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Characterization of Dermotheca sp. Infection in a midwestern state-endangered salamander (Ambystoma platineum) and a co-occurring common species (Ambystoma texanum)

Published online by Cambridge University Press:  08 January 2020

Laura Adamovicz Open the ORCID record for Laura Adamovicz [Opens in a new window] ,
Daniel B. Woodburn ,
Stephany Virrueta Herrera ,
Kelsey Low ,
Christopher A. Phillips ,
Andrew R. Kuhns ,
John A. Crawford  and
Matthew C. Allender
Laura Adamovicz*
Affiliation:
Wildlife Epidemiology Lab, University of Illinois, 2001 S Lincoln Ave, Urbana, IL61802, USA
Daniel B. Woodburn
Affiliation:
Zoological Pathology Program, College of Veterinary Medicine, University of Illinois, 3300 Golf Road, Brookfield, Illinois, USA
Stephany Virrueta Herrera
Affiliation:
Program in Ecology, Evolution, and Conservation Biology, University of Illinois, 505 South Goodwin Ave, Urbana, IL61801, USA Illinois Natural History Survey, Prairie Research Institute, 615 E Peabody Dr, Champaign, IL61820, USA
Kelsey Low
Affiliation:
Program in Ecology, Evolution, and Conservation Biology, University of Illinois, 505 South Goodwin Ave, Urbana, IL61801, USA Illinois Natural History Survey, Prairie Research Institute, 615 E Peabody Dr, Champaign, IL61820, USA
Christopher A. Phillips
Affiliation:
Illinois Natural History Survey, Prairie Research Institute, 615 E Peabody Dr, Champaign, IL61820, USA
Andrew R. Kuhns
Affiliation:
Illinois Natural History Survey, Prairie Research Institute, 615 E Peabody Dr, Champaign, IL61820, USA
John A. Crawford
Affiliation:
National Great Rivers Research and Education Center, One Confluence Way, East Alton, IL62024, USA
Matthew C. Allender
Affiliation:
Wildlife Epidemiology Lab, University of Illinois, 2001 S Lincoln Ave, Urbana, IL61802, USA
*
Author for correspondence: Laura Adamovicz, E-mail: adamovi2@illinois.edu
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Abstract

Ichthyosporean parasites (order Dermocystida) can cause morbidity and mortality in amphibians, but their ecology and epidemiology remain understudied. We investigated the prevalence, gross and histologic appearance, and molecular phylogeny of a novel dermocystid in the state-endangered silvery salamander (Ambystoma platineum) and the co-occurring, non-threatened small-mouthed salamander (Ambystoma texanum) from Illinois. Silvery salamanders (N = 610) were sampled at six ephemeral wetlands from 2016 to 2018. Beginning in 2017, 1–3 mm raised, white skin nodules were identified in 24 silvery salamanders and two small-mouthed salamanders from five wetlands (prevalence = 0–11.1%). Skin biopsy histology (N = 4) was consistent with dermocystid sporangia, and necropsies (N = 3) identified infrequent hepatic sporangia. Parasitic 18S rRNA sequences (N = 5) from both salamander species were identical, and phylogenetic analysis revealed a close relationship to Dermotheca viridescens. Dermocystids were not identified in museum specimens from the same wetlands (N = 125) dating back to 1973. This is the first report of Dermotheca sp. affecting caudates in the Midwestern United States. Future research is needed to determine the effects of this pathogen on individual and population health, and to assess whether this organism poses a threat to the conservation of ambystomatid salamanders.

Keywords

Ambystoma jeffersonianum complexamphibianemerging infectious diseaseIchthyosporeaMesomycetozoea.
Type
Research Article
Information
Parasitology , Volume 147 , Issue 3 , March 2020 , pp. 360 - 370
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Copyright
Copyright © Cambridge University Press 2019

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References

Andreou, D, Arkush, KD, Guégan, J-F and Gozlan, RE (2012) Introduced pathogens and native freshwater biodiversity: a case study of Sphaerotheceum destruens. PLoS ONE 7, e36998.CrossRefGoogle ScholarPubMed
Benson, DA, Karsch-Mizrachi, I, Lipman, DJ, Ostell, J and Wheeler, DL (2008) Genbank. Nucleic Acids Research 36, D25–D30.CrossRefGoogle ScholarPubMed
Berger, L, Speare, R, Hines, HB, Marantelli, G, Hyatt, AD, McDonald, KR, Skerratt, LF, Olsen, V, Clarke, JM, Gillespie, G, Mahony, M, Sheppard, N, Williams, C and Tyler, MJ (2004) Effect of season and temperature on mortality in amphibians due to chytridiomycosis. Australian Veterinary Journal 82, 434–439.CrossRefGoogle ScholarPubMed
Blaustein, AR, Gervasi, SS, Johnson, PTJ, Hoverman, JT, Belden, LK, Bradley, PW and Xie, GY (2012) Ecophysiology meets conservation: understanding the role of disease in amphibian population declines. Philosophical Transactions of the Royal Society B: Biological Sciences 367, 1688–1707.CrossRefGoogle ScholarPubMed
Borteiro, C, Cruz, JC, Kolenc, F, Verdes, JM, Moraña, A, Martínez Debat, C, Kun, A, Ubilla, M and Okada, K (2014) Dermocystid-chytrid coinfection in the Neotropical frog Hypsiboas pulchellus (Anura: Hylidae). Journal of Wildlife Diseases 50, 150–153.CrossRefGoogle Scholar
Borteiro, C, Baldo, D, Maronna, MM, BaÊta, D, Sabbag, AF, Kolenc, F, Debat, CM, Haddad, CFB, Cruz, JC, Verdes, JM and Ubilla, M (2018a) Amphibian parasites of the order Dermocystida (Ichthyosporea): current knowledge, taxonomic review and new records from Brazil. Zootaxa 4461, 499–518.CrossRefGoogle Scholar
Borteiro, C, Gobel, N, Kolenc, F, Laufer, G, Martínez Debat, C and Ubilla, M (2018b) Skin-mates or neighbors? A seasonal study of amphibian chytrid and dermocystid infection in Boana pulchella (Anura: Hylidae). Cuadernos de Herpetología 32, 101–108.CrossRefGoogle Scholar
Broz, O and Kulda, J (1954) Dermosporidium Multigranulare n.sp parasite z kuze Rana esculenta. Acta Societatis Zoologicae Bohemicae 18, 91–97.Google Scholar
Broz, O and Privora, M (1952) Two skin parasites of Rana Temporaria: Dermocystidium ranae Guyénot et Naville and Dermosporidium granulosum n. sp. Parasitology 42, 65–69.CrossRefGoogle Scholar
Campbell, CR, Voyles, J, Cook, DI and Dinudom, A (2012) Frog skin epithelium: electrolyte transport and chytridiomycosis. International Journal of Biochemistry and Cell Biology 44, 431–434.CrossRefGoogle ScholarPubMed
Carini, A (1940) Sobre um parasito semelhante a um “Rhinosporidium”, encontrado em quistos da pele de uma “Hyla”. Arquivos do Instituto Biológico (São Paulo) 11, 93–98.Google Scholar
Cavalier-Smith, T (1998) Neomonada and the origin of animals and fungi. In Coombs, GH, Vickerman, K, Sleigh, MA and Warren, A (eds), Evolutionary Relationships Among Protozoa. Norwell, Massachusetts, USA: Kluwer Academic Publishers, pp. 375–407.Google Scholar
Converse, KA and Green, DE (2005) Diseases of frogs and toads. In Majumdar, SK, Huffman, JE, Brenner, FJ and Panah, AI (eds), Wildlife Diseases: Landscape Epidemiology, Spatial Distribution and Utilization of Remote Sensing Technology. Easton, PA: The Pennsylvania Academy of Science, pp. 89–117.Google Scholar
Courtois, EA, Cornuau, JH, Loyau, A and Schmeller, DS (2013) Distribution of Amphibiocystidium sp. in palmate newts (Lissotriton helveticus) in Ariege, France. Herpetology Notes 6, 539–543.Google Scholar
Daszak, P, Cunningham, AA and Hyatt, AD (2003) Infectious disease and amphibian population declines. Diversity and Distributions 9, 141–150.CrossRefGoogle Scholar
Diego-Rasilla, FJ (2017) Parasitic dermic cyst in Mesotriton alpestris (caudata: salamandridae). Boletín de la Asociación Herpetológica Española 28, 56–57.Google Scholar
Di Rosa, I, Simoncelli, F, Fagotti, A and Pascolini, R (2007) Ecology: the proximate cause of frog declines? Nature 447, E4–E5.CrossRefGoogle ScholarPubMed
Duffus, ALJ and Cunningham, AA (2010) Major disease threats to European amphibians. Herpetological Journal 20, 117–127.Google Scholar
Fagotti, A, Morosi, L, Di Rosa, I, Clarioni, R, Simoncelli, F, Pascolini, R, Pellegrino, R, Guex, GD and Hotz, H (2005) Bioaccumulation of organochlorine pesticides in frogs of the Rana esculenta complex in central Italy. Amphibia-Reptilia 26, 93–104.Google Scholar
Fagotti, A, Rossi, R, Canestrelli, D, La Porta, G, Paracucchi, R, Lucentini, L, Simoncelli, F and Di Rosa, I (2019) Longitudinal study of Amphibiocystidium sp. Infection in a natural population of the Italian stream frog (Rana italica). Parasitology 28, 1–8.Google Scholar
Farrer, RA, Weinert, LA, Bielby, J, Garner, TW, Balloux, F, Clare, F, Bosch, J, Cunningham, AA, Weldon, C, du Preez, LH, Anderson, L, Pond, SL, Shahar-Golan, R, Henk, DA and Fisher, MC (2011) Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proceedings of the National Academy of Sciences USA 108, 18732–18736.CrossRefGoogle ScholarPubMed
Federici, E, Rossi, R, Fidati, L, Paracucchi, R, Scargetta, S, Montalbani, E, Franzetti, A, La Porta, G, Fagotti, A, Simonceli, F, Cenci, G and Di Rosa, I (2015) Characterization of the skin microbiota in Italian stream frogs (Rana italica) infected and uninfected by a cutaneous parasitic disease. Microbes and Environments 30, 262–269.CrossRefGoogle ScholarPubMed
Feldman, SH, Wimsatt, JH and Green, DE (2005) Phylogenetic classification of the frog pathogen Amphibiothecum (Dermosporidium) penneri based on small ribosomal subunit sequencing. Journal of Wildlife Disease 41, 701–706.CrossRefGoogle ScholarPubMed
Fiegna, C, Clarke, CL, Shaw, DJ, Baily, JL, Clare, FC, Gray, A, Garner, TW and Meredith, AL (2017) Pathological and phylogenetic characterization of Amphibiothecum sp. Infection in an isolated amphibian (Lissotriton helveticus) population on the island of Rum (Scotland). Parasitology 144, 484–496.CrossRefGoogle Scholar
Fisher, MC, Henk, DA, Briggs, CJ, Brownstein, JS, Madoff, LC, McCraw, SL and Gurr, SJ (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194.CrossRefGoogle ScholarPubMed
Galán, P and Dopereiro, D (2017) Infección por dermocistidios (Dermocystida) en una población de Lissotriton helveticus de A Limia (Ourense, Galicia). Boletín de la Asociación Herpetológica Española 28, 74–77.Google Scholar
Gambier, H (1924) Sur un Protiste parasite et pathogene des Tritons: Hepatosphera molgarum n. g., n. sp. Comptes rendus des séances de la Société de biologie et de ses filiales 90, 439–441.Google Scholar
González-Hernández, M, Denoël, M, Duffus, AJL, Garner, TWJ, Cunningham, AA and Acevedo-Whitehouse, K (2010) Dermocystid infection and associated skin lesions in free-living palmate newts (Lissotriton helveticus) from southern France. Parasitology International 59, 44–350.CrossRefGoogle ScholarPubMed
Gozlan, RE, St-Hilaire, S, Feist, SW, Martin, P and Kent, ML (2005) Biodiversity: disease threat to European fish. Nature 435, 1046.CrossRefGoogle ScholarPubMed
Granata, L (1919) Dermomycoides beccarii n. g. n. sp. nuovo enigmatico parassita di Molge vulgaris. Monitore zoologico italiano 20, 153–160.Google Scholar
Green, DE and Sherman, CK (2001) Diagnostic histological findings in yosemite toads (Bufo Canorus) from a die-off in the 1970s. Journal of Herpetology 35, 92–103.CrossRefGoogle Scholar
Green, DE, Converse, KA and Schrader, AK (2002) Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996–2001. Annals of the New York Academy of Sciences 969, 323–339.CrossRefGoogle Scholar
Guyénot, E and Naville, A (1922) Un nouveau protiste du genre Dermocystidium parasite de la Grenouille Dermocystidium ranae nov. spec. Revue Suisse de Zoologie 29, 133–145.Google Scholar
Hershberger, PK, van der Leeuw, BK, Gregg, JL, Grady, CA, Lujan, KM, Gutenberger, SK, Purcell, MK, Woodson, JC, Winton, JR and Parsley, MJ (2010) Amplification and transport of an endemic fish disease by an introduced species. Biological Invasions 12, 3665–3675.CrossRefGoogle Scholar
Illinois Endangered Species Protection Board (2015) Checklist of Endangered and Threatened Animals and Plants of Illinois. Retrieved from the Illinois Department of Natural Resources website: https://www.dnr.illinois.gov/ESPB/Documents/2015_ChecklistFINAL_for_webpage_051915.pdf (Accessed 15 September 2018).Google Scholar
Jancovich, JK, Davidson, EW, Parameswaran, N, Mao, J, Chinchar, VG, Collins, JP, Jacobs, BL and Storfer, A (2005) Evidence for emergence of an amphibian iridoviral disease because of human-enhanced spread. Molecular Ecology 14, 213–224.CrossRefGoogle ScholarPubMed
Jay, JM and Pohley, WJ (1981) Dermosporidium penneri sp n from the skin of the American toad, Bufo americanus (Amphibia, Bufonidae). Journal of Parasitology 67, 108–110.CrossRefGoogle Scholar
Katoh, K and Standley, DM (2013) MAFFT Multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.CrossRefGoogle ScholarPubMed
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Mentjies, P and Drummond, A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics (Oxford, England) 28, 1647–1649.CrossRefGoogle ScholarPubMed
Kiesecker, JM, Blaustein, AR and Belden, LK (2001) Complex causes of amphibian population declines. Nature 410, 681–684.CrossRefGoogle ScholarPubMed
Kosmidis, I (2017) brglm: Bias reduction in binary-response generalized linear models. R package version 0.6.1, http://www.ucl.ac.uk/~ucakiko/software.html.Google Scholar
Kriger, KM and Hero, J-M (2007) Large-scale seasonal variation in the prevalence and severity of chytridiomycosis. Journal of Zoology 271, 352–359.Google Scholar
Lanfear, R, Senfeld, T, Frandsen, P, Wright, A and Calcott, B (2017) Partitionfinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.Google ScholarPubMed
Lenth, R (2016) Least-squares means: the R package lsmeans. Journal of Statistical Software 69, 1–33.CrossRefGoogle Scholar
MacDiarmid, SC (1988) Future options for brucellosis surveillance in New Zealand beef herds. New Zealand Veterinary Journal 36, 39–42.CrossRefGoogle ScholarPubMed
McAllister, CT, Bursey, CR, Crawford, JA, Kuhns, AR, Shaffer, C and Trauth, SE (2010) Metacercariae of Clinostomum (Trematoda: Digenea) from three species of Ambystoma (Caudata: Ambystomatidae) from Arkansas and Illinois, U.S.A. Comparative Parasitology 77, 25–30.Google Scholar
McCallum, H and Dobson, A (1995) Detecting disease and parasite threats to endangered species and ecosystems. Trends in Ecology and Evolution 10, 190–194.CrossRefGoogle ScholarPubMed
Mendoza, L, Taylor, JW and Ajello, L (2002) The class Mesomycetozoea: a heterogeneous group of microorganisms at the animal-fungal boundary. Annual Reviews of Microbiology 56, 315–344.CrossRefGoogle ScholarPubMed
Minton, SA Jr. (2001) Amphibians and Reptiles of Indiana. Indianapolis, IN: Indiana Academy of Science.Google Scholar
Moral, H (1913) Über das Auftreten von Dermocystidium Pusula (Pérez), einem einzelligen parasiten der haut des molches bei Triton cristatus. Archiv für mikroskopische Anatomie 81, 381–393.CrossRefGoogle Scholar
Morris, MA and Brandon, RA (1984) Gynogenesis and hybridization between Ambystoma Platineum and Ambystoma texanum in Illinois. Copeia 1984, 324–337.CrossRefGoogle Scholar
Pascolini, R, Daszak, P, Cunningham, AA, Tei, S, Vagnetti, D, Bucci, S, Fagotti, A and Di Rosa, I (2003) Parasitism by Dermocystidium Ranae in a population of Rana esculenta complex in Central Italy and description of Amphibiocystidium n. gen. Diseases of Aquatic Organisms 56, 65–74.CrossRefGoogle Scholar
Pereira, CN, Di Rosa, I, Fagotti, A, Simoncelli, F, Pascolini, R and Mendoza, L (2005) The pathogen of frogs Amphibiocystidium Ranae is a member of the order Dermocystida in the class Mesomycetozoea. Journal of Clinical Microbiology 43, 192–198.CrossRefGoogle ScholarPubMed
Pérez, C (1907) Dermocystidium Pusula, organismenouveu parasite de lapeaudestritons. Comptesrendus de Seances de Societe de Biologie 63, 445–446.Google Scholar
Pérez, C (1913) Dermocystidium Pusula: parasite de la peau des tritons. Archives de Zoologie Experimentale et Generale 52, 343–357.Google Scholar
Pessier, AP (2008) Management of disease as a threat to amphibian conservation. International Zoo Yearbook 42, 30–39.CrossRefGoogle Scholar
Phillips, CA, Uzzell, T, Spolsky, CM, Serb, JM, Szafoni, RE and Pollowy, TR (1997) Persistent high levels of tetraploidy in salamanders of the Ambystoma Jeffersonianum complex. Journal of Herpetology 31, 530–535.CrossRefGoogle Scholar
Phillips, CA, Johnson, JR, Dreslik, MJ and Petzing, JE (2002) Effects of hydroperiod on recruitment of mole salamanders (genus Ambystoma) at a temporary pond in Vermilion County, Illinois. Transactions of the Illinois State Academy of Science 95, 131–139.Google Scholar
Picco, AM and Collins, JP (2008) Amphibian commerce as a likely source of pathogen pollution. Conservation Biology 22, 1582–1589.CrossRefGoogle ScholarPubMed
Picco, AM, Brunner, JL and Collins, JP (2007) Susceptibility of the endangered California tiger salamander, Ambystoma californiense, to ranavirus infection. Journal of Wildlife Diseases 43, 286–290.CrossRefGoogle ScholarPubMed
Poisson, C (1937) Sur une nouvelle espèce du genre Dermomycoides Granata 1919: Dermomycoides armoriacus Poisson 1936 parasite cutane de Triturus palmatus (Schneider). Genèse et structure de la zoospore. Bulletin Biologique de la France et de la Belgique 71, 91–116.Google Scholar
Price, SJ, Garner, TWJ, Nichols, RA, Balloux, F, Ayres, C, de Alba, AMC and Bosch, J (2014) Collapse of amphibian communities due to an introduced ranavirus. Current Biology 24, 2586–2591.CrossRefGoogle Scholar
Raffel, TR, Bommarito, T, Barry, DS, Witiak, SM and Shackelton, LA (2008) Widespread infection of the eastern redspotted newt (Notophthalmus viridescens) by a new species of Amphibiocystidium, a genus of fungus-like Mesomycetozoan parasites not previously reported in North America. Parasitology 135, 203–215.CrossRefGoogle Scholar
Rambaut, A and Drummond, AJ (2007) Tracer, Vol. 1.6. Available at: http://tree.bio.ed.ac.uk/software/tracer/.Google Scholar
R Core Team (2018) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. URL https://www.R-project.org/.Google Scholar
Remy, P (1931) Presence de Dermocystidium Ranae (Guyénot et Naville) chez une Rana esculenta L. de Lorraine. Annals of Parasitology 9, 1–3.Google Scholar
Rollins-Smith, LA (2009) The role of amphibian antimicrobial peptides in protection of amphibians from pathogens linked to global amphibian declines. Biochimica et Biophysica Acta–Biomembranes 1788, 1593–1599.CrossRefGoogle ScholarPubMed
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 3, 539–542.CrossRefGoogle Scholar
Rowley, J and Alford, RA (2007) Behaviour of Australian rainforest stream frogs may affect the transmission of chytridiomycosis. Diseases of Aquatic Organisms 77, 1–9.CrossRefGoogle ScholarPubMed
Rowley, JJL, Gleason, FH, Andreou, D, Marshall, W, Lilje, O and Goslan, R (2013) Impacts of Mesomycetozoean parasites on amphibian and freshwater fish populations. Fungal Biology Reviews 27, 100–111.CrossRefGoogle Scholar
Scheid, P, Balczun, C, Dehling, JM, Ammon, A and Sinsch, U (2015) Rhinosporidiosis in African reed frogs Hyperolius Spp. Caused by a new species of Rhinosporidium. Diseases of Aquatic Organisms 115, 111–120.CrossRefGoogle ScholarPubMed
Schloegel, LM, Toledo, LF, Longcore, JE, Greenspan, SE, Vieira, CA, Lee, M, Zhao, S, Wangen, C, Ferreira, CM, Hipolito, M, Davies, AJ, Cuomo, CA, Daszak, P and James, TY (2012) Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade Molecular Ecology 21, 5162–5177.CrossRefGoogle ScholarPubMed
Simoncelli, F, Fagotti, A, Dall'Olio, R, Vagnetti, D, Pascolini, R and Di Rosa, I (2005) Evidence of Batrachochytrium Dendrobatidis infection in water frogs of the Rana esculenta complex in central Italy. EcoHealth 2, 307–312.CrossRefGoogle Scholar
Skerratt, LF, Berger, L, Speare, R, Cashins, S, Mcdonald, KR, Phillott, A, Hines, H and Kenyon, N (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4, 125–134.CrossRefGoogle Scholar
Spolsky, C, Phillips, CA and Uzzell, T (1992) Gynogenetic reproduction in hybrid mole salamanders (Genus Ambystoma. Evolution 46, 1935–1944.Google ScholarPubMed
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics (Oxford, England) 30, 1312–1313.CrossRefGoogle ScholarPubMed
Stark, T and Guex, G-D (2014) Infecties bij amfi bieën in Nederland: Amphibiocystidium. Ravon 54, 54–56.Google Scholar
Sugiura, N (1978) Further analysis of the data by Akaike's information criterion and the finite corrections. Communications in Statistics 7, 13–26.CrossRefGoogle Scholar
Teltser, C and Greenwald, KR (2015) Survivorship of ploidy-variable unisexual Ambystoma Salamanders across developmental stages. Herpetologica 71, 81–87.CrossRefGoogle Scholar
Uzzell, TM Jr (1964) Relations of the diploid and triploid species of the Ambystoma Jeffersonianum complex (Amphibia, Caudata). Copeia 2, 257–300.CrossRefGoogle Scholar
Uzzell, TM Jr and Goldblatt, SM (1967) Serum proteins of salamanders of the Ambystoma Jeffersonianum complex, and the origin of the triploid species of this group. Evolution 21, 345–354.CrossRefGoogle ScholarPubMed
Warren, DL, Geneva, AJ and Lanfear, R (2017) RWTY (R We There Yet): an R package for examining convergence of Bayesian phylogenetic analyses. Molecular Biology and Evolution 34, 1016–1020.Google Scholar
Woodhams, DC, Rollins-Smith, LA, Alford, RA, Simon, MA and Harris, RN (2007) Innate immune defenses of amphibian skin: antimicrobial peptides and more. Animal Conservation 10, 425–428.CrossRefGoogle Scholar