Larval development and habitat usage of stream-breeding Fire salamanders in an urban environment

  • István Kiss Szent István University, Department of Zoology and Animal Ecology H-2103 Gödöllő, Páter K. u. 1., Hungary https://orcid.org/0000-0002-0821-8667
  • Judit Vörös Hungarian Natural History Museum, Department of Zoology, H-1088 Budapest, Baross u. 13, Hungary https://orcid.org/0000-0001-9707-1443
  • Andrew J. Hamer Institute of Aquatic Ecology, Centre for Ecological Research, H-1113 Budapest, Karolina u. 29., Hungary https://orcid.org/0000-0001-6031-7841
Keywords: aggregation, drifting, larval density, metamorphosis, stream habitat, Salamandra salamandra, urbanisation

Abstract

Urbanisation adversely affects the abiotic and biotic characteristics of watercourses, including freshwater streams that support the development of stream-breeding salamanders. We conducted a study over four years on an isolated fire salamander population inhabiting a stream valley northwest of Budapest, Hungary. Our aim was to understand aspects of larval development and habitat usage within this population. The maximum number of larvae was observed in April and the first weeks of May. Due to drifting caused by heavy rainfall, there was a mean decrease of 63.3% in the number of larvae. The abundance of larval salamanders within 16 stream segments showed strong temporal and spatial variation, and there was a strong relationship between larval abundance and the % cover of fine gravel substrate. Some of the larvae could escape drift by entering pools with slower water flow and shelter. Larvae were predominantly solitary in smaller pools but occasionally aggregated in high numbers in some segments. The first larvae with yellow spots (indicative of metamorphosis) appeared in June, and by early September, all larvae were metamorphosing. Our results show that in this urbanised environment, larval development through to metamorphosis is occurring, but increasing urbanisation and alterations to stream flow threaten the persistence of the local population.

References

Altig, R. & McDiarmid R. W. (1999): Body plan, development and morphology. Pp. 24–51. In: McDiarmid, R. W. & Altig, R. (eds): Tadpoles, the biology of Anuran larvae. – The University of Chicago Press, Chicago, 458 pp.

Arnold, A. (1983): Zur Verbreitung des Feuersalamanders im Tal der Zwickauer Mulde. – Veröffentlichungen aus dem Museum für Naturkunde Karl-Marx-Stadt 12: 71–79.

Barrett, K. & Guyer, C. (2008): Differential responses of amphibians and reptiles in riparian and stream habitats to land use disturbances in western Georgia, USA. – Biological Conservation 141: 2290–2300. https://doi.org/10.1016/j.biocon.2008.06.019

Barrett, K., Helms, B. S., Guyer, C. & Schoonover, J. E. (2010a): Linking process to pattern: causes of stream-breeding amphibian decline in urbanised watersheds. – Biological Conservation 143: 1998–2005. https://doi.org/10.1016/j.biocon.2010.05.001

Barrett, K., Helms, B. S., Samoray, S. T. & Guyer, C. (2010b): Growth patterns of a stream vertebrate differ between urban and forested catchments. – Freshwater Biology 55: 1628–1635. https://doi.org/10.1111/j.1365-2427.2009.02393.x

Baumgartner, N., Waringer A. & Waringer, J. (1999): Hydraulic microdistribution patterns of larval fire salamanders (Salamandra salamandra salamandra) in the Weidlingbach near Vienna, Austria. – Freshwater Biology 41: 31–41. https://doi.org/10.1046/j.1365-2427.1999.00378.x

Brooks, S. P. & Gelman, A. (1998): General methods for monitoring convergence of iterative simulations. – Journal of Computational and Graphical Statistics, 7: 434–455. ­https://doi.org/10.1080/10618600.1998.10474787

Bruce, R. C. (1985): Larval periods, population structure and the effects of stream drift in larvae of the salamanders Desmognathus quadramaculatus and Leurognathus marmoratus in a Southern Appalachian stream. – Copeia 1985: 847–854. https://doi.org/10.2307/1445232

Caspers, B. A., Steinfartz, S. & Krause, E. T. (2015): Larval deposition behaviour and maternal investment of females reflect differential habitat adaptation in a genetically diverging salamander population. – Behavioral Ecology and Sociobiology 69: 407–413. https://doi.org/10.1007/s00265-014-1853-1

Cecala, K. K., Price S. J. & Dorcas, M. E. (2009): Evaluating existing movement predictions in linear systems using larval stream salamanders. – Canadian Journal of Zoology 87: 292–98. https://doi.org/10.1139/Z09-013

Csilléry, K. & Lengyel, S. (2004): Density dependence in stream-dwelling larvae of fire salamander (Salamandra salamandra): a field experiment. Amphibia-Reptilia, 25: 343–349.

Dely, O. Gy. (1967): Kétéltűek–Amphibia, Magyarország Állatvilága. – Fauna Hungariae 20(3), – Akadémia Kiadó, Budapest, 80 pp.

Eitam, A., Blaustein, L. & Mangel, M. (2005): Density and intercohort priority effects on larval Salamandra salamandra in temporary pools. – Oecologia 146: 36–42. https://doi.org/10.1007/s00442-005-0185-2

Gelman, A. & Rubin, D. B. (1992): Inference from iterative simulation using multiple sequences. – Statistical Science 7: 457-472. https://doi.org/10.1214/ss/1177011136

Griffiths, R. G. A. (1996): Newts and Salamanders of Europe. – T & AD Poyser Natural History, London, 188 pp.

Hamer, A. J. & McDonnell, M. J. (2008): Amphibian ecology and conservation in the urbanising world: a review. – Biological Conservation 141: 2432–2449. https://doi.org/10.1016/j.biocon.2008.07.020

Hendrix, R., Schmidt, B. R., Schaub, M., Krause, E. T. & Steinfartz, S. (2017): Differentiation of movement behaviour in an adaptively diverging salamander population. – Molecular Ecology 26: 6400–6413. https://doi.org/10.1111/mec.14345

Heyer, W. R., Donnelly, M. A., Mcdiarmid, R. W., Hyek L-A. C. & Foster, M. S. (eds) (1994): Measuring and monitoring biological diversity: standard methods for amphibians. – Smithsonian Institution Press. Washington and London, 364 pp.

Hutton, J. M., Price, S. J., Bonner, S. J., Richter S. C. & Barton C. D. (2020): Occupancy and abundance of stream salamanders along a specific conductance gradient. – Freshwater Science 39: 433–446. https://doi.org/10.1086/709688

Johnson, B. R. & Wallace, J. B. (2005): Bottom-up limitation of a stream salamander in a detritus-based food web. – Canadian Journal of Fisheries and Aquatic Sciences 62: 301–311. https://doi.org/10.1139/f04-197

Kiss, I., Hamer, A. J. & Vörös, J. (2021): Life history modelling reveals trends in fitness and apparent survival of an isolated Salamandra salamandra population in an urbanised landscape. – European Journal of Wildlife Research 67: 1–16. https://doi.org/10.1007/s10344-021-01521-2

Kiss, I., Vörös, J. & Hamer, J. A. (2022): Movement patterns within an urban population of fire salamanders highlight the importance of conserving small habitat patches. – Journal of Zoology 316: 240–249. https://doi.org/10.1111/jzo.12949

Krause, E. T. & Caspers, B. A. (2015): The influence of a water current on the larval deposition pattern of females of a diverging fire salamander population (Salamandra salamandra). – Salamandra 51: 156–160.

Krause, E. T., Steinfartz, S. & Caspers, B. A. (2011): Poor nutritional conditions during the early larval stage reduce risktaking activities of fire salamander larvae (Salamandra salamandra). – Ethology 117: 416–421. https://doi.org/10.1111/j.1439-0310.2011.01886.x

Lowe, W. H., McPeek, M. A., Likens, G. E. & Cosentino, B. J. (2008): Linking movement behaviour to dispersal and divergence in plethodontid salamanders. – Molecular Ecology 17: 449–4469. https://doi.org/10.1111/j.1365-294X.2008.03928.x

Macklem, D. C., Helton, A. M., Tingley, M. W., Dickson, J. M. & Rittenhouse, T. A. (2020): Stream salamander persistence influenced by the interaction between exurban housing age and development. – Urban Ecosystems 23: 117–132. https://doi.org/10.1007/s11252-019-00883-5

Manenti, R., Denoël, M. & Ficetola, G. F. (2013): Foraging plasticity favours adaptation to new habitats in fire salamanders. – Animal Behaviour 86: 375–382. https://doi.org/10.1016/j.anbehav.2013.05.028

Miller, J. E., Hess, G. R. & Moorman, C. E. (2007): Southern two-lined salamanders in urbanising watersheds. – Urban Ecosystems 10: 73–85. https://doi.org/10.1007/s11252-006-0012-5

Microsoft Corporation (2018): Microsoft Excel.

Naman, S. M., Rosenfeld, J. S. & Richardson, J. S. (2016): Causes and consequences of invertebrate drift in running waters: from individuals to populations and trophic fluxes. – Canadian Journal of Fisheries and Aquatic Sciences 73: 1292–305. https://doi.org/10.1139/cjfas-2015-0363

Paul, M. J., & Meyer, J. L. (2001): Streams in the urban landscape. – Annual Review of Ecology and Systematics 32: 333–365. https://doi.org/10.1007/978-0-387-73412-5_12

Petranka, J. W. (1983): Fish predation: a factor affecting the spatial distribution of a stream-breeding salamander. – Copeia 1983: 624–628. https://doi.org/10.2307/1444326

Plummer, M. (2017): JAGS Version 4.3.0 user manual. Retrieved from https://sourceforge.net/projects/mcmc-jags/files/

Price, S. J., Dorcas, M. E., Gallant, A. L., Klaver, R. W., Willson, J. D. (2006): Three decades of urbanisation: estimating the impact of land-cover change on stream salamander populations. – Biological Conservation 133: 436–441. https://doi.org/10.1016/j.biocon.2006.07.005

QGIS Development Team (2020): QGIS Geographic Information System. – Open Source Geospatial Foundation Project, http://qgis.org/

R Core Team (2019): R: A language and environment for statistical computing. – R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

Rebelo, R. & Leclair, M. H. (2003): Differences in size at birth and brood size among Portuguese populations of the fire alamander, Salamandra salamandra. – Herpetological Journal 13: 179–188.

Reinhardt, T., Baldauf, L., Ilić, M. & Fink, P. (2018): Cast away: drift as the main determinant for larval survival in western fire salamanders (Salamandra salamandra) in headwater streams. – Journal of Zoology 306: 171–179. https://doi.org/10.1111/jzo.12581

Reinhardt, T., Paetzold, A., Steinfartz, S. & Weitere, M. (2013): Linking the evolution of habitat choice to ecosystem functioning: direct and indirect effects of pond-reproducing fire salamanders on aquatic-terrestrial subsidies. – Oecologia 173: 281–291. https://doi.org/10.1007/s00442-013-2592-0

Royle, J. A. (2004): N-mixture models for estimating population size from spatially replicated counts. – Biometrics 60:108-115. https://doi.org/10.1111/j.0006-341X.2004.00142.x

Royle, J. A., Nichols, J. D. & Kéry, M. (2005): Modelling occurrence and abundance of species when detection is imperfect. – Oikos 110: 353–359. https://doi.org/10.1111/j.0030-1299.2005.13534.x

Royle, J.A., Dorazio, R.M. (2008): Hierarchical modeling and inference in ecology: the analysis of data from populations, metapopulations and communities. – Academic Press, London, 444 pp. https://doi.org/10.1016/B978-0-12-374097-7.50001-5

Schafft, M., Wagner, N., Schuetz, T. & Veith, M. (2022): A near-natural experiment on factors influencing larval drift in Salamandra salamandra. – Scientific Reports 12: 1–10. https://doi.org/10.1038/s41598-022-06355-9

Schmidt, B. R., G. Gschwend, J. A. Bachmann & P. Dermond (2015): Use of removal sampling to estimate abundance of larval fire salamanders (Salamandra salamandra) in streams. – Amphibia-Reptilia 36: 87–92. https://doi.org/10.1163/15685381-00002981

Steinfartz, S., Weitere, M. & Tautz, D. (2007): Tracing the first step to speciation: ecological and genetic differentiation of a salamander population in a small forest. – Molecular Ecology 16: 4550–4561. https://doi.org/10.1111/j.1365-294X.2007.03490.x

Su, Y. & Yajima, M. (2015): Package ‘R2jags’: using R to run ‘JAGS’. Version 0.5-7. http://CRAN.R-project.org/package=R2jags

Szabó, I. (1959): Contributions á l’oecologie de la Salamandre tachetée (Salamandra salamandra L.). – Vertebrata Hungarica 1: 35–48.

Thiesmeier, B. & Schuhmacher, H. (1990): Causes of larval drift of the fire salamander, Salamandra salamandra terrestris, and its effects on population dynamics. – Oecologia 82: 259–263. https://doi.org/10.1007/BF00323543

Thiesmeier, B. & Sommerhäuser, M. (1995): Larvalökologische Merkmale einer Feuersalamanderpopulation (Salamandra salamandra terrestris) eines temporären Fließgewässers im nordwestdeutschen Tiefland. – Zeitschrift für Feldherpetologie 2: 23–35.

Thiesmeier, B. (1992): Ökologie des Feuersalamanders. – Westarp Wissenschaften, Essen, 125 pp.

Thiesmeier, B. (2004): Der Feuersalamander. 1st edn. – Bielefeld: Laurenti Verlag, 192 pp.

Thiesmeier, B., & Grossenbacher, K. (2004): Salamandra salamandra (Linnaeus, 1758) Feuersalamander. Pp. 1059–1132. In: Thiesmeier, B. & Grossenbacher, K. (eds): Handbuch der Reptilien und Amphibien Europas: Band 4/IIB Schwanzlurche, Urodela III. – Aula Verlag Germany, Wiesbaden, 391 pp.

Veith, M. (1996): Feuersalamander - Salamandra salamandra (Linnaeus, 1758). Pp. 65–82. In: Bitz, A., Fischer, K. Simon, L. Thiele, R. & Veith M. (eds): Die Amphibien und Reptilien in Rheinland-Pfalz. – GNOR-Eigenverlag, Nassau, 312 pp.

Veith, M., Baubkus, M., Kugel, S., Kulpa, C., Reifenrath, T., Schafft, M. & Wagner, N. (2019): Drift compensation in larval European fire salamanders, Salamandra salamandra (Amphibia: Urodela)? – Hydrobiologia 828: 315–325. https://doi.org/10.1007/s10750-018-3820-8

Vörös, J., Dankovics, R., Harmos, K., Dobay, G., Kiss, I. (2010): A foltos szalamandra (Salamandra salamandra) előfordulása és természetvédelmi helyzete Magyarországon. – Állattani Közlemények 95: 121–149.

Vörös, J., Kiss, I. & Puky, M. (2015): Conservation and decline of amphibians in Hungary. pp. 99–130. In: Heatwole, H. & Wilkinson, J. W. (eds): Amphibian Biology, Volume 11: Status of Conservation and Decline of Amphibian: Eastern Hemisphere, Part 4: Southern Europe and Turkey – Pelagic Publishing, Exeter, UK, 158 pp.

Vörös, J., Ursenbacher, S., Kiss, I., Jelić, D., Schweiger, S., Szabó, K. (2016): Increased genetic structuring of isolated Salamandra salamandra populations (Caudata: Salamandridae) at the margins of the Carpathian Mountains. – Journal of Zoological Systematics and Evolutionary Research 55: 138–149. https://doi.org/10.1111/jzs.12157

Wagner, N., Pfrommer, J. & Veith, M. (2020): Comparison of different methods to estimate abundances of larval fire salamanders (Salamandra salamandra) in first-order creeks. – Salamandra 56: 265–274.

Walsh, C. J., Roy, A. H., Feminella, J. W., Cottingham, P. D., Groffman, P. M. & Morgan, R. P. (2005): The urban stream syndrome: current knowledge and the search for a cure. – Journal of the North American Benthological Society 24: 706–723. https://doi.org/10.1899/04-028.1

Walsh, C. J., Sharpe, A. K. Breen, P. F. & Sonneman, J. A. (2001): Effects of urbanisation on streams of the Melbourne region, Victoria, Australia. I. Benthic macroinvertebrate communities. – Freshwater Biology 46: 535–551. https://doi.org/10.1046/j.1365-2427.2001.00690.x

Weitere, M., Tautz, D., Neumann, D. & Steinfartz, S. (2004): Adaptive divergence vs. environmental plasticity: tracing local genetic adaptation of metamorphosis traits in salamanders. – Molecular Ecology 13: 1665–1677. https://doi.org/10.1111/j.1365-294X.2004.02155.x

Wenger, S.J., Freeman, M.C. (2008): Estimating species occurrence, abundance, and detection probability using zero-inflated distributions. – Ecology 89: 2953–2959. https://doi.org/10.1890/07-1127.1

Werner, P., Lötters, S.& Schmidt B. R. (2014): Analysis of habitat determinants in contact zones of parapatric European salamanders. – Journal of Zoology 292: 31–38. https://doi.org/10.1111/jzo.12079

Willson, J. D., Dorcas, M. E. (2003): Effects of habitat disturbance on stream salamanders: implications for buffer zones and watershed management. – Conservation Biology 17: 763–771. https://doi.org/10.1046/j.1523-1739.2003.02069.x

Published
2022-10-28
How to Cite
KissI., VörösJ., & HamerA. J. (2022). Larval development and habitat usage of stream-breeding Fire salamanders in an urban environment. Acta Zoologica Academiae Scientiarum Hungaricae, 68(4), 321-340. https://doi.org/10.17109/AZH.68.4.321.2022