Skip to main content
Log in

Dietary (periphyton) and aqueous Zn bioaccumulation dynamics in the mayfly Centroptilum triangulifer

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Diet is often the predominant route of trace metal exposure in aquatic insects. In freshwater ecosystems, periphyton serves as a primary source of food to many aquatic insects and is a major sink for trace metals. We investigated the bioconcentration of the essential metal Zn by periphyton using 65Zn as a radiotracer. At relatively low dissolved concentrations (2–20 μg L−1), non steady state Zn bioconcentration by periphyton averaged 6,099 ± 2,430-fold, with much of the variability determined by loading regime (number of renewals and duration of exposures). Labeled periphyton was used as a food source for dietary accumulation studies with the mayfly Centroptilum triangulifer. After 29 days, larvae concentrated Zn 19-, 16- and 17-fold relative to dietary Zn concentrations of 8.1, 43.2 and 82.3 μg g−1 (dry weight), respectively. Adults from that same cohort only concentrated Zn 8-, 3- and 3- fold relative to those same dietary concentrations, revealing that mayflies lose significant Zn prior to reaching adulthood. Anecdotal evidence suggests that this loss occurs prior to emergence to the subimago, as negligible Zn was found in the subimago to imago exuvium. Across a range of adult tissue concentrations, maternal transfer consistently averaged 26.7 %. Uptake (ku, 0.26 L g−1 d−1) and efflux rate constants (ke, 0.001–0.007 d−1) were measured and assimilation efficiencies from dietary Zn concentrations of 4.9 and 59.7 μg Zn g−1 were estimated to be 88 ± 4 % and 64 ± 15 %, respectively. Both life cycle and biodynamic modeling approaches point towards diet being the primary route of Zn bioaccumulation in this mayfly.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Ancion PY, Lear G, Lewis GD (2010) Three common metal contaminants of urban runoff (Zn, Cu & Pb) accumulate in freshwater biofilm and modify embedded bacterial communities. Environ Pollut 158(8):2738–2745

    Article  CAS  Google Scholar 

  • Arini A, Baudrimont M, Feurtet-Mazel A, Coynel A, Blanc G, Coste M, Delmas F (2011) Comparison of periphytic biofilm and filter-feeding bivalve metal bioaccumulation (Cd and Zn) to monitor hydrosystem restoration after industrial remediation: a year of biomonitoring. J Environ Monit 13(12):3386–3398

    Article  CAS  Google Scholar 

  • Behra R, Landwehrjohann R, Vogal L, Wagner B, Sigg L (2002) Copper and zinc content of periphyton from two rivers as a function of dissolved metal concentration. Aquat Sci 64(3):300–306

    Article  CAS  Google Scholar 

  • Biggs BJF, Tuchman NC, Lowe RL, Stevenson RJ (1999) Resource stress alters hydrological disturbance effects in a stream periphyton community. Oikos 85(1):95–108

    Article  Google Scholar 

  • Brix KV, DeForest DK, Adams WJ (2011) The sensitivity of aquatic insects to divalent metals: a comparative analysis of laboratory and field data. Sci Total Environ 409(20):4187–4197

    Article  CAS  Google Scholar 

  • 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(13):4821–4828

    Article  CAS  Google Scholar 

  • Cain D, Croteau MN, Luoma S (2011) Bioaccumulation dynamics and exposure routes of Cd and Cu among species of aquatic mayflies. Environ Toxicol Chem 30(11):2532–2541

    Article  CAS  Google Scholar 

  • Cid N, Ibanez C, Prat N (2008) Life history and production of the burrowing mayfly Ephoron virgo (Olivier, 1791) (Ephemeroptera: Polymitarcyidae) in the lower Ebro river: a comparison after 18 years. Aquat Insect 30(3):163–178

    Article  Google Scholar 

  • Conley JM, Funk DH, Buchwalter DB (2009) Selenium bioaccumulation and maternal transfer in the mayfly Centroptilum triangulifer in a life-cycle, periphyton-biofilm trophic assay. Environ Sci Technol 43(20):7952–7957

    Article  CAS  Google Scholar 

  • Conley J, Funk D, Cariello N, Buchwalter D (2011) Food rationing affects dietary selenium bioaccumulation and life cycle performance in the mayfly Centroptilum triangulifer. Ecotoxicology 20(8):1840–1851

    Article  CAS  Google Scholar 

  • De Schamphelaere KAC, Canli M, Van Lierde V, Forrez I, Vanhaecke F, Janssen CR (2004) Reproductive toxicity of dietary zinc to Daphnia magna. Aquat Toxicol 70(3):233–244

    Article  Google Scholar 

  • Doi H, Katano I, Kikuchi E (2006) The use of algal-mat habitats by aquatic insect grazers: Effects of microalgae cues. Basic Appl Ecol 7(2):153–158

    Article  Google Scholar 

  • Farag AM, Woodward DF, Goldstein JN, Brumbaugh W, Meyer JS (1998) Concentrations of metals associated with mining waste in sediments, biofilm, benthic macroinvertebrates, and fish from the Coeur d’Alene River Basin. Idaho. Arch Environ Contam Toxicol 34(2):119–127

    Article  CAS  Google Scholar 

  • Funk DH, Jackson JK, Sweeney BW (2006) Taxonomy and genetics of the parthenogenetic mayfly Centroptilum triangulifer and its sexual sister Centroptilum alamance (Ephemeroptera: Baetidae). J N Am Benthol Soc 25(2):417–429

    Article  Google Scholar 

  • Irving EC, Baird DJ, Culp JM (2003) Ecotoxicological responses of the mayfly Baetis tricaudatus to dietary and waterborne cadmium: implications for toxicity testing. Environ Toxicol Chem 22(5):1058–1064

    CAS  Google Scholar 

  • Ledger ME, Hildrew AG (1998) Temporal and spatial variation in the epilithic biofilm of an acid stream. Freshw Biol 40(4):655–670

    Article  Google Scholar 

  • Luoma SN, Rainbow PS (2005) Why is metal bioaccumulation so variable? Biodynamics as a unifying concept. Environ Sci Technol 39(7):1921–1931

    Article  CAS  Google Scholar 

  • Martin CA, Luoma SN, Cain DJ, Buchwalter DB (2007) Cadmium ecophysiology in seven stonefly (Plecoptera) species: delineating sources and estimating susceptibility. Environ Sci Technol 41(20):7171–7177

    Article  CAS  Google Scholar 

  • Meylan S, Behra R, Sigg L (2003) Accumulation of copper and zinc in periphyton in response to dynamic variations of metal speciation in freshwater. Environ Sci Technol 37(22):5204–5212

    Article  CAS  Google Scholar 

  • Mihuc T, Toetz D (1994) Determination of diets of alpine aquatic insects using stable isotopes and gut analysis. Am Midl Nat 131(1):146–155

    Article  Google Scholar 

  • Munger C, Hare L (1997) Relative importance of water and food as cadmium sources to an aquatic insect (Chaoborus punctipennis): implications for predicting Cd bioaccumulation in nature. Environ Sci Technol 31(3):891–895

    Article  CAS  Google Scholar 

  • Patrick R (1969) Some effects of temperature on fresh water algae. In: Krenkel PA, Parker FL (eds) Biological aspects of thermal pollution, Illus maps: Xx + 407P. Vanderbilt University Press, Nashville, Tenn, pp 161–198

    Google Scholar 

  • Paulsson M, Nystrom B, Blanck H (2000) Long-term toxicity of zinc to bacteria and algae in periphyton communities from the river Gota Alv, based on a microcosm study. Aquat Toxicol 47(3–4):243–257

    Article  CAS  Google Scholar 

  • Peterson CG, Jones TL (2003) Diatom viability in insect fecal material: comparison between two species, Achnanthidium lanceolatum and Synedra ulna. Hydrobiologia 501(1–3):93–99

    Article  Google Scholar 

  • Rhea DT, Harper DD, Farag AM, Brumbaugh WG (2006) Biomonitoring in the Boulder River watershed, Montana, USA: metal concentrations in biofilm and macroinvertebrates, and relations with macroinvertebrate assemblage. Environ Monit Assess 115(1–3):381–393

    Article  CAS  Google Scholar 

  • Sensenig AT, Kiger KT, Shultz JW (2009) The rowing-to-flapping transition: ontogenetic changes in gill-plate kinematics in the nymphal mayfly Centroptilum triangulifer (Ephemeroptera, Baetidae). Biol J Linn Soc 98(3):540–555

    Article  Google Scholar 

  • Sensenig AT, Kiger KT, Shultz JW (2010) Hydrodynamic pumping by serial gill arrays in the mayfly nymph Centroptilum triangulifer. J Exp Biol 213(19):3319–3331

    Article  Google Scholar 

  • Standley LJ, Sweeney BW, Funk DH (1994) Maternal transfer of chlordane and its metabolites to the eggs of a stream mayfly Centroptilum triangulifer. Environ Sci Technol 28(12):2105–2111

    Article  CAS  Google Scholar 

  • Timmermans KR, Spijkerman E, Tonkes M, Govers H (1992) Cadmium and zinc uptake by 2 species of aquatic invertebrate predators from dietary and aqueous sources. Can J Fish Aquat Sci 49(4):655–662

    Article  CAS  Google Scholar 

  • Xie L, Buchwalter DB (2011) Cadmium exposure route affects antioxidant responses in the mayfly Centroptilum triangulifer. Aquat Toxicol 105(3–4):199–205

    Article  CAS  Google Scholar 

  • Xie L, Flippin JL, Deighton N, Funk DH, Dickey DA, Buchwalter DB (2009) Mercury(II) bioaccumulation and antioxidant physiology in four aquatic insects. Environ Sci Technol 43(3):934–940

    Article  CAS  Google Scholar 

  • Xie L, Funk DH, Buchwalter DB (2010) Trophic transfer of Cd from natural periphyton to the grazing mayfly Centroptilum triangulifer in a life cycle test. Environ Pollut 158(1):272–277

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Research Foundation of Korea Grant funded by the Korean Government [NRF-2009-352-F00033], and the National Science Foundation [IOS 0919614]. Gerald LeBlanc, Monica Poteat and Justin Conley (NCSU) provided valuable editorial contributions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. B. Buchwalter.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, K.S., Funk, D.H. & Buchwalter, D.B. Dietary (periphyton) and aqueous Zn bioaccumulation dynamics in the mayfly Centroptilum triangulifer . Ecotoxicology 21, 2288–2296 (2012). https://doi.org/10.1007/s10646-012-0985-1

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-012-0985-1

Keywords

Navigation