Estimation of the body condition of European cave salamanders (genus Speleomantes) from digital images

Published 2025-03-03
Keywords
- body condition index,
- conservation,
- Hydromantes,
- monitoring,
- morphometry
- photography ...More
How to Cite
Copyright (c) 2025 Eleonora Cialente, Ben Oetken, Luca Coppari, Enrico Lunghi

This work is licensed under a Creative Commons Attribution 4.0 International License.
Abstract
Species monitoring is a key activity for conservation studies. Some of the monitoring methods require individual handling, which may provoke negative effects on animal fitness. We here present a new non-invasive method that allows to estimate the body condition of the European cave salamanders (genus Speleomantes) using the tail area as a proxy, since these species usually accumulate fat tissue in their tail. We selected 915 high-quality images of individuals belonging to the eight Speleomantes species. Using the ImageJ program we calculated the tail measurements (length and area) from which we obtained the Fat Tail Index (FTI). The FTI was then correlated with the Scaled Mass Index (SMI) of individuals. We used GLMM to assess whether SMI is correlated to FTI, individual sex, species identity and the type of inhabited environment. We observed a significant correlation between SMI and FTI (R2 = 0.62). The GLMM analysis showed a significant effect on SMI due to sex, species and the type of environment. Females and individuals from surface environments showed the highest SMI. Among species, we observed a significant variability in their body condition and in the correlation between SMI and FTI. This study provided a reliable and non-invasive method that allows to estimate the body condition for terrestrial salamanders of the genus Speleomantes.
References
- Beebee, T.J.C., Griffiths, R.A. (2005): The amphibian decline crisis: a watershed for conservation biology? Biol. Conserv. 125: 271-285.
- Bendik, N.F., Gluesenkamp, A.G. (2013): Body length shrinkage in an endangered amphibian is associated with drought. J. Zool. 290: 35-41.
- Bliley, J.M., Woodley, S.K. (2012): The effects of repeated handling and corticosterone treatment on behavior in an amphibian (Ocoee salamander: Desmognathus ocoee). Physiol. Behav. 105: 1132-1139.
- Cianferoni, F., Lunghi, E. (2023): Inferring on Speleomantes foraging behavior from gut contents examination. Animals 13: 2782.
- Coppari, L., Di Gregorio, M., Corti, C., Merilli, S., Mulargia, M., Cogoni, R., Manenti, R., Ficetola, G.F., Lunghi, E. (2024): Four years monitoring of the endangered European plethodontid salamanders. Sci. Data 11: 706.
- Costa, A., Crovetto, F., Salvidio, S. (2016): European plethodontid salamanders on the forest floor: local abundance is related to fine-scale environmental factors. Herpetol. Conserv. Biol. 11(2): 344-349.
- Culver, D.C., Pipan, T. (2019). The biology of caves and other subterranean habitats. New York, Oxford University Press.
- Davis, T.M., Ovaska, K. (2001): Individual recognition of amphibians: effects of toe clipping and fluorescent tagging on the salamander Plethodon vehiculum. J. Herpetol. 35(2): 217-225.
- Dunn, E.H., Ralph, C.J. (2004): Use of mist nets as a tool for bird population monitoring Stud. Avian Biol. 29: 1-6.
- Ficetola, G.F., Barzaghi, B., Melotto, A., Muraro, M., Lunghi, E., Canedoli, C., Lo Parrino, E., Nanni, V., Silva-Rocha, I., Urso, A., Carretero, M.A., Salvi, D., Scali, S., Scarì, G., Pennati, R., Andreone, F., Manenti, R. (2018a): N-mixture models reliably estimate the abundance of small vertebrates. Sci. Rep. 8: 10357.
- Ficetola, G.F., Lunghi, E., Canedoli, C., Padoa-Schioppa, E., Pennati, R., Manenti, R. (2018b): Differences between microhabitat and broad-scale patterns of niche evolution in terrestrial salamanders. Sci. Rep. 8: 10575.
- Ficetola, G.F., Pennati, R., Manenti, R. (2013): Spatial segregation among age classes in cave salamanders: habitat selection or social interactions? Popul. Ecol. 55: 217-226.
- Fitzpatrick, L.C. (1973): Energy allocation in the Allegheny mountain salamander, Desmognathus ochrophaeu. Ecol. Monogr. 43(1): 43-58.
- Gabor, C.R., Bosch, J., Fries, J.N., Davis, D.R. (2013): A non-invasive water-borne hormone assay for amphibians. Amphib-reptil. 34: 151-162.
- Golay, N., Durrer, H. (1994): Inflammation due to toe-clipping in natterjack toads (Bufo calamita). Amphib-reptil. 15: 81-96.
- Howarth, F.G., Moldovan, O.T. (2018). The ecological classification of cave animals and their adaptations. In: Cave Ecology, pp. 41-67. Moldovan, O.T., Kováč, L.,Halse, S. Berlin, Springer.
- Husain, N., Roy, P., Hussain Trak, T. (2017): Photography as a Conservation Tool in Science. Trends Biosci. 10: 9317-9321.
- Lanza, B., Pastorelli, C., Laghi, P., Cimmaruta, R. (2006): A review of systematics, taxonomy, genetics, biogeography and natural history of the genus Speleomantes Dubois, 1984 (Amphibia Caudata Plethodontidae). Atti Mus. civ. stor. nat. Trieste 52: 5-135.
- Lunghi, E. (2022): Doubling the lifespan of European plethodontid salamanders. Ecology 103(2): 1-4.
- Lunghi, E., Bacci, F., Zhao, Y. (2021a): How can we record reliable information on animal colouration in the wild? Diversity 13: 356.
- Lunghi, E., Bruni, G. (2018): Long-term reliability of Visual Implant Elastomers in the Italian cave salamander (Hydromantes italicus). Salamandra 54(4): 283-286.
- Lunghi, E., Cianferoni, F., Ceccolini, F., Veith, M., Manenti, R., Mancinelli, G., Corti, C., Ficetola, G.F. (2018a): What shapes the trophic niche of European plethodontid salamanders? PLoS ONE 13(10): e0205672.
- Lunghi, E., Cianferoni, F., Corti, C., Zhao, Y., Manenti, R., Ficetola, G.F., Mancinelli, G. (2022): The trophic niche of subterranean populations of Speleomantes italicus: a multi-temporal analysis. Sci. Rep. 12: 18257.
- Lunghi, E., Cianferoni, F., Giachello, S., Zhao, Y., Manenti, R., Corti, C., Ficetola, G.F. (2021b): Updating salamander datasets with phenotypic and stomach content information for two mainland Speleomantes. Sci. Data 8: 150.
- Lunghi, E., Corti, C. (2021): Predation of European cave salamanders (Speleomantes) by the spider Meta bourneti. Spixiana 44(1): 54.
- Lunghi, E., Corti, C., Manenti, R., Barzaghi, B., Buschettu, S., Canedoli, C., Cogoni, R., De Falco, G., Fais, F., Manca, A., Mirimin, V., Mulargia, M., Mulas, C., Muraro, M., Murgia, R., Veith, M., Ficetola, G.F. (2018b): Comparative reproductive biology of European cave salamanders (genus Hydromantes): nesting selection and multiple annual breeding. Salamandra 54(2): 101-108.
- Lunghi, E., Corti, C., Mulargia, M., Zhao, Y., Manenti, R., Ficetola, G.F., Veith, M. (2020a): Cave morphology, microclimate and abundance of five cave predators from the Monte Albo (Sardinia, Italy). Biodivers. Data J. 8: 1-16.
- Lunghi, E., Giachello, S., Manenti, R., Zhao, Y., Corti, C., Ficetola, G.F., Bradley, J.G. (2020b): The post hoc measurement as a safe and reliable method to age and size plethodontid salamanders. Ecol. Evol. 10(20): 11111-11116.
- Lunghi, E., Giachello, S., Zhao, Y., Corti, C., Ficetola, G.F., Manenti, R. (2020c): Photographic database of the European cave salamanders, genus Hydromantes. Sci. Data 7: 171.
- Lunghi, E., Manenti, R., Canciani, G., Scarì, G., Pennati, R., Ficetola, G.F. (2016): Thermal equilibrium and temperature differences among body regions in European plethodontid salamanders. J. Therm. Biol. 60: 79-85.
- Lunghi, E., Manenti, R., Ficetola, G.F. (2015): Seasonal variation in microhabitat of salamanders: environmental variation or shift of habitat selection? PeerJ 3: e1122.
- Lunghi, E., Romeo, D., Mulargia, M., Cogoni, R., Manenti, R., Corti, C., Ficetola, G.F., Veith, M. (2019): On the stability of the dorsal pattern of European cave salamanders (genus Hydromantes). Herpetozoa 32: 249-253.
- Lunghi, E., Zhao, Y. (2020): Do Chinese cavefish show intraspecific variability in morphological traits? Ecol. Evol. 10(14): 7723-7730.
- MacCracken, J.G., Stebbings, J.L. (2012): Test of a Body Condition Index with Amphibians. J. Herpetol. 46(3): 346-350.
- McCravy, K.W. (2018): A review of sampling and monitoring methods for beneficial arthropods in agroecosystems. Insects 9: 170.
- Peig, J., Green, A.J. (2009): New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118: 1883-1891.
- Perry, G., Wallace, M.C., Perry, D., Curzer, H., Muhlberger, P. (2011): Toe clipping of amphibians and reptiles: science, ethics, and the law. J. Herpetol. 45(4): 547-555.
- 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.
- Rosa, G., Costa, A., Renet, J., Romano, A., Roner, L., Salvidio, S. (2021): Energy storage in salamanders’ tails: the role of sex and ecology. Sci. Nat. 108: 27.
- Salvidio, S., Pasmans, F., Bogaerts, S., Martel, A., van de Loo, M., Romano, A. (2017): Consistency in trophic strategies between populations of the Sardinian endemic salamander Speleomantes imperialis. Anim. Biol. 67: 1-16.
- Soto-Azat, C., Clarke, B.T., Fisher, M.C., Walker, S.F., Cunningham, A.A. (2009): Non-invasive sampling methods for the detection of Batrachochytrium dendrobatidis in archived amphibians. Dis. Aquat. Org. 84: 163-166.
- Speybroeck, J., Steenhoudt, K. (2017): A pattern-based tool for long-term, large-sample capture-mark-recapture studies of fire salamanders Salamandra species (Amphibia: Urodela: Salamandridae). Acta Herpetol. 12(1): 55-63.
- Wake, D.B., Dresner, I.G. (1967): Functional morphology and evolution of tail autotomy in salamanders. J. Morphol. 122: 265-306.
- Wilder, S.M., Raubenheimer, D., Simpson, S.J. (2016): Moving beyond body condition indices as an estimate of fitness in ecological and evolutionary studies. Funct. Ecol. 30(1): 108-115.