Vol. 21 No. 1 (2026)
Articles

Detection of CMTV-like ranavirus following a Rana temporaria mass mortality event in a northern Italian alpine lake

PDF Suppl. Mat. HTML
  • Matteo Riccardo Di Nicola,
  • Chiara Beltramo,
  • Paolo Pastorino,
  • Giuseppe Esposito,
  • Anna Cerullo,
  • Arianna Meletiadis,
  • Marino Prearo,
  • Simone Peletto,
  • Pier Luigi Acutis
Matteo Riccardo Di Nicola
Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d’Aosta, Via Bologna 148, 10154 Torino, Italy
Chiara Beltramo
Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d’Aosta, Via Bologna 148, 10154 Torino, Italy
Paolo Pastorino
Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d’Aosta, Via Bologna 148, 10154 Torino, Italy
Giuseppe Esposito
Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d’Aosta, Via Bologna 148, 10154 Torino, Italy
Anna Cerullo
Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d’Aosta, Via Bologna 148, 10154 Torino, Italy
Arianna Meletiadis
Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d’Aosta, Via Bologna 148, 10154 Torino, Italy
Marino Prearo
Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d’Aosta, Via Bologna 148, 10154 Torino, Italy
Simone Peletto
Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d’Aosta, Via Bologna 148, 10154 Torino, Italy
Pier Luigi Acutis
Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d’Aosta, Via Bologna 148, 10154 Torino, Italy
DOI: https://doi.org/10.36253/a_h-18382

Published 2026-02-09

Keywords

  • Acinetobacter,
  • CMTV,
  • Cottian Alps,
  • Disease ecology,
  • Emerging infectious diseases,
  • Germanasca Valley,
  • Outbreak,
  • Ranavirus
    • ...More
    Less

How to Cite

Di Nicola, M. R., Beltramo, C., Pastorino, P., Esposito, G., Cerullo, A., Meletiadis, A., Prearo, M., Peletto, S., & Acutis, P. L. (2026). Detection of CMTV-like ranavirus following a Rana temporaria mass mortality event in a northern Italian alpine lake. Acta Herpetologica, 21(1), 49–62. https://doi.org/10.36253/a_h-18382

Copyright (c) 2026 Matteo Riccardo Di Nicola, Chiara Beltramo, Paolo Pastorino, Giuseppe Esposito, Anna Cerullo, Arianna Meletiadis, Marino Prearo, Simone Peletto, Pier Luigi Acutis

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Crossref
Scopus
Google Scholar
Europe PMC

Abstract

High-mountain lakes are vulnerable to climatic and anthropogenic stressors, and infectious disease may further exacerbate impacts on alpine communities, particularly during seasonal temperature peaks. In August 2024, a mass mortality event of common frogs (Rana temporaria) occurred in a high-altitude lake in the Cottian Alps (Piedmont, Italy). During a one-hour survey, 78 dead frogs were recorded; nine carcasses (all adult males) were sampled for diagnostic tests. Six showed ventral red discolouration and three of them had ulcerative lesions of the digits. Eight out of nine vitreous humour samples were culture-positive, with isolates including Hafnia alvei, Acinetobacter guillouiae, Acinetobacter proteolyticus, and Serratia proteamaculans. PCR screening of skin and pooled organs detected ranavirus in four out of nine frogs, while Batrachochytrium dendrobatidis and herpesvirus tested negative. Phylogenetic analysis of sequenced major capsid protein and DNA polymerase fragments grouped the virus within the CMTV-like clade, with high similarity to reference sequences. This represents the first geolocated detection of a CMTV-like ranavirus in free-ranging amphibians in Italy. Although the advanced state of decomposition precluded histopathological evaluation and causality cannot be conclusively established, the concordance between molecular detection and gross lesions consistent with ranaviral infection supports a plausible role of ranavirus in the observed die-off. Our findings highlight the need for targeted surveillance in Italy’s alpine amphibians, including environmental DNA sampling and screening of non-native fish. Given ecological simplification and short reproductive seasons at high altitude, longitudinal monitoring is advisable to assess persistence, seasonality and potential spillover across life stages and sympatric species.

PDF Suppl. Mat. HTML

References

  1. Akçakaya, H.R., Neam, K., Hobin, L., Lötters, S., Martel, A., Pasmans, F. (2023): Assessing the extinction risks of amphibians impacted by infectious diseases. Biol. Conserv. 284: 110205. DOI: https://doi.org/10.1016/j.biocon.2023.110205
  2. Allain, S.J., Duffus, A.L. (2019): Emerging infectious disease threats to European herpetofauna. Herpetol. J. 29: 189-206. DOI: https://doi.org/10.33256/hj29.4.189-206
  3. Allasia, P., Audisio, C., Baldo, M., Cirio, C.G., Lollino, G., Giordan, D., Godone, F., Nigrelli, G., Alpe, F., Ambrogio, S., Giardino, M., Perotti, L., Sambuelli, L., De Renzo, G., Fontan, D., Barbero, T. (2004): Instrumented experimental sites for the control of landslide hazards in mountain environments: the Germanasca and Susa Valleys (Northwestern Italy). In: Field trip guidebooks, 32nd International Geological Congress, Florence, Italy, 20-28 August 2004, pp. 37-54. APAT, Roma.
  4. Aree Protette Alpi Marittime (2019): Ranavirus a rischio la rana temporaria. Aree Protette Alpi Marittime.
  5. Ariel, E., Holopainen, R., Olesen, N.J., Tapiovaara, H. (2010): Comparative study of ranavirus isolates from cod (Gadus morhua) and turbot (Psetta maxima) with reference to other ranaviruses. Arch. Virol. 155: 1261-1271. DOI: https://doi.org/10.1007/s00705-010-0715-z
  6. Ariel, E., Subramaniam, K., Imnoi, K., Sriwanayos, P., Ahasan, M.S., Olesen, N.J., Amedeo, M., Toffan, A., Waltzek, T.B. (2017): Genomic sequencing of Ranaviruses isolated from edible frogs (Pelophylax esculentus). Genome Announc. 5: 10-1128. DOI: https://doi.org/10.1128/genomeA.01015-17
  7. Balseiro, A., Dalton, K., Del Cerro, A., Marquez, I., Cunningham, A., Parra, F., Prieto, J., Casais, R. (2009): Pathology, isolation and molecular characterisation of a Ranavirus from the common midwife toad Alytes obstetricans on the Iberian Peninsula. Dis. Aquat. Org. 84: 95-104. DOI: https://doi.org/10.3354/dao02032
  8. Bates, K.A., Rosa, G.M., Gamer, T.W.J. (2025): Ranavirus. Trends Microbiol. 33: 701-702. DOI: https://doi.org/10.1016/j.tim.2025.02.008
  9. Bergò, P.E., Andreone, F. (2002): A terrestrial viviparous salamander into water: Notes on the unusual larval aquatic development in Salamandra lanzai. Herpetol. Bull. 81: 29-31.
  10. Bianchessi, L., Flach, E., Monacchia, G., Dagleish, M., Maley, M., Turin, L., Rocchi, M.S. (2024): Identification and characterisation of gamma-herpesviruses in zoo artiodactyla. Virol. J. 21: 1-15. DOI: https://doi.org/10.1186/s12985-024-02311-3
  11. Bison, M., Yoccoz, N.G., Carlson, B.Z., Klein, G., Laigle, I., Van Reeth, C., Delestrade, A. (2021): Earlier snowmelt advances breeding phenology of the common frog (Rana temporaria) but increases the risk of frost exposure and wetland drying. Front. Ecol. Evol. 9: 1-12. DOI: https://doi.org/10.3389/fevo.2021.645585
  12. Bosch, J., Carrascal, L.M., Durán, L., Walker, S., Fisher, M.C. (2007): Climate change and outbreaks of amphibian chytridiomycosis in a montane area of Central Spain: Is there a link? Proc. R. Soc. B. 274: 253-260. DOI: https://doi.org/10.1098/rspb.2006.3713
  13. Bosch, J., Monsalve-Carcaño, C., Price, S.J., Bielby, J. (2020): Single infection with Batrachochytrium dendrobatidis or Ranavirus does not increase probability of co-infection in a montane community of amphibians. Sci. Rep. 10: 21115. DOI: https://doi.org/10.1038/s41598-020-78196-3
  14. Bosch, J., Mora-Cabello De Alba, A., Marquínez, S., Price, S.J., Thumsová, B., Bielby, J. (2021): Long-term monitoring of amphibian populations of a national park in northern Spain reveals negative persisting effects of Ranavirus, but not Batrachochytrium dendrobatidis. Front. Vet. Sci. 8: 645491. DOI: https://doi.org/10.3389/fvets.2021.645491
  15. Box, E.K., Cleveland, C.A., Subramaniam, K., Waltzek, T.B., Yabsley, M.J. (2021): Molecular confirmation of Ranavirus infection in amphibians from Chad, Africa. Front. Vet. Sci. 8: 733939. DOI: https://doi.org/10.3389/fvets.2021.733939
  16. Boyle, D., Boyle, D., Olsen, V., Morgan, J., Hyatt, A. (2004): Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis. Aquat. Org. 60: 141-148. DOI: https://doi.org/10.3354/dao060141
  17. Brunner, J.L., Olson, D.H., Gray, M.J., Miller, D.L., Duffus, A.L.J. (2021): Global patterns of Ranavirus detections. FACETS 6: 912-924. DOI: https://doi.org/10.1139/facets-2020-0013
  18. Catalan, J., Ninot, J.M., Aniz, M.M. (2017): High mountain conservation in a changing world. Cham, Springer International Publishing. DOI: https://doi.org/10.1007/978-3-319-55982-7
  19. Claytor, S.C., Subramaniam, K., Landrau-Giovannetti, N., Chinchar, V.G., Gray, M.J., Miller, D.L., Mavian, C., Salemi, M., Wisely, S., Waltzek, T.B. (2017): Ranavirus phylogenomics: Signatures of recombination and inversions among bullfrog ranaculture isolates. Virology 511: 330-343. DOI: https://doi.org/10.1016/j.virol.2017.07.028
  20. Di Nicola, M.R., Cavigioli, L., Luiselli, L., Andreone, F. (2021): Anfibi & Rettili d’Italia. Edizione aggiornata. Latina; Edizioni Belvedere.
  21. Di Nicola, M.R., Rubiola, S., Cerullo, A., Basciu, A., Massone, C., Zabbia, T., Dorne, J.L.M.C., Acutis, P.L., Marini, D. (2025): Microorganisms in wild European reptiles: Bridging gaps in neglected conditions to inform disease ecology research. Int. J. Parasitol. Parasites. Wildl. 27: 101113. DOI: https://doi.org/10.1016/j.ijppaw.2025.101113
  22. Duffus, A.L., Nichols, R.A., Garner, T.W. (2014): Detection of a frog virus 3-like Ranavirus in native and introduced amphibians in the United Kingdom in 2007 and 2008. Herpetol. Rev. 45: 608-610.
  23. Ehlers, B., Borchers, K., Grund, C., Frölich, K., Ludwig, H., Buhk, H.-J. (1999): Detection of new DNA polymerase genes of known and potentially novel herpesviruses by PCR with degenerate and deoxyinosine-substituted primers. Virus Genes 18: 211-220. DOI: https://doi.org/10.1023/A:1008064118057
  24. Farina, T., Ed. (2008): Alpi Cozie. Supplemento a Piemonte Parchi 5(XXIII). Torino, Regione Piemonte.
  25. Fisher, M.C., Garner, T.W.J. (2020): Chytrid fungi and global amphibian declines. Nat. Rev. Microbiol. 18: 332-343. DOI: https://doi.org/10.1038/s41579-020-0335-x
  26. Fisher, M.C., Henk, D.A., Briggs, C.J., Brownstein, J.S., Madoff, L.C., McCraw, S.L., Gurr, S.J. (2012): Emerging fungal threats to animal, plant and ecosystem health. Nature 484: 186-194. DOI: https://doi.org/10.1038/nature10947
  27. Flechas, S., Urbina, J., Crawford, A., Gutiérrez, K., Corrales, K., Castellanos, L., González, M., Cuervo, A., Catenazzi, A. (2023): First evidence of ranavirus in native and invasive amphibians in Colombia. Dis. Aquat. Org. 153: 51-58. DOI: https://doi.org/10.3354/dao03717
  28. Forno, M.G., Lingua, A., Lo Russo, S., Taddia, G. (2011): Improving digital tools for Quaternary field survey: A case study of the Rodoretto Valley (NW Italy). Environ. Earth. Sci. 64: 1487-1495. DOI: https://doi.org/10.1007/s12665-011-0971-6
  29. Forzán, M.J., Jones, K.M., Ariel, E., Whittington, R.J., Wood, J., Markham, R.J.F., Daoust, P.-Y. (2017): Pathogenesis of frog virus 3 (Ranavirus, Iridoviridae) infection in wood frogs (Rana sylvatica). Vet. Pathol. 54: 531-548. DOI: https://doi.org/10.1177/0300985816684929
  30. Franklinos, L., Fernandez, J., Hydeskov, H., Hopkins, K., Everest, D., Cunningham, A., Lawson, B. (2018): Herpesvirus skin disease in free-living common frogs Rana temporaria in Great Britain. Dis. Aquat. Org. 129: 239-244. DOI: https://doi.org/10.3354/dao03246
  31. Guo, L., Jin, X., Yang, D., Wei, L., Chen, J., Lin, Z., Ma, L. (2025): Identification and characterization of Serratia nematophila and Acinetobacter guillouiae from putrid-skin disease lesions in farmed Chinese spiny frog (Quasipaa spinosa). Microbiol. Spectr. 13: e02096-24. DOI: https://doi.org/10.1128/spectrum.02096-24
  32. Hanna, P.E., Bellamy, J.E., Donald, A. (1990): Postmortem eyefluid analysis in dogs, cats and cattle as an estimate of antemortem serum chemistry profiles. Can. J. Vet. Res. 54: 487-494.
  33. Hartmann, A.M., Maddox, M.L., Ossiboff, R.J., Longo, A.V. (2022): Sustained Ranavirus outbreak causes mass mortality and morbidity of imperiled amphibians in Florida. EcoHealth 19: 8-14. DOI: https://doi.org/10.1007/s10393-021-01572-6
  34. Hick, P.M., Subramaniam, K., Thompson, P., Whittington, R.J., Waltzek, T.B. (2016): Complete genome sequence of a Bohle iridovirus isolate from ornate burrowing frogs (Limnodynastes ornatus) in Australia. Genome Announc. 4: e00632-16. DOI: https://doi.org/10.1128/genomeA.00632-16
  35. Herath, J., Sun, D., Ellepola, G., Subramaniam, K., Meegaskumbura, M. (2023): Emerging threat of Ranavirus: Prevalence, genetic diversity, and climatic drivers of Ranavirus (Iridoviridae) in ectothermic vertebrates of Asia. Front. Vet. Sci. 10: 1291872. DOI: https://doi.org/10.3389/fvets.2023.1291872
  36. Hoberg, E.P., Brooks, D.R. (2015): Evolution in action: Climate change, biodiversity dynamics and emerging infectious disease. Philos. Trans. R. Soc. B 370: 20130553. DOI: https://doi.org/10.1098/rstb.2013.0553
  37. Holopainen, R., Ohlemeyer, S., Schütze, H., Bergmann, S., Tapiovaara, H. (2009): Ranavirus phylogeny and differentiation based on major capsid protein, DNA polymerase and neurofilament triplet H1-like protein genes. Dis. Aquat. Org. 85: 81-91. DOI: https://doi.org/10.3354/dao02074
  38. Hyatt, A.D., Gould, A.R., Zupanovic, Z., Cunningham, A.A., Hengstberger, S., Whittington, R.J., Kattenbelt, J., Coupar, B.E.H. (2000): Comparative studies of piscine and amphibian iridoviruses. Arch. Virol. 145: 301-331. DOI: https://doi.org/10.1007/s007050050025
  39. Ilić, M., Bugarski-Stanojević, V., Jovanović, B., Stamenković, G., Zorić, K., Paunović, M., Crnobrnja-Isailović, J. (2024): Phylogeographic substructuring in the southernmost refugium of the European common frog Rana temporaria. Animals 14: 1430. DOI: https://doi.org/10.3390/ani14101430
  40. Ionescu, M.I., Neagoe, D. Ștefan, Crăciun, A.M., Moldovan, O.T. (2022): The gram-negative bacilli isolated from caves – Sphingomonas paucimobilis and Hafnia alvei and a review of their involvement in human infections. Int. J. Environ. Res. Public Health 19: 2324. DOI: https://doi.org/10.3390/ijerph19042324
  41. Jancovich, J.K., Steckler, N.K., Waltzek, T.B. (2015): Ranavirus taxonomy and phylogeny. In: Ranaviruses; pp. 59-70. Gray, M.J., Chinchar, V.G., Eds, Cham, Springer International Publishing. DOI: https://doi.org/10.1007/978-3-319-13755-1_3
  42. Knapp, R.A., Briggs, C.J., Smith, T.C., Maurer, J.R. (2011): Nowhere to hide: Impact of a temperature-sensitive amphibian pathogen along an elevation gradient in the temperate zone. Ecosphere 2: art93. DOI: https://doi.org/10.1890/ES11-00028.1
  43. Kumar, S., Stecher, G., Tamura, K. (2016): MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for Bigger Datasets. Mol. Biol. Evol. 33: 1870-1874. DOI: https://doi.org/10.1093/molbev/msw054
  44. Lisachova, L.S., Lisachov, A.P., Ermakov, O.A., Svinin, A.O., Chernigova, P.I., Lyapkov, S.M., Zamaletdinov, R.I., Pavlov, A.V., Zaks, S.S., Fayzulin, A.I., Korzikov, V.A., Simonov, E. (2025): Continent-wide distribution of CMTV-like Ranavirus, from the Urals to the Atlantic Ocean. EcoHealth 22: 173-184. DOI: https://doi.org/10.1007/s10393-025-01703-3
  45. Luedtke, J.A., Chanson, J., Neam, K., Hobin, L., Maciel, A.O., Catenazzi, A., Borzée, A., Hamidy, A., Aowphol, A., Jean, A., Sosa-Bartuano, Á., Fong G., A., De Silva, A., Fouquet, A., Angulo, A., Kidov, A.A., Muñoz Saravia, A., Diesmos, A.C., Tominaga, A., Shrestha, B., Gratwicke, B., Tjaturadi, B., Martínez Rivera, C.C., Vásquez Almazán, C.R., Señaris, C., Chandramouli, S.R., Strüssmann, C., Cortez Fernández, C.F., Azat, C., Hoskin, C.J., Hilton-Taylor, C., Whyte, D.L., Gower, D.J., Olson, D.H., Cisneros-Heredia, D.F., Santana, D.J., Nagombi, E., Najafi-Majd, E., Quah, E.S.H., Bolaños, F., Xie, F., Brusquetti, F., Álvarez, F.S., Andreone, F., Glaw, F., Castañeda, F.E., Kraus, F., Parra-Olea, G., Chaves, G., Medina-Rangel, G.F., González-Durán, G., Ortega-Andrade, H.M., Machado, I.F., Das, I., Dias, I.R., Urbina-Cardona, J.N., Crnobrnja-Isailović, J., Yang, J.-H., Jianping, J., Wangyal, J.T., Rowley, J.J.L., Measey, J., Vasudevan, K., Chan, K.O., Gururaja, K.V., Ovaska, K., Warr, L.C., Canseco-Márquez, L., Toledo, L.F., Díaz, L.M., Khan, M.M.H., Meegaskumbura, M., Acevedo, M.E., Napoli, M.F., Ponce, M.A., Vaira, M., Lampo, M., Yánez-Muñoz, M.H., Scherz, M.D., Rödel, M.-O., Matsui, M., Fildor, M., Kusrini, M.D., Ahmed, M.F., Rais, M., Kouamé, N.G., García, N., Gonwouo, N.L., Burrowes, P.A., Imbun, P.Y., Wagner, P., Kok, P.J.R., Joglar, R.L., Auguste, R.J., Brandão, R.A., Ibáñez, R., Von May, R., Hedges, S.B., Biju, S.D., Ganesh, S.R., Wren, S., Das, S., Flechas, S.V., Ashpole, S.L., Robleto-Hernández, S.J., Loader, S.P., Incháustegui, S.J., Garg, S., Phimmachak, S., Richards, S.J., Slimani, T., Osborne-Naikatini, T., Abreu-Jardim, T.P.F., Condez, T.H., De Carvalho, T.R., Cutajar, T.P., Pierson, T.W., Nguyen, T.Q., Kaya, U., Yuan, Z., Long, B., Langhammer, P., Stuart, S.N. (2023): Ongoing declines for the world’s amphibians in the face of emerging threats. Nature 622: 308-314. DOI: https://doi.org/10.1038/s41586-023-06578-4
  46. Machate, O., Schmeller, D.S., Schulze, T., Brack, W. (2023): Review: Mountain lakes as freshwater resources at risk from chemical pollution. Environ. Sci. Eur. 35: 3. DOI: https://doi.org/10.1186/s12302-022-00710-3
  47. Mahlen, S.D. (2011): Serratia infections: From military experiments to current practice. Clin Microbiol. Rev. 24: 755-791. DOI: https://doi.org/10.1128/CMR.00017-11
  48. Mao, J., Hedrick, R.P., Chinchar, V.G. (1997): Molecular characterization, sequence analysis, and taxonomic position of newly isolated fish iridoviruses. Virology 229: 212-220. DOI: https://doi.org/10.1006/viro.1996.8435
  49. Marschang, R.E., Meddings, J.I., Waltzek, T.B., Hick, P., Allender, M.C., Wirth, W., Duffus, A.L.J. (2025): Ranavirus distribution and host range. In: Ranaviruses; pp. 155-230. Gray, M.J., Chinchar, V.G., Eds, Cham, Springer. DOI: https://doi.org/10.1007/978-3-031-64973-8_6
  50. Masli, S., Vega, J.L. (2011): Ocular immune privilege sites. Methods Mol. Biol. 677: 449-458. DOI: https://doi.org/10.1007/978-1-60761-869-0_28
  51. Mavian, C., López-Bueno, A., Balseiro, A., Casais, R., Alcamí, A., Alejo, A. (2012): The genome sequence of the emerging common midwife toad virus identifies an evolutionary intermediate within ranaviruses. J. Virol. 86: 3617-3625. DOI: https://doi.org/10.1128/JVI.07108-11
  52. Meletiadis, A., Di Nicola, M.R., Bovero, S., Favelli, M., Pezzolato, M., Grella, S., Rezza, G., Acutis, P.L. (2025): Prevalence of Batrachochytrium dendrobatidis in amphibians in northwestern Italy’s protected areas. Animals 15: 157. DOI: https://doi.org/10.3390/ani15020157
  53. Miaud, C., Arnal, V., Poulain, M., Valentini, A., Dejean, T. (2019): eDNA increases the detectability of Ranavirus infection in an alpine amphibian population. Viruses 11: 526. DOI: https://doi.org/10.3390/v11060526
  54. Miaud, C., Pozet, F., Gaudin, N.C.G., Martel, A., Pasmans, F., Labrut, S. (2016): Ranavirus causes mass die-offs of alpine amphibians in the southwestern alps, France. J. Wildl. Dis. 52: 242-252. DOI: https://doi.org/10.7589/2015-05-113
  55. Miller, D.L., Pessier, A.P., Hick, P., Whittington, R.J., Forzán, M.J. (2025): Pathology and diagnostics. In: Ranaviruses; pp. 271-312. Gray, M.J., Chinchar, V.G., Eds, Cham, Springer. DOI: https://doi.org/10.1007/978-3-031-64973-8_8
  56. Nigrelli, G. (2005): Analysis and characteristics of pluviometric events in the Germanasca Valley (Italian Western Alps). Geogr. Fis. Din. Quat. 28: 147-158.
  57. North, A.C., Hodgson, D.J., Price, S.J., Griffiths, A.G.F. (2015): Anthropogenic and ecological drivers of amphibian disease (Ranavirosis). PLoS ONE 10: e0127037. DOI: https://doi.org/10.1371/journal.pone.0127037
  58. Origgi, F.C., Schmidt, B.R., Lohmann, P., Otten, P., Meier, R.K., Pisano, S.R.R., Moore-Jones, G., Tecilla, M., Sattler, U., Wahli, T., Gaschen, V., Stoffel, M.H. (2018): Bufonid herpesvirus 1 (BfHV1) associated dermatitis and mortality in free ranging common toads (Bufo bufo) in Switzerland. Sci. Rep. 8: 14737. DOI: https://doi.org/10.1038/s41598-018-32841-0
  59. Padilla, D., Acosta, F., Ramos-Vivas, J., Grasso, V., Bravo, J., El Aamri, F., Real, F. (2015): The pathogen Hafnia alveiin veterinary medicine: A review. J. Appl. Anim. Res. 43: 231-235. DOI: https://doi.org/10.1080/09712119.2014.963086
  60. Pastorino, P., Barceló, D., Prearo, M. (2024): Alps at risk: High-mountain lakes as reservoirs of persistent and emerging contaminants. J. Contam. Hydrol. 264: 104361. DOI: https://doi.org/10.1016/j.jconhyd.2024.104361
  61. Pastorino, P., Colussi, S., Pizzul, E., Varello, K., Menconi, V., Mugetti, D., Tomasoni, M., Esposito, G., Bertoli, M., Bozzetta, E., Dondo, A., Acutis, P.L., Prearo, M. (2021): The unusual isolation of carnobacteria in eyes of healthy salmonids in high-mountain lakes. Sci. Rep. 11: 2314. DOI: https://doi.org/10.1038/s41598-021-82133-3
  62. Pastorino, P., Prearo, M. (2020): High-mountain lakes, indicators of global change: Ecological characterization and environmental pressures. Diversity 12: 260. DOI: https://doi.org/10.3390/d12060260
  63. Peñafiel-Ricaurte, A., Price, S.J., Fisher, M.C., Bosch, J., Cunningham, A.A., Azat, C. (2025): Ranavirus in native amphibians from the Pyrenees National Park, France: A case study. Eur. J. Wildl. Res. 71: 39. DOI: https://doi.org/10.1007/s10344-025-01917-4
  64. Pigaiani, N., Bertaso, A., De Palo, E.F., Bortolotti, F., Tagliaro, F. (2020): Vitreous humor endogenous compounds analysis for post-mortem forensic investigation. Forensic Sci. Int. 310: 110235. DOI: https://doi.org/10.1016/j.forsciint.2020.110235
  65. Piemonte Parchi (2019): Ranavirus minaccia la rana temporaria. Piemonte Parchi.
  66. Price, S.J., Ariel, E., Maclaine, A., Rosa, G.M., Gray, M.J., Brunner, J.L., Garner, T.W.J. (2017): From fish to frogs and beyond: Impact and host range of emergent ranaviruses. Virology 511: 272-279. DOI: https://doi.org/10.1016/j.virol.2017.08.001
  67. Price, S.J., Garner, T.W.J., Nichols, R.A., Balloux, F., Ayres, C., Mora-Cabello de Alba, A., Bosch, J. (2014): Collapse of amphibian communities due to an introduced Ranavirus. Curr. Biol. 24: 2586-2591. DOI: https://doi.org/10.1016/j.cub.2014.09.028
  68. Price, S.J., Leung, W.T.M., Owen, C.J., Puschendorf, R., Sergeant, C., Cunningham, A.A., Balloux, F., Garner, T.W.J., Nichols, R.A. (2019): Effects of historic and projected climate change on the range and impacts of an emerging wildlife disease. Glob. Change Biol. 25: 2648-2660. DOI: https://doi.org/10.1111/gcb.14651
  69. Råman Vinnå, L., Medhaug, I., Schmid, M., Bouffard, D. (2021): The vulnerability of lakes to climate change along an altitudinal gradient. Commun. Earth. Environ. 2: 35. DOI: https://doi.org/10.1038/s43247-021-00106-w
  70. Rondinini, C., Battistoni, A., Teofili, C. (2022): Lista Rossa IUCN dei vertebrati italiani 2022. Roma, Comitato Italiano IUCN e Ministero dell’Ambiente e della Sicurezza Energetica.
  71. Rosa, G.M., Sabino-Pinto, J., Laurentino, T.G., Martel, A., Pasmans, F., Rebelo, R., Griffiths, R.A., Stöhr, A.C., Marschang, R.E., Price, S.J., Garner, T.W.J., Bosch, J. (2017): Impact of asynchronous emergence of two lethal pathogens on amphibian assemblages. Sci. Rep. 7: 43260. DOI: https://doi.org/10.1038/srep43260
  72. Rosa, G.M., Ayala Botto, G., Mitra, A.T., Almeida, J.S.D., Hofmann, M., Leung, W.T.M., Alves De Matos, A.P., Caeiro, M.F., Froufe, E., Loureiro, A., Price, S.J., Owen, C., Rebelo, R., Soares, C. (2022): Invasive fish disrupt host-pathogen dynamics leading to amphibian declines. Biol. Conserv. 276: 109785. DOI: https://doi.org/10.1016/j.biocon.2022.109785
  73. Ruggeri, J., Ribeiro, L.P., Pontes, M.R., Toffolo, C., Candido, M., Carriero, M.M., Zanella, N., Sousa, R.L.M., Toledo, L.F. (2019): Discovery of wild amphibians infected with Ranavirus in Brazil. J. Wildl. Dis. 55: 897-902. DOI: https://doi.org/10.7589/2018-09-224
  74. Schilliger, L., Paillusseau, C., François, C., Bonwitt, J. (2023): Major emerging fungal diseases of reptiles and amphibians. Pathogens 12: 429. DOI: https://doi.org/10.3390/pathogens12030429
  75. Seglie, D. (2020): L’erpetofauna del Parco Naturale di Conca Cialancia, con una nota sulla colorazione atipica di due individui di Salamandra lanzai. Riv. Piem. Stor. Nat. 41: 157-166.
  76. Smith, K.F., Acevedo-Whitehouse, K., Pedersen, A.B. (2009): The role of infectious diseases in biological conservation. Anim. Conserv. 12: 1-12. DOI: https://doi.org/10.1111/j.1469-1795.2008.00228.x
  77. Smith, K.F., Sax, D.F., Lafferty, K.D. (2006): Evidence for the role of infectious disease in species extinction and endangerment. Conserv. Biol. 20: 1349-1357. DOI: https://doi.org/10.1111/j.1523-1739.2006.00524.x
  78. Stöhr, A.C., Hoffmann, A., Papp, T., Robert, N., Pruvost, N.B.M., Reyer, H.-U., Marschang, R.E. (2013): Long-term study of an infection with ranaviruses in a group of edible frogs (Pelophylax kl. esculentus) and partial characterization of two viruses based on four genomic regions. Vet. J. 197: 238-244. DOI: https://doi.org/10.1016/j.tvjl.2013.02.014
  79. Stöhr, A.C., López-Bueno, A., Blahak, S., Caeiro, M.F., Rosa, G.M., Alves De Matos, A.P., Martel, A., Alejo, A., Marschang, R.E. (2015): Phylogeny and differentiation of reptilian and amphibian ranaviruses detected in Europe. PLoS ONE 10: e0118633. DOI: https://doi.org/10.1371/journal.pone.0118633
  80. Teacher, A.G.F., Cunningham, A.A., Garner, T.W.J. (2010): Assessing the long‐term impact of Ranavirus infection in wild common frog populations. Anim. Conserv. 13: 514-522. DOI: https://doi.org/10.1111/j.1469-1795.2010.00373.x
  81. Thumsová, B., Alarcos, G., Ayres, C., Rosa, G.M., Bosch, J. (2024): Relationship between two pathogens in an amphibian community that experienced mass mortalities. Conserv. Biol. 38: e14196. DOI: https://doi.org/10.1111/cobi.14196
  82. Thumsová, B., Martínez-Silvestre, A., Pérez-Vallejo, M., Palomar, G., Rohr, J.R., Bosch, J. (2025): Temperature and precipitation mismatches increase infection risk in amphibians. Curr. Biol. 35: 4285-4292. DOI: https://doi.org/10.1016/j.cub.2025.07.053
  83. Thumsová, B., Price, S.J., González-Cascón, V., Vörös, J., Martínez-Silvestre, A., Rosa, G.M., Machordom, A., Bosch, J. (2022): Climate warming triggers the emergence of native viruses in Iberian amphibians. iScience 25: 105541. DOI: https://doi.org/10.1016/j.isci.2022.105541
  84. Tiberti, R., Rogora, M., Tartari, G., Callieri, C. (2014b): Ecological impact of transhumance on the trophic state of alpine lakes in Gran Paradiso National Park. Knowl. Managt. Aquat. Ecosyst. 415: 05. DOI: https://doi.org/10.1051/kmae/2014030
  85. Tiberti, R., Von Hardenberg, A. (2012): Impact of introduced fish on Common frog (Rana temporaria) close to its altitudinal limit in alpine lakes. Amphib.-Reptil. 33: 303-307. DOI: https://doi.org/10.1163/156853812X634044
  86. Tiberti, R., Von Hardenberg, A., Bogliani, G. (2014a): Ecological impact of introduced fish in high altitude lakes: A case of study from the European Alps. Hydrobiologia 724: 1-19. DOI: https://doi.org/10.1007/s10750-013-1696-1
  87. Trinh, L.L., Nguyen, H.H. (2024): Role of plant-associated microbes in plant health and development: The case of the Serratia genus. Technol. Agron. 4: e028. DOI: https://doi.org/10.48130/tia-0024-0025
  88. Vörös, J., Herczeg, D., Papp, T., Monsalve-Carcaño, C., Bosch, J. (2020): First detection of Ranavirus infection in amphibians in Hungary. Herpetol. Notes 13: 213-217.
  89. White, C.L., Dusek, R.J. (2015): Wildlife specimen collection, preservation, and shipment. U.S. Geological survey techniques and methods, book 15, chap. C4, 24 p. DOI: https://doi.org/10.3133/tm15C4
  90. Yu, Z., Zhang, W., Gu, C., Chen, J., Zhao, M., Fu, L., Han, J., He, M., Xiao, Q., Xiao, W., He, L., Zhang, Z. (2021): Genomic analysis of Ranavirus and exploring alternative genes for phylogenetics. Transbound. Emerg. Dis. 68: 2161-2170. DOI: https://doi.org/10.1111/tbed.13864

Most read articles by the same author(s)