Skip to main content
Log in

Assessing the toxicity and teratogenicity of pond water in north-central minnesota to amphibians

  • Research Articles
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Background

Incidence of amphibian deformities have increased in recent years, especially in the northern region of the United States. While many factors have been proposed as being responsible for generating deformities (e.g., contaminants, ultraviolet radiation [UV], parasites), no single cause has been definitively established.

Methods

To determine whether waterborne chemicals are responsible for amphibian deformities in ponds in north-central Minnesota, we deployed semipermeable membrane devices (SPMDs) in an imparted and a reference site to accumulate lipophilic contaminants. We then exposed native tadpoles (northern leopard frogs;Rana pipiens) to the SPMD extracts combined with two agricultural pesticides (atrazine, carbaryl) at two levels of UV radiation.

Results and Discussion

UV radiation alone caused a slight increase in hatching success and tadpole growth rate. Deformity rate among hatchlings was high following exposure to SPMD extracts from the reference site in the absence of UV, suggesting that chemicals present at this site are broken down by UV to less harmful forms, or become less bioavailable. Conversely, impacted site SPMD extracts caused hatchling deformities only in the presence of UV, suggesting that UV potentiates the teratogenicity of the compounds present there. Impacted site SPMD extracts significantly increased the number of bony triangles among metamorphs, a common deformity observed at this site. The incidence of skin webbings increased significantly with SPMD extracts from both sites as well as with our pesticide control containing atrazine and carbaryl alone.

Conclusions

Higher deformity rates among tadpoles reared in the presence of UV radiation and SPMD extracts from sites where deformities are common indicates a chemical compound (or compounds) in the water at this site may be causing the deformities.

Recommendations and Oudook

It is important to examine the effects of chemical stressors in the presence of other natural stressors (e.g., UV radiation) to gain a better understanding of how multiple stressors work to impact amphibians and amphibian populations.

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.

Similar content being viewed by others

References

  • Ankley GT, Tietge JE, Holcombe GW, DeFoe DL, Diamond SA, Jensen KM, Degitz SJ (2000): Effects of laboratory ultraviolet radiation and natural sunlight on survival and development ofRana pipiens. Canadian Journal of Zoology 78, 1092–1100

    Article  Google Scholar 

  • Applegate LA, Ley RD (1998): Ultraviolet radiation-induced lethality and repair of pyrimidine dimmers in fish embryos. Mutation Research 198, 85–92

    Google Scholar 

  • Blaustein AR, Kiesecker JM, Olivers DP, Anthony RG (1997): Ambient UV-B radiation causes deformities in amphibian embryos. Proceedings of the National Academy of Sciences 94, 13735–13737

    Article  CAS  Google Scholar 

  • Blaustein AR, Kiesecker JM, Chivers DP, Hokit DG, Marco A, Belden LK, Hatch A (1998): Effects of ultraviolet radiation on amphibians: field experiments. American Zoologist 38, 799–812

    Google Scholar 

  • Bonin J, Ouellet M, Rodrigue J, DesGranges J-L (1997): Measuring the health of frogs in agricultural habitats subjected to pesticides. Herpetological Conservation 1, 246–257

    Google Scholar 

  • Bridges CM, Boone MD (2003): The interactive effects of UV-B and insecticide exposure on tadpoles survival, growth, and development. Biological Conservation 113, 49–54

    Article  Google Scholar 

  • Bridges CM, Semlitsch RD (2000): Variation in pesticide tolerance of tadpoles among and within species of ranidae and patterns of amphibian decline. Conservation Biology 14, 1490–1499 239

    Article  Google Scholar 

  • Broomhall SD, Osborne WS, Cunningham RB (2000): Comparative effects of ambient ultraviolet-B radiation on two sympatric species of Australian frogs. Conservation Biology 14, 420–427

    Article  Google Scholar 

  • Burkhart JG, Ankley G, Bell H, Carpenter H, Fort D, Gardiner D, Gardner H, Hale R, Helgen JC, Jepson P, Johnson D, Lannoo M, Lee D, Lary J, Levey R, Magner J, Meteyer C, Shelby MD, Lucier G (2000): Strategies for assessing the implications of malformed frogs for environmental health. Environmental Health Perspectives 108, 83–90

    Article  CAS  Google Scholar 

  • Burkhart JG, Helgen JC, Fort DJ, Gallagher D, Bowers D, Propst TL, Gernes M, Magner J, Shelby MD, Lucier G (1998): Induction of mortality and malformation inXenopus laevis embryos by water sources associated with frog deformities. Environmental Health Perspectives 106, 841–848

    Article  CAS  Google Scholar 

  • Canfield JT, Kersten SM, Vanselow P (2000): 1997–1999 Field Season Report, Minnesota Pollution Control Agency, Minneapolis, Minnesota, USA

    Google Scholar 

  • Carman EN, Ferguson GW, Gehrmann WH, Chen TC, Holick MF (2000): Photobiosynthetic opportunity and ability for UV-B generated vitamin D synthesis in free-living house geckos (Hemi- dactylus turcicus) and Texas spiny lizards (Scleroporus olivaceous). Copeia 2000, 245–250

    Article  Google Scholar 

  • Crump D, Berrill M, Coulson D, Lean D, McGillivray L, Smith A (1999): Sensitivity of amphibian embryos, tadpoles, and larvae to enhanced UV-B radiation in natural pond conditions. Canadian Journal of Zoology 77, 1956–1966

    Article  Google Scholar 

  • Fort DJ, Rogers RL, Copley HF, Bruning, LA, Stover EL, Helgen JC, Burkhart JC (1999a): Progress toward identifying causes maldevelopment induced inXenopus by pond water and sediment extracts from Minnesota, USA. Environmental Toxicology and Chemistry 18, 2316–24

    Article  CAS  Google Scholar 

  • Fort DJ, Propst TL, Stover EL, Helgen JC, Levey RB, Gallagher K, Burkhart JC (1999b): Effects of pond water, sediment, and sediment extracts from Minnesota and Vermont, USA, on early development and metamorphosis ofXenopus. Environmental Toxicology and Chemistry 18, 2305–2315

    Article  CAS  Google Scholar 

  • Gardiner DM, Hoppe DM (1999): Environmentally induced limb malformations in mink frogs(Rana septentrionalis). Journal of Experimental Zoology 284, 207–216

    Article  CAS  Google Scholar 

  • Gosner KL (1960): A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16,183–190

    Google Scholar 

  • Helgen JC, Gernes MC, Kersten SM, Chirhard JW, Canfield JT, Bowers D, Haferman J, McKinnell RG, Hoppe DM (2000): Field investigations of malformed frogs in Minnesota 1993-1997. Journal of the Iowa Academy of Sciences 107, 96–112

    Google Scholar 

  • Hoppe DM (2000): History of Minnesota frog abnormalities: do recent findings represent a new phenomenon? Journal of the Iowa Academy of Sciences 107, 86–89

    Google Scholar 

  • Huckins JN, Manuweera GK, Petty JD, Mackay D, Lebo JA (1993): Lipid-containing semipermeable membrane devices for monitoring organic contaminants in water. Environmental Science and Technology 27, 2489–2496

    Article  CAS  Google Scholar 

  • Huckins JN, Petty JD, Prest HF, Clark RC, Alvarez DA, Orazio CE, Lebo JA, Cranor WL, Johnson BT (2002): A Guide for the use of semipermeable membrane devices (SPMDs) as samplers of waterborne hydrophobic organic contaminants. Report prepared for the American Petroleum Institute (API), API no. 4690, 186 pp

  • Johnson PJT, Lunde KB, Ritchie EG, Launer AE (1999): The effect of trematode infection on amphibian limb development and survivorship. Science 284, 802–804

    Article  CAS  Google Scholar 

  • Lannoo MJ (2000): Conclusions drawn from the malformity and disease session, Midwest declining amphibians conference 1998. Journal of the Iowa Academy of Sciences 107, 212–216

    Google Scholar 

  • Little EE, Calfee R, Cleveland L, Skinker R, Zaga-Parkhurst A, Barron MG (2000): Photo-enhanced toxicity in amphibians: synergistic interactions of solar ultraviolet radiation and aquatic contaminants. Journal of the Iowa Academy of Sciences 107, 67–771

    Google Scholar 

  • Little EE, Fabacher DL (1996): Exposure of freshwater fish to simulated solar UVB radiation. In: Techniques in Aquatic Toxicology. Ostrander G (ed.). Lewis Publishers, New York, pp 141–158

    Google Scholar 

  • Lizana M, Pedraza EM (1998): The effects of UV-B radiation on toad mortality in mountainous areas of central Spain. Conservation Biology 12, 703–707

    Article  Google Scholar 

  • Mackay D, Shiu W-Y, Ma K-C (1991): Illustrated Handbook of Physical-Chemical Properties and Environmental Fate for Organic Chemicals. Volume I. Lewis Publishers, Chelsea, Michigan, USA. 704 pp

  • Mackay D, Shiu W-Y, Ma, K-C (1992): Illustrated Handbook of Physical-Chemical Properties and Environmental Fate for Organic Chemicals. Volume II. Lewis Publishers, Chelsea, Michigan, USA. 608 pp

  • Mackay D, Shiu W-Y, Ma K-C (1997): Illustrated Handbook of Physical-Chemical Properties and Environmental Fate for Organic Chemicals. Volume V. Lewis Publishers, Chelsea, Michigan, USA. 832 pp

  • Merila J, Laurila A, Pahkala M (2000): Effects of ambient UV-B radiation on early development of the common frog(Rana temporaria) embryos in the subarctic. Annals Zoologica Fennici 37, 51–58

    Google Scholar 

  • Meteyer CU (2000): Field guide to malformations of frogs and toads with radiographic interpretations. Biological Sciences Report USGS/BRD/BSR-2000–0005

  • Meteyer CU, Cole RA, Converse KA, Docherty DE, Wolcott M, Helgen JC, Levey R, Eaton-Poole L, Burkhart JG (2000): Defining anuran malformations in the context of a developmental problem. Journal of Iowa Academy of Sciences 107, 72–7800

    Google Scholar 

  • Ouellet M (2000): Amphibian deformities: current state of knowledge. In: Ecotoxicology of Amphibians and Reptiles. Sparling DW, Linder G, Bishop CA (eds). SETAC Press, Pensacola, pp. 617–661

    Google Scholar 

  • Ouellet M, Bonin J, Rodrigue J, DesGranges J-L, Lair S (1997): Hindlimb deformities (ectromelia, ectrodactyly) in free-living anurans from agricultural habitats. Journal of Wildlife Disease 33, 95–104

    CAS  Google Scholar 

  • Pahkala M, Merila J, Ots I, Laurila A (2003) Effects of ultraviolet B radiation on metamorphic traits in the common frogRana temporaria. Journal of Zoology 259, 57–62

    Article  Google Scholar 

  • Petty JD, Orazio CE, Huckins JN, Gale RW, Lebo JA, Meadows JC, Echols KR, Cranor WL (2000): Considerations involved with the use of semipermeable membrane devices for monitoring environmental contaminants. Journal of Chromatography A 879, 83–95

    Article  CAS  Google Scholar 

  • Petty JD, Jones SB, Huckins JN, Cranor WL, Parris JT, McTague TB, Boyle TP (2000): An approach for assessment of water quality using semipermeable membrane devices (SPMDs) as bioindicator tests. Chemosphere 41, 311–321

    Article  CAS  Google Scholar 

  • SAS Institute, Inc (1998): SAS / STAT User’s Guide, Release 6.03 Edition, SAS Institute, Inc., Cary, NC, USA

    Google Scholar 

  • Souder W (2000): A Plague of Frogs: the Horrifying True Story. Hyperion Press, New York. 320 pp

  • Starnes SM, Kennedy CA, Petranka JW (2000) Sensitivity of embryos of southern Appalachian amphibians to ambient solar UV B radiation. Conservation Biology 14, 277–282

    Article  Google Scholar 

  • Smith GR, Waters MA, Rettig JE (2000): Consequences of embryonic UV-B exposure for embryos and tadpoles of the plains leopard frog. Conservation Biology 14, 1903–1907

    Article  Google Scholar 

  • Wilbur HM, Collins JP (1973): Ecological aspects of amphibian metamorphosis. Science 182, 1305–1314

    Article  Google Scholar 

  • Zaga A, Little EE, Rabeni CF, Ellersieck MR (1998): Photoenhanced toxicity of a carbamate insecticide to early life stage anuran amphibians. Environmental Toxicology and Chemistry 17, 2543–2553

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christine Bridges.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bridges, C., Little, E., Gardiner, D. et al. Assessing the toxicity and teratogenicity of pond water in north-central minnesota to amphibians. Environ Sci & Pollut Res 11, 233–239 (2004). https://doi.org/10.1007/BF02979631

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02979631

Keywords

Navigation