Advertisement

Isotopic niche of the Neotropical otter, Lontra longicaudis (Carnivora, Mustelidae), in different coastal aquatic systems in southern Brazil

  • Thayara S. CarrascoEmail author
  • Silvina Botta
  • Rodrigo Machado
  • Paulo C. Simões-Lopes
  • Oldemar Carvalho-Junior
  • Paulo H. Ott
  • Elton P. Colares
  • Eduardo R. Secchi
Primary Research Paper
  • 27 Downloads

Abstract

The Neotropical otter, Lontra longicaudis, is an opportunistic species usually found in freshwater habitats; however, it has also been recorded in environments with marine influence (e.g., islands and estuaries). Thus, we hypothesized that the isotopic niche of the Neotropical otter is wider in a coastal island (Santa Catarina Island—SC) and in a river basin composed of a series of lagoons and an estuary (Tramandaí River Basin—RS) than in a wetland (Taim Wetland—RS) due a greater occurrence of the species in the marine environment of the former areas. In order to test this hypothesis, the stable isotope ratios of carbon and nitrogen in otter samples from different regions were analyzed. Long-term isotopic niche of otters was wider in Santa Catarina Island, followed by Taim Wetland, and Lagunar System of Tramandaí. Therefore, we conclude that otters from Santa Catarina Island and Taim Wetland use both freshwater and marine environments as foraging areas. The sampled otters of the Lagunar System of Tramandaí, on the other hand, used predominantly freshwater environments to forage. The differences found among the otters from different regions are probably related to a variety of factors, such as landscape characteristics, sampling and prey availability.

Keywords

Carbon Diet Habitat use Nitrogen Stable isotopes 

Notes

Acknowledgements

We are thankful to the Laboratório de Ecologia e Conservação da Megafauna Marinha—ECOMEGA (Universidade Federal do Rio Grande—FURG) for all the logistical support during the study. We are also grateful to the researchers from Grupo de Estudos de Mamíferos Aquáticos do Rio Grande do Sul—GEMARS, Laboratório de Mamíferos Aquáticos—LAMAQ (Universidade Federal de Santa Catarina—UFSC), Projeto Lontra (Instituto Ekko Brasil—IEB), Núcleo de Educação e Monitoramento Ambiental—NEMA, and Centro de Estudos Costeiros, Limnológicos e Marinhos—CECLIMAR (Universidade Federal do Rio Grande do Sul—UFRGS) for providing otter and prey samples. ESEC do Taim (Instituto Chico Mendes—ICMBio) also provided logistical support for sampling at the Taim Wetland. Finally, we are grateful to Dr. Leandro Bugoni and Dr. Marcelo Lopes Rheingantz for their critical review of a previous version of this manuscript. T.S.C. received a scholarship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—CAPES. E.R.S. is a Research Fellow (PQ 307843/2014-0) of the Conselho Nacional para Desenvolvimento Científico e Tecnológico (CNPq), Brazilian Government. This study is a contribution of the Research Group “ECOMEGA/CNPq.”

Supplementary material

10750_2019_3931_MOESM1_ESM.docx (21 kb)
Supplementary material 1 (DOCX 21 kb)

References

  1. Alarcon, G. G. & P. C. Simões-Lopes, 2003. Preserved versus degraded coastal environments: a case study of the Neotropical otter in the Environmental Protection Area of Anhatomirim, Southern Brazil. IUCN Otter Specialist Group Bulletin 20: 6–18.Google Scholar
  2. Alarcon, G. G. & P. C. Simões-Lopes, 2004. The Neotropical otter Lontra longicaudis deeding habits in a marine coastal area, southern Brazil. IUCN Otter Specialist Group Bulletin 21: 24–30.Google Scholar
  3. Araújo, M. S., D. I. Bolnick & C. A. Layman, 2011. The ecological causes of individual specialization. Ecology Letters 14: 948–958.PubMedCrossRefGoogle Scholar
  4. Artioli, L. G. S., 2012. As assembleias de peixes da zona litoral de lagoas costeiras subtropicais do sistema do Rio Tramandaí/RS: aspectos amostrais, variações espaciais e temporais de descritores ecológicos e suas relações com a variabilidade ambiental. Universidade Federal do Rio Grande do Sul – UFRGS. Programa de Pós-graduação em Biologia Animal.Google Scholar
  5. Bagchi, S., S. P. Goyal & K. Sankar, 2003. Prey abundance and prey selection by tigers (Panthera tigris) in a semi-arid, dry deciduous forest in western India. Journal of Zoology, London 260: 285–290.CrossRefGoogle Scholar
  6. Barbieri, F., R. Machado, C. A. Zappes & L. R. Oliveira, 2012. Interactions between the Neotropical otter (Lontra longicaudis) and gillnet fishery in the southern Brazilian coast. Ocean & Coastal Management 63: 16–23.CrossRefGoogle Scholar
  7. Barros, N. B. & R. S. Wells, 1998. Prey and feeding patterns of resident bottlenose dolphins (Tursiops truncatus) in Sarasota Bay, Florida. Journal of Mammalogy 79: 1045–1059.CrossRefGoogle Scholar
  8. Ben-David, M., R. W. Flynn & D. M. Schell, 1997. Annual and seasonal changes in diets of martens: evidence from stable isotopes analysis. Oecologia 111: 280–291.PubMedCrossRefGoogle Scholar
  9. Bocherens, H. & D. G. Drucker, 2013. Terrestrial teeth and bones. In Elias, S. A. & C. J. Mock (eds), Encyclopedia of Quaternary Science, 2nd ed. Elsevier, Amsterdam: 304–314.CrossRefGoogle Scholar
  10. Bodkin, J. L., J. A. Ames, R. J. Jameson, A. M. Johnson & G. M. Matson, 1997. Estimating age of Sea otters with cementum layers in the first premolar. Journal of Wildlife Management 61: 967–973.CrossRefGoogle Scholar
  11. Bolnick, D. I., R. Svanbäck, M. S. Araújo & L. Persson, 2007. Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. Proceedings of the National Academy of Sciences of the United States of America 104: 10075–10079.PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bouzon, J. L., J. P. Salles, Z. Bouzon & P. A. Horta, 2006. Aspectos florísticos e fitogeográficos das macroalgas marinhas das baías da Ilha de Santa Catarina, SC, Brasil. Insula 35: 69–84.Google Scholar
  13. Britto, V. O. & L. Bugoni, 2015. The contrasting feeding ecology of the great egrets and roseate spoonbills in limnetic and estuarine colonies. Hydrobiologia 744: 187–210.CrossRefGoogle Scholar
  14. Buchheister, A. & R. J. Latour, 2010. Turnover and fractionation of carbon and nitrogen stable isotopes in tissues of a migratory coastal predator, summer flounder (Paralichthys dentatus). Canadian Journal of Fisheries and Aquatic Sciences 67: 445–461.CrossRefGoogle Scholar
  15. Carlisle, A. B., S. L. Kim, B. X. Semmens, D. J. Madigan, S. J. Jorgensen, C. R. Perle, S. D. Anderson, T. K. Chapple, P. E. Kanive & B. A. Block, 2012. Using stable isotope analysis to understand the migration and trophic ecology of northeastern Pacific white sharks (Carcharodon carcharias). PLoS ONE 7: 1–15.CrossRefGoogle Scholar
  16. Caro, T. M. & C. J. Stoner, 2003. The potential for interspecific competition among African carnivores. Biological Conservation 110: 67–75.CrossRefGoogle Scholar
  17. Carrasco, T. S., S. Botta, R. Machado, E. P. Colares & E. R. Secchi, 2018. Effects of acidification on the isotopic rations of Neotropical otter tooth dentin. Rapid Communications in Mass Spectrometry 32: 784–788.PubMedCrossRefGoogle Scholar
  18. Carvalho-Junior, O., A. B. Birolo & L. C. P. Macedo-Soares, 2010. Ecological aspects of Neotropical otter (Lontra longicaudis) in Peri Lagoon, south Brazil. IUCN Otter Specialist Group Bulletin 27: 105–115.Google Scholar
  19. Carvalho-Junior, O., A. Fillipini & C. Salvador, 2012. Distribution of Neotropical otter Lontra longicaudis (Olfers, 1818) (Mustelidae) in coastal islands of Santa Catarina, Southern Brazil. IUCN Otter Specialist Group Bulletin 29: 95–108.Google Scholar
  20. Carvalho-Junior, O., L. Macedo-Soares, A. B. Birolo & T. Snyder, 2013. A comparative diet analysis of the Neotropical otter in Santa Catarina Island, Brazil. IUCN Otter Specialist Group Bulletin 30: 67–77.Google Scholar
  21. Castro, R. L., F. Saporiti, D. G. Vales, N. A. García, L. Cardona & E. A. Crespo, 2015. Feeding ecology of dusky dolphins Lagenorhynchus obsurus: evidence from stable isotopes. Journal of Mammalogy 97: 310–320.CrossRefGoogle Scholar
  22. Caut, S., E. Angulo & F. Courchamp, 2007. Discrimination factors (∆15N and ∆13C) in an omnivorous consumer: effect of diet isotopic ratio. Functional Ecology 22: 255–263.CrossRefGoogle Scholar
  23. Caut, S., E. Angulo & F. Courchamp, 2009. Variation in discrimination factors (∆15N and ∆13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46: 443–453.CrossRefGoogle Scholar
  24. Chemes, S. B., A. R. Giraudo & G. Gil, 2010. Dieta de Lontra longicaudis (Carnivora, Mustelidae) en el Parque Nacional el Rey (Salta, Argentina) y su comparación con otra poblaciones de la cuenca del Paraná. Mastozoología Neotropical 17: 19–29.Google Scholar
  25. Cherel, Y., K. A. Hobson & C. Guinet, 2015. Milk isotopic values demonstrate that nursing fur seal pups are a full trophic level higher than their mothers. Rapid Communications in Mass Spectrometry 29: 1485–1490.PubMedCrossRefGoogle Scholar
  26. Chiaradia, A., F. Ramírez, M. G. Forero & K. A. Hobson, 2016. Stable isotope (δ13C, δ15N) combined with conventional dietary approaches reveal plasticity in central-place foraging behavior of little penguins Eudyptula minor. Frontiers in Ecology and Evolution 3: 154.CrossRefGoogle Scholar
  27. Clementz, M. T. & P. L. Koch, 2001. Differentiating aquatic mammal habitat and foraging ecology with stable isotopes in tooth enamel. Oecologia 129: 461–472.PubMedCrossRefGoogle Scholar
  28. Colares, E. P. & H. F. Waldemarin, 2000. Feeding of the Neotropical river otter (Lontra longicaudis) in the coastal region of the Rio Grande do Sul state, southern Brazil. IUCN Otter Specialist Group Bulletin 17: 6–13.Google Scholar
  29. Cordazzo, C. V. & U. Seeliger, 1995. Guia Ilustrado da Vegetação Costeira do Extremo Sul do Brasil. Editora da Fundação Universidade do Rio Grande, Rio Grande.Google Scholar
  30. De Andrade, H. K., 1997. Food and feeding habits of the Neotropical river otter Lontra longicaudis (Carnivora, Mustelidae). Mammalia 61: 193–203.Google Scholar
  31. DeNiro, M. J. & S. Epstein, 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42: 495–506.CrossRefGoogle Scholar
  32. Drago, M., V. Franco-Trecu, L. Carbona & P. Inchausti, 2015. Diet-to-female and female-to-pup isotopic discrimination in South American sea lions. Rapid Communications in Mass Spectrometry 29: 1513–1520.PubMedCrossRefGoogle Scholar
  33. Evacitas, F. C., W. Kao, G. A. J. Worthy & L. Chou, 2017. Annual variability in dentin δ15N and δ13C reveal sex differences in weaning age and feeding habits in Risso’s dolphins (Grampus griseus). Marine Mammal Sience 33: 748–770.CrossRefGoogle Scholar
  34. Faria, F. A., A. Silva-Costa, D. Gianuca & L. Bugoni, 2016. Cocoi heron (Andrea cocoi) connects estuarine, coastal, limnetic and terrestrial environments: an assessment based on conventional dietary and stable isotope analysis. Estuaries and Coasts 39: 1271–1281.CrossRefGoogle Scholar
  35. Ferreira, N. C., R. M. Guereschi, C. Machado, C. A. Lopes & A. P. O. Nuñer, 2016. Structure and diversity of fishes in a freshwater and coastal subtropical lagoon. Journal of Fish Biology 90: 1265–1282.PubMedCrossRefGoogle Scholar
  36. Fischer, L. G., L. E. D. Pereira & J. P. Vieira, 2011. Peixes Estuarinos e Costeiros (Segunda Edição). Editora Conscientia, Rio Grande.Google Scholar
  37. Garcia, A. M., M. A. Bemvenutti, J. P. Vieira, D. M. L. M. Marques, M. D. M. Burns, A. Moresco & M. V. L. Condini, 2006. Checklist comparison and dominance patterns of the fish fauna at Taim Wetland, South Brazil. Neotropical Ichthyology 4: 261–268.CrossRefGoogle Scholar
  38. Gomes, N. & L. Krause, 1982. Lista preliminar de répteis da Estação Ecológica do Taim, Rio Grande do Sul. Revista Brasileira de Zoologia 1: 71–77.CrossRefGoogle Scholar
  39. Gori, M., G. M. Carpaneto & P. Ottino, 2003. Spatial distribution and diet of the Neotropical otter Lontra longicaudis in the Ibera Lake (Northern Argentina). Acta Theriologica 48: 495–504.CrossRefGoogle Scholar
  40. Gregg, W. W., N. W. Casey & C. R. McClain, 2005. Recent trends in global ocean chlorophyll. Geophysical Research Letters 32: L03606.Google Scholar
  41. Heggberget, T. M., 1984. Age determination in the European otter Lutra lutra. Zeitschrift für Säugetierkunde 49: 299–305.Google Scholar
  42. Hoeinghaus, D. J., J. P. Vieira, C. S. Costa, C. E. Bemvenuti, K. O. Winemiller & A. M. Garcia, 2011. Estuary hydrogeomorphology affects carbon sources supporting aquatic consumers within and among ecological guilds. Hydrobiologia 673: 79–92.CrossRefGoogle Scholar
  43. Hutchinson, G. E., 1957. Concluding remarks. Cold Spring Harbor Symposia on Quantitative Biology 22: 415–427.CrossRefGoogle Scholar
  44. Iversen, M., J. Aars, T. Haug, I. G. Alsos, C. Lydersen, L. Bachmann & K. M. Kovacs, 2013. The diet of polar bears (Ursus maritimus) from Svalbard, Norway, inferred from scat analysis. Polar Biology 36: 561–571.CrossRefGoogle Scholar
  45. Jackson, A. L., R. Inger, A. C. Parnell & S. Bearhop, 2011. Comparing isotopic niche widths among and within communities: SIBER—Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80: 595–602.PubMedCrossRefGoogle Scholar
  46. Kasper, C. B., J. Salvi & H. C. Z. Grillo, 2004a. Estimativa do tamanho de duas espécies de ciclídeos (Osteichthyes, Perciformes) predados por Lontra longicaudis (Olfers) (Carnivora, Mustelidae), através de análise das escamas. Revista Brasileira de Zoologia 21: 499–503.CrossRefGoogle Scholar
  47. Kasper, C. B., M. J. Feldens, J. Salvi & H. C. Z. Grillo, 2004b. Estudo preliminar sobre a ecologia de Lontra longicaudis (Olfers) (Carnivora, Mustelidae) no Vale do Taquari, sul do Brasil. Revista Brasileira de Zoologia 21: 65–72.CrossRefGoogle Scholar
  48. Kasper, C. B., V. A. G. Bastazini, J. Salvi & H. C. Z. Grillo, 2008. Trophic ecology and use of shelters and latrines by the Neotropical otter (Lontra longicaudis) in the Taquari Valley, southern Brazil. Iheringia, Série Zoologia 98: 469–474.CrossRefGoogle Scholar
  49. Kasper, C. B., F. B. Peters, A. U. Christoff & T. R. O. Freitas, 2016. Trophic relationships of sympatric small carnivores in fragmented landscapes of southern Brazil: niche overlap and potential for competition. Mammalia 80: 143–152.CrossRefGoogle Scholar
  50. Kim, S. L., C. M. Rio, D. Casper & P. L. Koch, 2012. Isotopic incorporation rates for shark tissues from a long-term captive feeding study. Journal of Experimental Biology 215: 2495–2500.PubMedCrossRefGoogle Scholar
  51. Klare, U., J. F. Kamler & D. W. McDonald, 2011. A comparison and critique of different scat-analysis methods for determining carnivore diet. Mammal Review 41: 294–312.CrossRefGoogle Scholar
  52. Kruuk, H., 2006. Otters: Ecology, Behaviour and Conservation. Oxford University Press, New York.CrossRefGoogle Scholar
  53. Kruuk, H. & A. Moorhouse, 1990. Seasonal and spatial differences in food selection by otters (Lutra lutra) in Shetland. Journal of Zoology, London 221: 621–637.CrossRefGoogle Scholar
  54. Kruuk, H. & A. Moorhouse, 1991. The spatial organization of otters (Lutra lutra) in Shetland. Journal of Zoology, London 224: 41–57.CrossRefGoogle Scholar
  55. Louzada-Silva, D., T. M. Vieira, J. P. Carvalho, A. P. Hercos & B. M. Souza, 2003. Uso de espaço e alimento por Lontra longicaudis no Lago Paranoá, Brasília, DF. Ciências da Saúde 1: 305–316.Google Scholar
  56. Lübcker, N., R. R. Reisinger, W. C. Oosthuizen, P. J. N. Bruyn, A. Tonder, P. A. Pistorius & M. N. Bester, 2017. Low trophic level diet of juvenile southern elephant seals Mirounga leonina from Marion Island: a stable isotope investigation using vibrissal regrowths. Marine Ecology Progress Series 577: 237–250.CrossRefGoogle Scholar
  57. Macías-Sánchez, S. & M. Aranda, 1999. Análisis de la alimentación de la nutria Lontra longicaudis (Mammalia: Carnivora) en un sector del rio Los Pescadores, Veracruz, México. Acta Zoológica Mexicana 76: 49–57.Google Scholar
  58. Madigan, D. J., S. Y. Litvin, B. N. Popp, A. B. Carlisle, C. J. Farwell & B. A. Block, 2012. Tissue turnover rates and isotopic trophic discrimination factors in the endothermic teleost, Pacific bluefin tuna (Thunnus orientalis). PLoS ONE 7: e49220.PubMedPubMedCentralCrossRefGoogle Scholar
  59. Malabarba, L. R., P. C. Neto, V. A. Bertaco, T. P. Carvalho, J. F. Santos & L. G. S. Artioli, 2013. Guia de Identificação dos Peixes da Bacia do Rio Tramandaí. Editora Via Sapiens, Porto Alegre.Google Scholar
  60. Marques, D. M., L. R. Rodrigues, C. R. Fragoso, L. Crossetii, L. S. Cardoso, W. Collischonn, R. Tassi, N. H. They, M. Bemvenuti, A. Garcia, J. P. Vieira, E. B. Canterle, M. A. Cardoso, V. Becker, V. Gazulha, J. M. Bravo, R. Souza, C. Volkmer-Ribeiro, V. L. Callegaro, S. Alves-da-Silva, V. Werner, Z. Rosa, A. Villanueva, A. Moresco, M. V. Condini, M. Burns & N. Würdig, 2013. O Sistema Hidrológico do Taim. In Tabarelli, M., C. F. D. Rocha, H. P. Romanowski, O. Rocha & L. D. Lacerda (eds), PELD-CNPq Dez Anos do Programa de Pesquisas Ecológicas de Longa Duração no Brasil: Achados, Lições e Perspectivas. Editora Universitária UFPE, Recife: 197–222.Google Scholar
  61. Mayor-Victoria, R. & A. Botero-Botero, 2010. Dieta de la nutra Neotropical Lontra longicaudis (Carnívora, Mustelidae) en el Río Roble, Alto Cauca, Colombia. Acta Biológica Colombiana 15: 237–244.Google Scholar
  62. Nakano-Oliveira, E., R. Fusco, E. A. V. Santos & E. L. A. Monteiro-Filho, 2004. New information about the behavior of Lontra longicaudis (Carnivora: Mustelidae) by radio-telemetry. IUCN Otter Specialist Group Bulletin 21: 31–35.Google Scholar
  63. Newsome, S. D., C. M. Rio, S. Bearhop & D. L. Phillips, 2007. A niche for isotopic ecology. Frontiers in Ecology and the Environment 5: 429–436.CrossRefGoogle Scholar
  64. Newsome, S. D., M. T. Tinker, D. H. Monson, O. T. Oftedal, K. Ralls, M. M. Staedler, M. L. Fogel & J. A. Estes, 2009. Using stable isotopes to investigate individual diet specialization in California sea otters (Enhydra lutris nereis). Ecology 90: 961–974.PubMedCrossRefGoogle Scholar
  65. Newsome, S. D., K. Ralls, C. V. H. Job, M. L. Fogel & B. L. Cypher, 2010a. Stable isotopes evaluate exploitation of anthropogenic foods by the endangered San Joaquin kit fox (Vulpes macrotis mutica). Journal of Mammalogy 91: 1313–1321.CrossRefGoogle Scholar
  66. Newsome, S. D., M. T. Clementz & P. L. Koch, 2010b. Using stable isotope biogeochemistry to study marine mammal ecology. Marine Mammal Science 26: 509–572.Google Scholar
  67. Newsome, S. D., M. T. Tinker, V. A. Gill, Z. N. Hoyt, A. Doroff, L. Nichol & J. L. Bodkin, 2015. The interaction of intraspecific competition and habitat on individual diet specialization: a near range-wide examination of sea otters. Oecologia 178: 45–59.PubMedCrossRefGoogle Scholar
  68. Noernberg, M. A., M. Kampel & F. P. Brandini, 2007. Estudo da variabilidade temporal da concentração de clorofila estimada por satélite na plataforma continental catarinense: latitude 26º46′S. Anais XIII Simpósio Brasileiro de Sensoriamento Remoto: 4635–4642.Google Scholar
  69. Norrdahl, K. & E. Korpimäki, 2000. The impact of predation risk from small mustelids on prey populations. Mammal Review 30: 147–156.CrossRefGoogle Scholar
  70. Oliveira, G. C., J. F. M. Barcellos & F. C. W. Rosas, 2007. Age estimation in giant otters (Pteronura brasiliensis) using growth layers groups in canine teeth. Latin-American Journal of Aquatic Mammals 6: 155–160.CrossRefGoogle Scholar
  71. Oliveira, M. C. L., R. F. Bastos, M. C. Claudino, C. M. Assumpção & A. M. Garcia, 2014. Transport of marine-derive nutrients to subtropical freshwater food webs by juvenile mullets: a case study in southern Brazil. Aquatic Biology 20: 91–100.CrossRefGoogle Scholar
  72. Pardini, R., 1998. Feeding ecology of the Neotropical river otter Lontra longicaudis in an Atlantic Forest stream, south-eastern Brazil. Journal of Zoology 245: 385–391.CrossRefGoogle Scholar
  73. Pardini, R. & E. Trajano, 1999. Use of shelters by the Neotropical river otter (Lontra longicaudis) in an Atlantic Forest stream, southeastern Brazil. Journal of Mammalogy 80: 600–610.CrossRefGoogle Scholar
  74. Parnell, A. & R. Inger, 2016. Stable isotope mixing models in R with simmr. https://cran.r-project.org/web/packages/simmr/vignettes/simmr.html. Accessed on 02 September 2017.
  75. Peres, B., 2014. Variação espacial e intra-anual na dieta de Lontra longicaudis (Olfers, 1818) em três áreas do extremo sul do Brasil. Universidade Federal do Rio Grande—FURG. Programa de Pós-graduação em Biologia de Ambientes Aquáticos Continentais.Google Scholar
  76. Perini, A. A., E. M. Vieira & U. W. Schulz, 2009. Evaluation of methods used for diet analysis of the Neotropical otter. Mammalian Biology 74: 230–235.CrossRefGoogle Scholar
  77. Post, D. M., 2002. Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83: 703–718.CrossRefGoogle Scholar
  78. Post, D. M., C. A. Layman, D. A. Arrington, G. Takimoto, J. Quattrochi & C. G. Montaña, 2007. Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152: 179–189.PubMedCrossRefGoogle Scholar
  79. Prado, J. F., 2009. Vegetação de ambientes aquáticos do litoral norte do estado do Rio Grande do Sul. In Würdig, N. L. & S. M. F. Freitas, S. M. F. (eds), Ecossistemas e Biodiversidade do Litoral Norte do RS. Editora Nova Prova, Porto Alegre: 76–89.Google Scholar
  80. Quadros, J. & E. L. A. Monteiro-Filho, 2001. Diet of the Neotropical otter, Lontra longicaudis, in an Atlantic forest area, Santa Catarina state, southern Brazil. Studies on Neotropical Fauna and Environment 36: 15–21.CrossRefGoogle Scholar
  81. Quintela, F. M., R. A. Porciuncula & E. P. Colares, 2008. Dieta de Lontra longicaudis (Olfers) (Carnivora, Mustelidae) em um arroio costeiro da região sul do Estado do Rio Grande do Sul, Brasil. Neotropical Biology and Conservation 3: 119–125.CrossRefGoogle Scholar
  82. Quintela, F. M., L. G. S. Artioli & R. A. Porciuncula, 2012. Diet of Lontra longicaudis (Olfers, 1818) (Carnivora: Mustelidae) in three limnic systems in southern Rio Grande do Sul state, Brazil. Brazilian Archives of Biology and Technology 55: 877–886.CrossRefGoogle Scholar
  83. R Core Team, 2017. R: A Language and Environment for Statistical Computing. R Core Team, Geneva.Google Scholar
  84. Rheingantz, M. L., H. F. Waldemarin, L. Rodrigues & T. P. Moulton, 2011. Seasonal and spatial differences in feeding habits of the Neotropical otter Lontra longicaudis (Carnivora: Mustelidae) in a coastal catchment of southeastern Brazil. Zoologia 28: 37–44.CrossRefGoogle Scholar
  85. Rheingantz, M. L., L. G. Oliveira-Santos, H. F. Waldemarin & E. P. Caramaschi, 2012. Are otters generalists or do they prefer larger, slower prey? Feeding flexibility of the Neotropical otter Lontra longicaudis in the Atlantic Forest. IUCN Otter Specialist Group Bulletin 29: 80–94.Google Scholar
  86. Rheingantz, M. L., J. F. S. Menezes, M. Galliez & F. A. S. Fernandez, 2017. Biogeographic patterns in the feeding habits of the opportunist and semiaquatic Neotropical otter. Hydrobiologia 792: 1–15.CrossRefGoogle Scholar
  87. Ripple, W. J., J. A. Estes, R. L. Beschta, C. C. Wilmers, E. G. Ritchie, M. Hebblewhite, J. Berger, B. Elmhagen, M. Letnic, M. P. Nelson, O. J. Schmitz, D. W. Smith, A. D. Wallach & A. J. Wirsing, 2014. Status and ecological effects of the world’s largest carnivores. Science 343: 151–162.CrossRefGoogle Scholar
  88. Robbins, C. T., L. A. Felicetti & M. Sponheimer, 2005. The effect of dietary protein quality on nitrogen isotope discrimination in mammals and birds. Oecologia 144: 534–540.PubMedCrossRefGoogle Scholar
  89. Rosa-Filho, J. S., C. E. Bemvenuti & M. Elliott, 2004. Predicting biological parameters of estuarine benthic communities using models based on environmental data. Brazilian Archives of Biology and Technology 47: 613–627.CrossRefGoogle Scholar
  90. Ruiz-Cooley, R. I., D. Gendron, S. Aguíñiga, S. Mesnick & J. D. Carriquiry, 2004. Trophic relationships between sperm whales and jumbo squid using stable isotopes of C and N. Marine Ecology Progress Series 277: 275–283.CrossRefGoogle Scholar
  91. Schäfer, A., 1988. Tipificação ecológica das lagoas costeiras do Rio Grande do Sul, Brasil. Acta Limnologica Brasiliensia 11: 29–55.Google Scholar
  92. Silva-Costa, A. & L. Bugoni, 2013. Feeding ecology of Kelp Gulls (Larus dominicanus) in marine and limnetic environments. Aquatic Ecology 47: 211–224.CrossRefGoogle Scholar
  93. Silva, R. E., E. Nakano-Oliveira & E. L. A. Monteiro-Filho, 2005. Methodology for test occurrence and distribution of Neotropical otter (Lontra longicaudis, Olfers, 1818) in Cananéia, south coast of the state of São Paulo, Brazil. IUCN Otter Specialist Group Bulletin 18: 29–33.Google Scholar
  94. Silva, F. A., E. M. Nascimento & F. M. Quintela, 2012. Diet of Lontra longicaudis (Carnivora: Mustelidae) in a pool system in Atlantic Forest of Minas Gerais state, southeastern Brazil. Acta Scientiarum. Biological Sciences 34: 407–412.Google Scholar
  95. Smith, J. A., D. Mazumder, I. M. Suthers & M. D. Taylor, 2013. To fit or not to fit: evaluating stable isotope mixing models using simulated mixing polygons. Methods in Ecology and Evolution 4: 612–618.CrossRefGoogle Scholar
  96. Sousa, K. S., V. A. G. Bastazini & E. P. Colares, 2013. Feeding ecology of the Neotropical otter Lontra longicaudis in the Lower Arroio Grande River, southern Brazil. Anais da Academia Brasileira de Ciências 85: 285–294.CrossRefGoogle Scholar
  97. Stephenson, A. B., 1977. Age determination and morphological variation of Ontario otters. Canadian Journal of Zoology 55: 1577–1583.CrossRefGoogle Scholar
  98. Syväranta, J., A. Lensu, T. J. Marjomäki, S. Oksanen & R. I. Jones, 2013. An empirical evaluation of the utility of convex hull and standard ellipse areas for assessing population niche widths from stable isotope data. PLoS ONE 8: e56094.PubMedPubMedCentralCrossRefGoogle Scholar
  99. Szpak, P., T. J. Orchard, I. McKechnie & D. R. Gröcke, 2012. Historical ecology of late Holocene Sea otters (Enhydra lutris) from Northern British Columbia: isotopic and zooarchaelogical perspectives. Journal of Archaelogical Science 39: 1553–1571.CrossRefGoogle Scholar
  100. Trinca, C. S., C. F. Jaeger & E. Eizirik, 2013. Molecular ecology of the Neotropical otter (Lontra longicaudis): non-invasive sampling yields insights into local population dynamics. Biological Journal of the Linean Society 109: 932–948.CrossRefGoogle Scholar
  101. Troina, G., S. Botta, E. R. Secchi & F. Dehairs, 2016. Ontogenetic and sexual characterization of the feeding habits of franciscanas, Pontoporia blainvillei, based on tooth dentin carbon and nitrogen stable isotopes. Marine Mammal Science 32: 1115–1137.CrossRefGoogle Scholar
  102. Uchôa, T., G. P. Vidolin, T. M. Fernandes, G. O. Valastin & P. R. Mangini, 2004. Aspectos ecológicos e sanitários da lontra (Lontra longicaudis OLFERS, 1818) na Reserva Natural Salto Morato, Guaraqueçaba, Paraná, Brasil. Cadernos da Biodiversidade 4: 19–28.Google Scholar
  103. Valenzuela, A. E. J., A. R. Rey, L. Fasola, R. A. S. Samaniego & A. Schiavini, 2013. Trophic ecology of a top predator colonizing the southern extreme of South America: feeding habits of invasive American mink (Neovison vison) in Tierra del Fuego. Mammalian Biology 78: 104–110.CrossRefGoogle Scholar
  104. Villwock, J. A., 2009. Geografia, geologia e gênese do litoral norte. In Würdig, N. L. & S. M. F. Freitas (eds), Ecossistemas e Biodiversidade do Litoral Norte do RS. Editora Nova Prova, Porto Alegre: 12–25.Google Scholar
  105. Wrege, M. S., S. Steinmetz, C. R. Júnior & I. R. Almeida, 2012. Atlas Climático da Região Sul do Brasil: Estados do Paraná, Santa Catarina e Rio Grande do Sul (Segunda Edição). Embrapa, Brasília.Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Thayara S. Carrasco
    • 1
    • 2
    Email author
  • Silvina Botta
    • 2
  • Rodrigo Machado
    • 3
  • Paulo C. Simões-Lopes
    • 4
  • Oldemar Carvalho-Junior
    • 5
  • Paulo H. Ott
    • 3
    • 6
  • Elton P. Colares
    • 1
  • Eduardo R. Secchi
    • 1
    • 2
  1. 1.Programa de Pós-graduação em Biologia de Ambientes Aquáticos Continentais, Instituto de Ciências BiológicasUniversidade Federal do Rio Grande - FURGRio GrandeBrazil
  2. 2.Laboratório de Ecologia e Conservação da Megafauna Marinha – ECOMEGA, Instituto de OceanografiaUniversidade Federal do Rio Grande - FURGRio GrandeBrazil
  3. 3.Grupo de Estudos de Mamíferos Aquáticos do Rio Grande do Sul – GEMARSTorresBrazil
  4. 4.Laboratório de Mamíferos Aquáticos – LAMAQ, Departamento de Ecologia e ZoologiaUniversidade Federal de Santa CatarinaFlorianópolisBrazil
  5. 5.Instituto Ekko Brasil – IEB, Gerencia de Projetos e PesquisaFlorianópolisBrazil
  6. 6.Laboratório de Biodiversidade e ConservaçãoUniversidade Estadual do Rio Grande do Sul – UERGSOsórioBrazil

Personalised recommendations