Abstract
Stable oxygen and hydrogen isotope analyses of fossil aquatic organisms, such as the chitinous head capsules of chironomid larvae (Chironomidae: Diptera), are promising proxies for inferring paleoecological conditions. In order for analyses of stable oxygen (δ18O) and hydrogen isotope ratios (δ2H) of fossil chironomid head capsules to be used effectively in paleoecological research, it is necessary to understand the factors controlling their stable oxygen and hydrogen composition. We cultured chironomid larvae in two isotopically distinct waters under controlled, replicated laboratory conditions. Chironomid larvae were fed on identical diets, to examine the degree to which water and diet influence the δ18O and δ2H of these organisms. We used a two-end member mixing model to determine the proportional contributions of oxygen and hydrogen from water to the oxygen and hydrogen of chironomid larvae. Our experiment demonstrated that 69.0 ± 0.4% of oxygen and 30.8 ± 2.6% of hydrogen in chironomid larvae are derived from habitat water. Our results show that oxygen isotopes from chironomid remains can better constrain past habitat water isotopic changes compared to hydrogen, due to 69% of the chironomid oxygen being influenced by habitat water. Our data add to a small but growing suite of comparative data on the sources of oxygen and hydrogen in animal tissues, and provide the first such analyses from aquatic insects.
Similar content being viewed by others
References
Ambler RP, Macko SA, Sykes B, Griffiths JB, Bada J, Eglinton G (1999) Documenting the diet in ancient human populations through stable isotope analysis of hair—discussion. Philos Trans R Soc Lond Ser B Biol Sci 354:75–76
Boutton TW, Arshad MA, Tieszen LL (1983) Stable isotope analysis of termite food habits in East African grassland. Oecologia 59:1–6
Bowen GJ, Revenaugh J (2003) Interpolating the isotopic composition of modern meteoric precipitation. Water Resour Res 39(10):1299. doi:1029/2003WR002086
Bowen GJ, Wilkinson B (2002) Spatial distribution of delta O-18 in meteoric precipitation. Geology 30:315–318
Bowen GJ, Chesson L, Nielson K, Cerling TE, Ehleringer JR (2005a) Treatment methods for the determination of delta H-2 and delta O-18 of hair keratin by continuous-flow isotope-ratio mass spectrometry. Rapid Commun Mass Spectrom 19:2371–2378
Bowen GJ, Wassenaar LI, Hobson KA (2005b) Global application of stable hydrogen and oxygen isotopes to wildlife forensics. Oecologia 143:337–348
Brodersen KP, Pedersen O, Lindegaard C, Hamburger K (2004) Chironomids (Diptera) and oxy-regulatory capacity: an experimental approach to paleolimnological interpretation. Limnol Oceanogr 49:1549–1559
Brooks SJ (2000) Late-glacial fossil midge stratigraphies (Insecta: Diptera: Chironomidae) from the Swiss Alps. Palaeogeogr Palaeoclimatol Palaeoecol 159:261–279
Cormie AB, Schwarcz HP, Gray J (1994a) Determination of the hydrogen isotopic composition of bone-collagen and correction for hydrogen-exchange. Geochim Cosmochim Acta 58:365–375
Cormie AB, Schwarcz HP, Gray J (1994b) Relation between hydrogen isotopic-ratios of bone-collagen and rain. Geochim Cosmochim Acta 58:377–391
Crowley TJ (2000) Causes of climate change over the past 1,000 years. Science 289:270–277
Ehleringer JR, Bowen GJ, Chesson LA, West AG, Podlesak DW, Cerling TE (2008) Hydrogen and oxygen isotope ratios in human hair are related to geography. Proc Natl Acad Sci USA 105:2788–2793
EPA (1997) Standard operating procedures (SOP): culture of Chironomonus tentans. EPA, Duluth
Fogel ML, Tuross N, Johnson BJ, Miller GH (1997) Biogeochemical record of ancient humans. Org Geochem 27:275–287
Fry B, Sherr EB (1984) Delta-C-13 measurements as indicators of carbon flow in marine and fresh-water ecosystems. Contrib Mar Sci 27:13–47
Gat JR (1996) Oxygen and hydrogen isotopes in the hydrologic cycle. Annu Rev Earth Planet Sci 24:225–262
Gat JR, Alrey PL (2006) Stable water isotopes in the atmosphere/biosphere/lithosphere interface: scaling-up from the local to continental scale, under humid and dry conditions. Glob Planet Chang 51:25–33
Grocke DR, Schimmelmann A, Elias S, Miller RF (2006) Stable hydrogen-isotope ratios in beetle chitin: preliminary European data and re-interpretation of North American data. Quat Sci Rev 25:1850–1864
Gullan PJ, Cranston PS (2000) Aquatic insects, vol 2. Blackwell Science, Guthrie
Heinrichs ML, Walker IR, Mathewes RW, Hebda RJ (1999) Holocene chironomid-inferred salinity and paleovegetation reconstruction from Kilpoola Lake, British Columbia. Geog Phys Quat 53:211–221
Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326
Hobson KA, Atwell L, Wassenaar LI (1999) Influence of drinking water and diet on the stable-hydrogen isotope ratios of animal tissues. Proc Natl Acad Sci USA 96:8003–8006
Kreuzer-Martin HW, Lott MJ, Dorigan J, Ehleringer JR (2003) Microbe forensics: oxygen and hydrogen stable isotope ratios in Bacillus subtilis cells and spores. Proc Natl Acad Sci USA 100:815–819
Kreuzer-Martin HW, Lott MJ, Ehleringer JR, Hegg EL (2006) Metabolic processes account for the majority of the intracellular water in log-phase Escherichia coli cells as revealed by hydrogen isotopes. Biochemistry 45:13622–13630
Langdon PG, Ruiz Z, Brodersen KP, Foster IDL (2006) Assessing lake eutrophication using chironomids: understanding the nature of community response in different lake types. Freshw Biol 51:562–577
Levin NE, Cerling TE, Passey BH, Harris JM, Ehleringer JR (2006) A stable isotope aridity index for terrestrial environments. Proc Natl Acad Sci USA 103:11201–11205
Macko SA, Engel MH, Andrusevich V, Lubec G, O’Connell TC, Hedges REM (1999) Documenting the diet in ancient human populations through stable isotope analysis of hair. Philos Trans R Soc Lond Ser B Biol Sci 354:65–75
Maier KJ, Kosalwat P, Knight AW (1990) Culture of Chironomus-Decorus (Diptera, Chironomidae) and the effect of temperature on its life-history. Environ Entomol 19:1681–1688
Miller RF, Fritz P, Morgan AV (1988) Climatic implications of D/H ratios in beetle chitin. Palaeogeogr Palaeoclimatol Palaeoecol 66:277–288
Miller RF, Vossfoucart MF, Toussaint C, Jeuniaux C (1993) Chitin preservation in quaternary coleoptera—preliminary-results. Palaeogeogr Palaeoclimatol Palaeoecol 103:133–140
O’Brien DM, Wooller MJ (2007) Tracking human travel using stable oxygen and hydrogen isotope analyses of hair and urine. Rapid Commun Mass Spectrom 21:2422–2430
Oliver DR (1971) Life history of the Chironomidae. Annu Rev Entomol 16:211–230
Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320
Schimmelmann A, DeNiro MJ (1986a) Stable Isotopic studies on chitin, measurements on chitin/chitosan isolates and d-glucosamine hydrochloride from chitin. In: Muzzarelli RAA, Jeuniaux C, Gooday GW (eds) Chitin in nature and technology. Plenum, New York, pp 357–364
Schimmelmann A, DeNiro MJ (1986b) Stable isotopic studies on chitin. 2. The C-13-C-12 and N-15-N-16 ratios in arthropod chitin. Contrib Mar Sci 29:113–130
Schimmelmann A, Deniro MJ (1986c) Stable isotopic studies on chitin. 3. The D/H and O-18/O-16 ratios in arthropod chitin. Geochim Cosmochim Acta 50:1485–1496
Schwarcz HP (1991) Some theoretical aspects of isotope paleodiet studies. J Archaeol Sci 18:261–275
Sessions AL, Hayes JM (2005) Calculation of hydrogen isotopic fractionations in biogeochemical systems. Geochim Cosmochim Acta 69:593–597
Sharp ZD, Atudorei V, Panarello HO, Fernandez J, Douthitt C (2003) Hydrogen isotope systematics of hair: archeological and forensic applications. J Archaeol Sci 30:1709–1716
Walker IR (1987) Chironomidae (Diptera) in paleoecology. Quat Sci Rev 6:29–40
Walker IR (1995) Chironomids as indicators of past environmental change. In: Armitage PD, Cranston PS, Pinder LCV (eds) The Chironomidae: the biology and ecology of non-biting midges. Chapman & Hall, London, pp 403–422
Walker IR (2001) Midges: Chironomidae and related diptera. In: Smol JP, Birks HJB, Last WM (eds) Tracking environmental change using lake sediments. Volume 4: zoological indicators. Kluwer, Dordrecht, pp 43–66
Wang Y, Francis DR, O’Brien DM, Wooller MJ (2008) A protocol for preparing subfossil chironomid head capsules (Diptera: Chiornomidae) for stable isotope analysis in paleoclimate reconstruction and consideration of contamination sources. J Paleolimnol 40:771–781
Wassenaar LI, Hobson KA (2002) Comparative equilibration and online technique for determination of non-exchangeable hydrogen of keratins for use in animal migration studies. Isot Environ Health Stud 39:211–217
Wooller MJ, Francis D, Fogel ML, Miller GH, Walker IR, Wolfe AP (2004) Quantitative paleotemperature estimates from delta O-18 of chironomid head capsules preserved in arctic lake sediments. J Paleolimnol 31:267–274
Wooller MJ, Wang Y, Axford Y (2008) A multiple stable isotope record of Late Quaternary limnological changes and chironomid paleoecology from northeastern Iceland. J Paleolimnol 40:63–77
Acknowledgements
This research was supported by a National Science Foundation grant (ESH-0317766) and a National Institute for Water Research grant (no. G-3077) awarded to Dr Matthew Wooller. This publication is also the result, in part, of research sponsored by the Cooperative Institute for Arctic Research (project CIPY-01) with funds from the National Oceanic and Atmospheric Administration under cooperative agreement NA17RJ1224 with the University of Alaska. We thank the Wilson Environmental Laboratories and EPA Mid-continent Ecology Division for supplying chironomid egg masses. We thank the WERC at UAF for accommodating our growth experiment. Special thanks to the WERC laboratory manager Shane Billing for numerous suggestions to modify our growth chamber setup and also for helping us fetch water. Our thanks also go to Tim Howe and Norma Haubenstock at the ASIF for laboratory support. We also thank Dr Jonathan Grey and an anonymous reviewer for their very constructive and positive reviews of our paper.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Craig Osenberg.
Rights and permissions
About this article
Cite this article
Wang, Y.V., O’Brien, D.M., Jenson, J. et al. The influence of diet and water on the stable oxygen and hydrogen isotope composition of Chironomidae (Diptera) with paleoecological implications. Oecologia 160, 225–233 (2009). https://doi.org/10.1007/s00442-009-1303-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-009-1303-3