Conservation Genetics

, Volume 12, Issue 3, pp 637–646 | Cite as

Genetic relationships of hellbenders in the Ozark highlands of Missouri and conservation implications for the Ozark subspecies (Cryptobranchus alleganiensis bishopi)

  • Rachel S. Crowhurst
  • Kaitlyn M. Faries
  • Jennifer Collantes
  • Jeffrey T. Briggler
  • Jeffrey B. Koppelman
  • Lori S. Eggert
Research Article


The hellbender (Cryptobranchus alleganiensis) is an obligately aquatic salamander that is in decline due to habitat loss and disease. Two subspecies of hellbender have been described based on morphological characteristics: C. a. alleganiensis (eastern subspecies) and C. a. bishopi (Ozark hellbender). Current conservation strategies include captive propagation for restorative releases even though information regarding the current levels of genetic variability and structure within populations is not sufficient to effectively plan for conservation of the genetic diversity of the species. To investigate patterns of population structure in the hellbender, we genotyped 276 hellbenders from eight Missouri River drainages, representing both subspecies. Our results showed low levels of within-drainage diversity but strong population structure among rivers, and three distinct genetic clusters. FST values ranged from 0.00 to 0.61 and averaged 0.40. Our results confirmed previous reports that C. a. bishopi and C. a. alleganiensis are genetically distinct, but also revealed an equidistant relationship between two groups within C. a. bishopi and all populations of C. a. alleganiensis. Current subspecies delineations do not accurately incorporate genetic structure, and for conservation purposes, these three groups should be considered evolutionarily significant units.


Amphibian Salamander Population genetics Microsatellites Cryptobranchus 


  1. Arntzen JW, Smithson A, Oldham RS (1999) Marking and tissue sampling effects on body condition and survival in the newt Triturus cristatus. J Herpetol 33:567–576CrossRefGoogle Scholar
  2. Bishop SC (1941) Salamanders of New York. New York State Museum Bulletin 324, 1–365Google Scholar
  3. Briggler JT, Ettling J, Wanner M, Schuette C, Duncan M, Goellner K (2007a) Cryptobranchus alleganiensis: Chytrid fungus. Herpetol Rev 38:174Google Scholar
  4. Briggler JT, Utrup J, Davidson C, Humphries J, Groves J, Johnson T, Ettling J, Wanner M, Traylor-Holzer K, Reed D, Lindgren V, Byers O (eds) (2007b) Hellbender population and viability assessment: final report. IUCN/SSC Conservation Breeding Specialist Group, Apple ValleyGoogle Scholar
  5. Briggler JT, Larson KA, Irwin KJ (2008) Presence of the amphibian chytrid fungus (Batrachochytrium dendrobatidis) on hellbenders (Cryptobranchus alleganiensis) in the Ozark Highlands. Herpetol Rev 39:443–444Google Scholar
  6. Crandall KA, Bininda-Edmonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295PubMedCrossRefGoogle Scholar
  7. Cunningham AA (1996) Disease risks of wildlife translocations. Conserv Biol 10:349–353CrossRefGoogle Scholar
  8. Dundee HA, Dundee DS (1965) Observations on the systematics and ecology of Cryptobranchus from the Ozark Plateaus of Missouri and Arkansas. Copeia 1965:369–370CrossRefGoogle Scholar
  9. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software Structure: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  10. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50PubMedGoogle Scholar
  11. Gates JE, Stouffer RH Jr, Stauffer JR Jr, Hocutt CH (1985) Dispersal patterns of translocated Cryptobranchus alleganiensis in a Maryland stream. J Herpetol 19:436–438CrossRefGoogle Scholar
  12. Hillis RE, Bellis ED (1971) Some aspects of the ecology of the hellbender, Cryptobranchus a. alleganiensis, in a pennysylvania stream. J Herpetol 5:121–126CrossRefGoogle Scholar
  13. Johnson JR, Faries KM, Rabenold JJ, Crowhurst RS, Briggler JT, Koppelman JB, Eggert LS (2009) Polymorphic microsatellite loci for studies of the Ozark hellbender Cryptobranchus alleganiensis). Conserv Genet 10:1795–1797CrossRefGoogle Scholar
  14. Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189CrossRefGoogle Scholar
  15. Kucuktas H, Wagner BK, Shopen R, Gibson M, Dunham R, Zhanjiang L (2001) Genetic analysis of Ozark analysis of Ozark hellbenders utilizing RAPD markers. In: Proc Annu Conf SEAFWA, pp 126–137Google Scholar
  16. Merkle DA, Guttman SI, Nickerson MA (1977) Genetic uniformity throughout the range of the hellbender, Cryptobranchus alleganiensis. Copeia 3:549–553CrossRefGoogle Scholar
  17. Moritz C (1994) Defining “Evolutionarily Significant Units” for conservation. Trends Ecol Evol 9:373–375PubMedCrossRefGoogle Scholar
  18. Mullen LB, Woods HA, Schwartz MK, Sepulveda AJ, Lowe WH (2010) Scale-dependent genetic structure of the Idaho giant salamander (Dicamptodon aterrinum) in stream networks. Mol Ecol 19:898–909PubMedCrossRefGoogle Scholar
  19. Murphy RW, Fu J, Upton DE, De Lema T, Zhao E (2000) Genetic variability among endangered Chinese giant salamanders, Andrias davidianus. Mol Ecol 9:1539–1547PubMedCrossRefGoogle Scholar
  20. Nickerson MA, Briggler JT (2007) Harvesting as a factor in population decline of a long-lived salamander; the Ozark hellbender, Cryptobranchus alleganiensis bishopi Grobman. Appl Herpetol 4:207–216CrossRefGoogle Scholar
  21. Nickerson MA, Mays CE (1973a) The hellbenders: North American “giant salamanders”. Milwaukee Public Museum Press, MilwaukeeGoogle Scholar
  22. Nickerson MA, Mays CE (1973b) A study of the Ozark hellbender, Cryptobranchus alleganiensis bishopi. Ecology 54:1163–1165CrossRefGoogle Scholar
  23. Peterson CL (1979) Age and growth of the Ozark hellbender. Master’s thesis, Southwest Missouri State University, SpringfieldGoogle Scholar
  24. Peterson CL, Metter DE, Miller BT (1988) Demography of the hellbender Cryptobranchus alleganiensis in the Ozarks. Am Midl Nat 119:291–303CrossRefGoogle Scholar
  25. Petranka JW (1998) Salamanders of United States and Canada. Smithsonian Institution Press, WashingtonGoogle Scholar
  26. Phillimore AB, Hadfield JD, Jones OR, Smithers RJ (2010) Differences in spawning date between populations of common frog reveal local adaptation. Proc Natl Acad Sci 107:8292–8297PubMedCrossRefGoogle Scholar
  27. Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Heredity 95:536–539CrossRefGoogle Scholar
  28. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  29. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9221PubMedCrossRefGoogle Scholar
  30. Raymond M, Rousset F (1995) GENEPOP (version 3.4): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  31. Rousset F (1996) Equilibrium values of measure of population subdivision for stepwise mutation processes. Genetics 142:1357–1362PubMedGoogle Scholar
  32. Routman E (1993) Mitochondrial DNA variation in Cryptobranchus alleganiensis, a salamander with extremely low allozyme diversity. Copeia 2:407–416CrossRefGoogle Scholar
  33. Routman E, Wu R, Templeton AR (1994) Parsimony, molecular evolution, and biogeography: the case of the North American giant salamander. Evolution 48:1799–1809CrossRefGoogle Scholar
  34. Sabatino SJ, Routman EJ (2009) Phylogeography and conservation genetics of the hellbender salamander (Cryptobranchus alleganiensis). Conserv Genet 10:1235–1246CrossRefGoogle Scholar
  35. Shaffer HG, Breden F (1989) The relationship between allozyme variation and life history: non-transforming salamanders are less variable. Copeia 1989:1016–1023CrossRefGoogle Scholar
  36. Smith BG (1907) The life history and habits of Cryptobranchus alleganiensis. Biol Bull 13:5–39CrossRefGoogle Scholar
  37. Taber CA, Wilkinson RD Jr, Topping MS (1975) Age and growth of hellbenders in the Niangua River, Missouri. Copeia 1975:633–639CrossRefGoogle Scholar
  38. Trauth SE, Wilhide JD, Daniel P (1992) Status of the Ozark hellbender, Cryptobranchus bishopi (Urodela: Cryptobranchidae), in the Spring River, Fulton County, Arkansas. Proc Arkansas Acad Sci 46:83–86Google Scholar
  39. Trenham PC, Marsh DM (2002) Amphibian translocation programs: reply to Seigel and Dodd. Conserv Biol 16:555–556CrossRefGoogle Scholar
  40. Unger SD, Fike JA, Sutton T, Rhodes OE Jr, Williams RN (2010) Isolation and development of 12 polymorphic tetranucleotide microsatellite markers for the eastern hellbender (Cryptobranchus alleganiensis alleganiensis). Conserv Genet Res Online Early. doi:10.1007/s12686-009-9170-0
  41. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  42. Wang X, Zhang K, Wang Z, Ding Y, Wu W, Huang S (2004) The decline of the Chinese giant salamander and implications for its conservation. Oryx 38:197–202CrossRefGoogle Scholar
  43. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  44. Wheeler BA, Prosen E, Mathis A, Wilkinson RF (2003) Population declines of a long-lived salamander: a 20+-year study of hellbenders, Cryptobranchus alleganiensis. Biol Conserv 109:151–156CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Rachel S. Crowhurst
    • 1
    • 2
  • Kaitlyn M. Faries
    • 3
  • Jennifer Collantes
    • 1
  • Jeffrey T. Briggler
    • 4
  • Jeffrey B. Koppelman
    • 1
  • Lori S. Eggert
    • 3
  1. 1.Missouri Department of ConservationResource Science CenterColumbiaUSA
  2. 2.Department of Fisheries and WildlifeOregon State UniversityCorvallisUSA
  3. 3.Division of Biological SciencesUniversity of MissouriColumbiaUSA
  4. 4. Missouri Department of ConservationJefferson CityUSA

Personalised recommendations