The influence of land cover and within-pool characteristics on larval, froglet, and adult wood frogs along a rural to suburban gradient

  • Carly J. EakinEmail author
  • Malcolm L. HunterJr
  • Aram J. K. Calhoun


Urbanization is known to extirpate many species, but far less is known about how suburbanization may affect amphibian populations. We studied wood frogs (Lithobates sylvaticus) to test the effects of site characteristics (within-pool conditions and land cover indicative of suburbanization within 1000 m) and larval morphology on newly emerged froglets and post-breeding males across a suburbanization gradient in 15 pools in greater Bangor, Maine, USA. We raised field-captured larvae in microcosms and examined froglet morphology and locomotor performance at emergence and one month post-emergence. Larval mass was positively correlated with 50% of froglet responses (survival, size, and locomotor performance) but was negatively associated with adult size. Among site characteristics, egg density had the most salient influence with negative effects on larval survival and morphology as well as on 11 of 14 froglet responses. Vegetation, hydrology, and suburban-associated cover near pools also influenced froglet performance, and hydrology and suburban-associated cover was associated with larger and smaller adult morphology. However the influence of suburban-associated cover on froglet performance and adult morphology was small compared to that of within-pool characteristics. Specifically, our findings support the idea that within-pool conditions experienced by larvae can influence terrestrial stages with potentially life-long consequences. Nevertheless, in suburban landscapes where there is evidence of population declines, it is likely that suburbanization has the greatest impact on populations via direct effects on terrestrial stages. We encourage planners to maintain high-quality habitat for aquatic and terrestrial stage wood frogs in suburbanizing landscapes to avoid extirpation.


Vernal pool Suburbanization Latent effects Locomotor performance Morphology Conspecific competition 



We thank an anonymous reviewer for comments that substantially improved this paper. We are grateful for support for this study provided by McIntire-Stennis, the Hatch Act, and the National Science Foundation under grant no. 313627. We thank H. Greig, R. Holberton, and M. Kinnison for help with study design, data analyses, and interpretation. This work has been completed with approval from the University of Maine Institutional Animal Care and Use Committee (Protocols A2015-03-03 and A2016-03-03). This is Maine Agriculture and Forestry Experiment Station Publication Number 3652. This project was supported by the USDA National Institute of Food and Agriculture, Hatch project number #ME0-21705 through the Maine Agricultural & Forest Experiment Station.

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  1. Álvarez D, Nicieza AG (2002) Effects of induced variation in anuran larval development on postmetamorphic energy reserves and locomotion. Oecologia 131:186–195CrossRefGoogle Scholar
  2. Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Manag 74:1175–1178CrossRefGoogle Scholar
  3. Azous A, Horner RR (eds) (2000) Wetlands and urbanization: implications for the future. CRC PressGoogle Scholar
  4. Barbasch T, Benard MF (2011) Past and present risk: exposure to predator chemical cues before and after metamorphosis influences juvenile wood frog behavior. Ethology 117:367–373CrossRefGoogle Scholar
  5. Bates D, Maechler M, Bolker B, et al (2017) Package ‘lme4.’ 117Google Scholar
  6. Berven KA (1990) Factors affecting population fluctuations in larval and adult stages of the wood frog (Rana sylvatica). Ecology 71:1599–1608CrossRefGoogle Scholar
  7. Berven KA (2009) Density dependence in the terrestrial stage of wood frogs: evidence from a 21-year population study. Copeia 2009:328–338. CrossRefGoogle Scholar
  8. Berven KA, Chadra BG (1988) The relationship among egg size, density and food level on larval development in the wood frog (Rana sylvatica). Oecologia 75:67–72CrossRefGoogle Scholar
  9. Berven KA, Grudzien TA (1990) Dispersal in the wood frog (Rana sylvatica): implications for genetic population structure. Evolution (N Y) 44:2047–2056Google Scholar
  10. Boes MW, Benard MF (2013) Carry-over effects in nature: effects of canopy cover and individual pond on size, shape, and locomotor performance of metamorphosing wood frogs. Copeia 2013:717–722Google Scholar
  11. Boone MD (2005) Juvenile frogs compensate for small metamorph size with terrestrial growth: overcoming the effects of larval density and insecticide exposure. J Herpetol 39:416–423CrossRefGoogle Scholar
  12. Brady SP (2013) Microgeographic maladaptive performance and deme depression in response to roads and runoff. PeerJ 1:e163. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer Science & Business MediaGoogle Scholar
  14. Calhoun AJK, Miller NA, Klemens MW (2005) Conserving pool-breeding amphibians in human-dominated landscapes through local implementation of best development practices. Wetl Ecol Manag 13:291–304CrossRefGoogle Scholar
  15. Callender E, Rice KC (2000) The urban environmental gradient: anthropogenic influences on the spatial and temporal distributions of lead and zinc in sediments. Environ Sci Technol 34:232–238. CrossRefGoogle Scholar
  16. Clark PJ, Reed JM, Tavernia BG, et al (2008) Urbanization effects on spotted salamander and wood frog presence and abundance. Urban Herpetol 1–9Google Scholar
  17. Cline BB, Hunter ML (2014) Different open-canopy vegetation types affect matrix permeability for a dispersing forest amphibian. J Appl Ecol 51:319–329CrossRefGoogle Scholar
  18. Cline BB, Hunter MLJ (2016) Movement in the matrix: substrates and distance-to-forest edge affect postmetamorphic movements of a forest amphibian. Ecosphere 7:1–23CrossRefGoogle Scholar
  19. Core Team R (2016) R: a language and environment for statistical computing. R Found. Stat, ComputGoogle Scholar
  20. Crespi EJ, Warne RW (2013) Environmental conditions experienced during the tadpole stage alter post-metamorphic glucocorticoid response to stress in an amphibian. Integr Comp Biol 53:989–1001CrossRefGoogle Scholar
  21. Dananay KL, Krynak KL, Krynak TJ, Benard MF (2015) Apparent positive larval effects counteracted by negative postmetamorphic effects in wood frogs. Environ Toxicol Chem 34:2417–2424CrossRefGoogle Scholar
  22. Denver RJ (2009) Stress hormones mediate environment-genotype interactions during amphibian development. Gen Comp Endocrinol 164:20–31CrossRefGoogle Scholar
  23. Earl JE, Semlitsch RD (2013) Carryover effects in amphibians: are characteristics of the larval habitat needed to predict juvenile survival? Ecol Appl 23:1429–1442CrossRefGoogle Scholar
  24. Earl JE, Whiteman HH (2015) Are commonly used fitness predictors accurate? A meta-analysis of amphibian size and age at metamorphosis. Copeia 103:297–309CrossRefGoogle Scholar
  25. Fry J, Xian G, Jin S et al (2011) Completion of the 2006 National Land Cover Database for the conterminous United States. Photogramm Eng Remote Sensing 77:858–566Google Scholar
  26. Furman BLS, Scheffers BR, Taylor M et al (2016) Limited genetic structure in a wood frog (Lithobates sylvaticus) population in an urban landscape inhabiting natural and constructed wetlands. Conserv Genet 17:19–30. CrossRefGoogle Scholar
  27. Gabrielsen CG, Kovach AI, Babbitt KJ, McDowell WH (2013) Limited effects of suburbanization on the genetic structure of an abundant vernal pool-breeding amphibian. Conserv Genet 14:1083–1097. CrossRefGoogle Scholar
  28. Gentz EJ (2007) Medicine and surgery of amphibians. ILAR J 48:255–259CrossRefGoogle Scholar
  29. Gervasi SS, Foufopoulos J (2008) Costs of plasticity: responses to desiccation decrease post-metamorphic immune function in a pond-breeding amphibian. Funct Ecol 22:100–108Google Scholar
  30. Gibbs JP (1998) Distribution of woodland amphibians along a forest fragmentation gradient. Landsc Ecol 13:263–268CrossRefGoogle Scholar
  31. Goater CP, Vandenbos RE (1997) Effects of larval history and lungworm infection on the growth and survival of juvenile wood frogs (Rana sylvatica). Herpetologica 53:331–338Google Scholar
  32. Gosner KL (1960) A simplified table for staging anuran embryos larvae with notes on identification. Herpetologica 16:183–190Google Scholar
  33. Grant EHC, Jung RE, Nichols JD, Hines JE (2005) Double-observer approach to estimating egg mass abundance of pool-breeding amphibians. Wetl Ecol Manag 13:305–320CrossRefGoogle Scholar
  34. Green AJ (2001) Mass/length residuals: measures of body condition or generators of spurious results? Ecology 82:1473–1483CrossRefGoogle Scholar
  35. Green AW, Bailey LL (2015) Reproductive strategy and carry-over effects for species with complex life histories. Popul Ecol 57:175–184CrossRefGoogle Scholar
  36. Greenspan SE, Calhoun AJK, Longcore JE, Levy MG (2012) Transmission of Batrachochytrium dendrobatidis to wood frogs (Lithobates sylvaticus) via a bullfrog (L. catesbeianus) vector. J Wildl Dis 48:575–582CrossRefGoogle Scholar
  37. Hall EM, Brady SP, Mattheus NM et al (2017) Physiological consequences of exposure to salinized roadside ponds on wood frog larvae and adults. Biol Conserv 209:98–106. CrossRefGoogle Scholar
  38. Halverson MA, Skelly DK, Kiesecker JM, Freidenburg LK (2003) Forest mediated light regime linked to amphibian distribution and performance. Oecologia 134:360–364CrossRefGoogle Scholar
  39. Herreid CF, Kinney S (1967) Temperature and development of the wood frog, Rana sylvatica, in Alaska. Ecology 48:579–590CrossRefGoogle Scholar
  40. Holgerson MA, Lambert MR, Freidenburg LK, Skelly DK (2017) Suburbanization alters small pond ecosystems: shifts in nitrogen and food web dynamics. Can J Fish Aquat Sci 75:641–652CrossRefGoogle Scholar
  41. Homan RN, Windmiller BS, Reed JM (2004) Critical thresholds associated with habitat loss for two vernal pool-breeding amphibians. Ecol Appl 14:1547–1553CrossRefGoogle Scholar
  42. Homola JJ (2018) Eco-evolutionary implications of environmental change across heterogeneous landscapesGoogle Scholar
  43. Jennette MA (2010) Variation in age, body size, and reproductive traits among urban and rural amphibian populations.
  44. Jeon SB, Olofsson P, Woodcock CE (2014) Land use change in New England: a reversal of the forest transition. J Land Use Sci 9:105–130. CrossRefGoogle Scholar
  45. Karraker NE, Gibbs JP (2009) Amphibian production in forested landscapes in relation to wetland hydroperiod: a case study of vernal pools and beaver ponds. Biol Conserv 142:2293–2302CrossRefGoogle Scholar
  46. Lambert MR, Skelly DK (2016) Diverse sources for endocrine disruption in the wild. Endocr Disruptors 4:e1148803. CrossRefGoogle Scholar
  47. Lambert MR, Giller GSJ, Barber LB et al (2015) Suburbanization, estrogen contamination, and sex ratio in wild amphibian populations. Proc Natl Acad Sci 112:11881–11886. CrossRefPubMedGoogle Scholar
  48. Lambert MR, Giller GSJ, Skelly DK, Bribiescas RG (2016) Septic systems, but not sanitary sewer lines, are associated with elevated estradiol in male frog metamorphs from suburban ponds. Gen Comp Endocrinol 232:109–114. CrossRefPubMedGoogle Scholar
  49. Lambert MR, Stoler AB, Smylie MS et al (2017) Interactive effects of road salt and leaf litter on wood frog sex ratios and sexual size dimorphism. Can J Fish Aquat Sci 74:141–146. CrossRefGoogle Scholar
  50. Lambert MR, Smylie MS, Roman AJ et al (2018) Sexual and somatic development of wood frog tadpoles along a thermal gradient. J Exp Zool Part A Ecol Integr Physiol 329:72–79. CrossRefGoogle Scholar
  51. Levine TR, Hullett CR (2002) Eta squared, partial eta squared, and misreporting of effect size in communication research. Hum Commun Res 28:612–625CrossRefGoogle Scholar
  52. Mazerolle MJ (2017) Package “AICcmodavg.” 189Google Scholar
  53. McKinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst 11:161–176CrossRefGoogle Scholar
  54. Nagy C, Aschen S, Christie R, Weckel M (2011) Japanese stilt grass (Microstegium vimineum), a nonnative invasive grass, provides alternative habitat for native frogs in a suburban forest. Methods 6:1–10Google Scholar
  55. Nicholls B, Manne LL, Veit RR (2017) Changes in distribution and abundance of anuran species of Staten Island, NY, over the last century. Northeast Nat 24:65–81. CrossRefGoogle Scholar
  56. Oksanen J, Blanchet GF, Friendly M et al (2017) Vegan: community ecology package. R package version 2:4–3Google Scholar
  57. Orizaola G, Laurila A (2009) Microgeographic variation in the effects of larval temperature environment on juvenile morphology and locomotion in the pool frog. J Zool 277:267–274CrossRefGoogle Scholar
  58. Pechenik JA (2004) Larval experience and latent effects — metamorphosis is not a new beginning. Annual Meeting of the Society for Integrative and Comparative Biology, In, pp 323–333Google Scholar
  59. Pinheiro J, Bates D, DebRoy S, et al (2017) Nlme: linear and nonlinear mixed effects models. R Packag. 3rd edn. 1–336Google Scholar
  60. Relyea RA (2001) The lasting effects of adaptive plasticity: predator-induced tadpoles become long-legged frogs. Ecology 82:1947–1955CrossRefGoogle Scholar
  61. Relyea RA, Hoverman JT (2003) The impact of larval predators and competitors on the morphology and fitness of juvenile treefrogs. 596–604Google Scholar
  62. Rowe CL, Dunson WA (1995) Impacts of hydroperiod on growth and survival of larval amphibians in temporary ponds of Central Pennsylvania, USA. Oecologia 102:397–403CrossRefGoogle Scholar
  63. Rubbo MJ, Kiesecker JM (2005) Amphibian breeding distribution in an urbanized landscape. Conserv Biol 19:504–511CrossRefGoogle Scholar
  64. Sanzo D, Hecnar SJ (2006) Effects of road de-icing salt (NaCl) on larval wood frogs (Rana sylvatica). Environ Pollut 140:247–256CrossRefGoogle Scholar
  65. Scheffers BR, Paszkowski CA (2016) Large body size for metamorphic wood frogs in urban stormwater wetlands. Urban Ecosyst 19:347–359CrossRefGoogle Scholar
  66. Schiesari L (2006) Pond canopy cover: a resource gradient for anuran larvae. Freshw Biol 51:412–423CrossRefGoogle Scholar
  67. Semlitsch RD, Scott DE, Pechmann JHK (1988) Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69:184–192CrossRefGoogle Scholar
  68. Shepack A, Freidenburg LK, Skelly DK (2017) Species absence in developed landscapes: an experimental evaluation. Landsc Ecol 32:609–615CrossRefGoogle Scholar
  69. Skelly DK, Freidenburg LK, Kiesecker JM (2002) Forest canopy and the performance of larval amphibians. Ecology 83:983–992CrossRefGoogle Scholar
  70. Skidds DE, Golet FC, Paton PWC, Mitchell JC (2007) Habitat correlates of reproductive effort in wood frogs and spotted salamanders in an urbanizing watershed. J Herpetol 41:439–450CrossRefGoogle Scholar
  71. Smith-Gill SJ, Berven KA (1979) Predicting amphibian metamorphosis. Am Nat 113:563–585CrossRefGoogle Scholar
  72. Smits AP, Skelly DK, Bolden SR (2014) Amphibian intersex in suburban landscapes. Ecosphere 5:1–9. CrossRefGoogle Scholar
  73. Theobald DM (2005) Landscape patterns of exurban growth in the USA from 1980 to 2020. Ecol Soc 10.
  74. U.S. Census Bureau (2011) 2010 Census demographic profileGoogle Scholar
  75. U.S. Census Bureau (2016) 2012–2016 American Community Survey 5-Year estimatesGoogle Scholar
  76. Vasconcelos D, Calhoun AJK (2004) Movement patterns of adult and juvenile Rana sylvatica (LeConte) and Ambystoma maculatum (Shaw) in three restored seasonal pools in Maine. J Herpetol 38:551–561CrossRefGoogle Scholar
  77. Veysey JS, Mattfeldt SD, Babbitt KJ (2011) Comparative influence of isolation, landscape, and wetland characteristics on egg-mass abundance of two pool-breeding amphibian species. Landsc Ecol 26:661–672CrossRefGoogle Scholar
  78. Wade AA, Theobald DM (2010) Residential development encroachment on U.S. protected areas. Conserv Biol 24:151–161. CrossRefPubMedGoogle Scholar
  79. Watkins TB, Vraspir J (2006) Both incubation temperature and posthatching temperature affect swimming performance and morphology of wood frog tadpoles (Rana sylvatica). Physiol Biochem Zool 79:140–149CrossRefGoogle Scholar
  80. Werner EE, Glennemeier KS (1999) Influence of forest canopy cover on the breeding pond distributions of several amphibian species. Copeia 1:1–12CrossRefGoogle Scholar
  81. White EM, Morzillo AT, Alig RJ (2009) Past and projected rural land conversion in the US at state, regional, and national levels. Landsc Urban Plan 89:37–48. CrossRefGoogle Scholar
  82. Wilbur HM (1977) Interactions of food level and population density in Rana sylvatica. Ecology 58:206–209CrossRefGoogle Scholar
  83. Wilcove DS, Rothstein D, Dubow J et al (1998) Quantifying threats to imperiled species in the United States. Bioscience 48:607–615. CrossRefGoogle Scholar
  84. Windmiller B, Homan RN, Regosin JV et al (2008) Breeding amphibian population declines following loss of upland forest habitat around vernal pools in Massachusetts, USA. Urban Herpetology, In, pp 41–52Google Scholar

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Authors and Affiliations

  1. 1.Department of Wildlife, Fisheries, and Conservation BiologyUniversity of MaineOronoUSA

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