Skip to main content
SpringerLink
Log in

Determinants of Eurasian otter (Lutra lutra) diet in a seasonally changing reservoir

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Otter diet in reservoirs is known to experience seasonal changes. We selected a reservoir with a large population of exclusively wintering great cormorants and seasonal changes in stored water volume to test the relative influence of abiotic and biotic factors on otter foraging ecology. DNA metabarcoding of otter spraints revealed a dietary change from autumn to winter. Otters had a diet dominated by the exotic goldfish in autumn, but predated intensively on the native northern straight-mouth nase in winter. This change was likely caused by predation of cormorants on goldfish and to fish biology. Secondly, macroscopic analysis of spraints revealed that otters shifted from a diet dominated by fish (in terms of biomass) to a diet dominated by red swamp crayfish during spring–summer, when the latter became overabundant. As revealed by modelling, this second shift was most likely influenced by the sudden increase in stored water volume in spring, but also by the cumulative effect of cormorant predation on fish during autumn–winter. Macroscopic analyses of otter spraints collected in a second reservoir with no cormorants revealed a lack of seasonality. Hence, the combined influence of both biotic and abiotic factors explained otter diet seasonality in a lentic-water novel ecosystem.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Altschul, S. F., W. Gish, W. Miller, E. W. Myers & D. J. Lipman, 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403–410.

    CAS  PubMed  Google Scholar 

  • Andreu-Soler, A., F. J. Oliva-Paterna & M. Torralva, 2006. A review of length–weight relationships of fish from the Segura River basin (SE Iberian Peninsula). Journal of Applied Ichthyology 22: 295–296.

    Google Scholar 

  • Augas de Galicia, 2009. Asistencia técnica para la toma de datos del indicador biológico peces en las redes de monitorización de aguas superficiales en el ámbito de la demarcación hidrográfica Galicia-costa (Expte. OH.688.244.SV). Consellería de Medio Ambiente, Territorio e Infraestructuras, Xunta de Galicia.

    Google Scholar 

  • Ayres, C. & P. García, 2009. Abandoned clay mines: an opportunity for Eurasian otters in NW Spain. IUCN Otter Specialist Group Bulletin 26: 67–72.

    Google Scholar 

  • Bartram, J., E. Mountjoy, T. Brooks, J. Hancock, H. Williamson, G. Wright, J. Moppett, N. Goulden & M. Hubank, 2016. Accurate sample assignment in a multiplexed, ultrasensitive, high-throughput sequencing assay for minimal residual disease. Journal of Molecular Diagnostics 18: 494–506.

    CAS  Google Scholar 

  • Basto, M. P., N. M. Pedroso, A. Mira & M. Santos-Reis, 2011. Use of small and medium-sized water dams by otters in a Mediterranean ecosystem. Animal Biology 61: 75–94.

    Google Scholar 

  • Beja, P. R., 1996a. An analysis of otter Lutra lutra predation on introduced American crayfish Procambarus clarkii in Iberian streams. Journal of Applied Ecology 33: 1156–1170.

    Google Scholar 

  • Beja, P. R., 1996b. Temporal and spatial patterns of rest-site use by four female otters Lutra lutra along the southwest coast of Portugal. Journal of Zoology 239: 741–753.

    Google Scholar 

  • Berry, O., C. Bulman, M. Bunce, M. Coghlan, D. C. Murray & R. D. Ward, 2015. Comparison of morphological and DNA metabarcoding analyses of diets in exploited marine fishes. Marine Ecology Progress Series 540: 167–181.

    CAS  Google Scholar 

  • Blanco-Garrido, F., J. Prenda & M. Narvaez, 2008. Eurasian otter (Lutra lutra) diet and prey selection in Mediterranean streams invaded by centrarchid fishes. Biological Invasions 10: 641–648.

    Google Scholar 

  • Bokulich, N. A., S. Subramanian, J. J. Faith, D. Gevers, J. I. Gordon, R. Knight, D. A. Mills & J. G. Caporaso, 2013. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nature Methods 10: 57–59.

    CAS  PubMed  Google Scholar 

  • Bouroş, G. & D. Murariu, 2017. Comparative diet analysis of the Eurasian otter (Lutra lutra) in different habitats: Putna-Vrancea Natural Park and Lower Siret Valley, south-eastern Romania. North-Western Journal of Zoology 13: 311–319.

    Google Scholar 

  • Britton, J. R., M. Berry, S. Sewell, C. Lees & P. Reading, 2017. Importance of small fishes and invasive crayfish in otter Lutra lutra diet in an English chalk stream. Knowledge and Management of Aquatic Ecosystems 418: 13.

    Google Scholar 

  • Caporaso, J. G., J. Kuczynski, J. Stombaugh, K. Bittinger, F. D. Bushman, E. K. Costello, N. Fierer, A. Gonzalez Peña, J. K. Goodrich, J. I. Gordon, G. A. Huttley, S. T. Kelley, D. Knights, J. E. Koenig, R. E. Ley, C. A. Lozupone, D. McDonald, B. D. Muegge, M. Pirrung, J. Reeder, J. R. Sevinsky, P. J. Turnbaugh, W. A. Walters, J. Widmann, T. Yatsunenko, J. Zaneveld & R. Knight, 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7: 335–336.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carss, D. N. & S. G. Parkinson, 1996. Errors associated with otter Lutra lutra faecal analysis I. Assessing general diet from spraints. Journal of Zoology 238: 301–317.

    Google Scholar 

  • Čech, M. & L. Vejřík, 2011. Winter diet of great cormorant (Phalacrocorax carbo) on the river Vltava: estimate of size and species composition and potential for fish stock losses. Folia Zoologica 60: 129–142.

    Google Scholar 

  • Chanin, P., 2003. Ecology of the European Otter. Conserving Natura 2000 Rivers Ecology Series No. 10. English Nature, Peterborough.

    Google Scholar 

  • Clavero, M., J. Prenda & M. Delibes, 2003. Trophic diversity of the otter (Lutra lutra L.) in temperate and Mediterranean freshwater habitats. Journal of Biogeography 20: 761–769.

    Google Scholar 

  • De Barba, M., C. Miquel, F. Boyer, C. Mercier, D. Rioux, E. Coissac & P. Taberlet, 2014. DNA metabarcoding multiplexing and validation of data accuracy for diet assessment: application to omnivorous diet. Molecular Ecology Resources 14: 306–323.

    PubMed  Google Scholar 

  • De Lima, F. T., D. A. Reynalte-Tataje & E. Zaniboni-Filho, 2017. Effects of reservoirs water level variations on fish recruitment. Neotropical Ichthyology 15: e160084.

    Google Scholar 

  • Delibes, M. (ed), 1990. La nutria (L. lutra) en España. ICONA Serie Técnica, Madrid.

    Google Scholar 

  • Doadrio, I., S. Perea, P. Garzón-Heydt & J. L. González, 2011. Ictiofauna continental española. Bases para su seguimiento. DG Medio Natural y Política Forestal. MARM, Madrid.

    Google Scholar 

  • Eckman, R. & F. Imbrock, 1996. Distribution and diel vertical migration of Eurasian perch (Perca fluviatilis) during winter. Annales Zoologici Fennici 33: 679–686.

    Google Scholar 

  • Edgar, R. C., 2004a. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792–1797.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Edgar, R. C., 2004b. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.

    PubMed  PubMed Central  Google Scholar 

  • Edgar, R. C., B. J. Haas, J. C. Clemente, C. Quince & R. Knight, 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194–2200.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Esling, P., F. Lejzerowicz & J. Pawlowski, 2015. Accurate multiplexing and filtering for high-throughput amplicon-sequencing. Nucleic Acids Research 43: 2513–2524.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandes, C. A., C. Ginja, I. Pereira, R. Tenreiro, M. W. Bruford & M. Santos-Reis, 2008. Species-specific mitochondrial DNA markers for identification of non-invasive samples from sympatric carnivores in the Iberian Peninsula. Conservation Genetics 9: 681–690.

    CAS  Google Scholar 

  • Fernández-Álvarez, F. Á., A. Machordom, R. García-Jiménez, C. A. Salinas-Zavala & R. Villanueva, 2018. Predatory flying squids are detritivores during their early planktonic life. Scientific Reports 8: 3440.

    PubMed  PubMed Central  Google Scholar 

  • Galán, P., 1997. Declive de poblaciones de anfibios en dos embalses de La Coruña (Noroeste de España) por introducción de especies exóticas. Boletín de la Asociación Herpetológica Española 8: 38–40.

    Google Scholar 

  • Hobbs, R., 2018. Novel ecosystems: can’t we just pretend they’re not there? In Kareiva, P., M. Marvier & B. Silliman (eds), Effective conservation science: data not dogma. Oxford University Press, Oxford: 45–50.

    Google Scholar 

  • Janzen, D. H., 1985. On ecological fitting. Oikos 45: 308–310.

    Google Scholar 

  • Jiménez, J., 2005. Ecology of the otter in tributaries of the river Ebro subjected to strong fluctuations of resources. PhD Dissertation. University of Valencia, Spain.

  • Kean, E. F., C. T. Müller & E. A. Chadwick, 2011. Otter scent signals age, sex, and reproductive status. Chemical Senses 36: 555–564.

    CAS  PubMed  Google Scholar 

  • Klimaszyk, P. & P. Rzymski, 2016. The complexity of ecological impacts induced by great cormorants. Hydrobiologia 771: 13–30.

    Google Scholar 

  • Krawczyk, A. J., M. Bogdziewicz, K. Majkowska & A. Glazaczow, 2016. Diet composition of the Eurasian otter Lutra lutra in different freshwater habitats of temperate Europe: a review and meta-analysis. Mammal Review 46: 106–113.

    Google Scholar 

  • Kruuk, H., 2006. Otters: ecology, behavior and conservation. Oxford University Press, Oxford.

    Google Scholar 

  • Kruuk, H. & A. Moorhouse, 1990. Seasonal and spatial differences in food selection by otters (Lutra lutra) in Shetland. Journal of Zoology 221: 621–637.

    Google Scholar 

  • Kuczynski, L., M. Chevalier, P. Laffaille, M. Legrand & G. Grenouillet, 2017. Indirect effect of temperature on fish population abundances through phenological changes. PLoS ONE 12: e0175735.

    PubMed  PubMed Central  Google Scholar 

  • Lanszki, J., I. Lehoczky, A. Kotze & M. J. Somers, 2016. Diet of otters (Lutra lutra) in various habitat types in the Pannonian biogeographical region compared to other regions of Europe. PeerJ 4: e2266.

    PubMed  PubMed Central  Google Scholar 

  • López-Martín, J. M. & J. Jiménez (eds), 2009. La nutria en España, veinte años de seguimiento de un mamífero amenazado. SECEM, Málaga.

    Google Scholar 

  • Lyach, R. & M. Čech, 2017. Do otters target the same fish species and sizes as anglers? A case study from a lowland trout stream (Czech Republic). Aquatic Living Resources 30: 11.

    Google Scholar 

  • Magoc, T. & S. L. Salzberg, 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27: 2957–2963.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martínez-Abraín, A. & J. Jiménez, 2016. Anthropogenic areas as incidental substitutes for original habitat. Conservation Biology 30: 593–598.

    PubMed  Google Scholar 

  • Mouriño, J., X. L. Otero, R. Salvadores, P. Alonso, F. Sierra-Abraín & F. Arcos, 2004. Los espacios naturales de Galicia. Edicións Nigra Trea S.L., Vigo.

    Google Scholar 

  • Mumma, M. A., J. R. Adams, C. Zieminski, T. K. Fuller, S. P. Mahoney & L. P. Waits, 2016. A comparison of morphological and molecular diet analyses of predator scats. Journal of Mammalogy 97: 112–120.

    Google Scholar 

  • Nichols, R. V., M. Åkesson & P. Kjellander, 2016. Diet assessment based on rumen contents: a comparison between DNA metabarcoding and macroscopy. PLoS ONE 11: e0157977.

    PubMed  PubMed Central  Google Scholar 

  • Noordhuis, R., 2002. The river Otter (Lontra canadensis) in Clarcke County (Georgia, USA)—survey, food habits and environmental factors. IUCN Otter Specialist Group Bulletin 19: 75–86.

    Google Scholar 

  • Oja, R., E. Soe, H. Valdmann & U. Saarma, 2017. Non-invasive genetics outperforms morphological methods in faecal dietary analysis, revealing wild boar as a considerable conservation concern for ground-nesting birds. PLoS ONE 12: e0179463.

    PubMed  PubMed Central  Google Scholar 

  • Orta, J., E. F. J. Garcia, F. Jutglar, G. M. Kirwan & P. Boesman, 2018. Great Cormorant (Phalacrocorax carbo). In del Hoyo, J., A. Elliott, J. Sargatal, D. A. Christie & W. de Juana (eds), Handbook of the Birds of the World Alive. Lynx Edicions, Barcelona.

    Google Scholar 

  • Palmeirim, A. F., C. A. Peres & F. C. W. Rosas, 2014. Giant otter population responses to habitat expansion and degradation by a mega hydroelectric dam. Biological Conservation 174: 30–38.

    Google Scholar 

  • Pedroso, N. M. & M. Santos-Reis, 2006. Summer diet of Eurasian otters in large dams of South Portugal. Hystrix, the Italian Journal of Mammalogy 17: 117–128.

    Google Scholar 

  • Pedroso, N. M., T. A. Marques & M. Santos-Reis, 2014. The response of otters to environmental changes imposed by the construction of large dams. Aquatic Conservation: Marine and Freshwater Ecosystems 24: 66–80.

    Google Scholar 

  • Remonti, L., C. Prigioni, A. Balestrieri & G. Priore, 2008. Trophic flexibility of the otter (Lutra lutra) in southern Italy. Mammalian Biology 73: 293–302.

    Google Scholar 

  • Roos, A., A. Loy, P. de Silva, P. Hajkova & B. Zemanová, 2015. Lutra lutra. The IUCN Red List of Threatened Species 2015: e.T12419A21935287.

    Google Scholar 

  • Rozen, S. & H. J. Skaletsky, 2000. Primer3 on the WWW for general users and for biologist programmers. In Krawetz, S. & S. Misener (eds), Bioinformatics Methods and Protocols: Methods in Molecular Biology. Humana Press, Totowa, NJ: 365–386.

    Google Scholar 

  • Ruiz-Olmo, J. & M. Delibes (eds), 1998. La nutria en España ante el horizonte del año 2.000. SECEM, Málaga.

    Google Scholar 

  • Ruiz-Olmo, J. & S. Palazón, 1997. The diet of the otter (Lutra lutra) in Mediterranean freshwater habitats. Journal of Wildlife Research 2: 171–181.

    Google Scholar 

  • Sales-Luis, T., N. M. Pedroso & M. Santos-Reis, 2007. Prey availability and diet of the Eurasian otter (Lutra lutra) on a large dam and associated tributaries. Canadian Journal of Zoology 85: 1125–1135.

    Google Scholar 

  • Schäffer, S., F. E. Zachos & S. Koblmüller, 2017. Opening the treasure chest: a DNA-barcoding primer set for most higher taxa of Central European birds and mammals from museum collections. PLoS ONE 12: e0174449.

    PubMed  PubMed Central  Google Scholar 

  • Taberlet, P., E. Coissac, R. Pompanon, C. Brochmann & E. Willerslev, 2012. Towards next-generation biodiversity assessment using DNA metabarcoding. Molecular Ecology 21: 2045–2050.

    CAS  PubMed  Google Scholar 

  • Thalinger, B., J. Oehm, H. Mayr, A. Obwexer, C. Zeisler & M. Traugott, 2016. Molecular prey identification in Central European piscivores. Molecular Ecology Resources 16: 123–137.

    CAS  PubMed  Google Scholar 

  • Vierna, J., J. Doña, A. Vizcaíno, D. Serrano & R. Jovani, 2017. PCR cycles above routine numbers do not compromise high-throughput DNA barcoding results. Genome 60: 868–873.

    CAS  PubMed  Google Scholar 

  • Weinberger, I. C., S. Muff, A. de Jongh, A. Kranz & F. Bontadina, 2016. Flexible habitat selection paves the way for a recovery of otter populations in the European Alps. Biological Conservation 199: 88–95.

    Google Scholar 

Download references

Acknowledgements

Fish samples to be used as positive controls for molecular analysis were kindly provided by Carlos Antunes, except for O. mykiss and Atlantic salmon S. salar that were purchased at a local fish market. David Stanton generously provided us with four otter tissue samples used during DNA metabarcoding optimisation. EMALCSA kindly provided data on water-level variation and Xunta de Galicia (Consellería de Medio Ambiente e Ordenación do Territorio) allowed us to have a copy of an unpublished report with detailed information about the structure of the fish community at the study reservoir. The long-term time series on great cormorant counts at the study reservoir was supplied by Xunta de Galicia (Dirección de Patrimonio Natural). Pablo Sierra helped us during field work at Eiras reservoir. We are thankful to Ignacio Doadrio, Juan Jiménez, Daniel Oro, three editors, Martin Čech and two anonymous referees for their valuable comments and suggestions. This work received funding from Xunta de Galicia (Grants GRC2014/050 and ED431C 2018/57) and Universidade da Coruña. A Martínez-Abraín was supported by an Isidro Parga Pondal research contract by Xunta de Galicia during the period 2011–2016.

Author information

Authors and Affiliations

  1. Departamento de Bioloxía, Facultade de Ciencias, Universidade da Coruña, Campus da Zapateira, 15008, A Coruña, Spain

    Alejandro Martínez-Abraín, Carlos Veloy, Moraima Amboage, Amanda Guitián-Caamaño & Marta Vila

  2. AllGenetics & Biology SL, Edificio CICA, Campus de Elviña, 15008, A Coruña, Spain

    Neus Marí-Mena, Antón Vizcaíno & Joaquín Vierna

  3. School of Ocean Sciences, Bangor University, Menai Bridge, Anglesey, LL59 5AB, UK

    Charlie Key

Authors
  1. Alejandro Martínez-Abraín
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Neus Marí-Mena
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Antón Vizcaíno
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joaquín Vierna
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carlos Veloy
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Moraima Amboage
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Amanda Guitián-Caamaño
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Charlie Key
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Marta Vila
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marta Vila.

Additional information

Handling editor: Begoña Santos

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martínez-Abraín, A., Marí-Mena, N., Vizcaíno, A. et al. Determinants of Eurasian otter (Lutra lutra) diet in a seasonally changing reservoir. Hydrobiologia 847, 1803–1816 (2020). https://doi.org/10.1007/s10750-020-04208-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-020-04208-y

Keywords

Search

Navigation