ORIGINAL RESEARCH
Tissue-Specific Nickel Accumulation
and Detoxification in Pomacea insularum:
A Biomonitoring Tool for Freshwater Ecosystems
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1
Department of Biology, Faculty of Science, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia
2
Department of Biology, Faculty of Science, University of Tabuk, Tabuk, P.O. Box 741, Saudi Arabia
Submission date: 2024-12-04
Final revision date: 2025-02-15
Acceptance date: 2025-05-01
Online publication date: 2025-07-03
Corresponding author
Chee Kong Yap
Biology, Universiti Putra Malaysia, Department of Biology, Faculty of Science, 43400, Serdang, Malaysia
KEYWORDS
TOPICS
ABSTRACT
This study investigates the tissue-specific accumulation and detoxification of nickel (Ni)
in Pomacea insularum, a freshwater snail, collected from 13 sites in Peninsular Malaysia. Ni
concentrations ranged from 3.24 to 33.38 mg/kg dry weight across eight tissues, including the shell,
cephalic tentacle, mantle, digestive tract (DT), foot, remaining soft tissues, pineal sac, and operculum.
The shell exhibited the highest Ni accumulation (22.12-33.38 mg/kg), serving as the primary long-term
repository, while soft tissues such as the DT (5.55-27.44 mg/kg), mantle (5.44-16.60 mg/kg), and foot
(4.49-10.14 mg/kg) played critical roles in initial Ni uptake and redistribution. A field transplantation
study further confirmed these findings, demonstrating significant Ni accumulation in soft tissues
within seven weeks of exposure to a polluted site, followed by substantial depuration upon transfer to
a cleaner environment. Correlation and factor analyses revealed strong interactions between soft tissues
and the shell, indicating a coordinated Ni detoxification and storage system. These results underscore
the suitability of P. insularum as an effective biomonitor for assessing both short-term and long-term Ni
pollution in freshwater ecosystems.
CONFLICT OF INTEREST
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
REFERENCES (67)
1.
NIZEYIMANA J.C., NDAGIJIMANA P., KHAN J., XIANGRU L., TWAGIRAYEZU G., MANZI H.P., IRUMVA O., YU C.-P., HU A., LIN S. A hybrid system for nickel ions removal from synthesized wastewater using adsorption assisted with electrocoagulation. Environmental Science and Pollution Research. 31, 28321, 2024.
https://doi.org/10.1007/s11356....
2.
RIZWAN M., USMAN K., ALSAFRAN M. Ecological impacts and potential hazards of nickel on soil microbes, plants, and human health. Chemosphere. 357, 142028, 2024.
https://doi.org/10.1016/j.chem....
3.
YAP C.K., TAN W.S., ISMAIL M.S., ARIFFIN N., CHENG W.H., BINTAL A., ZAKALY H.M.H., PENG S.H.T., YAP C.W., EDWARD F.B. Shells of intertidal mudflat snails: A promising biomonitoring material of nickel pollution. Environmental Protection Research. 2 (1), 1, 2022.
https://doi.org/10.37256/epr.2....
4.
BEGUM W., RAI S., BANERJEE S., BHATTACHARJEE S., MONDAL M.H., BHATTARAI A., SAHA B. A comprehensive review on the sources, essentiality and toxicological profile of nickel. RSC Advances. 12, 9139, 2022.
https://doi.org/10.1039/D2RA00....
5.
MATTSSON M., CRÉMAZY A. The effects of temperature on nickel bioaccumulation and toxicity in the freshwater snail Lymnaea stagnalis. Environmental Pollution. 337, 122505, 2023.
https://doi.org/10.1016/j.envp....
6.
PANE E.F., SMITH C., MCGEER J.C., WOOD C.M. Mechanisms of acute and chronic waterborne nickel toxicity in the freshwater cladoceran, Daphnia magna. Environmental Science & Technology. 37 (19), 4382, 2003b.
https://doi.org/10.1021/es0343....
7.
PURNAMA M.F., PRAYITNO S.B., MUSKANANFOLA M.R., SURYANTI S. Existing conditions of gastropod communities in areas affected by overburden nickel mining in the mangrove ecosystem of Dawi-Dawi, Southeast Sulawesi. Biotropia. 31 (2), 266, 2024.
https://doi.org/10.11598/btb.2....
8.
HE J., WANG C., SCHLEKAT C.E., WU F., MIDDLETON E., GARMAN E.R., PETERS A. Validation of nickel bioavailability models for algae, invertebrates, and fish in Chinese surface waters. Environmental Toxicology and Chemistry. 42 (6), 1257, 2023.
https://doi.org/10.1002/etc.55....
9.
PETERS A., NYS C., LEVERETT D., WILSON I., VAN SPRANG P., MERRINGTON G., MIDDLETON E.R., SCHLEKAT C.E. Updating the chronic freshwater ecotoxicity database and biotic ligand model for nickel for regulatory applications in Europe. Environmental Toxicology and Chemistry. 42 (3), 566, 2023.
https://doi.org/10.1002/etc.55....
10.
RAGI A.S., LEENA P.P., CHERIYAN E., NAIR S.M. Heavy metal concentrations in some gastropods and bivalves collected from the fishing zone of South India. Marine Pollution Bulletin. 118 (1), 452, 2017.
https://doi.org/10.1016/j.marp....
11.
STRUNGARU S.-A., NICOARA M., TEODOSIU C., MICU D., PLAVAN G. Toxic metals biomonitoring based on prey-predator interactions and environmental forensics techniques: A study at the Romanian-Ukraine cross border of the Black Sea. Marine Pollution Bulletin. 124 (1), 321, 2017.
https://doi.org/10.1016/j.marp....
12.
REOLID M., BOATENG M.C., MAHU E. Geochemical fractionation of trace elements in ostreid and gastropod shells: A potential proxy for heavy metal pollution in Ghana's coastal environment. Estudios Geologicos. 80 (1), 1085, 2024.
https://doi.org/10.3989/egeol.....
13.
CRAVO A., BEBIANNO M.J., FOSTER P. Partitioning of trace metals between soft tissues and shells of Patella aspera. Environment International. 30 (1), 87, 2003.
https://doi.org/10.1016/S0160-....
14.
PUNT A.G., MILLWARD G., JONES M.B. Uptake and depuration of 63Ni by Mytilus edulis. Science of The Total Environment. 214 (1), 71, 1998.
https://doi.org/10.1016/S0048-....
15.
YAP C.K., PANG B.H., CHENG W.H., KUMAR K., AVTAR R., OKAMURA H., HORIE Y., SHARIFINIA M., KESHAVARZIFARD M., ONG M.C., NAJI A., ISMAIL M.S., TAN W.S. Heavy metal exposures on freshwater snail Pomacea insularum: Understanding its biomonitoring potentials. Applied Sciences (Switzerland). 13 (2), 1042, 2023.
https://doi.org/10.3390/app130....
16.
YAP C.K., AL-MUTAIRI K.A. Comparative study of potentially toxic nickel and their potential human health risks in seafood (fish and mollusks) from Peninsular Malaysia. Biology. 11 (3), 376, 2022.
https://doi.org/10.3390/biolog....
17.
BANERJEE S., DEOLI N.T., WHITLOW H.J., KLERKS P.L. Invasive or biomonitoring species? Use of Pomacea maculata operculum as a tool to determine metal pollutants: A micro-PIXE investigation. Water, Air, and Soil Pollution. 234 (6), 353, 2023.
https://doi.org/10.1007/s11270....
18.
YAP C.K., BERANDAH F.E., PANG B.H., ISMAIL A., TAN S.G. Distribution of heavy metal concentrations in the different soft tissues of the freshwater snail Pomacea insularum (D'Orbigny, 1839; Gastropoda), and sediments collected from polluted and unpolluted sites from Malaysia. Toxicological & Environmental Chemistry. 91 (1), 17, 2009.
https://doi.org/10.1080/027722....
19.
GARCÍA-RISCO M., CALATAYUD S., NIEDERWANGER M., ALBALAT R., PALACIOS Ò., CAPDEVILA M., DALLINGER R. Two unconventional metallothioneins in the apple snail Pomacea bridgesii have lost their metal specificity during adaptation to freshwater habitats. International Journal of Molecular Sciences. 22 (1), 95, 2021.
https://doi.org/10.3390/ijms22....
20.
KANG Y.T., WU Y., HSU C.H., TANG S.C., KO J.L. Exposure to nickel chloride induces epigenetic modification on detoxification enzyme glutathione S-transferase M2. Environmental Toxicology. 39 (3), 1729, 2023.
https://doi.org/10.1002/tox.24....
21.
CRÉMAZY A., BRIX K.V., SMITH D.S., CHEN W., GROSELL M., SCHLEKAT C.E., GARMAN E.R., MIDDLETON E.T., WOOD C.M. A mystery tale: Nickel is fickle when snails fail - Investigating the variability in Ni toxicity to the great pond snail. Integrated Environmental Assessment and Management. 16 (6), 983, 2020.
https://doi.org/10.1002/ieam.4....
22.
PENA R.V., SILVA BRITO R., ARAÚJO O.A., DAMACENA-SILVA L., HARAYASHIKI C.A.Y., ROCHA T.L. Hazardous effects of nickel ferrite nanoparticles and nickel chloride in early life stages of the freshwater snail Biomphalaria glabrata (Say, 1818). Environmental Science and Pollution Research. 31 (48), 58324, 2024.
https://doi.org/10.1007/s11356....
23.
SAGNER S., KNEER R., WANNER G., COSSON J., DEUS-NEUMANN B., ZENK M.H. Hyperaccumulation, complexation and distribution of nickel in Sebertia acuminata. Phytochemistry. 47 (3), 339, 1998.
https://doi.org/10.1016/S0031-....
25.
CUADRADO J.T., BURLAT M.J.P., DIOLA J.L.U., CUSAP R.M.B. Levels of heavy metals in the water, sediments, and tissues of golden apple snail (Pomacea canaliculata) from Lake Dakong Napo, Esperanza, Agusan del Sur, Philippines. Pollution. 8 (4), 1164, 2022.
27.
BHANDARI U., ARULKUMAR A., GANESHKUMAR A., PARAMASIVAM S., RAJARAM R., MIRANDA J.M. Metal accumulation and biomineralisation of coastal and mangrove-associated molluscs of Palk Bay, Southeastern India. Marine Pollution Bulletin. 167, 112259, 2021.
https://doi.org/10.1016/j.marp....
28.
RAINBOW P.S., WHITE S.L. Comparative strategies of heavy metal accumulation by crustaceans: Zinc, copper, and cadmium in a decapod, an amphipod, and a barnacle. Hydrobiologia. 174 (3), 245, 1989.
https://doi.org/10.1007/BF0000....
29.
GANGULY A., MONIRUZZAMAN M., CHAKRABORTY S.K., KARAN S., MUKHERJEE J. Impact of metal accumulation pattern on the annual rhythmicity of antioxidants and their interrelationship to maintain the oxidative balance in mollusc. Biological Rhythm Research. 50 (4), 603, 2019.
https://doi.org/10.1080/092910....
30.
ANAGHA B., ATHIRA P.S., ANISHA P., CHARLES P.E., ANANDKUMAR A., RAJARAM R. Biomonitoring of heavy metals accumulation in molluscs and echinoderms collected from southern coastal India. Marine Pollution Bulletin. 184, 114169, 2022.
https://doi.org/10.1016/j.marp....
31.
GIRAUD-BILLOUD M., CAMPOY-DIAZ A.D., MUÑOZ E.M., VEGA I.A. Evaluation of female masculinization in Pomacea canaliculata (Caenogastropoda, Ampullariidae) induced by tributyltin, heavy metals, and uranium in culture water. Environmental Analysis Health and Toxicology. 37 (3), e2022023, 2022.
https://doi.org/10.5620/eaht.2....
32.
YANG W., LI X., PEI J., SUN T., SHAO D., BAI J., LI Y. Bioavailability of trace metals in sediments of a recovering freshwater coastal wetland in China's Yellow River Delta, and risk assessment for the macrobenthic community. Chemosphere. 189, 661, 2017.
https://doi.org/10.1016/j.chem....
33.
ALEJANDRA D.C., CAMPOY-DIAZ M., ARRIBÉRE M., RIBEIRO S.G., VEGA I.A. Bioindication of mercury, arsenic and uranium in the apple snail Pomacea canaliculata (Caenogastropoda, Ampullariidae): Bioconcentration and depuration in tissues and symbiotic corpuscles. Chemosphere. 196, 196, 2017.
https://doi.org/10.1016/j.chem....
34.
VEGA I.A., ARRIBÉRE M., ALMONACID A.V., RIBEIRO S.G., CASTRO-VAZQUEZ A. Apple snails and their endosymbionts bioconcentrate heavy metals and uranium from contaminated drinking water. Environmental Science and Pollution Research. 19, 3307, 2012.
https://doi.org/10.1007/s11356....
35.
ANDRIANI Y., PRATAMA R.I., ROSTINI I. A review of the potential of golden apple snail (Pomacea canaliculata) as a raw material for aquaculture feed. International Journal of Scientific Multidisciplinary Research. 1 (6), 655, 2023.
https://doi.org/10.55927/ijsmr....
36.
YAO F., CHEN Y., QIN Z., SHI Z.-P., ZHANG J. A bibliometric analysis of research on apple snails (Ampullariidae). Agronomy. 13 (7), 1671, 2023.
https://doi.org/10.3390/agrono....
37.
AMADI C.N., FRAZZOLI C., ORISAKWE O.E. Sentinel species for biomonitoring and biosurveillance of environmental heavy metals in Nigeria. Journal of Environmental Science and Health, Part C: Toxicology and Carcinogenesis. 38 (1), 21, 2020.
https://doi.org/10.1080/268965....
38.
OSWALD C. Gastrointestinal and tissue levels of nickel in deer mice (Peromyscus maniculatus) and woodrats (Neotoma fuscipes) from serpentine and non-serpentine areas. Ecotoxicology. 49 (3), 419, 2004.
https://doi.org/10.1007/BF0319....
39.
BICI M., MAZREKU I., HYSENI B., HALILI J., KRASNIQI Y., BISLIMI K. Effect of lead, nickel, and zinc pollution in some parameters of oxidative stress in hepatopancreas of snail Helix pomatia L. in power plant of Obiliq. Journal of Ecological Engineering. 24 (9), 385, 2023.
https://doi.org/10.12911/22998....
40.
TARDUGNO R., VIRGA A., NAVA V., MANNINO F., SALVO A., MONACO F., GIORGIANNI M., CICERO N. Toxic and potentially toxic mineral elements of edible gastropods land snails (Mediterranean Escargot). Toxics. 11 (4), 317, 2023.
https://doi.org/10.3390/toxics....
41.
BARRICK A., PARHAM S., JOHNSON P., BREWER S., HOANG T. Sensitivity of Alabama freshwater gastropod species to nickel exposure. Environmental Toxicology and Chemistry. 43 (120), 2578, 2024.
https://doi.org/10.1002/etc.59....
42.
ZHAO N., SANG C., CAO R., YAO Z., GAO F., TIAN S., HOU Y. Impacts of mining on the diversity of benthic macroinvertebrates - A case study of molybdenum mining area in Luanchuan county. Environmental Pollution. 364, 125335, 2025.
https://doi.org/10.1016/j.envp....
43.
PIWONI-PIÓREWICZ A., KUKLINSKI P., STREKOPYTOV S., HUMPHREYS-WILLIAMS E., NAJORKA J., IGLIKOWSKA A. Size effect on the mineralogy and chemistry of Mytilus trossulus shells from the southern Baltic Sea: Implications for environmental monitoring. Environmental Monitoring and Assessment. 189, 1, 2017.
https://doi.org/10.1007/s10661....
44.
WANG Z., YEUNG K.W.Y., ZHOU G.-J., YUNG M.M.N., SCHLEKAT C.E., GARMAN E.R., GISSI F., STAUBER J.L., MIDDLETON E.T., LIN W.Y.Y., LEUNG K.M.Y. Acute and chronic toxicity of nickel on freshwater and marine tropical aquatic organisms. Ecotoxicology and Environmental Safety. 206, 111373, 2020.
https://doi.org/10.1016/j.ecoe....
45.
NIYOGI S., BRIX K.V., GROSELL M. Effects of chronic waterborne nickel exposure on growth, ion homeostasis, acid-base balance, and nickel uptake in the freshwater pulmonate snail, Lymnaea stagnalis. Aquatic Toxicology. 150, 36, 2014.
https://doi.org/10.1016/j.aqua....
46.
BRIX K.V., SCHLEKAT C.E., GARMAN E. The mechanisms of nickel toxicity in aquatic environments: An adverse outcome pathway analysis. Environmental Toxicology and Chemistry. 36 (5), 1128, 2016.
https://doi.org/10.1002/etc.37....
47.
MARIMOUTOU M., ORIOT J., BALDONI-ANDREY P., BAREILLE G., BOULLEMANT A., GELBER C., COURRÈGES C., MOUNICOU S., TABOURET H., LE FAUCHEUR S. Metal localisation in gastropod shells: New insights from mass spectrometry techniques. Chemosphere. 344, 140375, 2023.
https://doi.org/10.1016/j.chem....
48.
HÉDOUIN L., GÓMEZ-BATISTA M., MÉTIAN M., BUSCHIAZZO E., WARNAU M. Metal and metalloid bioconcentration capacity of two tropical bivalves for monitoring the impact of land-based mining activities in the New Caledonia lagoon. Marine Pollution Bulletin. 61, 554, 2010.
https://doi.org/10.1016/j.marp....
49.
DIAS H.Q., NAYAK G.N. Geochemistry and bioavailability of mudflats and mangrove sediments and their effect on bioaccumulation in selected organisms within a tropical (Zuari) estuary, Goa, India. Marine Pollution Bulletin. 105 (1), 227, 2016.
https://doi.org/10.1016/j.marp....
50.
EMAMI H., ABTAHI B., SHOKRI M.R. Heavy metal bioaccumulation (Ni, V, and Hg) in soft tissues of crustaceans, bivalves, and gastropods: A case study on the Northern Persian Gulf. Caspian Journal of Environmental Sciences. 22 (2), 255, 2024.
51.
GISSI F., STAUBER J.L., BINET M.T., TRENFIELD M.A., DAM J.W.V., JOLLEY D.F. Assessing the chronic toxicity of nickel to a tropical marine gastropod and two crustaceans. Ecotoxicology and Environmental Safety. 159, 284, 2018.
https://doi.org/10.1016/j.ecoe....
52.
GALAY M., RAINBOW P.S. Uptake, accumulation and excretion by Corophium volutator (Crustacea: Amphipoda) of zinc, cadmium and cobalt added to sewage sludge. Estuarine, Coastal and Shelf Science. 47 (5), 603, 1998.
https://doi.org/10.1006/ecss.1....
53.
BLEWETT T.A., LEONARD E.M. Mechanisms of nickel toxicity to fish and invertebrates in marine and estuarine waters. Environmental Pollution. 223, 311, 2017.
https://doi.org/10.1016/j.envp....
54.
NIGARIGA P., SAREN D., VARMA R., SUGUMAR V. Assessment of trace metal bioaccumulation on the shells of edible gastropod Chicoreus ramosus and Hemifusus pugilinus. Environmental Monitoring and Assessment. 195 (5), 608, 2023.
https://doi.org/10.1007/s10661....
55.
ZHANG S., YANG X., CHENG Q., WANG M., HU C., CHAI B., LI J. Treatment of wastewater containing nickel by electrocoagulation process using photovoltaic energy. Environmental Engineering Science. 35 (5), 484, 2017.
https://doi.org/10.1089/ees.20....
56.
RISTIYANTI M., MARWOTO N.R., ISNANINGSIH N. Notes on the distribution of invasive freshwater snail Pomacea canaliculata (Lamarck, 1822) and P. insularum (d'Orbigny, 1835) in Indonesia. Biotropia. 18 (10), 123, 2011.
https://doi.org/10.11598/btb.2....
57.
DE OLIVEIRA M.F., RODRIGUES E., JR SUDA C.N.K., VANI G.S., DONATTI L., LAVRADO H.P. Evidence of metabolic microevolution of the limpet Nacella concinna to naturally high heavy metal levels in Antarctica. Ecotoxicology and Environmental Safety. 135, 1, 2017.
https://doi.org/10.1016/j.ecoe....
58.
DE SILVA N.A.L., MARSDEN I.D., GAW S., GLOVER C.N. Assessment of Amphibola crenata as a bioindicator of estuarine trace element pollution using biochemical and physiological endpoints. Marine Pollution Bulletin. 206, 116693, 2024.
https://doi.org/10.1016/j.marp....
59.
SZEFER P., GEŁDON J., ALI A.A.M., PÁEZ-OSUNA F., RUÍZ-FERNÁNDEZ A.C., GALVAN S. Distribution and association of trace metals in soft tissue and byssus of Mytella strigata and other benthal organisms from Mazatlan Harbour, Mangrove Lagoon of the northwest coast of Mexico. Environment International. 24 (3), 359, 1998.
https://doi.org/10.1016/S0160-....
60.
CASTILLO A., VALDÉS J., MARAMBIO Y., FIGUEROA L., LETELIER J., CÁRCAMO F. Metal(loid)s content in Concholepas concholepas (Mollusca) and human health assessment in a coastal environmental sacrifice zone, central Chile (~32ºS). Marine Pollution Bulletin. 197, 115738, 2023.
https://doi.org/10.1016/j.marp....
61.
FERREIRA D., DO AMARAL V.S. Ecotoxicological water assessment of an estuarine river from the Brazilian Northeast, potentially affected by industrial wastewater discharge. Science of the Total Environment. 572, 324, 2016.
https://doi.org/10.1016/j.scit....
62.
NOTT J.A., NICOLAIDOU A. Transfer of metal detoxification along marine food chains. Journal of the Marine Biological Association of the United Kingdom. 70 (4), 905, 1990.
https://doi.org/10.1017/S00253....
63.
BIAN B., ZHOU Y., FANG B.B. Distribution of heavy metals and benthic macroinvertebrates: Impacts from typical inflow river sediments in the Taihu Basin, China. Ecological Indicators. 69, 348, 2016.
https://doi.org/10.1016/j.ecol....
64.
BINET M.T., ADAMS M.S., GISSI F., GOLDING L.A., SCHLEKAT C.E., GARMAN E.R., MERRINGTON G., STAUBER J.L. Toxicity of nickel to tropical freshwater and sediment biota: A critical literature review and gap analysis. Environmental Toxicology and Chemistry. 37 (2), 293, 2018.
https://doi.org/10.1002/etc.39....
65.
LADERRIERE V., MORIN S., EON M., FORTIN C. Vulnerability and tolerance to nickel of periphytic biofilm harvested in summer and winter. Environmental Pollution. 315, 120223, 2022.
https://doi.org/10.1016/j.envp....
66.
ZHOU C., HOU J., LIN D. A ferritin gene in the marine copepod Acartia tonsa as a highly sensitive biomonitor for nano-contamination. Aquatic Toxicology. 253, 106353, 2022.
https://doi.org/10.1016/j.aqua....
67.
ZUYKOV M., PELLETIER É., HARPER D.A.T. Bivalve mollusks in metal pollution studies: From bioaccumulation to biomonitoring. Chemosphere. 93 (2), 201, 2013.
https://doi.org/10.1016/j.chem....