, Volume 36, Issue 1, pp 101–110 | Cite as

Restored Agricultural Wetlands in central Iowa: Habitat Quality and Amphibian Response

  • Rebecca A. ReevesEmail author
  • Clay L. Pierce
  • Kelly L. Smalling
  • Robert W. Klaver
  • Mark W. Vandever
  • William A. Battaglin
  • Erin Muths
Original Research


Amphibians are declining throughout the United States and worldwide due, partly, to habitat loss. Conservation practices on the landscape restore wetlands to denitrify tile drainage effluent and restore ecosystem services. Understanding how water quality, hydroperiod, predation, and disease affect amphibians in restored wetlands is central to maintaining healthy amphibian populations in the region. We examined the quality of amphibian habitat in restored wetlands relative to reference wetlands by comparing species richness, developmental stress, and adult leopard frog (Lithobates pipiens) survival probabilities to a suite of environmental metrics. Although measured habitat variables differed between restored and reference wetlands, differences appeared to have sub-lethal rather than lethal effects on resident amphibian populations. There were few differences in amphibian species richness and no difference in estimated survival probabilities between wetland types. Restored wetlands had more nitrate and alkaline pH, longer hydroperiods, and were deeper, whereas reference wetlands had more amphibian chytrid fungus zoospores in water samples and resident amphibians exhibited increased developmental stress. Restored and reference wetlands are both important components of the landscape in central Iowa and maintaining a complex of fish-free wetlands with a variety of hydroperiods will likely contribute to the persistence of amphibians in this landscape.


Lithobates pipiens Mark-recapture Fluctuating asymmetry Batrachochytrium dendrobatidis Hydroperiod Nitrate 



This project was funded by the Fort Collins Science Center as a part of ongoing technical assistance given to the USDA Farm Service Agency and the USGS Amphibian Research and Monitoring Initiative (ARMI). The authors thank L. Bailey, T. Grant, D. Otis, D. Green, D. Cook, J. Niemi, S. Richmond, M. Lechtenberg, M. McWayne, C. Sanders and M. Hladik for helpful advice and comments, J. Oberheim-Vorwald, K. Edmunds, L. Truong, J. Harmon, and K. Flood for help in the field, and the landowners that allowed us access to their land. Exact wetland locations are proprietary and we obtained written permission for access to wetlands from all landowners and public land managers prior to the start of sampling. This study was performed under the auspices of Iowa State University Institutional Animal Care and Use Committee (IACUC) protocol # 3-12-7324-D, and animals were collected under state permit #SC699. This is a contribution 519 of the U.S. Geological Survey Amphibian Research and Monitoring Initiative (ARMI). Use of trade, product, or firm names is descriptive and does not imply endorsement by the U.S. Government.

Supplementary material

13157_2015_720_MOESM1_ESM.doc (63 kb)
Figure S1 Capture-mark-recapture sampling design for population and survival estimation of adult leopard frogs in restored and reference wetlands in central Iowa. Sampling was structured in a Robust Design framework with two primary periods per year and three secondary occasions within each primary period. Populations were considered open between and closed within primary periods. (DOC 63 kb)
13157_2015_720_MOESM2_ESM.doc (53 kb)
Figure S2 Locations of fluctuating asymmetry measurements on leopard frogs in restored and reference wetlands in central Iowa. The snout to urostyle length (SUL) was measured along with the length of the thumb (T), radioulna (RU), tibiofibula (TF), femur (FE), and foot (FO). (Image adapted from Cooper, Sarah. Animal Life. New York: Harper & Brothers, 1887. “Frog Skeleton.” Retrieved April 4, 2014, from (DOC 53 kb)
13157_2015_720_MOESM3_ESM.doc (37 kb)
Table S1 Spearman correlation matrices for water chemistry variables in restored and reference wetlands in 2012 and 2013 that were included in the multivariate analysis of variance (MANOVA). (DOC 37 kb)
13157_2015_720_MOESM4_ESM.doc (39 kb)
Table S2 Amphibian species detected using automated recording units (ARUs) in restored and reference wetlands in central Iowa. An “x” denotes that a species was detected during that season, a “-” denotes that it was not detected. (DOC 39 kb)
13157_2015_720_MOESM5_ESM.doc (36 kb)
Table S3 Capture-mark-recapture statistics for leopard frogs in restored and reference wetlands in central Iowa. (DOC 35 kb)
13157_2015_720_MOESM6_ESM.doc (94 kb)
Table S4 Complete model selection results for estimating the probability of survival for leopard frogs in central Iowa using the robust design with Huggin’s estimator in RMark and Program MARK. We ran all possible combinations of parameter types and used the corrected Akaike’s information criterion (AICc) to select the best models. (DOC 94 kb)
13157_2015_720_MOESM7_ESM.doc (52 kb)
Table S5 Environmental and amphibian characteristics of restored and reference wetlands in central Iowa. Where differences between years were not significant, the means of the pooled 2012 and 2013 data are shown. Fluctuating asymmetry is the absolute value of the difference between mean measurements for right and left tibiofibulae. Abbreviations: Batrachochytrium dendrobatidis (Bd); not detected (ND); not sampled; (--); leopard frog (LIPI); and fluctuating asymmetry (FA). (DOC 51 kb)


  1. Adams MJ, Miller DAW, Muths E, Corn PS, Grant EHC et al (2013) Trends in amphibian occupancy in the United States. PLoS ONE 8(5), e64347. doi: 10.1371/journal.pone.0064347 PubMedCentralCrossRefPubMedGoogle Scholar
  2. Beaupre S, Jacobson E, Lillywhite H, Zamudio K (2004) Guidelines for use of live amphibians and reptiles in field and laboratory research. A publication of the American Society of Ichthyologists and Herpetologists, approved by board of GovernorsGoogle Scholar
  3. Bogue AG (1963) From prairie to corn belt: farming on the Illinois and Iowa prairies in the nineteenth century. Iowa State University Press, AmesGoogle Scholar
  4. Boone MD, James SM (2003) Interactions of an insecticide, herbicide, and natural stressors in amphibian community mesocosms. Ecological Applications 13:829–841. doi: 10.1890/1051-0761(2003)013[0829:Ioaiha]2.0.Co;2 CrossRefGoogle Scholar
  5. Boone MD, Little EE, Semlitsch RD (2004) Overwintered bullfrog tadpoles negatively affect salamanders and anurans in native amphibian communities. Copeia 3:683–690. doi: 10.1643/CE-03-229R1 CrossRefGoogle Scholar
  6. Boone MD, Semlitsch RD, Little EE, Doyle MC (2007) Multiple stressors in amphibian communities: effects of chemical contamination, bullfrogs, and fish. Ecological Applications 17:291–301. doi: 10.1890/1051-0761(2007)017[0291:MSIACE]2.0.CO;2 CrossRefPubMedGoogle Scholar
  7. Casper GS, Hendricks R (2005) Rana catesbeiana. In: Lannoo M (ed) Amphibian declines. University of California Press, BerkeleyGoogle Scholar
  8. Chestnut T, Anderson C, Popa R, Blaustein AR, Voytek M, Olson DH, Kirshtein J (2014) Heterogeneous occupancy and density estimates of the pathogenic fungus Batrachochytrium dendrobatidis in waters of North America. PLoS ONE 9(9), e106790. doi: 10.1371/journal.pone.0106790 PubMedCentralCrossRefPubMedGoogle Scholar
  9. Collins JP, Storfer A (2003) Global amphibian declines: sorting the hypotheses. Diversity and Distributions 9:89–98. doi: 10.1046/j.1472-4642.2003.00012.x CrossRefGoogle Scholar
  10. Dodd CK (2013) Frogs of the United States and Canada, 2-vol. set. Johns Hopkins University PressGoogle Scholar
  11. Doherty PF, White GC, Burnham KP (2012) Comparison of model building and selection strategies. Journal of Ornithology 152:317–323. doi: 10.1007/s10336-010-0598-5 CrossRefGoogle Scholar
  12. Ferner J (2007) A review of marking and individual recognition techniques for amphibian and reptiles. herpetological circular 35. Society for the Study of Amphibians and Reptiles, AtlantaGoogle Scholar
  13. Forrest MJ, Schlaepfer MA (2011) Nothing a Hot Bath Won’t Cure: infection rates of amphibian chytrid fungus correlate negatively with water temperature under natural field settings. PLoS ONE 6(12), e28444. doi: 10.1371/journal.pone.0028444 PubMedCentralCrossRefPubMedGoogle Scholar
  14. Gallant N, Teather K (2001) Differences in size, pigmentation, and fluctuating asymmetry in stressed and nonstressed northern leopard frogs (Rana pipiens). Ecoscience 8:430–436Google Scholar
  15. Green DE (2001) Anesthesia of amphibians in the field. United States Geological Survey, MadisonGoogle Scholar
  16. Groner ML, Relyea RA (2011) A tale of two pesticides: How common insecticides affect aquatic communities. Freshwater Biology 56:2391–2404. doi: 10.1111/j.1365-2427.2011.02667.x CrossRefGoogle Scholar
  17. Hecnar SJ (1995) Acute and chronic toxicity of ammonium-nitrate fertilizer to amphibians from Southern Ontario. Environmental Toxicology and Chemistry 14:2131–2137. doi: 10.1002/etc.5620141217 CrossRefGoogle Scholar
  18. Hecnar SJ, MCloskey RT (1996) Amphibian species richness and distribution in relation to pond water chemistry in south-western Ontario, Canada. Freshwater Biology 36(1):7–15. doi: 10.1046/j.1365-2427.1996.00054.x CrossRefGoogle Scholar
  19. Hubert WA, Pope KL, Dettmers JM (2012) Passive capture techniques. In: Zale AV, Parrish DL, Sutton TM (eds) Fisheries techniques. American Fisheries Society, Bethesda, pp 223–265Google Scholar
  20. IDALS (2009) Landowner guide to CREP. Iowa Department of Agriculture and Land StewardshipGoogle Scholar
  21. IDALS (2013) Iowa Conservation Reserve Enhancement Program (CREP) landowner guide to operation and maintenance. Iowa Department of Agriculture and Land StewardshipGoogle Scholar
  22. IDNR (2006) Iowa Wildlife Action Plan. Iowa Department of Natural ResourcesGoogle Scholar
  23. Iovanna R, Hyberg S, Crumpton W (2008) Treatment wetlands: cost-effective practice for intercepting nitrate before it reaches and adversely impacts surface waters. Journal of Soil and Water Conservation 63:14A–15A. doi: 10.2489/jswc.63.1.14A CrossRefGoogle Scholar
  24. Johnson ML, Berger L, Philips L, Speare R (2003) Fungicidal effects of chemical disinfectants, UV light, desiccation and heat on the amphibian chytrid Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 57:255–260. doi: 10.3354/dao057255 CrossRefPubMedGoogle Scholar
  25. Johnson PTJ, Chase JM, Dosch KL, Hartson RB, Gross JA, Larson DJ, Sutherland DR, Carpenter SR (2007) Aquatic eutrophication promotes pathogenic infection in amphibians. Proceedings of the National Academy of Sciences of the United States of America 104:15781–15786. doi: 10.1073/pnas.0707763104 PubMedCentralCrossRefPubMedGoogle Scholar
  26. Kendall W (2014) The ‘robust design’. In E Cooch, GC White (eds.), Program MARK:‘A gentle introduction. Available via:
  27. Kendall WL, Nichols JD (1995) On the use of secondary capture-recapture samples to estimate temporary emigration and breeding proportions. Journal of Applied Statistics 22:751–762. doi: 10.1080/02664769524595 CrossRefGoogle Scholar
  28. Kirshtein JD, Anderson CW, Wood JS, Longcore JE, Voytek MA (2007) Quantitative PCR detection of Batrachochytrium dendrobatidis DNA from sediments and water. Diseases of Aquatic Organisms 77:11. doi: 10.3354/dao01831 CrossRefPubMedGoogle Scholar
  29. Knutson MG, Sauer JR, Olsen DA, Mossman MJ, Hemesath LM, Lannoo MJ (1999) Effects of landscape composition and wetland fragmentation on frog and toad abundance and species richness in Iowa and Wisconsin, USA. Conservation Biology 13(6):1437–1446. doi: 10.1046/j.1523-1739.1999.98445.x CrossRefGoogle Scholar
  30. Knutson MG, Richardson WB, Reineke DM, Gray BR, Parmelee JR, Weick SE (2004) Agricultural ponds support amphibian populations. Ecological Applications 14:669–684. doi: 10.1890/02-5305 CrossRefGoogle Scholar
  31. Laake J (2013) RMark: an R interface for analysis of capture-recapture data with MARK. Alaska Fisheries Science Center, NOAA National Marine Fisheries Service, SeattleGoogle Scholar
  32. Lannoo MJ (1998) Status and conservation of midwestern amphibians. University of Iowa Press, Iowa CityGoogle Scholar
  33. Leclair R Jr, Castanet J (1987) A skeletochronological assessment of age and growth in the frog Rana pipiens Schreber (Amphibia, Anura) from southwestern Quebec. Copeia:361–369Google Scholar
  34. Mann RM, Hyne RV, Choung CB, Wilson SP (2009) Amphibians and agricultural chemicals: review of the risks in a complex environment. Environmental pollution 157(11):2903–2927. doi: 10.1016/j.envpol.2009.05.015 CrossRefPubMedGoogle Scholar
  35. Marco A, Quilchano C, Blaustein AR (1999) Sensitivity to nitrate and nitrite in pond‐breeding amphibians from the Pacific Northwest, USA. Environmental Toxicology and Chemistry 18(12):2836–2839CrossRefGoogle Scholar
  36. McCaffery RM, Eby LA, Maxell BA, Corn PS (2014) Breeding site heterogeneity reduces variability in frog recruitment and population dynamics. Biological Conservation 170:169–176. doi: 10.1016/j.biocon.2013.12.013 CrossRefGoogle Scholar
  37. Merrell DJ (1977) Life history of the leopard frog, Rana pipiens, in Minnesota. Bell Museum of Natural History, University of MinnesotaGoogle Scholar
  38. Miller BA, Crumpton WG, van der Valk AG (2009) Spatial distribution of historical wetland classes on the Des Moines Lobe, Iowa. Wetlands 29:1146–1152. doi: 10.1672/08-158.1 CrossRefGoogle Scholar
  39. NDMC, USDA, NOAA (2014) United States drought monitor archives. National Drought Mitigation Center, U.S. Department of Agriculture, National Oceanic and Atmospheric AdministrationGoogle Scholar
  40. O’Neal BJ, Heske EJ, Stafford JD (2008) Waterbird response to wetlands restored through the Conservation Reserve Enhancement Program. The Journal of Wildlife Management 72:654–664. doi: 10.2193/2007-165 CrossRefGoogle Scholar
  41. Pachauri RK, Allen MR, Barros VR, Broome J, Cramer W, Christ R et al. (2014) Climate Change 2014: synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate ChangeGoogle Scholar
  42. Patton CJ, Kryskalla JR (2003) Methods of analysis by the US Geological Survey National Water Quality Laboratory: evaluation of alkaline persulfate digestion as an alternative to kjeldahl digestion for determination of total and dissolved nitrogen and phosphorus in water. US Department of the Interior, US Geological SurveyGoogle Scholar
  43. Parris MJ, Cornelius TO (2004) Fungal pathogen causes competitive and developmental stress in larval amphibian communities. Ecology 85:3385–3395. doi: 10.1890/04-0383 CrossRefGoogle Scholar
  44. Pollock KH (1982) A capture-recapture design robust to unequal probability of capture. The Journal of Wildlife Management:752–757Google Scholar
  45. Pulliam HR (1988) Sources, sinks and population regulation. The American Naturalist 132:652–661CrossRefGoogle Scholar
  46. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available:
  47. Reeves RA (2014). Amphibian stress, survival, and habitat quality in restored agricultural wetlands in central Iowa. Thesis, Iowa State UniversityGoogle Scholar
  48. Rorabaugh JC (2005) Rana pipiens. In: Lannoo M (ed) Amphibian declines. University of California Press, BerkeleyGoogle Scholar
  49. Rowe JC, Garcia TS (2014) Impacts of wetland restoration efforts on an amphibian assemblage in a multi-invader community. Wetlands 34:141–153. doi: 10.1007/s13157-013-0492-z CrossRefGoogle Scholar
  50. Smalling KL, Reeves RA, Muths E, Vandever M, Battaglin WA, Hladik ML, Pierce CL (2015) Pesticide concentrations in frog tissue and wetland habitats in a landscape dominated by agriculture. Science of the Total Environment 502:80–90. doi: 10.1016/j.scitotenv.2014.08.114 CrossRefPubMedGoogle Scholar
  51. Schmidt BR, Kéry M, Ursenbacher S, Hyman OJ, Collins JP (2013) Site occupancy models in the analysis of environmental DNA presence/absence surveys: a case study of an emerging amphibian pathogen. Methods in Ecology and Evolution 4(7):646–653CrossRefGoogle Scholar
  52. St-Amour V, Garner TW, Schulte-Hostedde AI, Lesbarreres D (2010) Effects of two amphibian pathogens on the developmental stability of green frogs. Conservation Biology: the journal of the Society for Conservation Biology 24:788–794. doi: 10.1111/j.1523-1739.2009.01400.x CrossRefGoogle Scholar
  53. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786CrossRefPubMedGoogle Scholar
  54. USDA (2009) Iowa Conservation Reserve Enhancement Program (CREP) Landowner guide to CREP: Iowa Department of Agriculture and Land Stewardship (IDALS) and US Department of AgricultureGoogle Scholar
  55. USFWS (2002) National wetlands inventory. U.S. Department of the Interior, U.S. Fish and Wildlife Service, WashingtonGoogle Scholar
  56. Van der Valk A, Davis C (1978) The role of seed banks in the vegetation dynamics of prairie glacial marshes. Ecology:322–335Google Scholar
  57. Waddle JH, Thigpen TF, Glorioso BM (2009) Efiicacy of automatic vocalization recognition software for anuran monitoring. Herpetological Conservation and Biology 4:384–388Google Scholar
  58. Wake DB, Vredenburg VT (2008) Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proceedings of the National Academy of Sciences of the United States of America 105:11466–11473PubMedCentralCrossRefPubMedGoogle Scholar
  59. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:120–139CrossRefGoogle Scholar
  60. Whitney GC (1994) From coastal wilderness to fruited plain: a history of environmental change in temperate North America, 1500 to the present. Cambridge University Press, CambridgeGoogle Scholar

Copyright information

© US Government 2015

Authors and Affiliations

  • Rebecca A. Reeves
    • 1
    • 6
    Email author
  • Clay L. Pierce
    • 2
  • Kelly L. Smalling
    • 3
  • Robert W. Klaver
    • 2
  • Mark W. Vandever
    • 4
  • William A. Battaglin
    • 5
  • Erin Muths
    • 4
  1. 1.Department of Natural Resource Ecology and ManagementIowa State UniversityAmesUSA
  2. 2.U.S. Geological Survey, Iowa Cooperative Fish and Wildlife Research UnitIowa State UniversityAmesUSA
  3. 3.U.S. Geological SurveyNew Jersey Water Science CenterLawrencevilleUSA
  4. 4.U.S. Geological SurveyFort Collins Science CenterFort CollinsUSA
  5. 5.U.S. Geological SurveyColorado Water Science CenterLakewoodUSA
  6. 6.U.S. Fish and Wildlife ServiceOceanvilleUSA

Personalised recommendations