Comparison of two non-lethal methods for dietary studies in terrestrial salamanders
Federico Crovetto A , Antonio Romano B and Sebastiano Salvidio A CA DIPTERIS – Università di Genova, Corso Europa 26, I-16132 Genova, Italy.
B Dipartimento di Biologia, Università di Roma ‘Tor Vergata’, Via Della Ricerca Scientifica, I-00133 Roma, Italy.
C Corresponding author. Email: salvidio@dipteris.unige.it
Wildlife Research 39(3) 266-270 https://doi.org/10.1071/WR11103
Submitted: 15 June 2011 Accepted: 8 February 2012 Published: 23 April 2012
Abstract
Context: Concerns about conservation and ethics in amphibian research have been raised recently; therefore, non-lethal methods should always be preferred to investigate food habits in wild populations. However, there are no studies that compared the data obtained by different non-lethal dietary methods in amphibians.
Aims: We compared the dietary habits obtained from stomach flushing, a method validated against stomach dissection, and faecal analysis on the same 31 individuals of the European plethodontid Speleomantes strinatii, a completely terrestrial salamander.
Methods: After being stomach-flushed in the field, salamanders were kept in the laboratory at constant humidity and temperature to obtain faecal samples. Analyses comprised diversity and niche overlap indexes, as well as permutation, repeated-measures tests and graphical methods.
Key results: Niche overlap between the two samples was low (Ojk = 0.58) and prey diversity was significantly (P = 0.001) higher in stomach contents. There were also differences in the abundance of fly larvae, springtails and ants and the interpretation of the population trophic strategy varied according to the sampling method used.
Key conclusions: Stomach flushing and faecal analysis gave different information, because, apparently, a differential prey degradation occurred. During the digestive process, ants became dominant, whereas springtails and fly larvae became under-represented in faecal samples. Therefore, on the basis of faecal analysis, diet diversity was underestimated and many individuals improperly appeared as ant-specialist feeders.
Implications: In terrestrial salamanders, results from stomach flushing and faecal analysis should not be compared among studies, populations or species. Moreover, stomach flushing should always be preferred when assessing the trophic strategy and the role in food webs of salamanders.
Additional keywords: amphibians, animal welfare, food habits, selective digestion.
References
Amundsen, P. A., Gabler, H. M., and Staldvik, F. J. (1996). A new approach to graphical analysis of feeding strategy from stomach contents data – modification of the Costello (1990) method. Journal of Fish Biology 48, 607–614.Angelici, F. M., Luiselli, L., and Ruggiero, L. (1997). Food habits of the green lizard, Lacerta bilineata, in central Italy and a reliability test of faecal pellet analysis. The Italian Journal of Zoology 64, 267–272.
| Food habits of the green lizard, Lacerta bilineata, in central Italy and a reliability test of faecal pellet analysis.Crossref | GoogleScholarGoogle Scholar |
Blaustein, A. R., Han, B. A., Relyea, R. A., Johnson, P. T. J., Buck, J. C., Gervasi, S. S., and Kats, L. B. (2011). The complexity of amphibian population declines: understanding the role of cofactors in driving amphibian losses. Annals of the New York Academy of Sciences 1223, 108–119.
| The complexity of amphibian population declines: understanding the role of cofactors in driving amphibian losses.Crossref | GoogleScholarGoogle Scholar |
Cecala, K. K., Price, S. J., and Dorcas, M. E. (2007). Diet of larval red salamanders (Pseudotriton ruber) examined using a nonlethal technique. Journal of Herpetology 41, 741–745.
| Diet of larval red salamanders (Pseudotriton ruber) examined using a nonlethal technique.Crossref | GoogleScholarGoogle Scholar |
Crump, M. L. (2010). Amphibian diversity and life history. In ‘Amphibian Ecology and Conservation – A Handbook of Techniques’. (Ed. C. K. Dodd Jr.) pp. 3–19. (Oxford University Press: Oxford, UK.)
Daszak, P., Berger, L., Cunningham, A. A., Hyatt, A. D., Green, D. E., and Speare, R. (1999). Emerging infectious diseases and amphibian population declines. Emerging Infectious Diseases 5, 735–748.
| Emerging infectious diseases and amphibian population declines.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2FntVChtQ%3D%3D&md5=2d7e60259ea028332b185808cf665be1CAS |
Diaz, P. H. Jr., (2010). Diet and mesohabitat association of the threatened San Marcos salamander (Eurycea nana). Paper 34. Theses and Dissertations – Biology, Texas University, San Marcos, USA.
Fenolio, D. B., Graening, G. O., Collier, B. A., and Stout, J. F. (2007). Coprophagy in a cave-adapted salamander; the importance of bat guano examined through nutritional and stable isotope analyses. Proceedings. Biological Sciences 273, 439–443.
| Coprophagy in a cave-adapted salamander; the importance of bat guano examined through nutritional and stable isotope analyses.Crossref | GoogleScholarGoogle Scholar |
Fraser, D. F. (1976). Coexistence of salamanders in the genus Plethodon, a variation of the Santa Rosalia theme. Ecology 57, 238–251.
| Coexistence of salamanders in the genus Plethodon, a variation of the Santa Rosalia theme.Crossref | GoogleScholarGoogle Scholar |
Hammer, Ø., Harper, D. A. T., and Ryan, P. D. (2001). PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 1–9.
Hodgkison, S., and Hero, J.-M. (2003). Seasonal, sexual and ontogenetic variations in the diet of the ‘declining’ frogs Litoria nannotis, Litoria rheocola and Nyctimystes dayi. Wildlife Research 30, 345–354.
| Seasonal, sexual and ontogenetic variations in the diet of the ‘declining’ frogs Litoria nannotis, Litoria rheocola and Nyctimystes dayi.Crossref | GoogleScholarGoogle Scholar |
Jaeger, R. G. (1980). Microhabitats of a terrestrial forest salamander. Copeia 1980, 265–268.
Lanza, B., Pastorelli, C., Laghi, P., and Cimmaruta, R. (2005). A review of systematics, taxonomy, genetics, biogeography and natural history of the genus Speleomantes Dubois, 1984 (Amphibia Caudata Plethodontidae). Atti Museo Civico Storia Naturale, Trieste 52, 5–135.
Magurran, A. (2004). ‘Measuring Biological Diversity.’ (Blackwell Publishing: Malden, MA.)
Maiorana, V. C. (1978). Behavior of an unobservable species: diet selection by a salamander. Copeia 1978, 664–672.
| Behavior of an unobservable species: diet selection by a salamander.Crossref | GoogleScholarGoogle Scholar |
May, R. M. (2004). Ethics and amphibians. Nature 431, 403.
| Ethics and amphibians.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnslemurw%3D&md5=407bfa8c4536eecc64fd8445aeab3d29CAS |
McWilliams, S. R., and Bachman, M. (1989). Foraging ecology and prey preference of a pond-form larval small-mouthed salamanders Ambystoma texanum. Copeia 1989, 948–961.
| Foraging ecology and prey preference of a pond-form larval small-mouthed salamanders Ambystoma texanum.Crossref | GoogleScholarGoogle Scholar |
Morisi, A. (1981). Osservazioni sulla dieta in natura del geotritone Hydromantes italicus Dunn (Amphibia Caudata Plethodontidae). Rivista Piemontese Storia Naturale 2, 79–87.
Pérez-Mellado, V., Pérez-Cembranos, A., Garrido, M., Luiselli, L., and Corti, C. (2011). Using faecal samples in lizard dietary studies. Amphibia-Reptilia 32, 1–7.
| Using faecal samples in lizard dietary studies.Crossref | GoogleScholarGoogle Scholar |
Pianka, E. R. (1973). The structure of lizard communities. Annual Review of Ecology and Systematics 4, 53–74.
| The structure of lizard communities.Crossref | GoogleScholarGoogle Scholar |
Regester, K. J., Lips, K. R., and Whiles, M. R. (2006). Energy flow and subsidies associated with the complex life cycle of ambystomatid salamanders in ponds and adjacent forest in southern Illinois. Oecologia 147, 303–314.
| Energy flow and subsidies associated with the complex life cycle of ambystomatid salamanders in ponds and adjacent forest in southern Illinois.Crossref | GoogleScholarGoogle Scholar |
Salvidio, S. (1992). Diet and food utilization in a rock-face population of Speleomantes ambrosii (Amphibia, Caudata, Plethodontidae). Vie et Milieu 42, 35–39.
Siegel, S., and Castellan, N. J. (1988). ‘Nonparametric Statistics for the Behavioral Sciences.’ (McGraw-Hill: New York.)
Solé, M., and Rödder, D. (2010). Dietary assessments of adult amphibians. In ‘Amphibian Ecology and Conservation – A Handbook of Techniques’. (Ed. C. K. Dodd Jr.) pp. 67–84. (Oxford University Press: Oxford, UK.)
Solé, M., Beckmann, O., Pelz, B., Kwet, A., and Engels, W. (2005). Stomach-flushing for diet analysis in anurans: an improved protocol evaluated in a case study in Araucaria forests, southern Brazil. Studies on Neotropical Fauna and Environment 40, 23–28.
| Stomach-flushing for diet analysis in anurans: an improved protocol evaluated in a case study in Araucaria forests, southern Brazil.Crossref | GoogleScholarGoogle Scholar |
Stuart, S. N., Chanson, J. S., Cox, N. A., Young, B. E., Rodriguez, A. S., Fischman, D. L., and Waller, R. W. (2004). Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783–1786.
| Status and trends of amphibian declines and extinctions worldwide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVKitb7E&md5=9a13d04933623c44d363f70fa95732d3CAS |
Trakimas, G., Jardine, T. D., Bariseviciute, R., Garbaras, A., Skipityte, R., and Remeikis, V. (2011). Ontogenetic dietary shifts in European common frog (Rana temporaria) revealed by stable isotopes. Hydrobiologia 675, 87–95.
| Ontogenetic dietary shifts in European common frog (Rana temporaria) revealed by stable isotopes.Crossref | GoogleScholarGoogle Scholar |
Utzeri, C., Antonelli, D., and Angelini, C. (2004). A note on terrestrial activity and feeding in the spectacled salamander, Salamandrina terdigitata (Urodela Salamandridae). Herpetological Bulletin 90, 27–31.
Walton, B. M. (2005). Salamanders in forest-floor food webs: environmental heterogeneity affects the strength of top-down effects. Pedobiologia 49, 381–393.
| Salamanders in forest-floor food webs: environmental heterogeneity affects the strength of top-down effects.Crossref | GoogleScholarGoogle Scholar |
Walton, B. M., Tsatiris, D., and Rivera-Sostre, M. (2006). Salamanders in forest-floor food webs: invertebrate species composition influences top-down effects. Pedobiologia 50, 313–321.
| Salamanders in forest-floor food webs: invertebrate species composition influences top-down effects.Crossref | GoogleScholarGoogle Scholar |
Wanger, T. C., Wielgoss, A. C., Motzke, I., Clough, Y., Brook, B. W., Sodhj, N. S., and Tscharntke, T. (2011). Endemic predators, invasive prey and native diversity. Proceedings. Biological Sciences 278, 690–694.
| Endemic predators, invasive prey and native diversity.Crossref | GoogleScholarGoogle Scholar |
Wells, K. D. (2007). ‘The Ecology and Behavior of Amphibians.’ (The University of Chicago Press: Chicago, IL.)
Wu, Z. J., Li, Y. M., and Wang, Y. P. (2007). A comparison of stomach flush and stomach dissection in diet analysis of four frog species. Acta Zoologica Sinica 53, 364–372.