Effects of Mercury (Hg) on Soil Nematodes: A Microcosm Approach

  • Joey Genevieve MartinezEmail author
  • Shiela Pearl Quiobe
  • Tom Moens


Mercury (Hg), one of the most toxic heavy metals, is commonly used in the gold extraction process in small-scale mining operations in many countries. Our previous field work on the impact of mining on soil nematode assemblages in a small-scale mining area in Sibutad, the Philippines, revealed no significant negative effects despite sometimes strongly elevated Hg concentrations. Using a microcosm approach, we now applied similar Hg concentrations as commonly found in these field sites (2.5, 5, and 10 mg/kg Hg) and determined their impact on nematode assemblages from a different soil with different physicochemical soil attributes. Our results demonstrate (a) limited “bottling” effects (incubation effects) after a 45-day incubation period: a nematode abundance decrease of up to 37%, but absence of significant differences in diversity and nematode assemblage composition; (b) that total nematode abundance already decreased at Hg concentrations (2.5 mg/kg), which did not yield significant impacts on other nematode assemblage descriptors, such as assemblage composition and different diversity indices; and (c) that the Hg concentrations found in the Sibutad field sites can be detrimental to soil nematode assemblages. The discrepancy between our microcosm and the field-based results is probably related to differences in physicochemical soil attributes (e.g., OM contents, soil pH), which suggests that nematode-based environmental assessments should be interpreted in a context-dependent manner.



The first author acknowledges the full support of VLIR-UOS of the Belgian government for funding this Ph.D. project in Mindanao. The authors thank the staff of the Marine Biology Research Group of Ghent University and Mindanao State University-Iligan Institute of Technology (MSU-IIT) through the Complex Systems Initiative SO No. 00886-IIT, s. 2018 for the assistance. The two anonymous reviewers are acknowledged for their valuable input to improve the quality of the work.

Supplementary material

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  1. Akagi H, Castillo ES, Cortes-Maramba N, Francisco-Rivera AT, Timbang TD (2000) Health assessment for mercury exposure among schoolchildren residing near a gold processing and refining plant in Apokon, Tagum, Davao del Norte, Philippines. Sci Total Environ 259:31–43CrossRefGoogle Scholar
  2. Anderson MJ (2004) PERMDISP: a FORTRAN computer program for permutational analysis of multivariate dispersions (for any two-factor ANOVA design) using permutation tests. Department of Statistics, University of Auckland, New ZealandGoogle Scholar
  3. Anderson M, Gorley RN, Clarke RK (2008) Permanova+ for primer: guide to software and statistical methods. Primer-E LimitedGoogle Scholar
  4. Andrássy I (2005) Free-living nematodes of Hungary (Nematoda errantia). Pedozoologia Hungarica 3:518Google Scholar
  5. Antoniadis V, Robinson JS, Alloway BJ (2008) Effects of short-term pH fluctuations on cadmium, nickel, lead, and zinc availability to ryegrass in a sewage sludge-amended field. Chemosphere 71:759–764CrossRefGoogle Scholar
  6. Appleton JD, Weeks JM, Calvez JPS, Beinhoff C (2006) Impacts of mercury contaminated mining waste on soil quality, crops, bivalves, and fish in the Naboc River area, Mindanao, Philippines. Sci Total Environ 354:198–211CrossRefGoogle Scholar
  7. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Ann Rev Plant Biol 57:233–266CrossRefGoogle Scholar
  8. Bongers T (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14–19CrossRefGoogle Scholar
  9. Bongers T (1999) The maturity index, the evolution of nematode life history traits, adaptive radiation and cp-scaling. Plant Soil 212:13–22CrossRefGoogle Scholar
  10. Bongers T, Bongers M (1998) Functional diversity of nematodes. Appl Soil Ecol 10:239–251CrossRefGoogle Scholar
  11. Bongers T, De Goede RGM, Korthals GW, Yeates GW (1995) Proposed changes of cp classification for nematodes. Russ J Nematol 3:61–62Google Scholar
  12. Bongers T, Ferris H (1999) Nematode community structure as a bioindicator in environmental monitoring. Trends Ecol Evol 14:224–228CrossRefGoogle Scholar
  13. Buch AC, Niemeyer JC, Correia MEF, Silva-Filho EV (2016) Ecotoxicity of mercury to Folsomia candida and Proisotoma minuta (Collembola: Isotomidae) in tropical soils: baseline for ecological risk assessment. Ecotoxicol Environ Saf 127:22–29CrossRefGoogle Scholar
  14. Buchwalter DB, Cain DJ, Clements WH, Luoma SN (2007) Using biodynamic models to reconcile differences between laboratory toxicity tests and field biomonitoring with aquatic insects. Environ Sci Technol 41:4821–4828CrossRefGoogle Scholar
  15. Bueno PC, Bellido E, Rubí JAM, Ballesta RJ (2009) Concentration and spatial variability of mercury and other heavy metals in surface soil samples of periurban waste mine tailing along a transect in the Almadén mining district (Spain). Environ Geol 56:815–824CrossRefGoogle Scholar
  16. Burton DT, Turley SD, Fisher DJ, Green DJ, Shedd TR (2006) Bioaccumulation of total mercury and monomethylmercury in the earthworm Eisenia foetida. Water Air Soil Pollut 170:37–54CrossRefGoogle Scholar
  17. Cairns J, Pratt JR (1993) Trends in ecotoxicology. Sci Total Environ 134:7–22CrossRefGoogle Scholar
  18. Cortes-Maramba N, Reyes JP, Francisco-Rivera AT, Akagi H, Sunio R, Panganiban LC (2006) Health and environmental assessment of mercury exposure in a gold mining community in Western Mindanao, Philippines. J Environ Manag 81:126–134CrossRefGoogle Scholar
  19. Davies KG, Curtis RH (2011) Cuticle surface coat of plant-parasitic nematodes. Annu Rev Phytopathol 49:35–156CrossRefGoogle Scholar
  20. Ferris H, Bongers T, De Goede RGM (2001) A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Appl Soil Ecol 18:13–29CrossRefGoogle Scholar
  21. Fichet D, Boucher G, Radenac G, Miramand P (1999) Concentration and mobilisation of Cd, Cu, Pb and Zn by meiofauna populations living in harbour sediment: their role in the heavy metal flux from sediment to food web. Sci Total Environ 243:263–272CrossRefGoogle Scholar
  22. Fiscus DA, Neher DA (2002) Distinguishing sensitivity of free-living soil nematode genera to physical and chemical disturbances. Ecol Appl 12:565–575CrossRefGoogle Scholar
  23. Fleeger JW, Carman KR, Nisbet RM (2003) Indirect effects of contaminants in aquatic ecosystems. Sci Total Environ 317:207–233CrossRefGoogle Scholar
  24. Freckman DW (1988) Bacterivorous nematodes and organic-matter decomposition. Agric Ecosyst Environ 24:195–217CrossRefGoogle Scholar
  25. García-Giménez R, Jiménez-Ballesta R (2017) Mine tailings influencing soil contamination by potentially toxic elements. Environ Earth Sci 76:51CrossRefGoogle Scholar
  26. Gingold R, Moens T, Rocha-Olivares A (2013) Assessing the response of nematode communities to climate change-driven warming: a microcosm experiment. PLoS ONE 8:e66653CrossRefGoogle Scholar
  27. Göthberg A, Greger M (2006) Formation of methyl mercury in an aquatic macrophyte. Chemosphere 65:2096–2105CrossRefGoogle Scholar
  28. Gwyther D, Batterham GJ, Waworuntu J, Gultom TH, Prayogo W (2009) Recolonisation of mine tailing by meiofauna in mesocosm and microcosm experiments. Mar Pollut Bull 58:841–850CrossRefGoogle Scholar
  29. Harris-Hellal J, Vallaeys T, Garnier-Zarli E, Bousserrhine N (2009) Effects of mercury on soil microbial communities in tropical soils of French Guyana. Appl Soil Ecol 41:59–68CrossRefGoogle Scholar
  30. Heininger P, Höss S, Claus E, Pelzer J, Traunspurger W (2007) Nematode communities in contaminated river sediments. Environ Pollut 146:64–76CrossRefGoogle Scholar
  31. Hermi M, Mahmoudi E, Beyrem H, Aïssa P, Essid N (2009) Responses of a free-living marine nematode community to mercury contamination: results from microcosm experiments. Arch Environ Contam Toxicol 56:426–433CrossRefGoogle Scholar
  32. Höss S, Claus E, Von der Ohe PC, Brinke M, Güde H, Heininger P, Traunspurger W (2011a) Nematode species at risk—a metric to assess pollution in soft sediments of freshwaters. Environ Int 37:940–949CrossRefGoogle Scholar
  33. Höss S, Schlottmann K, Traunspurger W (2011b) Toxicity of ingested cadmium to the nematode Caenorhabditis elegans. Environ Sci Technol 45:10219–10225CrossRefGoogle Scholar
  34. Howell R, Smith L (1983) Binding of heavy metals by the marine nematode Enoplus brevis Bastian, 1865. Nematologica 29:39–48CrossRefGoogle Scholar
  35. Hunt DJ, Luc M, Manzanilla-López RH (2005) Identification, morphology and biology of plant parasitic nematodes. In Luc M, Sikora R, Bridge J (eds) Plant parasitic nematodes in subtropical and tropical agriculture. CAB International, WallingfordGoogle Scholar
  36. ISRIC FAO (2002) Procedures for soil analysis, 6th edn. Wageningen, ISRICGoogle Scholar
  37. Kidd K, Clayden M, Jardine T (2012) Bioaccumulation and biomagnification of mercury through food web. Environmental chemistry and toxicology of mercury. Wiley, Hoboken, pp 455–499Google Scholar
  38. Kim J, Koo SY, Kim JY, Lee EH, Lee SD, Ko KS, Ko DC, Cho KS (2009) Influence of acid mine drainage on microbial communities in stream and groundwater samples at Guryong Mine, South Korea. Environ Geol 58:1567–1574CrossRefGoogle Scholar
  39. Kjeldahl J (1883) A new method for the determination of nitrogen in organic matter. Z Anal Chem 22:366–382CrossRefGoogle Scholar
  40. Korthals GW, Popovici I, Iliev I, Lexmond TM (1998) Influence of perennial ryegrass on a copper and zinc affected terrestrial nematode community. Appl Soil Ecol 10:73–85CrossRefGoogle Scholar
  41. Lacastesantos GF (2000) The impact of gold mining on Murcielagos Bay (Sibutad, Zamboanga del Norte, Philippines): accumulation of mercury and other heavy metals in some edible marine molluscs. Doctoral Dissertation, MSc Thesis, RUCA/VUB, Antwerpen, BelgiumGoogle Scholar
  42. Lira VF, Santos GAP, Derycke S, Larrazabal MEL, Fonsêca-Genevois VG, Moens T (2011) Effects of barium and cadmium on the population development of the marine nematode Rhabditis (Pellioditis) marina. Mar Environ Res 72:151–159CrossRefGoogle Scholar
  43. Liu YR, Zheng YM, Shen JP, Zhang LM, He JZ (2010) Effects of mercury on the activity and community composition of soil ammonia oxidizers. Environ Sci Pollut Res 17:1237–1244CrossRefGoogle Scholar
  44. Mahbub KR, Krishnan K, Megharaj M, Naidu R (2016a) Mercury inhibits soil enzyme activity in a lower concentration than the guideline value. Bull Environ Contam Toxicol 96:76–82CrossRefGoogle Scholar
  45. Mahbub KR, Subashchandrabose SR, Krishnan K, Naidu R, Megharaj M (2016b) Mercury alters the bacterial community structure and diversity in soil even at concentrations lower than the guideline values. Appl Microbiol Biotechnol 101:2163–2175CrossRefGoogle Scholar
  46. Mahbub KR, Krishnan K, Naidu R, Andrews S, Megharaj M (2017) Mercury toxicity to terrestrial biota. Ecol Indic 74:451–462CrossRefGoogle Scholar
  47. Mahbub KR, Bahar MM, Megharaj M, Labbate M (2018) Are the existing guideline values adequate to protect soil health from inorganic mercury contamination? Environ Int 117:10–15CrossRefGoogle Scholar
  48. Martikainen E, Haimi J, Ahtiainen J (1998) Effects of dimethoate and benomyl on soil organisms and soil processes—a microcosm study. Appl Soil Ecol 9:381–387CrossRefGoogle Scholar
  49. Martinez JG, dos Santos G, Derycke S, Moens T (2012) Effects of cadmium on the fitness of, and interactions between, two bacterivorous nematode species. Appl Soil Ecol 56:10–18CrossRefGoogle Scholar
  50. Martinez JG, Torres MA, dos Santos G, Moens T (2018) Influence of heavy metals on nematode community structure in deteriorated soil by gold mining activities in Sibutad, southern Philippines. Ecol Indic 91:712–721CrossRefGoogle Scholar
  51. Monteiro L, Brinke M, dos Santos G, Traunspurger W, Moens T (2014) Effects of heavy metals on free-living nematodes: a multifaceted approach using growth, reproduction and behavioural assays. Eur J Soil Biol 62:1–7CrossRefGoogle Scholar
  52. Müller AK, Westergaard K, Christensen S, Sørensen SJ (2002) The diversity and function of soil microbial communities exposed to different disturbances. Microbial Ecol 44:49–58CrossRefGoogle Scholar
  53. Nelson PF, Morrison AL, Malfroy HJ, Cope M, Lee S, Hibberd ML, Meyer CM, McGregor J (2012) Atmospheric mercury emissions in Australia from anthropogenic, natural and recycled sources. Atmos Environ 62:291–302CrossRefGoogle Scholar
  54. Nwuche CO, Ugoji EO (2008) Effects of heavy metal pollution on the soil microbial activity. Int J Environ Sci Technol 5:409–414CrossRefGoogle Scholar
  55. Park BY, Lee JK, Ro HM, Kim YH (2011) Effects of heavy metal contamination from an abandoned mine on nematode community structure as an indicator of soil ecosystem health. Appl Soil Ecol 51:17–24CrossRefGoogle Scholar
  56. Pen-Mouratov S, Rakhimbaev M, Steinberger Y (2003) Seasonal and spatial variation in nematode communities in the Negev Desert ecosystem. J Nematol 35:157–166Google Scholar
  57. Pen-Mouratov S, Shukurov N, Steinberger Y (2008) Influence of industrial heavy metal pollution on soil free-living nematode population. Environ Pollut 152:172–183CrossRefGoogle Scholar
  58. Peredney CL, Williams PL (2000) Utility of Caenorhabditis elegans for assessing heavy metal contamination in artificial soil. Arch Environ Contam Toxicol 39:113–118Google Scholar
  59. Perez E, Appel PWU, Koester-Rasmussen R (2007) Training of small scale miners and their families in safe handling of mercury during extraction of gold in the Philippines: improving access to social services: Health services and income opportunities for small scale miners and their families. GEUS, Geological Survey of Denmark and GreenlandGoogle Scholar
  60. Pirrone N, Cinnirella S, Feng X, Finkelman RB, Friedli HR, Leaner J, Mason R, Mukherjee AB, Stracher GB, Streets DG, Telmer K (2010) Global mercury emissions to the atmosphere from anthropogenic and natural sources. Atmos Chem Phys 10:5951–5964CrossRefGoogle Scholar
  61. Postma-Blaauw MB, de Vries FT, De Goede RGM, Bloem J, Faber JH, Brussaard L (2005) Within-trophic group interactions of bacterivorous nematode species and their effects on the bacterial community and nitrogen mineralization. Oecologia 142:428–439CrossRefGoogle Scholar
  62. Richter S (1993) Phoretic association between the dauer juveniles of Rhabditis stammeri (Rhabditidae) and life history stages of the burying beetle Nicrophorus vespilloides (Coleoptera: Silphidae). Nematologica 39:346–355CrossRefGoogle Scholar
  63. Rieuwerts JS, Thornton I, Farago ME, Ashmore MR (1998) Factors influencing metal bioavailability in soils: preliminary investigations for the development of a critical loads approach for metals. Chem Speciat Bioavailab 10:61–75CrossRefGoogle Scholar
  64. Rohr JR, Salice CJ, Nisbet RM (2016) The pros and cons of ecological risk assessment based on data from different levels of biological organization. Crit Rev Toxicol 46:756–784CrossRefGoogle Scholar
  65. Šalamún P, Renco M, Miklisová D, Hanzelová V (2011) Nematode community structure in the vicinity of a metallurgical factory. Environ Monitor Assess 183:451–464CrossRefGoogle Scholar
  66. Šalamún P, Brazova T, Miklisova D, Hanzelova V (2015) Influence of selected heavy metals (As, Cd, Cr, Cu) on nematode communities in experimental soil microcosms. Helminthologia 52:341–347CrossRefGoogle Scholar
  67. Šalamún P, Hanzelová V, Miklisová D, Šestinová O, Findoráková L, Kováčik P (2017) The effects of vegetation cover on soil nematode communities in various biotopes disturbed by industrial emissions. Sci Total Environ 592:106–114CrossRefGoogle Scholar
  68. Samoiloff MR (1973) Nematode morphogenesis: pattern of transfer of protein to the cuticle of adult Panagrellus silusiae (Cephalobidae). Nematologica 19:15–18CrossRefGoogle Scholar
  69. Sandrin TR, Maier RM (2003) Impact of metals on the biodegradation of organic pollutants. Environ Health Perspect 111:1093CrossRefGoogle Scholar
  70. Sánchez-Moreno S, Navas A (2007) Nematode diversity and food web condition in heavy metal polluted soils in a river basin in southern Spain. Eur J Soil Biol 43:166–179CrossRefGoogle Scholar
  71. Shao Y, Zhang W, Shen J, Zhou L et al (2008) Nematodes as indicators of soil recovery in tailings of a lead/zinc mine. Soil Biol Biochem 40:2040–2046CrossRefGoogle Scholar
  72. Spann N, Goedkoop W, Traunspurger W (2015) Phenanthrene bioaccumulation in the nematode Caenorhabditis elegans. Environ Sci Technol 49:1842–1850CrossRefGoogle Scholar
  73. Spurgeon DJ, Hopkin SP (1995) Extrapolation of the laboratory-based OECD earthworm toxicity test to metal-contaminated field sites. Ecotoxicology 4:190–205CrossRefGoogle Scholar
  74. Stevenson FJ (1976) Stability constants of Cu2+, Pb2+, and Cd2+ complexes with humic acids. Soil Sci Soc Am J 40:665–672CrossRefGoogle Scholar
  75. Teh T, Ab Rahman NNN, Shahadat M, Wong Y, Syakir MI, Omar AM (2016) A comparative study of metal contamination in soil using the borehole method. Environ Monit Assess 188:1–16CrossRefGoogle Scholar
  76. Vranken G, Heip C (1986) Toxicity of copper, mercury and lead to a marine nematode. Mar Pollut Bull 17:453–457CrossRefGoogle Scholar
  77. Walkey A, Black IA (1934) Determination of organic matter in soil. Soil Sci 37:549–556Google Scholar
  78. Whitehead AG, Hemming JR (1965) A comparison of some quantitative methods of extracting small vermiform nematodes from soil. Ann Appl Biol 55:25–38CrossRefGoogle Scholar
  79. Wu Q, He K, Liu P, Li Y, Wang D (2011) Association of oxidative stress with the formation of reproductive toxicity from mercury exposure on hermaphrodite nematode Caenorhabditis elegans. Environ Toxicol Pharmacol 32:175–184CrossRefGoogle Scholar
  80. Xing XJ, Rui Q, Du M, Wang DY (2009) Exposure to lead and mercury in young larvae induces more severe deficits in neuronal survival and synaptic function than in adult nematodes. Arch Environ Contam Toxicol 56:732–741CrossRefGoogle Scholar
  81. Yeates GW, Coleman DC (1982) Role of nematodes in decomposition. Nematodes in soil ecosystems, vol 55. University of Texas Press, Austin, p 80Google Scholar

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Authors and Affiliations

  • Joey Genevieve Martinez
    • 1
    • 2
    • 3
    Email author
  • Shiela Pearl Quiobe
    • 2
  • Tom Moens
    • 1
  1. 1.Marine Biology Section, Biology DepartmentGhent UniversityGhentBelgium
  2. 2.Department of Biological Sciences, College of Science and MathematicsMindanao State University-Iligan Institute of Technology (MSU-IIT)IliganPhilippines
  3. 3.Complex Systems Group, Prime Research Institute of Science and Mathematics (PRISM)MSU-IITIliganPhilippines

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