Skip to main content

Advertisement

Log in

Apple snails and their endosymbionts bioconcentrate heavy metals and uranium from contaminated drinking water

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Purpose

The differential ability of apple snail tissues, endosymbionts, and eggs to bioaccumulate several metals (Sb, As, Ba, Br, Zn, Cr, Fe, Hg, Se, and U) was investigated.

Methods

Metal concentrations were determined by neutron activation analysis in several tissues, endosymbionts, and eggs from mature apple snails cultured in either drinking water or reconstituted water (prepared with American Society for Testing and Materials type I water).

Results

The highest bioconcentration factors (BCFs) in the midgut gland were found for Ba, Zn, Se, As, U, Br, and Hg (in decreasing order), while the highest in the kidney were for Ba, Br, and Hg. The foot showed the highest BCFs for Ba, Hg, Br, and Se (in decreasing order). Calcified tissues (uterus, shell) and eggs showed low BCFs, except for Ba. Both C corpuscles and gland tissue showed statistically higher BCFs than K corpuscles for Ba, Fe, U, Br, and Sb. The concentration of most of the studied elements was significantly lower in tissues and endosymbionts obtained from snails cultured in reconstituted water instead of drinking water. Snails cultured in reconstituted water and then exposed or not to Hg, As, and U (at the maximum contaminant level allowed by the US Environmental Protection Agency) also resulted in high levels accumulated in midgut gland, endosymbionts and kidney.

Conclusions

Our findings suggest that the midgut gland (and the symbionts contained therein), the kidney, and the foot of Pomacea canaliculata may be useful bioindicators of Hg, As and U pollution in freshwater bodies and that the unrestricted use of ampullariid snails as human and animal food must be considered with caution..

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Andrews EB (1965) The functional anatomy of the gut of the prosobranch gastropod Pomacea canaliculata and of some other pilids. J Zool 145:19–36

    Google Scholar 

  • Andrews EB (1981) Osmoregulation and excretion in prosobranch gastropods part 2: structure in relation to function. J Mollus Stud 47:248–289

    Google Scholar 

  • Andrews EB, Taylor PM (1990) Reabsorption of organic solutes in some marine and freswater prosobranch gastropods. J Mollus Stud 56:147–162

    Article  Google Scholar 

  • Baeyens W, Leemakers M, Papina T, Saprykin A, Brion N, Noyen J, De Gieter M, Elskens M, Goeyens L (2003) Bioconcentration and biomagnification of mercury and methylmercury in North Sea and Scheldt Estuary fish. Arch Environ Cont Tox 45:498–508

    Article  CAS  Google Scholar 

  • Baptista MS, Vasconcelos MT (2006) Cyanobacteria metal interactions: requirements, toxicity, and ecological implications. Crit Rev Microbiol 32:127–137

    Article  CAS  Google Scholar 

  • Bargagli R, Monaci F, Borghini F, Bravi F, Agnorelli C (2002) Mosses and lichens as biomonitors of trace metals. A comparison study on Hypnum cupressiforme and Parmelia caperata in a former mining district in Italy. Environ Pollut 116:279–287

    Article  CAS  Google Scholar 

  • Callil CT, Junk WJ (2001) Aquatic gastropods as mercury indicators in the Pantanal of Poconé Region (Mato Grosso, Brasil). Water Air Soil Pollut 125:319–330

    Article  CAS  Google Scholar 

  • Castro-Vazquez A, Albrecht EA, Vega IA, Koch E, Gamarra-Luques C (2002) Pigmented corpuscles in the midgut gland of Pomacea canaliculata and other Neotropical apple-snails (Prosobranchia, Ampullariidae): a possible symbiotic association. Biocell 26:101–109

    CAS  Google Scholar 

  • Catalán NM, Fernandez SN, Winik BC (2002) Oviductal structure and provision of egg envelops in the apple snail Pomacea canaliculata (Gastropoda, Prosobranchia, Ampullariidae). Biocell 26:91–100

    Google Scholar 

  • Catalán M, Dreon MS, Heras H, Pollero RJ, Fernandez SN, Winik B (2006) Pallial oviduct of Pomacea canaliculata (Gastropoda): ultrastructural studies of the parenchymal cellular types involved in the metabolism of perivitellins. Cell Tissue Res 324:523–533

    Article  Google Scholar 

  • Cavet JS, Borrelly GPM, Robinson NJ (2003) Zn, Cu and Co in Cyanobacteria: selective control of metal availability. FEMS Microbiol Rev 27:165–181

    Article  CAS  Google Scholar 

  • Cueto JA (2011) Pomacea canaliculata (Architaenioglossa, Ampullariidae): La hemolinfa y sus células. Thesis. Universidad Nacional de Cuyo, Argentina

    Google Scholar 

  • Cueto JA, Giraud-Billoud M, Vega IA, Castro-Vazquez A (2011) Haemolymph plasma constituents of the invasive snail Pomacea canaliculata (Architaenioglossa, Ampullariidae) and their biological significance. Mollus Res 31:57–60

    Google Scholar 

  • Deng PY, Shu WS, Lan CY, Liu W (2008) Metal contamination in the sediment, pondweed, and snails of a stream receiving effluent from a lead/zinc mine in southern China. Bull Environ Contam Toxicol 81:69–74

    Article  CAS  Google Scholar 

  • Devi CU, Rao KH, Shyamasundari K (1981) Observations on the histology and cytochemistry of the digestive gland in Pila virens (Lamarck)(Mollusca: Gastropoda). Proc Anim Sci 90:307–314

    Article  Google Scholar 

  • Diupotex-Chong ME, Cazzaniga NJ, Hernández-Santoyo A, Betancourt-Rule JM (2004) Karyotype description of Pomacea patula catemacensis (Caenogastropoda, Ampullariidae), with an assessment of the taxonomic status of Pomacea patula. Biocell 28:279–285

    Google Scholar 

  • Estebenet A, Martín P (2002) Pomacea canaliculata (Gastropoda: Ampullariidae): life history traits and their plasticity. Biocell 26:83–89

    Google Scholar 

  • Fiore MF, Moon DH, Trevors JT (1998) Metal resistance and accumulation in Cyanobacteria. Springer, Berlin

    Google Scholar 

  • Fretter V, Graham A (1962) British prosobranch molluscs. Their functional anatomy and ecology. Ray Society, London

    Google Scholar 

  • Goyal R, Seaward MRD (1981) Metal uptake in terricolous lichens. New Phytol 89:631–645

    Article  CAS  Google Scholar 

  • Haas JR, Bailey EH, Purvis OW (1998) Bioaccumulation of metals by lichens: uptake of aqueous uranium by Peltigera membranancea as a function of time and pH. Am Mineral 83:1494–1502

    CAS  Google Scholar 

  • Halwart M (1994) The golden apple snail Pomacea canaliculata in Asian rice farming systems: present impact and future threat. Int J Pest Manage 40:199–206

    Article  Google Scholar 

  • Hayes KA, Joshi RC, Thiengo SC, Cowie RH (2008) Out of South America: multiple origins of non-native apple snails in Asia. Divers Distrib 14:701–712

    Article  Google Scholar 

  • Hoang TC, Rogevich EC, Rand GM, Frakes RA (2008) Copper uptake and depuration by juvenile and adult Florida apple snails (Pomacea paludosa). Ecotoxicology 17:605–615

    Article  CAS  Google Scholar 

  • Koch E, Vega IA, Albrecht EA, Ortega HH, Castro-Vazquez A (2006) A light and electron microscopic study of pigmented corpuscles in the midgut gland and feces of Pomacea canaliculata (Caenogastropoda: Ampullariidae). Veliger 48:17–25

    Google Scholar 

  • Kolthoff IM, Elvin PJ (1986) Nuclear activation and radioisotopic methods of analysis. In: Kolthoff IM, Elvin PJ (eds) Treatise of analytical chemistry. Wiley, New York

    Google Scholar 

  • Kurttio P, Komulainen H, Leino A, Salonen L, Auvinen A, Saha H (2005) Bone as a possible target of chemical toxicity of natural uranium in drinking water. Environ Health Perspect 113:68–72

    Article  CAS  Google Scholar 

  • Little C (1968) Aestivation and ionic regulation in two species of Pomacea (Gastropoda, Prosobranchia). J Exp Biol 48:569–585

    Google Scholar 

  • Little C (1981) Osmoregulation and excretion in prosobranch gastropods. Part I: physiology and biochemistry. J Mollus Stud 47:221–247

    Google Scholar 

  • Maltez HF, Tagle MV, Fernández de la Campa MR, Sanz-Medel A (2009) Metal-metallothioneins like proteins investigation by heteroatom-tagged proteomics in two different snails as possible sentinel organisms of metal contamination in freshwater ecosystems. Anal Chim Acta 650:234–240

    Article  CAS  Google Scholar 

  • Marigómez I, Soto M, Kortabitarte M (1996) Tissue-level biomarkers and biological effect of mercury on sentinel slugs, Arion ater. Arch Environ Contam Toxicol 31:54–62

    Article  Google Scholar 

  • Marigómez I, Soto M, Cajaraville MP, Angulo E, Giamberini L (2002) Cellular and subcellular distribution of metals in molluscs. Microsc Res Tech 56:358–392

    Article  Google Scholar 

  • Martín PR, Estebenet AL (2002) Interpopulation variation in life-history traits of Pomacea canaliculata (Gastropoda: Ampullariidae) in southwestern Buenos Aires Province, Argentina. Malacologia 44:153–164

    Google Scholar 

  • Meenakshi VR (1955) The excretory spherioles in the digestive gland of Pila virens. J Anim Morphol Physiol (Bombay) 3:75–78

    Google Scholar 

  • Nieboer E, Richardson DHS (1980) The replacement of the nondescript term ‘heavy metals’ by a biologically and chemically significant classification of metal ions. Environ Pollut B 1:3–26

    Article  CAS  Google Scholar 

  • Piyatiratitivorakul P, Ruangareerat S, Vajarasathira B (2006) Comparative toxicity of heavy metal compounds to the juvenile golden apple snail, Pomacea sp. Fresen Environ Bull 15:379–384

    CAS  Google Scholar 

  • Rosenberg DM, Resh VH (1993) Freshwater biomonitoring and benthic macroinvertebrates. Chapman & Hall, New York

    Google Scholar 

  • Sari A, Tuzen M, Uluözlü ÖD, Soylak M (2007) Biosorption of Pb (II) and Ni (II) from aqueous solution by lichen (Cladonia furcata) biomass. Biochem Eng J 37:151–158

    Article  CAS  Google Scholar 

  • Seuffert ME, Martín PR (2012) A lentic dweller in lotic habitats: the behavior of the invasive South American apple snail Pomacea canaliculata in flowing water. Aquat Ecol 46:129–142

    Article  Google Scholar 

  • Snyder NFR, Snyder HA (1969) A comparative study of mollusk predation by limpkins, Everglade kites, and boattailed grackles. Living Bird 8:177–223

    Google Scholar 

  • Steinberg CEW, Geyer HJ, Kettrup AAF (1994) Evaluation of xenobiotic effects by ecological techniques. Chemosphere 28:357–374

    Article  CAS  Google Scholar 

  • Tamburi NE, Martín PR (2011) Effects of food availability on reproductive output, offspring quality and reproductive efficiency in the apple snail Pomacea canaliculata. Biol Invasion 13:2351–2360

    Article  Google Scholar 

  • Uluözlü OD, Sari A, Tuzen M, Soylak M (2008) Biosorption of Pb (II) and Cr (III) from aqueous solution by lichen (Parmelina tiliaceae) biomass. Bioresour Technol 99:2972–2980

    Article  Google Scholar 

  • Vega IA, Gamarra-Luques C, Koch E, Bussmann LE, Castro-Vazquez A (2005) A study of corpuscular DNA and midgut gland occupancy by putative symbiotic elements in Pomacea canaliculata (Caenogastropoda, Ampullariidae). Symbiosis 39:37–45

    CAS  Google Scholar 

  • Vega IA, Damborenea MC, Gamarra-Luques C, Koch E, Cueto JA, Castro-Vazquez A (2006) Facultative and obligate symbiotic associations of Pomacea canaliculata (Caenogastropoda, Ampullariidae). Biocell 30:367–375

    CAS  Google Scholar 

  • Vega IA, Giraud-Billoud M, Koch E, Gamarra-Luques C, Castro-Vazquez A (2007) Uric acid accumulation within intracellular crystalloid corpuscles of the midgut gland in Pomacea canaliculata (Caenogastropoda, Ampullariidae). Veliger 48:276–283

    Google Scholar 

  • Wilbur KM, Saleuddin ASM (1983) Shell formation. In: Wilbur KM, Saleuddin ASM (eds) The mollusca 4, physiology part I. Academic, New York, pp 235–287

    Google Scholar 

  • Yoshida K, Hoshikawa K, Wada T, Yusa Y (2009) Life cycle of the apple snail Pomacea canaliculata (Caenogastropoda: Ampullariidae) inhabiting Japanese paddy fields. Appl Entomol Zool 44:465–474

    Article  Google Scholar 

Download references

Acknowledgments

We thank Lic. Adriana M. Carrión for technical assistance. This work was supported by grants from the Universidad Nacional de Cuyo, Consejo Nacional de Investigaciones Científicas y Técnicas, and Fondo Nacional de Ciencia y Técnica (Argentina).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Israel A. Vega.

Additional information

Responsible Editor: Stuart Simpson

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

Bioconcentration factors (BCFs) by midgut gland, C and K corpuscles, and kidney in snails cultured from hatching to 4 months old in reconstituted water and then exposed for two additional months to either Hg, As, or U (DOC 53 kb)

ESM 2

Element concentrations (milligram per kilogram of dry mass) in different foods provided to apple snails in culture (mean ± SEM; N = 6, DOC 55 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vega, I.A., Arribére, M.A., Almonacid, A.V. et al. Apple snails and their endosymbionts bioconcentrate heavy metals and uranium from contaminated drinking water. Environ Sci Pollut Res 19, 3307–3316 (2012). https://doi.org/10.1007/s11356-012-0848-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-012-0848-6

Keywords

Navigation