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Conservation Status of United States Species, pp. 47–54. University ofCalifornia Press, Berkeley.––––––, ––––––, AND L. BLACKBURN. 2005. Acris crepitans. In M. J. Lannoo(ed.), Amphibian Declines: The Conservation Status of United StatesSpecies, pp. 441–443. University of California Press, Berkeley.HAMMERSON, G. A., AND L. J. LIVO. 1999. Conservation status of the northerncricket frog (Acris crepitans) in Colorado and adjacent areas at thenorthwestern extent of the range. Herpetol. Rev. 30:78–80.HAY, R. 1998. Blanchard’s cricket frogs in Wisconsin: a status report. InM. J. Lannoo (ed.), Status and Conservation of Midwestern Amphibians,pp. 79–82. University of Iowa Press, Iowa City.IRWIN, J. T. 2005. Overwintering in northern cricket frogs (Acris crepitans).In M. J. Lannoo (ed.), Amphibian Declines: The Conservation Statusof United States Species, pp. 55–58. University of California Press,Berkeley.JUNG, R. E. 1993. Blanchard’s cricket frogs (Acris crepitans blanchardi)in southwest Wisconsin. Trans. Wisconsin Acad. Sci., Arts Lett. 81:79–87.LANNOO, M. J. 1998. Amphibian conservation and wetland managementin the upper Midwest: A catch-22 for the cricket frog? In M. J. Lannoo(ed.), Status and Conservation of Midwestern Amphibians, pp. 330–339. University of Iowa Press, Iowa City.––––––, AND R. G. GRUNDEL. 2004. United States Northern Cricket FrogSymposium. Froglog 66:1.––––––, K. LANG, T. WALTZ, AND G. S. PHILLIPS. 1994. An altered amphibianassemblage: Dickinson County, Iowa, 70 years after FrankBlanchard’s survey. Am. Midl. Nat. 131:311–319.LEHTINEN, R. M. 2002. A historical study of the distribution of Blanchard’scricket frog in southeastern Michigan. Herpetol. Rev. 33:194–197.––––––, AND A. A. SKINNER. 2006. The enigmatic decline of Blanchard’scricket frog (Acris crepitans blanchardi): A test of the habitat acidificationhypothesis. Copeia 2006:159–167.LIPS, K. R., F. BREM, R. BRENES, J. D. REEVE, R. A. ALFORD, J. VOYLES, C.CAREY, L. LIVO, A. P. PESSIER, AND J. P. COLLINS. 2006. Emerging infectiousdisease and the loss of biodiversity in a Neotropical amphibiancommunity. PNAS 103:3165–3170.LONGCORE, J. R., J. E. LONGCORE, A. P. PESSIER, AND W. A. HALTEMAN.2007. Chytridiomycosis widespread in anurans of northeastern UnitedStates. J. Wildl. Manage. 71:435–444.LONGCORE, J. E., A. P. PESSIER, AND D. K. NICHOLS. 1999. Batrachochytriumdendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians.Mycologia 91:219–227.MANIERO, G. D., AND C. CAREY. 1997. Changes in selected aspects of immunefunction in the leopard frog, Rana pipiens, associated with exposureto cold. J. Comp. Phys. B. 167:256–263.MIERZWA, K. S. 1998. Status of northeastern Illinois amphibians. In M. J.Lannoo (ed.), Status and Conservation of Midwestern Amphibians, pp.115–124. University of Iowa Press, Iowa City.MOSSMAN, M. J., L. M. HARTMAN, R. HAY, J. R. SAUER, AND B. J. BHUEY.1998. Monitoring long-term trends in Wisconsin frog and toad populations.In M. J. Lannoo (ed.), Status and Conservation of MidwesternAmphibians, pp. 169–198. University of Iowa Press, Iowa City.OUELLET, M., I. MIKAELIAN, B. D. PAULI, J. RODRIGUE, AND D. M. GREEN.2005. Historical evidence of widespread chytrid infection in NorthAmerican amphibian populations. Conserv. Biol. 19:1431–1440.PEARL, C. A., E. L. BULL, D. E. GREEN, J. BOWERMAN, M. J. ADAMS, A.HYATT, AND W. H. WENTE. 2007. Occurrence of the amphibian pathogenBatrachochytrium dendrobatidis in the Pacific Northwest. J. Herpetol.41:145–149.REEDER, A. L., M. O. RUIZ, A. PESSIER, L. E. BROWN, J. M. LEVENGOOD, C.A. PHILLIPS, M. B. WHEELER, R. E. WARNER, AND V. R. BEASLEY. 2005.Intersexuality and the cricket frog decline: Historic and geographictrends. Environ. Health Perspect. 113:261–265.RETALLICK, R. W. R., H. MCCALLUM, AND R. SPEARE. 2004. Endemic infectionof the amphibian chytrid fungus in a frog community post-decline.PLoS Biol. 2:e351.RUSSELL, R. W., G. J. LIPPS, S. J. HECNAR, AND G. D. HAFFNER. 2002. Persistentorganic pollutants in Blanchard’s cricket frogs from Ohio. OhioJ. Sci. 102:119–122.WOODHAMS, D., R. A. ALFORD, AND G. MARANTELLI. 2003. Emerging diseaseof amphibians cured by elevated body temperature. Diseases Aquat.Org. 55:65–67.––––––, AND ––––––. 2005. Ecology of chytridiomycosis in rainforeststream frog assemblages of tropical Queensland. Conserv. Biol.19:1449–1459.––––––, L. ROLLINS-SMITH, C. CAREY, L. REINART, M. TYLER, AND R. ALFORD.2006. Population trends associated with skin peptide defenses againstchytridiomycosis in Australian frogs. Oecologia 146:531–540.ZIPPEL, K. C., AND C. TABAKA. 2008. Amphibian chytridiomycosis in captiveAcris crepitans blanchardi (Blanchard's cricket frog) collected fromOhio, Missouri, and Michigan, USA. Herpetol. Rev. 39:192–193.Herpetological Review, 2008, 39(2), 196–199.© 2008 by Society for the Study of Amphibians and ReptilesLow Prevalence of Batrachochytrium dendrobatidisAcross Rana sylvatica Populations in SoutheasternMichigan, USAAMANDA J. ZELLMER *CORINNE L. RICHARDSandLISA M. MARTENSUniversity of Michigan, Department of Ecology and Evolutionary Biologyand Museum of Zoology, 1109 Geddes AvenueAnn Arbor, Michigan 48109-1079, USA*Corresponding author; e-mail: azellmer@umich.eduThe emerging infectious disease chytridiomycosis has beenimplicated in the decline and extinction of numerous amphibianspecies worldwide (Berger et al. 1998; Lips et al. 2006; Skerratt etal. 2007). The fungus causing this disease, Batrachochytriumdendrobatidis (Bd), has been present in North American amphibianpopulations since at least the 1960s (Ouellet et al. 2005); however,in many areas of North America, there is little evidence ofnegative effects of the disease on amphibian population persistence.Understanding how environmental factors affect infectionprevalence is thus important for determining under what conditionschytridiomycosis is likely to have a devastating impact onpopulations.We conducted a preliminary assessment of the role of seasonand habitat quality on chytridiomycosis infection prevalence inpopulations of the Wood Frog, Rana sylvatica, in southeasternMichigan, USA. In laboratory studies, Bd appears to be limited bytemperatures outside the range of 4–25°C (Piotrowski et al. 2004).Several studies also have noted that the prevalence and severity ofinfections in wild populations tend to vary seasonally (Berger etal. 2004; Kriger and Hero 2006, 2007; Retallick et al. 2004;Woodhams and Alford 2005). Given this, we predicted that levelsof infection would be higher in the spring as opposed to the summerbecause the warmer temperatures experienced during the summermonths in southeastern Michigan should limit Bd infectionrates (Berger et al. 2004; Kriger and Hero 2006, 2007; Ouellet etal. 2005; Retallick et al. 2004; Woodhams and Alford 2005;Woodhams et al. 2003). Additionally, habitat quality may affect196 Herpetological Review 39(2), 2008
infection rates because the higher stress levels associated with lowquality habitats may make individuals more susceptible to infection(Carey and Bryant 1995). Ponds that are exposed to high levelsof agricultural and urban runoff may be particularly stressfulfor amphibians. For example, both pesticides (Relyea 2005) androad de-icing salt (Sanzo and Hecnar 2006) affect larval WoodFrog survivorship. Thus, we predicted that Wood Frog (Ranasylvatica) populations in ponds surrounded by agricultural or urbanareas would show higher levels of infection than populationssurrounded by intact, forested habitat.Methods.—To assess whether season affects infection prevalence,breeding adults and metamorphs were tested for the presenceof Bd DNA, since breeding adults often experience coldertemperatures than metamorphs. Adults were sampled from eightpopulations in March 2007 and metamorphs were sampled fromfive populations in June 2007. All adults and metamorphs weresampled from populations on the University of Michigan’s EdwinS. George Reserve (Fig. 1). Temperatures during the 30 days priorto sampling ranged from -16–23°C (mean temperature = 2°C) forthe adults and 5–33°C (mean temperature = 20°C) for themetamorphs. The dorsum, venter, and feet of adults andmetamorphs were swabbed with a sterile cotton swab. Swabs werestored in 95% ethanol until extraction.In addition, to assess the relationship between habitat qualityand Bd distribution, we collected larvae of R. sylvatica from 16populations across southeastern Michigan (Fig. 1) during June 2005and 2006. Aerial images (Michigan Department of Natural Resources1998) were used to select ponds with varying degrees ofsurrounding forest and wetland fragmentation. Larvae were storedin 95% ethanol until extraction. The oral discs of six individualsfrom each population were excised in the lab using sterilized razorblades and forceps.Extraction of Bd DNA was completed following the methodologyof Hyatt et al. (2007). DNA from larval samples was extractedfrom the oral discs, whereas DNA from the metamorphs and adultswas extracted from the swabs. DNA extracted from larvae waspooled in groups of three for each population. The pooled-larvalsamples and both the adult and metamorph samples were thendiluted 1:10 with double deionized water. Taqman diagnostic quantitativePCR (Boyle et al. 2004) was used to detect the presence ofBd DNA. Quantitative Taqman PCR assays were performed intriplicate using an Applied Biosystems Prism 7700 Sequence DetectionSystem following the protocol of Boyle et al. (2004). VIC TMExogenous Internal Positive Control reagents were used for thedetection of PCR inhibitors (Applied Biosystems following Hyattet al. 2007). Inhibitors did not appear to be present in any of thesamples. A sample was only considered positive for Bd if all threereplicates indicated the presence of the fungus. Samples testingpositive in one or two replicates were re-assayed once. If the secondassay produced a consistent negative or positive result for allthree replicates the sample was considered negative or positive,respectively. Samples testing positive in one or two replicates ofthe second assay were considered “suspicious.” Prevalence rateswere calculated by dividing the number of infected individuals bythe total number of sampled individuals, and 95% confidence intervalswere calculated based on a binomial distribution (StataIntercooled v. 10.0).The percentage of combined agricultural and urban land coverFIG. 1. Wood Frog (Rana sylvatica) sampling locations in southeasternMichigan, USA, showing areas sampled for Batrachochytriumdendrobatidis in adults (open circles), metamorphs (triangles), and larvae(squares). Agricultural and urban areas are white. Forests, wetlands,rivers, and lakes are gray.within 1 km (estimated genetic neighborhood size of R. sylvatica:Berven and Grudzien 1990) of each of the 16 ponds sampled forlarvae was calculated in ArcGIS v. 9.2 using the 2001 NationalLand-Cover Database (Homer et al. 2004). This percentage rangedfrom 6.18 to 78.55 (Table 1).Results.—Two of 239 (prevalence = 0.83%; 95% confidenceinterval = 0.1–3.0%) samples tested positive for the presence ofBd. One of 70 (1.4%) adults, zero of 73 metamorphs, and 1–3 of96 (1.0–3.1%) larvae tested positive in each of three replicates.The range surrounding the number of infected larvae arises frompooling the larvae into groups of three for the analyses. As a result,a positive sample indicates that at least one of the three individualswas positive for Bd. In addition, one of 70 (1.4%) adultstested positive in two out of three replicates and thus was classifiedas suspicious.Discussion.—We found a very low level of Bd infection in populationsof R. sylvatica in southeastern Michigan (0.83%). Otherstudies of North American R. sylvatica populations have foundmuch higher rates of infection (15.5%, Longcore et al. 2007; 6.6%,Ouellet et al. 2005). We calculated 95% confidence intervals foreach of these studies to assess the extent to which our results differedfrom these previous studies and found that our confidenceintervals did not overlap (Longcore et al. 2007: 6.4–29.4%; Ouelletet al. 2005: 3.4–11.1%). Our results are consistent with the ideathat the quality of the habitat and the season may be importantpredictors of infection rates. For the effects of season, we foundone adult that tested positive for Bd, while no metamorphs testedpositive. Temperatures during the adult breeding period remainedat or below the optimal temperature range for Bd, whereas duringthe metamorph sampling period, temperatures exceeded the maximumtemperature at which Bd can survive in the laboratory(Piotrowski et al. 2004). Similarly, we detected Bd in larvae in apond exposed to one of the largest areas of anthropogenic distur-Herpetological Review 39(2), 2008 197
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HerpetologicalReviewVolume 39, Numb
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About Our Cover: Zonosaurus maramai
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Prey-specific Predatory Behavior in
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TABLE 1. Time-line history of croco
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The Reptile House at the Bronx Zoo
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Page 32 and 33: TABLE 2. Summary of running (includ
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Page 36 and 37: PIANKA, E. R., AND W. S. PARKER. 19
Page 38 and 39: BUSTAMANTE, M. R. 2005. La cecilia
Page 40 and 41: Fig. 3. Mean clutch size (number of
Page 42 and 43: facilitated work in Thailand. I tha
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Page 46 and 47: FIG. 2A) Side view photo of Aechmea
Page 48 and 49: 364.DUELLMAN, W. E. 1978. The biolo
Page 50 and 51: incision, and placed one drop of Ba
Page 52 and 53: 13 cm deep (e.g., Spea hammondii; M
Page 54 and 55: FIG. 1. Medicine dropper (60 ml) wi
Page 56 and 57: esearchers and Hellbenders, especia
Page 58 and 59: FIG. 3. Relative success of traps p
Page 60 and 61: data on Hellbender population struc
Page 62 and 63: aits sometimes resulted in differen
Page 64 and 65: trapping system seems to be a relat
Page 66 and 67: AMPHIBIAN CHYTRIDIOMYCOSISGEOGRAPHI
Page 68 and 69: TABLE 1. Prevalence of B. dendrobat
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Page 74 and 75: TABLE 1. Anurans that tested positi
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Page 78 and 79: (10%) were dead but not obviously m
Page 80 and 81: Submitted by CHRIS T. McALLISTER, D
Page 82 and 83: FIG. 1. Oscillogram, spectrogram, a
Page 84 and 85: FIG. 1. Adult Physalaemus cuvieri r
Page 86 and 87: Répteis, Instituto Nacional de Pes
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Page 90 and 91: GRAPTEMYS GIBBONSI (Pascagoula Map
Page 92 and 93: College, and the Joseph Moore Museu
Page 94 and 95: FIG. 1. Common Ground Lizard (Ameiv
Page 96 and 97: havior unavailable elsewhere. Here
Page 98 and 99: 15% of predator mass, is typical fo
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Page 102 and 103: We thank Arlington James and the st
Page 104 and 105: mm) S. viridicornis in its mouth in
Page 106 and 107: NECTURUS MACULOSUS (Common Mudpuppy
Page 108 and 109: LITHOBATES CATESBEIANUS (American B
Page 110 and 111: Research and Collections Center, 13
Page 112 and 113: BRONCHOCELA VIETNAMENSIS (Vietnam L
Page 114 and 115: Oficina Regional Guaymas, Guaymas,
Page 116 and 117: MICRURUS TENER (Texas Coralsnake).
Page 118 and 119: declining in this recently discover
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this effort, 7% of the 10 × 10 km
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the knowledge of the group. The aut
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which is listed under “Rhodin, A.
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noting that Sphenomorphus bignelli
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256 Herpetological Review 39(2), 20
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ISSN 0018-084XThe Official News-Jou
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