Journal Article

Surveying Europe's only cave-dwelling chordate species (Proteus anguinus) using environmental DNA.

Vörös, J., Márton, O., Schmidt, B.R., Gál, J.T., & Jelić, D.

Record Number:
3876
Year:
2017
Journal:
PLoS ONE
Volume:
12(1): e0170945
Abstract:
In surveillance of subterranean fauna, especially in the case of rare or elusive aquatic species, traditional techniques used for epigean species are often not feasible. We developed a non-invasive survey method based on environmental DNA (eDNA) to detect the presence of the red-listed cave-dwelling amphibian, Proteus anguinus, in the caves of the Dinaric Karst. We tested the method in fifteen caves in Croatia, from which the species was previously recorded or expected to occur. We successfully confirmed the presence of P. anguinus from ten caves and detected the species for the first time in five others. Using a hierarchical occupancy model we compared the availability and detection probability of eDNA of two water sampling methods, filtration and precipitation. The statistical analysis showed that both availability and detection probability depended on the method and estimates for both probabilities were higher using filter samples than for precipitation samples. Combining reliable field and laboratory methods with robust statistical modeling will give the best estimates of species occurrence.
Times Cited:
1
Relevent Species:
Related Records:
Valvasor J.W. (1689)
Die Ehre des Herzogthums Crain.
Laurenti J.L. (1768)
Specimen Medicum, Exhibens Synopin Reptilium Emendatam cum Experimentis circa Venena et Antidota Reptilium Austriacorum.
Schreibers, C. von. (1801)
A historical and anatomical description of a doubtful amphibious animal of Germany called by Laurenti Proteus anguineus
Configliachi, P. and Rusconi, M. (1821)
Observations on the natural history and structure of the Proteus anguinus. Section 6. On the organs of respiration
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Fitzinger, L. (1850)
Ueber den Proteus anguinus der Autoren
Fejervary, G.J. (1926)
Note sur la variation du Protee et description d'individus provenants d'un nouvel habitat
Briegleb, W. (1962)
Zur Biologie und Oekologie des Grottenolms (Proteus anguinus Laur. 1768)
Briegleb, W. (1963)
Zur Kenntnis eines Ökotops von Proteus anguinus Laur.1768 (On the knowledge of the ecotope of the Proteus anguinus Laur. 1768)
Abrami, G. (1966)
Osservazioni sulla distribuzione del Proteus anguinus
Istenič, L. (1971)
Izhodišče za Reševanje Ekološke Problematike Človeške Ribice (Proteus anguinus Laur.1768.) (Approach to the solution of the problem of the ecology of Proteus)
Istenič, L. and Sojar, A. (1972)
Poraba kisika pri Močerilu - Proteus anguinus (Oxygen Consumption of Proteus anguinus)
Durand, J.P. (1972)
Recherches sur l'appareil visuel du protee, Proteus anguinus Laurenti, urodele hypoge
Durand, J.P. (1973)
Development et involution oculaire de Proteus anguinus Laurenti Urodele cavernicole
Thines, G. and Durand, J. (1973)
Connaissances actuelles sur l'appareil sensoriel da la ligne laterale chez les vertebres cavernicoles aquatique
Durand, J.P. (1976)
Rudimentation des yeux chez les poissons et urodeles souterraines
Sket, B. and Velkovrh, F. (1978)
The discovery of Proteus-eggs (Proteus anguinus Laurenti, Amphibia) in seminatural conditions
Istenič, L. (1979)
Pomanjkanje kisika v Putickovem jezeru Planinske jame (The oxygen deficit in Putick Lake of Planinska Jama)
Garasic, M. (1980)
Pronadjena covjecja ribica (Proteus anguinus) u podzemnoj rijeci Rokine bezdane kod Jezerana u Lici
Sojar, A., Istenič, L. and Musar, D. (1981)
Udisanje vazduha i problematika uloge pluća kod Proteus (Air Inhaling and problems of the role of lungs with the Proteus)
Kranjec, N. (1981)
Razsirjenost in variabilnost mocerila (Proteus anguinus Laurenti)
Durand, J.P. and Delay, B. (1981)
Influence of temperature on the development of Proteus anguinus (Caudata: Proteidae) and relation with its habitat in the subterranean world
Durand, J.P. (1982)
Donnees et hypotheses sur l'evolution des Proteidae
Istenič, L. (1986)
Evidence of hypoxic conditions in the habitat of the cave salamander Proteus anguinus in the Planinska Jama
Aljančič, M., Habič, P. and Mihevc, A. (1986)
Črni močeril iz Bele krajine [The Black olm from White Carniola]
Bulog, B. (1989)
Differentiation of the inner ear sensory epithelia of Proteus anguinus (Urodela, Amphibia)
Aljančič, M., Bulog, B., Kranjc, A., Josipovič, D., Sket, B. and Skoberne, P. (1993)
Proteus – The Mysterious Ruler of Karst Darkness
Sket, B. (1994)
"Yugoslavia" (Bosnia-Herzegovina, Croatia, Macedonia, Montenegro, Serbia, Slovenia)
Sket, B. and Arntzen, J.W. (1994)
A black, non-troglomorphic amphibian from the karst of Slovenia: Proteus anguinus parkelj n. ssp. (Urodela: Proteidae)
Grillitsch, H. and Tiedemann, F. (1994)
Die Grottenolm-Typen Leopold Fitzingers (Caudata: Proteidae: Proteus)
Kletecki, E., Jalzic, B. and Rada, T. (1996)
Distribution of the Olm (Proteus anguinus, Laur.) in Croatia
Sket, B. (1997)
Distribution of Proteus (Amphibia: Urodela: Proteidae) and its possible explanation
Šolaja, M., Pocrnjić, Z. and Topalić, L. (1998)
Uticaj termičke adaptacije na bazalni metabolizam Proteusa (Proteus anguinus). (Influence of thermal adaptation on the basal metabolism of Proteus)
Aljancic, G. and Aljancic. M (1998)
Cloveska ribica (Proteus anguinus)
Dumas, P. and Chris, B. (1998)
The olfaction in Proteus anguinus: a behavioural and cytological study
Durand, J.P. (1998)
Amphibia
Tvrtkovic, N. (1999)
Cavernicole vertebrates of the Dinaric karst
Weber, A. (2000)
Fish and amphibia
Tercafs, R. (2001)
The protection of the subterranean environment: Conservation principles and management tools
Kos, M., Bulog, B., Szél, Á. and Röhlich, P. (2001)
Immunocytochemical demonstration of visual pigments in the degenerate retinal and pineal photoreceptors of the blind cave salamander (Proteus anguinus).
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Behavioural, physiological and metabolic responses to long-term starvation and refeeding in a blind cave-dwelling (Proteus anguinus) and a surface-dwelling (Euproctus asper) salamander
Kletecki, E., Jalzic, B. and Rada, T. (2002)
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Sket, B. (2004)
Dinaric Karst: Biospeleology
Bulog, B. (2004)
Amphibia: Proteus
Weber, A. (2004)
Amphibia
Sket, B. (2005)
Dinaric Karst, Diversity in
Durand, J.P. (2005)
Salamanders
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Structure and evolution of the mitochondrial control region and flanking sequences in the European cave salamander Proteus anguinus
Trontelj, P., Gorički, Š., Polak, S., Verovnik, R., Zakšek, V. and Sket, B. (2007)
Age estimates for some subterranean taxa and lineages in the Dinaric Karst
Aljancic, G. (2008)
Jamski laboratorij Tular in cloveska ribica
Schlegel, P.A., Steinfartz, S. and Bulog, B. (2009)
Non-visual sensory physiology and magnetic orientation in the blind cave salamander, Proteus anguinus (and other cave-dwelling urodele species): review and new results on light-sensitivity and non-visual orientation in subterranean urodeles (Amphibia)
Issartel, J., Hervant, F., de Fraipont, M., Clobert, J.and Voituron, Y. (2009)
High anoxia tolerance in the subterranean salamander Proteus anguinus without oxidative stress nor activation of antioxidant defenses during reoxygenation
Aljancic, G. (2010)
Fifty years of Tular Cave laboratory
Voituron, Y., de Fraipont, M., Issartel, J., Guillaume, O. and Clobert, J. (2011)
Extreme lifespan of the human fish (Proteus anguinus): a challenge for ageing mechanisms
Pezdirc, M., Heath, E., Mali, L.B. and Bulog, B. (2011)
PCB accumulation and tissue distribution in cave salamander (Proteus anguinus anguinus, Amphibia, Urodela) in the polluted karstic hinterland of the Krupa River, Slovenia
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Vertebrate fauna in caves of eastern tennessee within the Appalachians karst region, USA
Bizjak Mali. L. and Bulog, B. (2016)
Functional morphology and environmental studies on Proteus
Bonacci, O. (2017)
Karst Hydrology : With Special Reference to the Dinaric Karst
Aljancic, G. (2017)
Trideset let od odkritja crne cloveske ribice
Gorički, S., Stanković, D., Snoj, A., Kuntner, M., Jeffery, W.R., Trontelj, P., Pavićević, M., Grizelj, Z., Năpăruş-Aljančič, M. and Aljančič, G. (2017)
Environmental DNA in subterranean biology: range extension and taxonomic implications for Proteus
Vörös, J., Márton, O., Schmidt, B.R., Gál, J.T., & Jelić, D. (2017)
Surveying Europe's only cave-dwelling chordate species (Proteus anguinus) using environmental DNA.
Bizjak-Mali, L. (2017)
Variability of testes morphology and the presence of testis-ova in the European blind cave salamander (Proteus anguinus)
Năpăruș-Aljančič, M., Gorički, Š., Stanković, D., Kuntner, M. and Aljančič, G. (2017)
GIS analysis to assess the groundwater habitat pollution of black proteus
Jelic, D. (2018)
Croatia.Cave Fauna. IX 1. Cave aquatic fauna
Gladstone, N.S., Carter, E.T., Niemiller, K.D.K., Hayter, L.E. and Niemiller, M.L. (2018)
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Vörös, J., Ursenbacher, S. and Jelić, D. (2018)
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Zakšek, V., Konec, M. and Trontelj, P. (2018)
First microsatellite data on Proteus anguinus reveal weak genetic structure between the caves of Postojna and Planina
Sremac, J. and Karaica, B. (2019)
Evolution and phylogenetic relationships
Aljančič, G. (2019)
History of research on Proteus anguinus Laurenti 1768 in Slovenia
Saric, K.K. and Jelic, D. (2019)
Proteus anguinus species
Kostanjšek, R., Prodan, Y., Stres, B. and Trontelj, P. (2019)
Composition of the cutaneous bacterial community of a cave amphibian, Proteus anguinus
Kolar, B. (2019)
The threshold concentration for nitrate in groundwater as a habitat of Proteus anguinus
Saric, K.K. (2019)
Habitat
Sket, B. (2019)
Proteus' co-residents
Saric, K.K., Jelic, D. and Aljancic, G. (2019)
A brief historical review of Proteus research in the Dinaric Karst
Saric, K.K. (2019)
Species distribution - Introduction
Bressi, N. (2019)
Italy - A brief historical review of research
Aljancic, G. (2019)
Slovenia - A brief historical review of research
Saric, K.K., Jalzic, B. and Jelic, D. (2019)
Croatia - a brief historical review of research
Saric, K.K. (2019)
Montenegro - a brief historical review of research
Saric, K.K. and Jelic, D. (2019)
Structure and anatomy
Saric, K.K. and Jelic, D. (2019)
Physiology
Saric, K.K. and Aljancic, G. (2019)
Reproductive biology
Šarić, K.K., Jelić, D., Konrad, P.K. and Jalžić, B. (2019)
Proteus
Konrad, P.K. and Saric, K.K. (2019)
Appendix 1. Introduction to Proteus research in Croatia as a part of a project "Karst - the Dinaric Arc karst biodiversity conservation programme"
Gorički, Š., Niemiller, M.L., Fenolio, D.B. and Gluesenkamp, AG. (2019)
Salamanders
Budic, M. (2019)
The Dinaric Karst phenomenon
Bozic, V. (2019)
Speleological research in Croatia
Konrad, P.K. and Cukusic, I. (2019)
Cave diving in Croatia
Bedek, J. and Lukic, M. (2019)
Speleobiological research on invertebrates in Croatia
Basara, D., Cvitanovic, H. and Saric, K.K. (2019)
Speleological publications
Jelic, D. and Saric, K.K. (2019)
Introduction
Balázs, G., Lewarne, B. and Herczeg, G. (2020)
Extreme site fidelity of the olm (Proteus anguinus) revealed by a long-term capture–mark–recapture study
Li. Z., Verbrugghe, E., Konstanjšek, R., Lukač, M., Pasmans, .F, Cizelj., I. and Martel, A. (2020)
Dampened virulence and limited proliferation of Batrachochytrium salamandrivorans during subclinical infection of the troglobiont olm (Proteus anguinus)
Gredar, T. (2020)
Development of non-destructive approaches for sex identification in the Proteus (Proteus anguinus, Urodela, Amphibia)
Mulec, J. (2020)
Interview with Rok Kotanjšek and Nina Gunde-Cimerman. Welcome to the -omics era of the 21st century: will Proteus anguinus finally reveal all its mysteries?
Anonymous (2020)
Books received - Proteus edited by Šarić, Jelić, Konrad, and Jalžić (2019)
Lewarne, B. and Balázs, G. (2020)
Observed air-breathing behaviour of Proteus anguinus individuals under an intermittent hypoxic scenario in their natural habitat, with details of the prevailing environmental conditions
Lewarne, B. and Allain, S.J.R. (2020)
The unnatural history of cave olms Proteus anguinus in England
Whittaker, K. and Koo, M.S. (2021)
Proteus anguinus: Olm
Garasic, M. (2021)
The Dinaric Karst System of Croatia. Speleology and Cave Exploration
Tesarová, M., Mancini, L., Mauri, E., Aljancic, G., Naparus-Aljancic, M., Kostanjšek, R., Mali, L.B., Zikmund, T., Kaucká, M., Papi, F., Goyens, J., Bouchnita, A., Hellander, A. (2022)
Living in darkness: Exploring adaptation of Proteus anguinus in 3 dimensions by X-ray imaging
Kostanjšek, R. et al. (2022)
Towards the massive genome of Proteus anguinus, illuminating longevity, regeneration, convergent evolution and metabolic disorders
Guillaume, O. (2022)
The cave salamander Proteus anguinus in captivity in Moulis, France for the scientific research
Barzaghi, B., Ficetola, F.G., Mauri, E., Restaino, M., Lombardi, B. and Manenti, R. (2022)
Preliminary study on differences characterizes the populations of olm (Proteus anguinus) in cave and those found in epigean environment
Niemiller, M.L., Carter, E.T., Fenolio, D.B., Gluesenkamp, A.G. and Phillips, J.G. (2022)
Subterranean colonisation and diversification of cave-dwelling salamanders
Niemiller, M.L., Carter, E.T., Gladstone, N.S., Niemiller, K.D.K., Hayter, L.E., Engel, A.S., Miller, B.T., and Fitzpatrick, B.M. (2022)
The distribution, ecology, life history, and conservation status of the Berry Cave salamander (Gyrinophilus gulolineatus)
Recknagel, H., Zakšek, V., Delić, T., Gorički, S. and Trontelj, P. (2023)
Multiple transitions between realms shape relict lineages of Proteus cave salamanders
Kostanjsek, R., Zaksek, V., Bizjak-Mali, L. and Trontelj, P. (2023)
Chapter 13. The olm (Proteus anguinus), a flagship groundwater species
Lewarne, B. and Allain, S.J.R. (2023)
Attempted predation of a cave olm Proteus anguinus by a dice water snake Natrix tessellata, in Bosnia and Herzegovina
Ravbar, N., Viršek, D. and Năpăruş-Aljančič, M. (2023)
New locality of Proteus anguinus in the area of the Tabor Ridge near Grosuplje, central Slovenia
Petrescu-Mag, V. (2023)
The olm (Proteus anguinus) and cave life
Voituron, Y., Guillaume, O., Dumet, A., Zahn. S and Criscuolo, F. (2023)
Temperature-independent telomere lengthening with age in the long-lived human fish (Proteus anguinus)
Barzaghi, B. (2023)
Between light and darkness: The round-trip of surface and subterranean animals
Manenti, R., Vinci, L., Barzaghi, B., Lombardi, B., Teodoro, C., Baglioni, L., Melotto, A. and Francesco Ficetola, G. (2024)
Sit-and-wait foraging is not enough in food-deprived environments: evidence from groundwater and salamanders
Anonymous (2024)
Wikipedia: Olm
Hoover, H., Manenti, R. and Melotto, A. (2024)
The role of experience in the visual and non-visual prey recognition of Fire Salamander populations from caves and streams