Skip to main content

Advertisement

SpringerLink
Log in

Mercury accumulation in bats near hydroelectric reservoirs in Peninsular Malaysia

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

In large man-made reservoirs such as those resulting from hydroelectric dam construction, bacteria transform the relatively harmless inorganic mercury naturally present in soil and the submerged plant matter into toxic methylmercury. Methylmercury then enters food webs and can accumulate in organisms at higher trophic levels. Bats feeding on insects emerging from aquatic systems can show accumulation of mercury consumed through their insect prey. In this study, we investigated whether the concentration of mercury in the fur of insectivorous bat species was significantly higher than that in the fur of frugivorous bat species, sampled near hydroelectric reservoirs in Peninsular Malaysia. Bats were sampled at Temenggor Lake and Kenyir Lake and fur samples from the most abundant genera of the two feeding guilds—insectivorous (Hipposideros and Rhinolophus) and frugivorous (Cynopterus and Megaerops) were collected for mercury analysis. We found significantly higher concentrations of total mercury in the fur of insectivorous bats. Mercury concentrations also differed significantly between insectivorous bats sampled at the two sites, with bats from Kenyir Lake, the younger reservoir, showing higher mercury concentrations, and between the insectivorous genera, with Hipposideros bats showing higher mercury concentrations. Ten bats (H. cf. larvatus) sampled at Kenyir Lake had mercury concentrations approaching or exceeding 10 mg/kg, which is the threshold at which detrimental effects occur in humans, bats and mice.

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

  • Agusa T, Kunito T, Yasunaga G, Iwata H, Subramanian A, Ismail A, Tanabe S (2005) Concentrations of trace elements in marine fish and its risk assessment in Malaysia. Mar Pollut Bull 51:896–911

    Article  CAS  Google Scholar 

  • AMNH (American Museum of Natural History) (2013) Wing punch and hair sampling protocols. http://research.amnh.org/vz/mammalogy/donating-bat-tissue-and-hair-samples-genomic-and-stable-isotope-studies/wing-punch-and-hair-sampling. Accessed 1 Oct 2013

  • Barbosa AC, de Souza J, Dórea JG, Jardim WF, Fadini PS (2003) Mercury biomagnification in a tropical black water, Rio Negro, Brazil. Arch Environ Contam Toxicol 45:235–246. doi:10.1007/s00244-003-0207-1

    Article  CAS  Google Scholar 

  • Barros N, Cole JJ, Tranvik LJ, Prairie YT, Bastviken D, Huszar VL et al (2011) Carbon emission from hydroelectric reservoirs linked to reservoir age and latitude. Nat Geosci 4:593–596

    Article  CAS  Google Scholar 

  • Basu N, Scheuhammer A, Grochowina N, Klenavic K, Evans D, O’Brien M, Chan HM (2005) Effects of mercury on neurochemical receptors in wild river otters (Lontra canadensis). Environ Sci Technol 39:3585–3591

    Article  CAS  Google Scholar 

  • Baxter RM (1977) Environmental effects of dams and impoundments. Annu Rev Ecol Syst 8:255–283

    Article  Google Scholar 

  • Benoit JM, Da Cato, Denison KC, Moreira AE (2013) Seasonal mercury dynamics in a New England vernal pool. Wetlands 33:887–894. doi:10.1007/s13157-013-0447-4

    Article  Google Scholar 

  • Bloom NS (1992) On the chemical form of mercury in edible fish and marine invertebrate tissue. Can J Fish Aquat Sci 49:1010–1017

    Article  CAS  Google Scholar 

  • Bodaly RA, Hecky RE, Fudge RJP (1984) Increases in fish mercury levels in lakes flooded by the Churchill River Diversion, Northern Manitoba. Can J Fish Aquat Sci 41:682–691. doi:10.1139/f84-079

    Article  CAS  Google Scholar 

  • Bogdanowicz W, Fenton MB, Daleszczyk K (1999) The relationships between echolocation calls, morphology and diet in insectivorous bats. J Zool 247:381–393

    Article  Google Scholar 

  • Brunet-Rossinni AK, Austad SN (2004) Ageing studies on bats: a review. Biogerontology 5:211–222

    Article  CAS  Google Scholar 

  • Burton GV, Alley RJ, Rasmussen GL, Orton P, Cox V, Jones P, Graff D (1977) Mercury and behavior in wild mouse populations. Environ Res 14:30–34

    Article  CAS  Google Scholar 

  • Chan HM, Scheuhammer AM, Ferran A, Loupelle C, Holloway J, Weech S (2003) Impacts of mercury on freshwater fish-eating wildlife and humans. Hum Ecol Risk Assess 9:867–883

    Article  CAS  Google Scholar 

  • Davidson GWH, Soepadma E, Yap SK (1995) The Malaysian heritage and scientific expedition to Belum: Temenggor Reservoir Forest, 1993–1994. Malayan Nat J 48:133–146

    Google Scholar 

  • Faure PA, Re DE, Clare EL (2009) Wound healing in the flight membranes of big brown bats. J Mammal 90:1148–1156

    Article  Google Scholar 

  • Fitzgerald WF, Engstrom DR, Mason RP, Nater EA (1998) The case for atmospheric mercury contamination in remote areas. Environ Sci Technol 32:1–7

    Article  CAS  Google Scholar 

  • Francis CM (2008) A field guide to the mammals of South-east Asia. New Holland, London

    Google Scholar 

  • Francis CM, Borisenko AV, Ivanova NV et al (2010) The role of DNA barcodes in understanding and conservation of mammal diversity in Southeast Asia. PLoS ONE 5:e12575

    Article  Google Scholar 

  • Fukui D, Murakami M, Nakano S, Aoi T (2006) Effect of emergent aquatic insects on bat foraging in a riparian forest. J Anim Ecol 75:1252–1258

    Article  Google Scholar 

  • Gerrard PM, St. Louis VL (2001) The effects of experimental reservoir creation on the bioaccumulation of methylmercury and reproductive success of tree swallows (Tachycineta bicolor). Environ Sci Technol 35:1329–1338

    Article  CAS  Google Scholar 

  • Hajeb P, Selamat J, Ismail A, Bakar FA, Bakar J, Lioe HN (2008) Hair mercury level of coastal communities in Malaysia: a linkage with fish consumption. Eur Food Res Technol 227:1349–1355

    Article  CAS  Google Scholar 

  • Hajeb P, Jinap S, Ismail A, Fatimah AB, Jamilah B, Abdul Rahim M (2009) Assessment of mercury level in commonly consumed marine fishes in Malaysia. Food Control 20:79–84

    Article  CAS  Google Scholar 

  • Hall BD, Rosenberg DM, Wiens AP (1998) Methyl mercury in aquatic insects from an experimental reservoir. Can J Fish Aquat Sci 55:2036–2047

    Article  Google Scholar 

  • Haro RJ, Bailey SW, Northwick RM, Rolfhus KR, Sandheinrich MB, Wiener JG (2013) Burrowing dragonfly larvae as biosentinels of methylmercury in freshwater food webs. Environ Sci Technol 47:8148–8156

    CAS  Google Scholar 

  • Herbertson K (2013) Sarawak’s Murum dam: What has changed since the indigenous blockade? International Rivers. http://www.internationalrivers.org/blogs/267/sarawak%E2%80%99s-murum-dam-what-has-changed-since-the-indigenous-blockade. Accessed 18 Nov 2013

  • Hickey MBC, Fenton MB, MacDonald KC, Soulliere C (2001) Trace elements in the fur of bats (Chiroptera: Vespertilionidae) from Ontario and Quebec, Canada. Bull Environ Contam Toxicol 66:699–706

    Article  CAS  Google Scholar 

  • Hylander LD, Gröhn J, Tropp M, Vikström A, Wolpher H et al (2006) Fish mercury increase in Lago Manso, a new hydroelectric reservoir in tropical Brazil. J Environ Manag 81:155–166

    Article  CAS  Google Scholar 

  • ICOLD (International Commission on Large Dams) (2014) Number of dams by country members. http://www.icold-cigb.org/GB/World_register/general_synthesis.asp?IDA=206. Accessed 23 Jan 2014

  • Ikingura JR, Akagi H (2003) Total mercury and methylmercury levels in fish from hydroelectric reservoirs in Tanzania. Sci Total Environ 304:355–368

    Article  CAS  Google Scholar 

  • Jiang T, Feng J, Sun K, Wang J (2008) Coexistence of two sympatric and morphologically similar bat species Rhinolophus affinis and Rhinolophus pearsoni. Prog Nat Sci 18:523–532

    Article  Google Scholar 

  • Jones G, Jacobs DS, Kunz TH, Willig MR, Racey PA (2009) Carpe noctem: the importance of bats as bioindicators. Endang Species Res 8:93–115

    Article  Google Scholar 

  • Kamaruddin IS, Kamal AM, Christianus A, Daud SK, Abit L (2011) Fish community in Pengkalan Gawi-Pulau Dula section of Kenyir Lake, Terengganu, Malaysia. J Sustain Sci Manag 6:89–97

    Google Scholar 

  • Khalik WMAWM, Abdullah MP (2012) Seasonal influence on water quality status of Temenggor Lake, Perak. Malay J Analytic Sci 16:163–171

    Google Scholar 

  • Kingston T, Boo Liat L, Zubaid A (2006) Bats of Krau wildlife reserve. Universiti Kebangsaan Malaysia Press, Bangi

    Google Scholar 

  • Lin CYO (2006) Autonomy re-constituted social and gendered implications of dam resettlement on the orang asli of Peninsular Malaysia. Gend Technol Dev 10:77–99

    Article  Google Scholar 

  • Lucotte M, Montgomery S, Bégin M (1999) Mercury dynamics at the flooded soil–water interfacein reservoirs of Northern Quebec: in situ observations. In: Tremblay A, Lucotte M, Schetagne R, Therien N, Langlois C (eds) Mercury in the biogeochemical cycle. Springer, Berling Heidelberg, pp 165–189

    Chapter  Google Scholar 

  • Mergler D, Anderson HA, Chan LHM, Mahaffey KR, Murray M et al (2007) Methylmercury exposure and health effects in humans: a worldwide concern. Ambio 36:3–11

    Article  CAS  Google Scholar 

  • Mogren CL, Walton WE, Parker DR, Trumble JT (2013) Trophic transfer of arsenic from an aquatic insect to terrestrial insect predators. PLoS ONE 8:e67817. doi:10.1371/journal.pone.0067817

    Article  CAS  Google Scholar 

  • Muda H (1991) Diet of small mammals in the secondary tropical forest in Malaysia. J Wildl Park 11:44–52

    Google Scholar 

  • Murata K, Weihe P, Renzoni A, Debes F, Vasconcelos R, Zino F et al (1999) Delayed evoked potentials in children exposed to methylmercury from seafood. Neurotoxicol Teratol 21:343–348

    Article  CAS  Google Scholar 

  • Nam DH, Yates D, Ardapple P, Evers DC, Schmerfeld J, Basu N (2012) Elevated mercury exposure and neurochemical alterations in little brown bats (Myotis lucifugus) from a site with historical mercury contamination. Ecotoxicology 21:1094–1101

    Article  CAS  Google Scholar 

  • Norizam MM, Ali A (2000) A comparative study on the secondary productivity of the littoral and limnetic zone of Temenggor Reservoir, Perak, Malaysia. J Bioscience 11:1–10

    Google Scholar 

  • Pacyna EG, Pacyna JM, Steenhuisen F, Wilson S (2006) Global anthropogenic mercury emission inventory for 2000. Atmos Environ 40:4048–4063

    Article  CAS  Google Scholar 

  • Patra M, Sharma A (2000) Mercury toxicity in plants. Bot Rev 66:379–422

    Article  Google Scholar 

  • Poulain AJ, Barkay T (2013) Cracking the mercury methylation code. Science 339:1280–1281

    Article  CAS  Google Scholar 

  • Razgour O, Clare EL, Zeale MR, Hanmer J, Schnell IB, Rasmussen M et al (2011) High-throughput sequencing offers insight into mechanisms of resource partitioning in cryptic bat species. Ecol Evol 1:556–570

    Article  Google Scholar 

  • Reidinger RF (1972) Factors influencing Arizona bat population levels. Dissertation University of Arizona

  • Rodgers DW, Dickman M, Han X (1995) Stores from old reservoirs: sediment Hg and Hg methylation in Ontario hydroelectric developments. Water Air Soil Pollut 80:829–839

    Article  CAS  Google Scholar 

  • Rojas D, Mancina CA, Flores-Martínez JJ, Navarro L (2013) Phylogenetic signal, feeding behaviour and brain volume in neotropical bats. J Evol Biol 26:1925–1933

    Article  CAS  Google Scholar 

  • Rouf AA, Phang SM, Ambak MA (2010) Depth distribution and ecological preferences of periphytic algae in Kenyir Lake, the largest tropical reservoir of Malaysia. Chinese J Oceanol Limnol 28:856–867

    Article  Google Scholar 

  • Selin NE, Jacob DJ, Park RJ, Yantosca RM, Strode S, Jaeglé L, Jaffe D (2007) Chemical cycling and deposition of atmospheric mercury: global constraints from observations. Atmos, J Geophys Res. doi:10.1029/2006JD007450

    Google Scholar 

  • Sing KW, Syaripuddin K, Wilson JJ (2013) Changing perspectives on the diversity of bats (Mammalia:Chiroptera) at Ulu Gombak since the establishment of the field study centre in 1965. Raffles Bull Zool S29:211–217

    Google Scholar 

  • Sivalingam PM, Sani AB (1980) Mercury content in hair from fishing communities of the State of Penang, Malaysia. Mar Pollut Bul 11:188–191

    Article  CAS  Google Scholar 

  • Stewart AR, Saiki MK, Kuwabara JS, Alpers CN, Marvin-DiPasquale M, Krabbenhoft DP (2008) Influence of plankton mercury dynamics and trophic pathways on mercury concentrations of top predator fish of a mining-impacted reservoir. Can J Fish Aquat Sci 65:2351–2366

    Article  CAS  Google Scholar 

  • Stokes PM, Wren CD (1987) Bioaccumulation of mercury by aquatic biota in hydroelectric reservoirs: a review and consideration of mechanisms. Lead mercury arsenic environ. In: Hutchinson TC, Meema KM (eds) Lead mercury arsenic environ. Wiley, New York, pp 255–278

    Google Scholar 

  • Thabah A, Rossiter SJ, Kingston T, Zhang S, Parsons S, Mya KM et al (2006) Genetic divergence and echolocation call frequency in cryptic species of Hipposideros larvatus sl (Chiroptera: Hipposideridae) from the Indo-Malayan region. Biol J Linn Soc 88:119–130

    Article  Google Scholar 

  • Thin LW (2013) Proposed Malaysia dams raise transparency, livelihood fears. Thomson Reuters Foundation. http://www.trust.org/item/20130521123410-dp5oe/?source=hptop. Accessed 3 Jan 2014

  • Tremblay A, Lucotte M (1997) Accumulation of total mercury and methyl mercury in insect larvae of hydroelectric reservoirs. Can J Fish Aquat Sci 54:832–841

    Article  CAS  Google Scholar 

  • Tweedy BN, Drenner RW, Chumchal MM, Kennedy JH (2013) Effects of fish on emergent insect-mediated flux of methyl mercury across a gradient of contamination. Environ Sci Technol 47:1614–1619

    CAS  Google Scholar 

  • US EPA (Environmental Protection Agency) (2001). Water quality criterion for the protection of human health: methylmercury, final. EPA-823-R-01-001. Washington. http://www.epa.gov/waterscience/criteria/methylmercury/document.html. Accessed 17 Feb 2013

  • US EPA (Environmental Protection Agency) (2007). Mercury in solids and solutions by thermal decomposition, amalgamation, and atomic absorption spectrophotometry. EPA Method 7473. http://www.epa.gov/osw/hazard/testmethods/sw846/pdfs/7473.pdf. Accessed 2 May 2014

  • Wada H, Yates DE, Evers DC, Taylor RJ, Hopkins WA (2010) Tissue mercury concentrations and adrenocortical responses of female big brown bats (Eptesicus fuscus) near a contaminated river. Ecotoxicology 19:1277–1284

    Article  CAS  Google Scholar 

  • Walker LA, Simpson VR, Rockett L, Wienburg CL, Shore RF (2007) Heavy metal contamination in bats in Britain. Environ Pollut 148:483–490

    Article  CAS  Google Scholar 

  • Wilson JJ, Sing K-W, Halim MRA, Ramli R, Hashim R, Sofian-Azirun M (2014) Utility of DNA barcoding for rapid and accurate assessment of bat diversity in Malaysia in the absence of formally described species. Genet Mol Res 13:920–925

  • Wolfe MF, Schwarzbach S, Sulaiman RA (1998) Effects of mercury on wildlife: a comprehensive review. Environ Toxicol Chem 17:146–160

    Article  CAS  Google Scholar 

  • Yates DE, Kunz TH, Evers DC, Divoll T (2011) Assessment of mercury accumulation in bat fur from 8 countries around the world. Poster presented at The 10th international conference on mercury as a global pollutant, Halifax, Nova Scotia

  • Yates DE, Adams EM, Angelo SE, Evers DC, Schmerfeld J, Moore MS et al (2014) Mercury in bats from the northeastern United States. Ecotoxicology 23:45–55

    Article  CAS  Google Scholar 

Download references

Acknowledgments

KS and KWS were supported in part by Research Assistantships at the Museum of Zoology through a special grant (A-21010-DA322-B29000) from the University of Malaya. Research expenses were supported by grants from the University of Malaya (PG099-2012B; RP003D-13SUS) to JJW and Mohd Sofian-Azirun (UM). The Department of Wildlife and National Parks provided a permit for fieldwork in Peninsular Malaysia. Noraishah Abdul-Aziz assisted in securing the permit. The Department of Forestry of Terengganu also issued a permit for fieldwork in Kenyir. Reuben Clements of RIMBA (myrimba.org) helped in planning, providing accommodation and engaging field guides at Temenggor and Kenyir. Field equipment was loaned from the Ecology and Biodiversity Program, Institute of Biological Sciences, UM. Locals from Pulau Tujuh Village, Gerik and Muhamad Fauzi Abdul Hamid assisted with fieldwork. We thank Dave Yates and Dave Evers, for providing access to unpublished data, and Kevin Regan at the Biodiversity Research Institute. Rosli Ramli (UM) provided comment on this project in his capacity as MSc co-supervisor to KS. Joanna Coleman (NUS) provided a venue for discussion which led to this collaboration.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Museum of Zoology, Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603, Kuala Lumpur, Malaysia

    Khairunnisa Syaripuddin, Kong-Wah Sing & John-James Wilson

  2. Ecology and Biodiversity Program, Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603, Kuala Lumpur, Malaysia

    Khairunnisa Syaripuddin, Kong-Wah Sing, Muhammad-Nasir Nursyereen & John-James Wilson

  3. Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA, 02139, USA

    Anjali Kumar

  4. Zoological and Ecological Research Network (ZEN), Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603, Kuala Lumpur, Malaysia

    Muhammad-Rasul Abdullah Halim

Authors
  1. Khairunnisa Syaripuddin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anjali Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kong-Wah Sing
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Muhammad-Rasul Abdullah Halim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Muhammad-Nasir Nursyereen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. John-James Wilson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John-James Wilson.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Syaripuddin, K., Kumar, A., Sing, KW. et al. Mercury accumulation in bats near hydroelectric reservoirs in Peninsular Malaysia. Ecotoxicology 23, 1164–1171 (2014). https://doi.org/10.1007/s10646-014-1258-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-014-1258-y

Keywords

Search

Navigation