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

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, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. 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 

  2. 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 

  3. 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 

  4. 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 

  5. 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  PubMed  Google Scholar 

  6. 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 

  7. 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 

  8. 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 

  9. 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 

  10. 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 

  11. 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 

  12. 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 

  13. 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 

  14. 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 

  15. 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 

  16. 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 

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

    Google Scholar 

  18. 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 

  19. 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 

  20. 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 

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

    Google Scholar 

  22. 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 

  23. 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 

  24. 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 

  25. 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 

  26. 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 

  27. 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 

  28. 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 

  29. 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 

  30. 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 

  31. 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 

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

    Google Scholar 

  33. 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.

  34. 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 

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

    Google Scholar 

  36. 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 

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

    Google Scholar 

  38. 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 

  39. 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 

  40. 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 

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

    Google Scholar 

  42. 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 

  43. 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 

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

    PubMed  Google Scholar 

  45. 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 

  46. 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 

  47. 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 

  48. 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 

  49. 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 

  50. 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 

  51. 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 

  52. 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 

  53. 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 

  54. 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 

  55. 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 

  56. 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 

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

    Google Scholar 

  58. 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 

  59. 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 

  60. 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 

  61. 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 

  62. 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 

  63. 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 

  64. 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

Affiliations

Authors

Corresponding author

Correspondence to Marta Vila.

Additional information

Publisher's Note

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

Handling editor: Begoña Santos

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

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

Keywords

  • Diet shifts
  • Interspecific competition
  • Foraging plasticity
  • DNA metabarcoding
  • Changes in stored water volume