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Habitat Characteristics in Created Vernal Pools Impact Spotted Salamander Water-Borne Corticosterone Levels

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Abstract

Spotted salamanders (Ambystoma maculatum) require vernal pools for breeding habitat. Limited protection and preservation of vernal pools makes suitable habitat creation important. Differences in corticosterone levels, a hormone associated with growth, development, and stress in amphibians, could indicate population health and habitat quality. Our objective was to determine if habitat characteristics in created vernal pools influence corticosterone levels of spotted salamander larvae. In May and June of 2015 and 2016, we sampled water-borne corticosterone levels of larval spotted salamanders in 34 created vernal pools constructed 1–5 years earlier. Using multiple regression, we determined the best model predicting corticosterone levels included larval total length, pool-water temperature, year sampled, and pool diameter. Pool-water pH, depth, and age; percent cover; and predator presence were not significant predictors. Annual variation in corticosterone levels and habitat characteristics, and positive associations with water temperature and salamander body size highlighted the importance of controlling for external influences. The negative association between pool diameter and corticosterone indicated that larvae in larger pools (up to 12.75-m maximum diameter) were less stressed and potentially healthier. These results indicate that pool diameter contributes to habitat quality and may be important when constructing vernal pools for spotted salamanders.

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References

  • Balcombe CK, Anderson JT, Fortney RH, Kordek WS (2005) Vegetation, invertebrate, and wildlife community rankings and habitat analysis of mitigation wetlands in West Virginia. Wetlands Ecology and Management 13:517–530

    Article  Google Scholar 

  • Barbour MG, Burk JH, Pitts WD, Gilliam FS, Schwartz MW (1999) Terrestrial plant ecology, Third Edition. Benjamin and Cummings, California

    Google Scholar 

  • Baugh AT, Bastien B, Still M, Stowell N (2018) Validation of water-borne steroid hormones in a tropical frog (Physalaemus pustulosus). General and Comparative Endocrinology 261:67–80

    Article  CAS  PubMed  Google Scholar 

  • Belden LK, Kiesecker JM (2005) Glucocorticosteroid hormone treatment of larval treefrogs increases infection by Alaria sp. trematode cercariae. The Journal of Parasitology 19:686–688

    Article  Google Scholar 

  • Bianchini K, Tattersall GJ, Sashaw J, Porteus CS, Wright PA (2012) Acid water interferes with salamander-green algae symbiosis during early embryonic development. Physiological and Biochemical Zoology 85:470–480

    Article  CAS  PubMed  Google Scholar 

  • Bonier F, Martin PR, Moore IT, Wingfield JC (2009) Do baseline glucocorticoids predict fitness? Trends in Ecology & Evolution 24:634–642

    Article  Google Scholar 

  • Brodman R (1993) The effect of acidity on interactions of Ambystoma salamander larvae. Journal of Freshwater Ecology 8:209–214

    Article  CAS  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer Science & Business Media, LLC, New York

    Google Scholar 

  • Calhoun AJK, Arrigoni J, Brooks RP, Hunter ML, Richter SC (2014) Creating successful vernal pools: a literature review and advice for practitioners. Wetlands 34:1027–1038

    Article  Google Scholar 

  • Carr JA, Norris DO (1988) Interrenal activity during metamorphosis of the tiger salamander, Ambystoma tigrinum. General and Comparative Endocrinology 71:63–69

    Article  CAS  PubMed  Google Scholar 

  • Chambers DL, Wojdak JM, Du P, Belden LK (2011) Corticosterone level changes throughout larval development in the amphibians Rana sylvatica and Ambystoma jeffersonianum reared under laboratory, mesocosm, or free-living conditions. Copeia 2011:530–538

    Article  Google Scholar 

  • Chambers DL, Wojdak JM, Du P, Belden LK (2013) Pond acidification may explain differences in corticosterone among salamander populations. Physiological and Biochemical Zoology 86:224–232

    Article  CAS  PubMed  Google Scholar 

  • Charbonnier JF, Pearlmutter J, Vonesh JR, Gabor CR, Forsburg ZR, Grayson KL (2018) Cross-life stage effects of aquatic larval density and terrestrial moisture on growth and corticosterone in the spotted salamander. Diversity 10:68

    Article  CAS  Google Scholar 

  • Clark KL (1986) Responses of Ambystoma maculatum populations in Central Ontario to habitat acidity. The Canadian Field-Naturalist 100:463–469

    Google Scholar 

  • Cree A, Tyrrell CL, Preest MR, Thorburn D, Guillette LJ Jr (2003) Protecting embryos from stress: corticosterone effects and the corticosterone response to capture and confinement during pregnancy in a live-bearing lizard (Hoplodactylus maculatus). General and Comparative Endocrinology 134:316–329

    Article  CAS  PubMed  Google Scholar 

  • Crespi EJ, Denver RJ (2005) Roles of stress hormones in food intake regulation in anuran amphibians throughout the life cycle. Comparative Biochemistry and Physiology, Part A 141:381–390

    Article  CAS  Google Scholar 

  • Dantzer B, Fletcher QE, Boonstra R, Sheriff MJ (2014) Measures of physiological stress: a transparent or opaque window into the status, management and conservation of species? Conservation Physiology 2:cou023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davis DR, Gabor CR (2015) Behavioral and physiological antipredator responses of the San Marcos salamander, Eurycea nana. Physiology & Behavior 139:145–149

    Article  CAS  Google Scholar 

  • Denton RD, Richter SC (2013) Amphibian communities in natural and constructed ridge top wetlands with implications for wetland construction. The Journal of Wildlife Management 77:886–896

    Article  Google Scholar 

  • DiBello FJ, Calhoun AJK, Morgan DE, Shearin AF (2016) Efficiency and detection accuracy using print and digital stereo aerial photography for remotely mapping vernal pools in New England landscapes. Wetlands 36:505–514

    Article  Google Scholar 

  • Dickens MJ, Romero LM (2013) A consensus endocrine profile for chronically stressed wild animals does not exist. General and Comparative Endocrinology 191:177–189

    Article  CAS  PubMed  Google Scholar 

  • Dupont W, Bourgeois P, Reinberg A, Vaillant R (1979) Circannual and circadian rhythms in the concentrations of corticosterone on the plasma of the edible frog (Rana esculenta L.). Journal of Endocrinology 80:117–125

    Article  CAS  PubMed  Google Scholar 

  • Egan RS, Paton PWC (2004) Within-pond parameters affecting oviposition by wood frogs and spotted salamanders. Wetlands 24:1–13

    Article  Google Scholar 

  • Felix ZI, Wang Y, Schweitzer CJ (2010) Effects of experimental canopy manipulation on amphibian egg deposition. Journal of Wildlife Management 74:496–503

    Article  Google Scholar 

  • Fonner CW, Woodley SK (2015) Testing the predation stress hypothesis: behavioural and hormonal responses to predator cues in Allegheny Mountain dusky salamanders. Behaviour 152:797–819

    Article  Google Scholar 

  • Formanowicz DR, Bobka MS (1989) Predation risk and microhabitat preference: an experimental study of the behavioral responses of prey and predator. Am Midl Nat 121:379–386

    Article  Google Scholar 

  • Fox J, Weisberg S (2011) An {R} companion to applied regression, second edition. Sage, Thousand Oaks URL: http://socserv.socsci.mcmaster.ca/jfox/Books/Companion

    Google Scholar 

  • Gabor CR, Bosch J, Fries JN, Davis DR (2013) A non-invasive water-borne hormone assay for amphibians. Amphibia-Reptilia 34:151–162

    Article  Google Scholar 

  • Gabor CR, Fisher MC, Bosch J (2015) Elevated corticosterone levels and changes in amphibian behavior are associated with Batrachochytrium dendrobatidis (Bd) infection and Bd lineage. PLoS One 10:e0122685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gabor CR, Zabierek KC, Kim DS, da Barbiano LA, Mondelli MJ, Bendik NF, Davis DR (2016) A non-invasive water-borne assay of stress hormones in aquatic salamanders. Copeia 104:172–181

    Article  Google Scholar 

  • Glennemeier KA, Denver RJ (2002) Role for corticoids in mediating the response of Rana pipiens tadpoles in intraspecific competition. Journal of Experimental Zoology 292:32–40

    Article  CAS  PubMed  Google Scholar 

  • Gormally BMG, Fuller R, McVey M, Romero LM (2018) DNA damage as an indicator of chronic stress: correlations with corticosterone and uric acid. Comparative Biochemistry and Physiology, Part A 227:116–122

    Article  CAS  Google Scholar 

  • Gosner KK, Black IH (1957) The effects of acidity on the development of New Jersey frogs. Ecology 38:256–262

    Article  CAS  Google Scholar 

  • Groff LA, Loftin CS, Calhoun AJK (2017) Predictors of breeding site occupancy by amphibians in montane landscapes. The Journal of Wildlife Management 81:269–278

    Article  Google Scholar 

  • Harris BN, Carr JA (2016) The role of the hypothalamus-pituitary-adrenal/interrenal axis in mediating predator-avoidance trade-offs. General and Comparative Endocrinology 230:110–142

    Article  CAS  PubMed  Google Scholar 

  • Holmes AM, Emmans CJ, Jones N, Coleman R, Smith TE, Hosie CA (2016) Impact of tank background on the welfare of the African clawed frog, Xenopus laevis (Daudin). Applied Animal Behaviour Science 185:131–136

    Article  Google Scholar 

  • Homan RN, Regosin JV, Rodrigues DM, Reed JM, Windmiller BS, Romero LM (2003) Impacts of varying habitat quality on the physiological stress of spotted salamanders (Ambystoma maculatum). Animal Conservation 6:11–18

    Article  Google Scholar 

  • Homyack JA (2010) Evaluating habitat quality of vertebrates using conservation physiology tools. Wildlife Research 37:332–342

    Article  Google Scholar 

  • Hopkins WA, Mendonca MT, Congdon JD (1999) Responsiveness of the hypothalamo-pituitary-interrenal axis in an amphibian (Bufo terrestris) exposed to coal combustion wastes. Comparative Biochemistry and Physiology, Part C 122:191–196

    Article  CAS  Google Scholar 

  • Hossie TJ, MacFarlane S, Clement A, Murray DL (2017) Threat of predation alters aggressive interactions among spotted salamander (Ambystoma maculatum) larvae. Ecology and Evolution 8:3131–3138

    Article  Google Scholar 

  • Janin A, Lena JP, Deblois S, Joly P (2012) Use of stress-hormone levels and habitat selection to assess functional connectivity of a landscape for an amphibian. Conservation Biology 26:923–931

    Article  PubMed  Google Scholar 

  • Kern MM, Nassar AA, Guzy JC, Dorcas ME (2013) Oviposition site selection by spotted salamanders (Ambystoma maculatum) in an isolated wetland. Journal of Herpetology 47:445–449

    Article  Google Scholar 

  • Kindt R, Coe R (2005) Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies. World agroforestry Centre (ICRAF), Nairobi. In: ISBN 92–9059-179-X

    Google Scholar 

  • Mazerolle MJ (2017) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 2.1–1. https://cran.r-project.org/package=AICcmodavg

  • McCormick SD, Romero M (2017) Conservation endocrinology. Bioscience 67:429–442

    Article  Google Scholar 

  • McEwin BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Hormones and Behavior 43:2–15

    Article  Google Scholar 

  • Moore IT, Jessop TS (2003) Stress, reproduction, and adrenocortical modulation in amphibians and reptiles. Hormones and Behavior 43:39–47

    Article  CAS  PubMed  Google Scholar 

  • Novarro AJ, Gabor CR, Goff CB, Mezebish TD, Thompson LM, Grayson KL (2018) Physiological responses to elevated temperature across the geographic range of a terrestrial salamander. Journal of Experimental Biology 221:jeb178236

    Article  PubMed  Google Scholar 

  • Petranka JW, Kennedy CA, Murray SS (2003a) Response of amphibians to restoration of a southern Appalachian wetland: a long-term analysis of community dynamics. Wetlands 23:1030–1042

    Article  Google Scholar 

  • Petranka JW, Kennedy CA, Murray SS (2003b) Response of amphibians to restoration of a southern Appalachian wetland: perturbations confound post-restoration assessment. Wetlands 23:278–290

    Article  Google Scholar 

  • Pough FH, Wilson RE (1977) Acid precipitation and reproductive success of Ambystoma salamanders. Water, Air, and Soil Pollution 7:307–316

    Article  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

  • Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends in Ecology and Evolution 19:249–255

    Article  PubMed  Google Scholar 

  • Romero LM, Reed JM (2005) Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comparative Biochemistry and Physiology, Part A 140:73–79

    Article  CAS  Google Scholar 

  • Romero L, Wikelski M (2001) Corticosterone levels predict survival probabilities of Galápagos marine iguanas during El Nino events. Proceedings of the National Academy of Sciences of the United States of America 98:7366–7370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rowe CL, Dunson WA (1993) Relationships among biotic parameters and breeding effort by three amphibians in temporary wetlands of Central Pennsylvania. Wetlands 13:237–246

    Article  Google Scholar 

  • Sandeno CM (2011) Project status report – Barton Bench ecological restoration Greenbrier ranger district Monongahela National Forest. WV Department of Environmental Protection, Division of Mining and Reclamation

  • Scheffers BR, Furman BL, Evans JP (2013) Salamanders continue to breed in ephemeral ponds following the removal of surrounding terrestrial habitat. Herpetological Conservation and Biology 8:715–723

    Google Scholar 

  • Scott AP, Ellis T (2007) Measurement of fish steroids in water–a review. General and Comparative Endocrinology 153:392–400

    Article  CAS  PubMed  Google Scholar 

  • Skidds DE, Golet FC, Paton PW, Mitchell JC (2007) Habitat correlates of reproductive effort in wood frogs and spotted salamanders in an urbanizing watershed. Journal of Herpetology 41:439–450

    Article  Google Scholar 

  • The Weather Underground Elkins-Randolph County Station. Weather history for Elkins-Randolph county, WV. Weather Underground, The Weather Company. https://www.wunderground.com/history/daily/us/wv/mill-creek/KEKN/date/2019-1-17?cm_ven=localwx_history. Accessed 15 Jan 2019

  • Thomas JR, Magyan AJ, Freeman PE, Woodley SK (2017) Testing hypotheses about individual variation in plasma corticosterone in free-living salamanders. Journal of Experimental Biology 220:1210–1221

    Article  PubMed  Google Scholar 

  • Troïanowski M, Mondy N, Dumet A, Arcanjo C, Lengagne T (2017) Effects of traffic noise on tree frog stress levels, immunity, and color signaling. Conservation Biology 31:1132–1140

    Article  PubMed  Google Scholar 

  • United States Forest Service (2014) Mower Tract ecological restoration final report

  • Vasconcelos D, Calhoun AJK (2006) Monitoring created seasonal pools for functional success: a six-year case study of amphibian responses, Sears Island, Maine, USA. Wetlands 26:992–1003

    Article  Google Scholar 

  • Wack CL, DuRant SE, Hopkins WA, Lovern MB, Feldhoff RC, Woodley SK (2012) Elevated plasma corticosterone increases metabolic rate in a terrestrial salamander. Comparative Biochemistry and Physiology, Part A 161:153–158

    Article  CAS  Google Scholar 

  • Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York

    Book  Google Scholar 

  • Wingfield JC, Maney DL, Breuner CW, Jacobs JD, Lynn S, Ramenofsky M, Richardson RD (1998) Ecological bases of hormone-behavior interactions: the “emergency life history stage.”. American Zoologist 38:191–206

    Article  CAS  Google Scholar 

  • Woodley SK, Freeman P, Ricciardella LF (2014) Environmental acidification is not associated with altered corticosterone levels in the stream-side salamander, Desmognathus ochrophaeus. General and Comparative Endocrinology 201:8–15

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was completed with approval from West Virginia University Institutional Animal Care and Use Committee (15-0409.3), the U.S. Forest Service, and the West Virginia Division of Natural Resources (Scientific Collecting Permit 2015.133, 2016.205). We thank J Rouda, J Strickland, M Mabry, A Magyan, A Bucher, and J Millikin for field and lab assistance, and D Brown for statistical advice. This research was funded by the U.S. Forest Service, Natural Resources Conservation Service, National Science Foundation (01A-1458952), West Virginia University Natural History Museum, National Institute of Food and Agriculture McStennis Project WVA00117, The Explorers Club Washington Group, Society of Wetland Scientists, Society of Wetland Scientists South Atlantic Chapter, West Virginia University Stitzel Graduate Enhancement Fund, and R and L Bowman. We also thank West Virginia Division of Natural Resources, Department of Biological Sciences at Duquesne University, and the Ruby Distinguished Doctoral Fellowship Program. This is scientific article number 3355 of the West Virginia Agricultural and Forestry Experiment Station, Morgantown.

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Authors and Affiliations

  1. School of Natural Resources, West Virginia University, PO Box 6125, Morgantown, WV, 26506, USA

    Alice R. Millikin & James T. Anderson

  2. Biological Sciences, Duquesne University, 600 Forbes Avenue, Pittsburgh, PA, 15282, USA

    Sarah K. Woodley

  3. School of Earth, Environmental, and Marine Sciences, University of Texas Rio Grande Valley, 100 Marine Lab Drive, South Padre Island, TX, 78597, USA

    Drew R. Davis

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  1. Alice R. Millikin
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Correspondence to Alice R. Millikin.

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Fig. S1

Monthly average temperatures separated by sample year based on the 12 months before and including sampling: July 2014 – June 2015 and July 2015 – June 2016. Weather data are from the nearest weather station (Elkins, WV), which is 40.23 km away. Data from The Weather Underground [United States] Elkins-Randolph County Station, WV. (DOCX 15.5 kb)

Fig. S2

Monthly total precipitation separated by sample year based on the 12 months before and including sampling: July 2014 – June 2015 and July 2015 – June 2016. Weather data are from the nearest weather station (Elkins, WV), which is 40.23 km away. Data from The Weather Underground [United States] Elkins-Randolph County Station, WV. (DOCX 15.5 kb)

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Millikin, A.R., Woodley, S.K., Davis, D.R. et al. Habitat Characteristics in Created Vernal Pools Impact Spotted Salamander Water-Borne Corticosterone Levels. Wetlands 39, 803–814 (2019). https://doi.org/10.1007/s13157-019-01130-5

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