cycle of the southwestern Atlantic estuarine crab Chasmagnatus granulatus (Brachyura: Grapsoidea: Varunidae). Scientia Marina, 68, 127–137.

    Article  Google Scholar 

  • Ituarte, R. B., Bas, C., Luppi, T., & Spivak, E. D. (2006). Interpopulational differences in the female reproductive cycle of the southwestern Atlantic estuarine crab Chasmagnathus granulatus Dana, 1851 (Brachyura: Grapsoidea: Varunidae). Scientia Marina, 70(4), 709–718.

    Article  Google Scholar 

  • Kabata Pendias, A. (2011). Trace elements in soils and plants. 4th Edition. Taylor & Francis Group, Boca Raton pp 548.

  • Lauer, M. M., de Olivera, C. B., Yano, N. L. I., & Bianchini, A. (2012). Copper effects on key metabolic enzymes and mitochondrial membrane potential in gills of the estuarine crab Neohelice granulata at different salinities. Comparative Biochemistry and Physiology - Part C, 156, 140–147.

    CAS  Google Scholar 

  • Luoma, S. N., & Rainbow, P. S. (2008). Metal contamination in aquatic environments: science and lateral management (p. 573). Cambridge: Cambridge University Press.

    Google Scholar 

  • MacFarlane, G. R., Booth, D. J., & Brown, K. R. (2000). The semaphore crab, Heloecious cordiformis: bio-indication potential for heavy metals in estuarine systems. Aquatic Toxicology, 50, 153–166.

    Article  CAS  Google Scholar 

  • MacGrath, S. P., & Cunliffe, C. H. (1985). A simplified method for the extraction of the metals Fe, Zn, Cu, Ni, Cd, Pb, Cr, Co and Mn from soils and sludges. Journal of the Science of Food and Agriculture, 36, 794–798.

    Article  Google Scholar 

  • Mahon, S., & Carman, K. R. (2008). The influence of salinity on the uptake, distribution, and excretion of metals by the smooth cordgrass, Spartina alterniflora (Loisel), grown in sediment contaminated by multiple metals. Estuaries and Coasts, 31, 1089–1097.

    Article  CAS  Google Scholar 

  • Markert, B. (2007). Definitions and principles for bioindication and biomonitoring of trace metals in the environment. Journal of Trace Elements in Medicine and Biology, 21(S1), 77–82.

    Article  Google Scholar 

  • Marsden, I. D., & Rainbow, P. S. (2004). Does the accumulation of trace metals in crustaceans affect their ecology – the amphipod example? Journal of Experimental Marine Biology and Ecology, 300, 373–408.

    Article  CAS  Google Scholar 

  • Mateos Naranjo, E., Redondo Gómez, S., Cambrollé, J., Luque, T., & Figueroa, E. (2008). Growth and photosynthetic responses to zinc stress of an invasive cordgrass, Spartina densiflora. Plant Biology, 10, 754–762.

    Article  CAS  Google Scholar 

  • Mertens, J., Luyssaert, S., & Verheyen, K. (2005). Use and abuse of trace metal concentrations in plant tissue for biomonitoring and phytoextraction. Environmental Pollution, 138, 1–4.

    Article  CAS  Google Scholar 

  • Montemayor, D. I., Canepuccia, A. D., Pascual, J., & Iribarne, O. O. (2014). Aboveground biomass pattern of dominant Spartina species and their relationship with selected abiotic variables in Argentinian SW Atlantic marshes. Estuaries and Coasts, 37, 411–420.

    Article  Google Scholar 

  • Niyogi, S., Blewett, T. A., Gallegher, T., Fehsenfeld, S., & Wood, C. (2015). Effects of salinity on short-term waterborne zinc uptake, accumulation and sub-lethal toxicity in the green shore crab (Carcinus maenas). Aquatic Toxicology, 178, 132–140.

    Article  Google Scholar 

  • Phillips, D. J. H., & Rainbow, P. S. (1993). Biomonitoring of trace aquatic contaminants (p. 371). London: Elsevier Science.

    Google Scholar 

  • Prasad,, M., Sajwan, K., & Naidu, R. (Eds) (2006). Trace elements in the environment: biogeochemistry, biotechnology, and bioremediation. 1st Edition. CRC Press. Boca Raton pp. 744.

  • Quan, W. M., Han, J. D., Shen, A. L., Ping, X. Y., Qian, P. L., Li, C. J., Shi, L. Y., & Chen, Y. Q. (2007). Uptake and distribution of N, P and heavy metals in three dominant salt marsh macrophytes from Yangtze River Estuary, China. Marine Environmental Research, 64, 21–37.

    Article  CAS  Google Scholar 

  • Rainbow, P. S. (1990). Heavy metal levels in marine invertebrates. In R. W. Furness & P. S. Rainbow (Eds.), Heavy metals in the marine environment (pp. 67–79). Boca Raton, Florida: CRC Press.

    Google Scholar 

  • Rainbow, P. S. (1997). Ecophysiology of trace metal uptake in crustaceans. Estuarine, Coastal and Shelf Science, 44, 169–175.

    Article  CAS  Google Scholar 

  • Rainbow, P. S. (2002). Trace metal concentrations in aquatic invertebrates: why and so what? Environmental Pollution, 120, 497–507.

    Article  CAS  Google Scholar 

  • Rainbow, P. S. (2007). Trace metal bioaccumulation: models, metabolic availability and toxicity. Environment International, 33, 576–582.

    Article  CAS  Google Scholar 

  • Redondo Gómez, S. (2013). Bioaccumulation of heavy metals in Spartina. Functional Plant Biology, 40, 913–921.

    Google Scholar 

  • Redondo Gómez, S., Andrades Moreno, L., Mateos Naranjo, E., Parra, R., Valera Burgos, J., & Arcoa, R. (2011). Synergic effect of salinity and zinc stress on growth and photosynthetic responses of the cordgrass, Spartina densiflora. Journal of Experimental Botany, 62(15), 5521–5530.

    Article  Google Scholar 

  • Sa, M. G., Valenti, W. C., & Zanotto, F. P. (2008). Dietary copper absorption and excretion in three semi-terrestrial grapsoid crabs with different levels of terrestrial adaptation. Comparative Biochemistry and Physiology - Part C, 148, 112–116.

    CAS  Google Scholar 

  • Sadiq, M. (1992). Toxic metal chemistry in marine environments. New York: Marcel Dekker 390 pp.

    Google Scholar 

  • Salla, V., Hardaway, C. J., & Sneddon, J. (2011). Preliminary investigation of Spartina alterniflora for phytoextraction of selected heavy metals in soils from Southwest Louisiana. Microchemical Journal, 97, 207–212.

    Article  CAS  Google Scholar 

  • Simonetti, P., Botté, S. E., Fiori, S. M., & Marcovecchio, J. E. (2011). Heavy-metal concentrations in soft tissues of the burrowing crab Neohelice granulata in Bahía Blanca Estuary, Argentina. Archives of Environmental Contamination and Toxicology, 62, 243–253. https://doi.org/10.1007/s00244-011-9692-9.

    Article  CAS  Google Scholar 

  • Simonetti, P., Botté, S. E., Fiori, S. M., & Marcovecchio, J. E. (2013). Burrowing crab (Neohelice granulata) as a potential bioindicator of heavy metals in the Bahía Blanca Estuary, Argentina. Archives of Environmental Contamination and Toxicology, 64, 110–118.

    Article  CAS  Google Scholar 

  • Spacie, A., McCarty, L. S., & Rand, G. M. (1995). Bioaccumulation and bioavailability in multiphase systems. In G. M. Rand (Ed.), Fundamentals of Aquatic Toxicology (pp. 493–521). Washington, DC: Taylor & Francis.

    Google Scholar 

  • Sundby, B., Vale, C., Caçador, I., Catarino, F., Madureira, M., & Caetano, M. (1998). Metal-rich concretions on the roots of the salt marsh plants: mechanism and rate of formation. Limnology Oceanography, 43, 245–252.

    Article  CAS  Google Scholar 

  • Tessier, A., Campbell, G. C., & Bisson, M. (1979). Sequential extraction procedure for the speciation of particulate trace metals. Analytical Chemistry, 51(7), 844–851.

    Article  CAS  Google Scholar 

  • Tsakovski, S., Kudlak, B., Simeonov, V., Wolska, L., Garcia, G., Dassenakis, M., & Namiesnik, J. (2009). N-way modelling of sediment monitoring data from Mar Menor lagoon, Spain. Talanta, 80, 935–941.

    Article  CAS  Google Scholar 

  • Vale, C., Catarino, F. M., Cortesao, C., & Cacador, M. I. (1990). Presence of metal-rich rhizoconcretions on the roots of Spartina maritima from the salt marshes of the Tagus Estuary, Portugal. Science of the Total Environment, 97(98), 617–626.

    Article  Google Scholar 

  • Vale, C., Caetano, M., & Raimundo, J. (2003). Incorporation of trace elements on iron-rich concretions around plant roots of Tagus Estuary salt marsh (Portugal). J Soils & Sediments, 3(3), 208–212.

    Article  CAS  Google Scholar 

  • Vitale, A. M., Monserrat, J. M., Castillo, P., & Rodriguez, E. M. (1999). Inhibitory effects of cadmium on carbonic anhydrase activity and ionic regulation of the estuarine crab Chasmagnathus granulata (Decapoda, Grapsidae). Comparative Biochemistry and Physiology - Part C, 122, 121–129.

    CAS  Google Scholar 

  • Weis, J., & Weis, P. (2004). Metal uptake, transport and release by wetland plants: implications for phytoremediation and restoration. Environment International, 30, 685–700.

    Article  CAS  Google Scholar 

  • Weisbrod, A. V., Burkhard, L. P., Arnot, J., Mekenyan, O., Howard, P. H., Russom, C., Boethling, R., Sakuratani, Y., Traas, T., Bridges, T., Lutz, C., Bonnell, M., Woodburn, K., & Parkerton, T. (2007). Workgroup report: review of fish bioaccumulation databases used to identify persistent, bioaccumulative, toxic subtances. Environmental Health Perspectives, 115(2), 255–261.

    Article  CAS  Google Scholar 

  • Williams, T. P., Bubb, J. M., & Lester, J. N. (1994). Metal accumulation within salt marsh environments: a review. Marine Pollution Bulletin, 28(5), 277–290.

    Article  CAS  Google Scholar 

  • Windham, L., Weis, J. S., & Weis, P. (2001). Patterns and processes of mercury (Hg) release from leaves of two dominant salt marsh macrophytes, Phragmites australis and Spartina alterniflora. Estuaries, 24, 787–795.

    Article  Google Scholar 

  • Windham, L., Weis, J. S., & Weis, P. (2003). Uptake and distribution of metals in two dominant salt marsh macrophytes, Spartina alterniflora (cordgrass) and Phragmites australis (common reed). Estuarine, Coastal and Shelf Science, 56, 63–72.

    Article  CAS  Google Scholar 

  • Yoon, J., Cao, X., Zhou, Q., & Ma, L. Q. (2006). Accumulation of Pb, Cu, and Zn in native plant growing on a contaminated Florida site. Science of the Total Environment, 368, 456–464.

    Article  CAS  Google Scholar 

  • Yoong, K. S. (1998). Determination of cadmium, chromium, cobalt, lead, and nickel in plant tissue. In Y. P. Kalra (Ed.), Handbook of reference methods for plant analysis (pp. 193–199). Boca Raton: CRC Press.

    Google Scholar 

  • Zhou, Q., Zhang, J., Fu, J., Shi, J., & Jiang, G. (2008). Biomonitoring: an appealing tool for assessment of metal pollution in the aquatic ecosystem. Analytica Chimica Acta, 606, 153–150.

    Article  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Mr. Bernabé Urtubey for checking the grammar and spelling of the manuscript. We appreciate the comments and corrections of the anonymous reviewers, which effectively contributed to the improvement of this manuscript.

Funding

This study was partially funded by CONICET, through a doctoral fellowship to the first author, and Secretaria de Ciencia y Técnica of Universidad Nacional de la Patagonia San Juan Bosco (PI 1281 to MG and CM).

Author information

Authors and Affiliations

  1. Centro para el Estudio de Sistemas Marinos, CCT CONICET-CENPAT, Bvd. Brown 2915, Puerto Madryn, Argentina

    C. H. Marinho, E. Giarratano & M. N. Gil

Authors
  1. C. H. Marinho
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. Giarratano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. N. Gil
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. H. Marinho.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Marinho, C.H., Giarratano, E. & Gil, M.N. Metal biomonitoring in a Patagonian salt marsh. Environ Monit Assess 190, 598 (2018). https://doi.org/10.1007/s10661-018-6975-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-018-6975-x

Keywords

Search

Navigation