Microhabitat use during brumation in the Japanese treefrog, Dryophytes japonicus

in Amphibia-Reptilia
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?

Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.


Have Institutional Access?

Access content through your institution. Any other coaching guidance?



Although amphibians undergo drastic changes in physiology and behaviour before hibernation, this phase of their life cycle (i.e., brumation) is the least understood. We investigated the patterns of microhabitat use by Dryophytes japonicus during brumation using a Harmonic Direction Finder to track 27 adults in October 2013. Most frogs used chestnut trees throughout their diel cycle. The species was most active within the “leafy vegetation” microhabitat, moving about 2 m within 72 h on average, and mostly circa 10 AM. Frogs moved less in the four other microhabitats, with individuals moving between 1 m and 50 cm, typically during the early afternoon. Around 3 pm, the microhabitat mostly used was “on bark”, with displacements almost totally halted. The use of microhabitats and shelters, as well as movements in relation to time of day, suggests that D. japonicus displays behavioural thermoregulation during brumation. This research is the first providing insights in the brumation ecology of a non-freeze-resistant Palearctic anuran.

Microhabitat use during brumation in the Japanese treefrog, Dryophytes japonicus

in Amphibia-Reptilia



  • BazinY.WhartonD.A.BishopP.J. (2007): Cold tolerance and overwintering of an introduced New Zealand frog, the brown tree frog (Litoria ewingii). CryoLetters 28: 347-358.

  • BeebeeT.J. (1988): The fascination of hibernation. Brit Herp Soc Bul 23: 21-22.

  • BermanD.MeshcheryakovaE.BulakhovaN. (2016): The Japanese tree frog (Hyla japonica), one of the most cold-resistant species of amphibians. Doklady Biological Sciences 471: 276-279.

  • BorzéeA.KimJ.Y.Da CunhaM.A.LeeD.SinE.OhS.YiY.JangY. (2016a): Temporal and spatial differentiation in microhabitat use: implications for reproductive isolation and ecological niche specification. Integr Zool 11: 375-387.

  • BorzéeA.KimJ.Y.JangY. (2016b): Asymmetric competition over calling sites in two closely related treefrog species. Sci Rep 6: 32569.

  • BoughtonR.G.StaigerJ.FranzR. (2000): Use of PVC pipe refugia as a sampling technique for hylid treefrogs. Am Midl Nat 144: 168-177.

  • BoutilierR.DonohoeP.TattersallG.WestT. (1997): Hypometabolic homeostasis in overwintering aquatic amphibians. J Exp Biol 200: 387-400.

  • BradfordD.F. (1983): Winterkill, oxygen relations, and energy metabolism of a submerged dormant amphibian, Rana muscosa. Ecology 64: 1171-1183.

  • ClausnitzerH.-J. (1986): Zur Ökologie und Ernährung des Laubfrosches Hyla a. arborea (Linnaeus, 1756) im Sommerlebensraum (Salientia: Hylidae). Salamandra 22: 162-172.

  • CostanzoJ.P.WrightM.F.Richard E.LeeJ. (1992): Freeze tolerance as an overwintering adaptation in Cope’s grey treefrog (Hyla chrysoscelis). Copeia 2: 565-569.

  • CroesS.A.ThomasR.E.BowkerR.G. (2000): Freeze tolerance and cryoprotectant synthesis of the Pacific tree frog Hyla regilla. Copeia 2000: 863-868.

  • CunjakR.A. (1986): Winter habitat of northern leopard frogs, Rana pipiens, in a southern Ontario stream. Can J Zoolog 64: 255-257.

  • DuellmanW.E.MarionA.B.HedgesS.B. (2016): Phylogenetics, classification, and biogeography of the treefrogs (Amphibia: Anura: Arboranae). Zootaxa 4104: 1-109.

  • DufresnesC.LitvinchukS.N.BorzéeA.JangY.LiJ.-T.MiuraI.PerrinN.StöckM. (2016): Phylogeography reveals an ancient cryptic radiation in east-Asian tree frogs (Hyla japonica group) and complex relationships between continental and island lineages. BMC Evol Biol 16: 253.

  • DürigenB. (1897): Deutschlands Amphibien und Reptilien: eine Beschreibung und Schilderung sämtlicher in Deutschland und den angrenzenden Gebieten vorkommenden Lurche und Kriechtiere. KreutzGermany.

  • EdwardsJ.R.KosterK.L.SwansonD.L. (2000): Time course for cryoprotectant synthesis in the freeze-tolerant chorus frog, Pseudacris triseriata. Comp Biochem Phys A 125: 367-375.

  • FairmanC.M.BaileyL.L.ChambersR.M.RussellT.M.FunkW.C. (2013): Species-specific effects of acidity on pond occupancy in Ambystoma salamanders. J Herpetol 47: 346-353.

  • FujiokaM.LaneS.J. (1997): The impact of changing irrigation practices in rice fields on frog populations of the Kanto Plain, central Japan. Ecol Res 12: 101-108.

  • GosnerK.L.BlackI.H. (1957): The effects of acidity on the development and hatching of New Jersey frogs. Ecology 38: 256-262.

  • HarlowH.J.HillmanS.S.HoffmanM. (1976): The effect of temperature on digestive efficiency in the herbivorous lizard, Dipsosaurus dorsalis. J Comp Physiol B 111: 1-6.

  • HarrisR.T. (1975): Seasonal activity and microhabitat utilization in Hyla cadaverina (Anura: Hylidae). Herpetologica 31: 236-239.

  • HiraiT.MatsuiM. (2000): Feeding habits of the Japanese Tree Frog, Hyla japonica, in the reproductive season. Zool Sci 17: 977-982.

  • IangraiA.J. (2011): Studies on ecology breathing behaviour and metamorphosis of tree frogs Polypedates leucomystax and Rhacophorus bipunctatus (anura: Rhacophoridae) in Meghalaya (North-East India). Ph.D. Thesis North Eastern Hill University.

  • IharaS. (1999): Site selection for hibernation by the tree frog, Rhacophorus schlegelii. Jpn J Herpetol 18: 39-44.

  • IrwinJ.T.CostanzoJ.P.Richard E.LeeJ. (1999): Terrestrial hibernation in the northern cricket frog, Acris crepitans. Can J Zoolog 77: 1240-1246.

  • ItoH.FukudaA. (2007): Assessment of artificial environment for reproduction of forest green treefrog along Nikko-Utsunomiya road using habitat evaluation procedure. Lowland technology international 9: 8-14.

  • Jacqmin-GaddaH.SibillotS.ProustC.MolinaJ.-M.ThiebautR. (2007): Robustness of the linear mixed model to misspecied error distribution: robustness of the linear mixed model. Comp Stat Data Anal 51: 5142-5154.

  • JohnsonJ.R. (2005): Multi-scale investigations of gray treefrong movements: patterns of migration dispersal and gene flow. Ph.D. thesis University of Missouri-Columbia.

  • JohnsonJ.R.MahanR.D.SemlitschR.D. (2008): Seasonal terrestrial microhabitat use by gray treefrogs (Hyla versicolor) in Missouri oak-hickory forests. Herpetologica 64: 259-269.

  • KimJ.Y. (2015): Lekking behavior in the Japanese treefrog Hyla japonica. Ph.D. thesis Ewha Womans University.

  • KowalewskiL. (1974): Observations on the phenology and ecology of Amphibia in the region of Czestochowa. Acta Zool Cracoviensia 19: 399-457.

  • KuhlmannM.NolteT. (1986): Biometrische und Ökologische Betrachtungen an Einer Laubfrosch Population Unter Zuhilfenahme Einer Speziellen Wiedererkennungsmethode; Abiturprüfung Biologie Ahlen. Ahlen Städtisches GymnasiumGermany.

  • LachmannH. (1890): Die Reptilien und Amphibien Deutschlands in Wort und Bild: Eine Systematische und Biologische Bearbeitung der Bisher in Deutschland Aufgefundenen Kriechtiere und Lurche. Paul HüttigGermany.

  • LambrinosJ.G.KleierC.C. (2003): Thermoregulation of juvenile Andean toads (Bufo spinulosus) at 4300 m. J Therm Biol 28: 15-19.

  • LanooM. (2006): Amphibian Declines: the Conservation Status of United States Species California. University of California PressUSA.

  • MahanR.D.JohnsonJ.R. (2007): Diet of the gray treefrog (Hyla versicolor) in relation to foraging site location. J Herpetol 41: 16-23.

  • MayhewW.W. (1968): Biology of desert amphibians and reptiles. In: Desert Biology. Special Topics on the Physical and Biological Aspects of Arid Regions p. 226-229. BrownG.W. Ed. AcademicsNew York, USA.

  • McCombW.C.NobleR.E. (1981): Herpetofaunal use of natural tree cavities and nest boxes. Wildlife Soc B 9: 261-267.

  • McEachernM.A.AdamsA.A.Y.KlugP.E.FitzgeraldL.A.ReedR.N. (2015): Brumation of introduced black and white tegus, Tupinambis merianae (Squamata: Teiidae), in southern Florida. Southeast Nat 14: 319-328.

  • MoenD.S.IrschickD.J.WiensJ.J. (2013): Evolutionary conservatism and convergence both lead to striking similarity in ecology, morphology and performance across continents in frogs. Proc R Soc B Biol Sci 280: 20132156.

  • ParkS.JeongG.JangY. (2013): No reproductive character displacement in male advertisement signals of Hyla japonica in relation to the sympatric H. suweonensis. Behav Ecol Sociobiol 67: 1345-1355.

  • PinheiroJ.BatesD. (1978): Mixed-Effects Models in S and S-PLUS. SpringerNew York, USA.

  • PratiharS.KunduJ.K. (2011): Life in Cold Lane: Hibernation in Anurans Saarbrücken. Lap Lambert Academic Publishing GmbH & Co. KGGermany.

  • RegosinJ.V.WindmillerB.S.ReedJ.M. (2003): Terrestrial habitat use and winter densities of the wood frog (Rana sylvatica). J Herpetol 37: 390-394.

  • ReichholfJ. (1986): Aspekte der Biologie des Laubfrosches Hyla arborea. Deutsche Gesellschaft für Herpetologie und Terrarienkunde Bonn Rundbrief 89: 1-2.

  • Rodríguez-PrietoI.Fernández-JuricicE. (2005): Effects of direct human disturbance on the endemic Iberian frog Rana iberica at individual and population levels. Biol Cons 123: 1-9.

  • SchaubD.L.LarsenJ.H. (1978): The reproductive ecology of the Pacific Treefrog (Hyla regilla). Herpetologica 34: 409-416.

  • SchmidW.D. (1982): Survival of frogs in low temperature. Science 215: 697-698.

  • SchneiderH. (1977): Acoustic behavior and physiology of vocalization in the European tree frog, Hyla arborea (L.). In: The Reproductive Biology of Amphibians p. 295-335. SpringerBoston, USA.

  • ShannonF.A. (1956): The reptiles and amphibians of Korea. Herpetologica 12: 22-49.

  • SnellC. (1985): Frozen frogs, a natural occurrence? Bulletin of the British Herpetological Society 14: 25-27.

  • StinnerJ.ZarlingaN.OrcuttS. (1994): Overwintering behavior of adult bullfrogs, Rana catesbeiana, in northeastern Ohio. Ohio J Sci 94: 8-13.

  • StöckM.DufresnesC.LitvinchukS.N.LymberakisP.BiollayS.BerroneauM.BorzéeA.GhaliK.OgielskaM.PerrinN. (2012): Cryptic diversity among western palearctic tree frogs: postglacial range expansion, range limits, and secondary contacts of three European tree frog lineages (Hyla arborea group). Mol Phylogenet Evol 65: 1-9.

  • StoreyK.B.StoreyJ.M. (1992): Natural freeze tolerance in ectothermic vertebrates. Annu. Rev. Physiol. 54: 619-637.

  • StumpelA.H.HanekampG. (1986): Habitat and ecology of Hyla arborea in the Netherlands. In: Studies in Herpetology p. 409-411. Charles UniversityPrague, Czech Republic.

  • StumpelA.H.P. (1990): On hibernation sites in the tree frog Hyla arborea. Amphibia-Reptilia 11: 304-306.

  • SugimotoK.JiangH. (2008): Cold stress and light signals induce the expression of cold-inducible RNA binding protein (cirp) in the brain and eye of the Japanese treefrog (Hyla japonica). Comp Biochem Physiol A Mol Integr Physiol 151: 628-636.

  • SwaineC.DrageT.S.SmithF. (1798): An Account of a Voyage for the Discovery of a North-west Passage by Hudson’s Streights to the Western and Southern Ocean of America: Performed in the Year 1746 and 1747 in the Ship California Capt. Francis Smith Commander. Mr. Jolliffe, Mr. Corbett, and Mr. ClarkeLondon, UK.

  • TyrrellJ.B. (1911): A Journey From Prince of Wales’ Fort in Hudson’s Bay to the Northern Ocean in the Years 1769 1770 1771 and 1772 by Samuel Hearne. The Champlain SocietyToronto, Canada.

  • Van GelderJ.OldersJ.BoschJ.StarmansP. (1986): Behaviour and body temperature of hibernating common toads Bufo bufo. Ecography 9: 225-228.

  • VerbekeG.MolenberghsG. (1997): Linear Mixed Models for Longitudinal Data New York. SpringerUSA.

  • VoituronY.BarréH.RamløvH.DouadyC.J. (2009): Freeze tolerance evolution among anurans: frequency and timing of appearance. Cryobiology 58: 241-247.

  • WellsK. (1977): The social behaviour of anuran amphibians. Anim Behav 25: 666-693.

  • WellsK.D.SchwartzJ.J. (2007): The Behavioral Ecology of Anuran Communication. The University of Chicago PressChicago.

  • WellsK.W. (2010): The Ecology and Behavior of Amphibians. University of Chicago PressChicago, USA.

  • ZacharowM.BarichivichW.J.Dodd JrC.K. (2003): Using ground-placed PVC pipes to monitor hylid treefrogs: capture biases. Southeast Nat 2: 575-590.


  • View in gallery

    Linear mixed-effects regression model results depicting the impact of abiotic variables on vertical space use above and below 5 meters height for Dryophytes japonicus in Paju, Korea.

  • View in gallery

    Variation in body temperature between sheltered (n=154) and non-sheltered individual (n=146) Dryophytes japonicus during brumation in Korea. The line within the box represents the mean; the top and bottom lines represent 75 and 25 percentiles of the data, respectively; top and bottom whiskers represent 95 and 5 percentiles, respectively; asterisks represent outliers. The body temperature was significantly different between the two groups.

  • View in gallery

    Linear mixed-effects regression model results explaining the impact of abiotic and abiotic variables on “shelter use” during brumation for Dryophytes japonicus in Korea.

  • View in gallery

    Tree species and microhabitat use by Dryophytes japonicus in Korea. One hundred percent of occurrences matches corresponds to the sum of all values for each of the three tree species and the six microhabitats.

  • View in gallery

    Mixed-effects regression with microhabitat use as dependent variable performed to define which variables were important for the use of a specific microhabitat by Dryophytes japonicus in Korea.

  • View in gallery

    Descriptive statistics for microhabitat use and the relation with tree species and total use. Dryophytes japonicus had a clear preference for chestnut trees and was found in majority on leafy vegetation. Air temp. (in °C) is the average when the corresponding microhabitats are used. The SD on the last row relates to the air temperature.

  • View in gallery

    Microhabitat use and body temperature during brumation for Dryophytes japonicus in Korea. The minimum and maximum temperatures were recorded when the individuals were on leafy vegetation and on the ground, respectively (below ground: n=8, below leafy vegetation n=69, below tree bark n=60, on ground n=49, on leafy vegetation n=85, on tree bark n=29). The line within the box represents the mean; the top and bottom lines represent 75 and 25 percentiles of the data, respectively; top and bottom whiskers represent 95 and 5 percentiles, respectively; asterisks represent outliers. LSD post hoc analyses showed that “on leafy vegetation” was significantly different from “on ground” (p=0.008), “under tree bark” (p<0.001), and “under leafy vegetation” (p<0.001).

  • View in gallery

    Displacement in relation with time of day for each microhabitat used by Dryophytes japonicus during brumation in Korea. All points from the same microhabitats share a centroid (rounds markers). The location of centroids represent the average time of day at which activity occur for a given microhabitat, and indicates an increase in activity in the early afternoon (below ground: n=8; below leafy vegetation: n=69; below tree bark: n=60; on ground: n=49: on leafy vegetation: n=85; on tree bark: n=29). Some aspects of the graphics might only be fully comprehensible in the PDF version where they are reproduced in colour.

  • View in gallery

    Linear Mixed-effects Regression Model with movement as dependent variable. Dryophytes japonicus was in movement at specific microhabitats and height only.

Index Card

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 88 88 10
Full Text Views 152 152 0
PDF Downloads 8 8 0
EPUB Downloads 0 0 0