Mercury accumulation in bats near hydroelectric reservoirs in Peninsular Malaysia
- 501 Downloads
- 12 Citations
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.
Keywords
Mercury Hipposideros Rhinolophus Megaerops Cynopterus Hydroelectric reservoirsNotes
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.
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 51:896–911CrossRefGoogle 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 CrossRefGoogle 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 4:593–596CrossRefGoogle 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 39:3585–3591CrossRefGoogle Scholar
- Baxter RM (1977) Environmental effects of dams and impoundments. Annu Rev Ecol Syst 8:255–283CrossRefGoogle 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 CrossRefGoogle Scholar
- Bloom NS (1992) On the chemical form of mercury in edible fish and marine invertebrate tissue. Can J Fish Aquat Sci 49:1010–1017CrossRefGoogle 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 CrossRefGoogle Scholar
- Bogdanowicz W, Fenton MB, Daleszczyk K (1999) The relationships between echolocation calls, morphology and diet in insectivorous bats. J Zool 247:381–393CrossRefGoogle Scholar
- Brunet-Rossinni AK, Austad SN (2004) Ageing studies on bats: a review. Biogerontology 5:211–222CrossRefGoogle 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 14:30–34CrossRefGoogle 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 9:867–883CrossRefGoogle Scholar
- Davidson GWH, Soepadma E, Yap SK (1995) The Malaysian heritage and scientific expedition to Belum: Temenggor Reservoir Forest, 1993–1994. Malayan Nat J 48:133–146Google Scholar
- Faure PA, Re DE, Clare EL (2009) Wound healing in the flight membranes of big brown bats. J Mammal 90:1148–1156CrossRefGoogle Scholar
- Fitzgerald WF, Engstrom DR, Mason RP, Nater EA (1998) The case for atmospheric mercury contamination in remote areas. Environ Sci Technol 32:1–7CrossRefGoogle Scholar
- Francis CM (2008) A field guide to the mammals of South-east Asia. New Holland, LondonGoogle 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:e12575CrossRefGoogle 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 75:1252–1258CrossRefGoogle 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 35:1329–1338CrossRefGoogle 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 227:1349–1355CrossRefGoogle 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 20:79–84CrossRefGoogle Scholar
- Hall BD, Rosenberg DM, Wiens AP (1998) Methyl mercury in aquatic insects from an experimental reservoir. Can J Fish Aquat Sci 55:2036–2047CrossRefGoogle 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 47:8148–8156Google 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 66:699–706CrossRefGoogle 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 81:155–166CrossRefGoogle 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 304:355–368CrossRefGoogle 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 18:523–532CrossRefGoogle Scholar
- Jones G, Jacobs DS, Kunz TH, Willig MR, Racey PA (2009) Carpe noctem: the importance of bats as bioindicators. Endang Species Res 8:93–115CrossRefGoogle 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 6:89–97Google Scholar
- Khalik WMAWM, Abdullah MP (2012) Seasonal influence on water quality status of Temenggor Lake, Perak. Malay J Analytic Sci 16:163–171Google Scholar
- Kingston T, Boo Liat L, Zubaid A (2006) Bats of Krau wildlife reserve. Universiti Kebangsaan Malaysia Press, BangiGoogle Scholar
- Lin CYO (2006) Autonomy re-constituted social and gendered implications of dam resettlement on the orang asli of Peninsular Malaysia. Gend Technol Dev 10:77–99CrossRefGoogle 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 165–189CrossRefGoogle 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 36:3–11CrossRefGoogle 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 CrossRefGoogle Scholar
- Muda H (1991) Diet of small mammals in the secondary tropical forest in Malaysia. J Wildl Park 11:44–52Google 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 21:343–348CrossRefGoogle 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 21:1094–1101CrossRefGoogle 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 11:1–10Google Scholar
- Pacyna EG, Pacyna JM, Steenhuisen F, Wilson S (2006) Global anthropogenic mercury emission inventory for 2000. Atmos Environ 40:4048–4063CrossRefGoogle Scholar
- Patra M, Sharma A (2000) Mercury toxicity in plants. Bot Rev 66:379–422CrossRefGoogle Scholar
- Poulain AJ, Barkay T (2013) Cracking the mercury methylation code. Science 339:1280–1281CrossRefGoogle 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 1:556–570CrossRefGoogle Scholar
- Reidinger RF (1972) Factors influencing Arizona bat population levels. Dissertation University of ArizonaGoogle Scholar
- Rodgers DW, Dickman M, Han X (1995) Stores from old reservoirs: sediment Hg and Hg methylation in Ontario hydroelectric developments. Water Air Soil Pollut 80:829–839CrossRefGoogle Scholar
- Rojas D, Mancina CA, Flores-Martínez JJ, Navarro L (2013) Phylogenetic signal, feeding behaviour and brain volume in neotropical bats. J Evol Biol 26:1925–1933CrossRefGoogle 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 28:856–867CrossRefGoogle 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 S29:211–217Google Scholar
- Sivalingam PM, Sani AB (1980) Mercury content in hair from fishing communities of the State of Penang, Malaysia. Mar Pollut Bul 11:188–191CrossRefGoogle 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 65:2351–2366CrossRefGoogle 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 255–278Google 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 88:119–130CrossRefGoogle 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 54:832–841CrossRefGoogle 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 47:1614–1619Google 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 19:1277–1284CrossRefGoogle Scholar
- Walker LA, Simpson VR, Rockett L, Wienburg CL, Shore RF (2007) Heavy metal contamination in bats in Britain. Environ Pollut 148:483–490CrossRefGoogle 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 13:920–925Google Scholar
- Wolfe MF, Schwarzbach S, Sulaiman RA (1998) Effects of mercury on wildlife: a comprehensive review. Environ Toxicol Chem 17:146–160CrossRefGoogle 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 ScotiaGoogle Scholar
- Yates DE, Adams EM, Angelo SE, Evers DC, Schmerfeld J, Moore MS et al (2014) Mercury in bats from the northeastern United States. Ecotoxicology 23:45–55CrossRefGoogle Scholar