Effects of habitat on mercury concentrations in fish: a case study of Nile perch (Lates niloticus) in Lake Nabugabo, Uganda

Abstract

This study focused on variation in fish mercury (Hg) concentrations in 185 Nile perch (Lates niloticus) samples collected across four different habitat types in Lake Nabugabo, Uganda, a tropical lake located proximate to Lake Victoria. We quantified the stomach contents of Nile perch using the % index of relative importance, as well as, nitrogen and carbon isotopic concentrations to assess the role of diet and trophic level on Hg concentrations. In each habitat, we also evaluated a suite of chemical and physical characteristics that are commonly associated with variation in Hg bioavailability in temperate systems. Using linear mixed models and ANOVA, we demonstrate that habitat of capture is an important predictor of Hg concentrations in Nile perch from Lake Nabugabo and that the relationship between habitat and Hg is size and diet dependent. Nile perch diet as well as dissolved oxygen concentration and pH were also correlated with observed differences in fish Hg. Overall, Hg concentrations in Nile perch were all well below the WHO/FAO recommended guideline of 500 ng/g (mean 13.6 ± 0.4 ng/g wet weight; range 4.9 and 29.3 ng/g wet weight). This work contributes to a growing awareness of intra-lake divergence in Nile perch, as well as, divergence in Hg concentrations between varying aquatic habitat types, particularly wetlands.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Balirwa JS (2007) Ecological, environmental and socioeconomic aspects of the Lake Victoria’s introduced Nile perch fishery in relation to the native fisheries and the species culture potential: lessons to learn. Afr J Ecol 45:120–129

    Article  Google Scholar 

  2. Balirwa JS, Chapman CA, Chapman LJ, Cowx IG, Geheb K, Kaufman L, Lowe-McConnell RH, Seehausen O, Wanink JH, Wlcomme RL, Witte F (2003) Biodiversity and fishery sustainability in the Lake Victoria basin: an unexpected marriage? Bioscience 53:703–715

    Article  Google Scholar 

  3. Basu N, Klenavic K, Gamberg M, O’Brien M, Evans D, Scheuhammer AM, Chan HG (2005) Effects of mercury on neurochemical receptor-binding characteristics in wild mink. Environ Toxicol Chem 24:1444–1450

    Article  CAS  Google Scholar 

  4. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. CRAN. http://cran.r-project.org/web/packages/lme4/index.html. Accessed 1 Apr 2015

  5. Benoit JM, Gilmour C, Heyes A, Mason RP, Miller C (2003) Geochemical and biological controls over methylmercury production and degradation in aquatic ecosystems. In: Chai Y, Braids OC (eds) Biogeochemistry of environmentally important trace elements. ACS Symposium Series 835. American Chemical Society, Washington, DC, pp 262–297

    Google Scholar 

  6. Black FJ, Bokhutlo T, Somoxa A, Maethamako M, Modisaemang O, Kemosedile T, Chimbari M (2011) The tropical African mercury anomaly: lower than expected mercury concentrations in fish and human hair. Sci Total Environ 409:1967–1975

    Article  CAS  Google Scholar 

  7. Braaten HFV, de Wit HA, Fjeld E, Rognerud S, Lydersen E, Larssen T (2014) Environmental factors influencing mercury speciation in Subarctic and Boreal lakes. Sci Total Environ 476–477:336–345

    Article  Google Scholar 

  8. Budeba YL, Cowx IG (2007) Contribution of Caridina nilotica (Roux) in the dagaa fishery in Lake Victoria, Tanzania. Aquat Ecosyst Health Manag 10:381–391

    Article  Google Scholar 

  9. Campbell LM, Dixon DG, Hecky RE (2003) A review of mercury in Lake Victoria, East Africa: implications for human and ecosystem health. J Toxicol Environ Health B 6:325–356

    Article  CAS  Google Scholar 

  10. Campbell LM, Balirwa J, Dixon D, Hecky R (2004) Biomagnification of mercury in fish from Thruston Bay, Napoleon Gulf, Lake Victoria (East Africa). Afr J Aquat Sci 29:91–96

    Article  CAS  Google Scholar 

  11. Caron S, Lucotte M, Teisserenc R (2008) Mercury transfer from watersheds to aquatic environments following the erosion of agrarian soils: a molecular biomarker approach. Can J Soil Sci 88:801–811

    Article  CAS  Google Scholar 

  12. Castro MS, Hilderbrand RH, Thompson J, Heft A, Rivers SE (2007) Relationship between wetlands and mercury in brook trout. Arch Environ Contam Toxicol 52:97–103

    Article  CAS  Google Scholar 

  13. Chapman LJ, Chapman CA, Schofield PJ, Olowo JP, Kaufman L, Seehausen O, Ogutu-Ohwayo R (2003) Fish faunal resurgence in Lake Nabugabo, East Africa. Conserv Biol 17:500–511

    Article  Google Scholar 

  14. Chen CY, Folt CL (2005) High plankton densities reduce mercury biomagnification. Environ Sci Technol 39:115–121

    Article  CAS  Google Scholar 

  15. Chen CY, Driscoll CT, Kamman NC (2012) Mercury hotspots in freshwater ecosystems: drivers, processes, and patterns. In: Bank MS (ed) Mercury in the environment: pattern and process. University of California Press, Berkley, pp 143–166

    Chapter  Google Scholar 

  16. Chételat J, Amyot M, Garcia E (2011) Habitat-specific bioaccumulation of methylmercury in invertebrates of small mid-latitude lakes in North America. Environ Pollut 159:10–17

    Article  Google Scholar 

  17. Chételat J, Cloutie L, Amyot M (2013) An investigation of enhanced mercury bioaccumulation in fish from offshore feeding. Ecotoxicology 22:1020–1032

    Article  Google Scholar 

  18. Chumchal MM, Drenner RW, Fry B, David K, Newland LW (2008) Habitat-specific differences in mercury concentration in a top predator from a shallow lake. Trans Am Fish Soc 137:195–208

    Article  Google Scholar 

  19. Clarkson TW, Magos L, Myers GJ (2003) The toxicology of mercury-current exposures and clinical manifestations. N Engl J Med 349:1731–1737

    Article  CAS  Google Scholar 

  20. Clayden MG, Kidd KA, Wyn B, Kirk JL, Muir DCG, O’Driscoll NJ (2013) Mercury biomagnification through food webs is affected by physical and chemical characteristics of lakes. Environ Sci Technol 47:12047–12053

    Article  CAS  Google Scholar 

  21. Cortés E (1997) A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Can J Fish Aquat Sci 54:726–738

    Article  Google Scholar 

  22. Driscoll CT, Han YJ, Chen CY, Evers DC, Lambert KF, Holsen TM, Kamman NC, Munson RK (2007) Mercury contamination in forest and freshwater ecosystems in the Northeastern United States. BioScience 57:17–28

    Google Scholar 

  23. Evers DC, Han YJ, Driscoll CT, Kamman NC, Goodale W, Lambert KF, Holsen TM, Chen CY, Clair TA, Butler T (2007) Biological mercury hotspots in the Northeastern United States and Southeastern Canada. BioScience 57:29–43

    Article  Google Scholar 

  24. Friedli HR, Radke LF, Lu JY, Banic CM, Leaitch WR, MacPherson JI (2003) Mercury emissions from burning of biomass from temperate North American forests: laboratory and airborne measurements. Atmos Environ 37:253–267

    Article  CAS  Google Scholar 

  25. Galloway MF, Branfireun BA (2004) Mercury dynamics of a temperate forested wetland. Sci Total Environ 325:239–254

    Article  CAS  Google Scholar 

  26. Gilmour CC, Henry EA, Mitchell R (1992) Sulfate stimulation of mercury methylation in freshwater sediments. Environ Sci Technol 26:2281–2287

    Article  CAS  Google Scholar 

  27. Grigal DF (2003) Mercury sequestration in forests and peatlands: a review. J Environ Qual 32:393–405

    Article  CAS  Google Scholar 

  28. Hanna DEL, Solomon C, Poste AE, Buck DG, Chapman LJ (2015) A review of mercury concentrations in freshwater fishes of Africa: patterns and predictors. Environ Toxicol Chem 34:215–223

    Article  CAS  Google Scholar 

  29. Hughes NF (1992) Growth and reproduction of the Nile perch, Lates niloticus, an introduced predator, in the Nyanza Gulf, Lake Victoria, East Africa. Environ Biol Fish 33:299–305

    Article  Google Scholar 

  30. Hyslop EJ (1980) Stomach contents analysis-a review of methods and their application. J Fish Biol 17:411–429

    Article  Google Scholar 

  31. Jackson A, Inger R, Parnell A, Bearhop S (2011) Comparing isotopic niche widths among and withing communities: sIBER-Stable Isotope Bayesian Ellipses in R. J Anim Ecol 3:595–602

    Article  Google Scholar 

  32. Karagas MR, Choi AL, Oken E, Horvat M, Schoeny R, Kamai E, Cowell W, Grandjean P, Korrick S (2012) Evidence on the human health effects of low-level methylmercury exposure. Environ Health Perspect 120:799–806

    Article  CAS  Google Scholar 

  33. Karimi R, Chen CY, Pickhardt PC, Fisher NS, Folt CL (2007) Stoichiometric controls of mercury dilution by growth. PNAS 104:7477–7482

    Article  CAS  Google Scholar 

  34. Kelly EN, Schindler DW, St. Louis VL, Donald DB, Vladicka KE (2006) Forest fire increases mercury accumulation by fishes via food web restructuring and increased mercury inputs. PNAS 103:19380–19385

    Article  CAS  Google Scholar 

  35. Kidd KA, Bootsma HA, Hesslein RH, Lyle Lockhart W, Hecky RE (2003) Mercury concentrations in the food web of Lake Malawi, East Africa. J Great Lakes Res 29:258–266

    Article  CAS  Google Scholar 

  36. Kitchell JF, Schindler DE, Ogutu-Ohwayo R, Reinthal PN (1997) The Nile perch in Lake Victoria: interactions between predation and fisheries. Ecol Appl 7:653–664

    Article  Google Scholar 

  37. Krabbenhoft DP, Wiener JG, Brumbaugh WG, Olson ML, DeWild JF, Sabin TJ (1999) A national pilot study of mercury contamination of aquatic ecosystems along multiple gradients. In US geological survey toxic substances hydrology program: proceedings of the technical meeting, Charleston, South Carolina, March 8–12, 1999, vol. 2. Contamination of Hydrologic Systems and Related Ecosystems. US Geological Survey Water-Resources Investigations Report no. 99-4018B (Eds. D.W. Morganwalp and H.T. Buxton), pp.147–160

  38. Lavoie RA, Jardine TD, Chumchal MM, Kidd KA, Campbell LM (2013) Biomagnification of mercury in aquatic food webs: a worldwide meta-analysis. Environ Sci Technol 47:13385–13394

    Article  CAS  Google Scholar 

  39. Layman CA, Araujo MS, Boucek R, Harrison E, Jud ZR, Matich P et al (2012) Applying stable isotopes to examine food web structure: an overview of analytical tools. Biol Rev 87:542–562

    Article  Google Scholar 

  40. Mazerolle MJ. (2015). R Package “AICcmodavg”. CRAN. https://cran.r-project.org/web/packages/AICcmodavg/AICcmodavg.pdf. Accessed 2 Sep 2015

  41. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  42. Nkalubo WN (2012) Life history traits and growth of Nile perch (Lates niloticus) in Lake Victoria, Uganda: Implications for the management of the fishery. PhD Dissertation, Makerere University, Uganda

  43. Nkalubo WN, Chapman LJ, Muyodi F (2014) Feeding ecology of the intensively fished Nile perch, Lates niloticus, in Lake Victoria, Uganda. Aquat Ecosyst Health Manag 17:62–69

    Google Scholar 

  44. Nyboer EA, Chapman LJ (2013a) Ontogenetic shifts in phenotype-environment associations in Nile perch, Lates niloticus (Perciformes: Latidae) from Lake Nabugabo, Uganda. Biol J Linn Soc 110:449–465

    Article  Google Scholar 

  45. Nyboer EA, Chapman LJ (2013b) Movement and home range of introduced Nile perch (Lates niloticus) in Lake Nabugabo, Uganda: implications for ecological divergence and fisheries management. Fish Res 137:18–29

    Article  Google Scholar 

  46. Nyboer EA, Gray SM, Chapman LJ (2014) A colourful youth: ontogenetic colour change is habitat-specific in the invasive Nile perch. Hydrobiologia 738:221–234

    Article  Google Scholar 

  47. Ogutu-Ohwayo R (1993) The effects of predation by Nile perch, Lates niloticus L., in the fish of Lake Nabugabo, with suggestions for conservation of endangered endemic cichlids. Conserv Biol 7:701–711

    Article  Google Scholar 

  48. Ogutu-Ohwayo R (1994) Adjustments in fish stocks and in life history characteristics of Nile perch, Lates niloticus L. in lakes Victoria, Kyota, and Nabugabo. PhD Dissertation, University of Manitoba, Winnipeg, Canada

  49. Ogutu-Ohwayo R (2004) Management of the Nile perch, Lates niloticus fishery in Lake Victoria in light of the changes in its life history characteristics. Afr J Ecol 42:306–314

    Article  Google Scholar 

  50. Parnell A, Jackson A (2014) R Package ‘siar’. http://cran.r-project.org/web/packages/siar/index.html. Accessed 1 Apr 2015

  51. Paterson JA, Chapman LJ (2009) Fishing down and fishing hard: ecological change in the Nile perch of Lake Nabugabo, Uganda. Ecol Freshw Fish 18:380–394

    Article  Google Scholar 

  52. Paterson JA, Chapman LJ, Schofield PJ (2010) Intraspecific variation in gill morphology of juvenile Nile perch, Lates niloticus, in Lake Nabugabo, Uganda. Environ Biol Fish 88:97–104

    Article  Google Scholar 

  53. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 181:293–320

    Article  Google Scholar 

  54. Pickhardt PC, Folt CL, Chen CY, Klaue B, Blum JD (2002) Algal blooms reduce the uptake of toxic methylmercury in freshwater food webs. PNAS 99:4419–4423

    Article  CAS  Google Scholar 

  55. Pringle RM (2005) The origins of the Nile perch in Lake Victoria. Bioscience 55:780–787

    Article  Google Scholar 

  56. R Core Team. (2013) R: A language and environment for statistical computing. Vienna, Austria. http://www.r-project.org/. Accessed 1 April 2015

  57. Regnell O, Tunlid A, Ewald G, Sangfors O (1996) Methyl mercury production in freshwater microcosms affected by dissolved oxygen levels: role of cobalamin and microbial community composition. Can J Fish Aquat Sci 53:1535–1545

    CAS  Google Scholar 

  58. Rypel AL (2010) Mercury concentrations in lentic fish populations related to ecosystem and watershed characteristics. Ambio 39:14–19

    Article  CAS  Google Scholar 

  59. Schetagne R, Doyo JF, Fournier JJ (2000) Export of mercury downstream from reservoirs. Sci Total Environ 260:135–145

    Article  CAS  Google Scholar 

  60. Schofield P, Chapman LJ (1999) Interactions between Nile perch, Lates niloticus, and other fishes in Lake Nabugabo, Uganda. Environ Biol Fish 55:343–358

    Article  Google Scholar 

  61. Selvendiran P, Driscoll CT, Montesdeoca MR, Bushey JT (2008) Inputs, storage and transport of total and methyl mercury in two temperate forest wetlands. J Geophys Res 113:G00C01

    Google Scholar 

  62. Simonin HA, Loukmas JJ, Skinner LC, Roy KM (2008) Lake variability: key factors controlling mercury concentrations in New York State fish. Environ Pollut 154:107–115

    Article  CAS  Google Scholar 

  63. St. Louis VL, Rudd JWM, Kelly CA, Beaty KG, Bloom NS, Flett RJ (1994) Importance of wetlands as sources of methyl mercury to boreal forest ecosystems. Can J Fish Aquat Sci 51:1065–1076

    Article  CAS  Google Scholar 

  64. Stager JC, Westwood J, Grzesik D, Cumming BF (2005) A 5500-year environmental history of Lake Nabugabo, Uganda. Palaeogeogr Palaeoclim Palaeoecol 218:347–354

    Article  Google Scholar 

  65. Tremblay A, Ransijn J (2013) R Package “LMERConvenienceFunctions”. http://cran.r-project.org/web/packages/LMERConvenienceFunctions/index.html

  66. Trueman CN, McGill RAR, Guyard PH (2005) The effect of growth rate on tissue-diet spacing in rapidly growing animals. An experimental study with Atlantic salmon (Salmo salar). Rapid Commun Mass Spectrom 19:3239–3247

    Article  CAS  Google Scholar 

  67. Turner TF, Collyer ML, Krabbenhoft TJ (2010) A general hypothesis-testing framework for stable isotope ratios in ecological studies. Ecology 91:2227–2233

    Article  Google Scholar 

  68. Ullrich SM, Tanto TW, Abdrashitova SA (2001) Mercury in the aquatic environment: a review of factors affecting methylation. Crit Rev Environ Sci Technol 31:241–293

    Article  CAS  Google Scholar 

  69. Vaccaro I, Chapman CA, Nyboer EA, Luke M, Byekwaso A, Morgan C, Mbabazi D, Twinomugisha D, Chapman LJ (2013) An interdisciplinary method to harmonize ecology, economy, and co-management: fisheries exploitation in Lake Nabugabo, Uganda. Afr J Aquat Sci 38:97–104

    Article  Google Scholar 

  70. Van Stratten P (2000) Mercury contamination associated with small-scale gold mining in Tanzania and Zimbabwe. Sci Total Environ 259:105–113

    Article  Google Scholar 

  71. Ward DM, Nislow KH, Chen CY, Folt CL (2010) Rapid, efficient growth reduces mercury concentrations in stream-dwelling Atlantic salmon. Trans Am Fish Soc 139:1–10

    Article  CAS  Google Scholar 

  72. Wiener JG, Krabbenhoft DP, Heinz GH, Scheuhammer AM (2003) Ecotoxicology of mercury. In: Hoffman D, Rattner B, Burton G, Cairns J (eds) Handbook of ecotoxicology. Lewis, Washington, DC, pp 409–464

    Google Scholar 

  73. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, Amsterdam

    Book  Google Scholar 

Download references

Acknowledgments

We would like to thank two anonymous reviewers for feedback on an earlier version of this manuscript, as well as, Amanda E. Poste and Hans Frederick Braaten from the Norweigian Institute of Water Research for their interest in Lake Nabugabo and their help with lab work. Thank you Vincent Fugère and Catherine Baltazar for help with statistical analyses and to the Timothy Moore lab at McGill University for their help running DOC and TN samples, as well as, the Marc Amyot lab at Université de Montréal, for guidance regarding field procedures.. Thank you to Kevin Regan at the Biodiversity Research Institute for assistance with mercury analysis on the DMA. Michael Collyer assisted with code in R for the isotopic analysis. This project would not have been possible without the help of dedicated Ugandan field assistants Jackson Mutebe, Geoffry Kiberu, and Fred Sseguya, as well as, Dr. Dennis Twinomuguisha. Funding for the project was provided by the Natural Science and Engineering Research Council of Canada (NSERC), the Fonds de recherche du Québec en nature et technologie, the Quebec Center of Biodiversity Science, the Norwegian Institute for Water Sciences, the National Geographic Society, and McGill University, as well as funds to Lauren Chapman (NSERC Discovery Grant, Canada Research Chair research funds).

Author information

Affiliations

Authors

Corresponding author

Correspondence to D. E. L. Hanna.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 2171 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hanna, D.E.L., Buck, D.G. & Chapman, L.J. Effects of habitat on mercury concentrations in fish: a case study of Nile perch (Lates niloticus) in Lake Nabugabo, Uganda. Ecotoxicology 25, 178–191 (2016). https://doi.org/10.1007/s10646-015-1578-6

Download citation

Keywords

  • Biomagnification
  • Wetlands
  • Freshwater
  • Contaminants
  • Africa