Conservation genetics of otters: Review about the use of non-invasive samples

Autores/as

  • Sandra L. Aristizabal Duque Universidad de Antioquia
  • Luz Y. Orozco-Jimenez Universidad de Antioquia
  • Carolina Zapata-Escobar Universidad de Antioquia
  • Jaime A. Palacio-Baena Universidad de Antioquia

Palabras clave:

genetic diversity, microsatellites, mitochondrial DNA, molecular markers, non-invasive sampling, otters

Resumen

Wild population management programs require determining some fundamental aspects for conservation, including population structure, flow between populations, evolutionary history and kinship, among others. Since sample collection from wild mammals for DNA extraction is a complex task, conservation genetics has developed non-invasive sampling techniques, which allow obtaining DNA without the need to capture individuals. For the genetic characterization of otter populations, stools are frequently used as source of DNA for amplification of molecular markers (microsatellites, mitochondrial segments and sequences for determining sex) in studies on genetic diversity, phylogeography, population structure and size, among others. This review summarizes the application of non-invasive sampling techniques in genetic studies of otter species. Genetic characterization studies that use stools as source of DNA support the usefulness of this material to get amplified markers in the genotyping of individuals. They also suggest the use of fresh samples and appropriate conservation methods to avoid DNA degradation, as well as quantify the potential errors in genotyping, such as false and null alleles.

Biografía del autor/a

Sandra L. Aristizabal Duque, Universidad de Antioquia

Soy Magister en Ciencias Ambientales de la Universidad de Antioquia, actualmente trabajo en el grupo GAIA de la Facultad de Ingeniería como prestadora de servicios en el área de análisis genético.

Luz Y. Orozco-Jimenez, Universidad de Antioquia

Es Bióloga con Maestría en Ciencias Básicas Biomédicas de la Universidad de Antioquia. Actualmente es la directora de la línea de genotoxicología y epigenética ambiental del Grupo GAIA adscrito a la facultad de Ingeniería de la Universidad de Antioquia.

Carolina Zapata-Escobar, Universidad de Antioquia

Es bióloga candidata a Magister en Ciencias Ambientales de la Universidad de Antioquia, actualmente trabaja en el grupo GAIA de la Facultad de Ingeniería como prestadora de servicios en el área de ecología.

Jaime A. Palacio-Baena, Universidad de Antioquia

Es Biólogo, Doctor en ciencias naturales de Bochum University. Actualmente coordina la linea de Ecotoxicología del Grupo GAIA de la facultad de Ingeniería de la Universidad de Antioquia.

Citas

Arrendal, J., C. Vilà , and M. Björklund. 2007. Reliability of noninvasive genetic census of otters compared to field censuses. Conservation Genetics 8:1097–1107.

Avise, J., J. Arnold, and R. Ball. 1987. Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annual review of ecology and systematics XX:489-522.

Avise, J. 1998. Conservation genetics in the marine realm. Journal of Heredity 89:377-382.

Avise, J. 2000. Phylogeography: the history and formation of species. Harvard University Press. Cambridge, U. S. A.

Bardier, G. 1992. Uso de recursos y características del hábitat del Lobito de río. Lutra longicaudis en el arroyo Sauce, SE de Uruguay. Boletín de la Sociedad Zoológica del Uruguay 7:59-60.

Barnett, R., N. Yamaguchi, I. Barnes, and A. Cooper. 2006. Lost populations and preserving genetic diversity in the lion Panthera leo: implications for its ex situ conservation. Conservation Genetics 7:507-514.

Beheler, A. S., J. A. Fike, G. Dharmarajan, O. E. Rhodes, and T. L. Serfass. 2005. Ten new polymorphic microsatellite loci for North American river otters (Lontra canadensis) and their utility in related mustelids . Molecular Ecology Notes 5:602–604.

Bermingham, E., and C. Moritz. 1998. Comparative phylogeography: concepts and applications. Molecular Ecology 7:367-369.

Broquet, T., and E. Petit. 2004. Quantifying genotyping errors in noninvasive population genetics. Molecular Ecology 13:3601–3068.

Brzeski, K. E., M. S. Gunther, and J. M. Black. 2013. Evaluating river otter demography using noninvasive genetic methods. The Journal of Wildlife Management 77:1523–1531.

Caballero, S., C. A. Correa-Cárdenas, and F. Trujillo. 2015. Population structure and genetic diversity of the endangered South American giant otter (Pteronura brasiliensis) from the Orinoco Basin in Colombia: management implications and application to current conservation programs. Journal of Heredity 106:469-477.

Cantanhede, A., and V. Da Silva. 2005. Phylogeography and population genetics of the endangered Amazonian manatee, Trichechus inunguis Natterer, 1883 (Mammalia, Sirenia). Molecular Ecology 14:401-413.

Cassens, I., and R. Tiedeman. 2000. Mitochondrial DNA variation in the European otter (Lutra lutra) and the use of spatial autocorrelation analysis in conservation. Journal of Heredity 9:31-35.

Centrón, D., B. Ramirez, L. Fasola, D. W. Macdonald, C. Chehébar, A. Schiavini, and M. H. Cassini. 2008. Diversity of mtDNA in Southern River Otter (Lontra provocax) from Argentinean Patagonia. The Journal of heredity 99:198–201.

Conroy, J., and P. Chanin. 2002. The status of the Eurasian otter (Lutra lutra). IUCN Otter Specialist Group Bulletin A Review 1:7-28.

Crawford, J., Z. Liu, and T. Nelson. 2008. Microsatellite analysis of mating and kinship in beavers (Castor canadensis). Journal of Mammalogy 89:575-581.

Creel, S., G. Spong, and J. Sands. 2003. Population size estimation in Yellowstone wolves with errorâ€prone noninvasive microsatellite genotypes. Molecular ecology 12:XX.

Dallas, J. F., D. N. Carss, F. Marshall, K. P. Koepfli, H. Kruuk, P. J. Bacon, and S. B. Piertney. 2000. Sex identification of the Eurasian otter Lutra lutra by PCR typing of spraints. Conservation Genetics 1:181–183.

Dallas, J. F., K. E. Coxon, T. Sykes, P. R.Chanin, F. Marshall, D. N. Carss, and P. A. Racey, P. 2003. Similar estimates of population genetic composition and sex ratio derived from carcasses and faeces of Eurasian otter Lutra lutra. Molecular Ecology 12:275–82.

Eisenberg, J. 1989. Mammals of the Neotropics: The Northern Neotropics (Vol. 1). University of Chicago Press. Chicago, U. S. A.

Eizirik, E., and S. Bonatto. 1998. Phylogeographic patterns and evolution of the mitochondrial DNA control region in two Neotropical cats (Mammalia, Felidae). Journal of Molecular Evolution 47:613-624.

Ferrando, A., M. Ponsà , J. Marmi, and X. Domingo-Roura. 2004. Eurasian otters, Lutra lutra, have a dominant mtDNA haplotype from the Iberian Peninsula to Scandinavia. The Journal of heredity 95:430- 435.

Ferrando, A., R. Lecis, X. Domingo-Roura, and M. Ponsà . 2007. Genetic diversity and individual identification of reintroduced otters (Lutra lutra) in north-eastern Spain by DNA genotyping of spraints. Conservation Genetics 9:129–139.

Foerster, K., and M. Valcu. 2006. A spatial genetic structure and effects of relatedness on mate choice in a wild bird population. Molecular Ecology 15:4555-4567.

Frankham, R. 1995. Conservation genetics. Annual Review of Genetics 29:305-327.

Frankham, R., D. A Briscoe, and J. D. Ballou. 2002. Introduction to Conservation Genetics, Cambridge University Press. Cambridge, Inglaterra.

Frantz, A., L. Pope, and P. Carpenter. 2003. Reliable microsatellite genotyping of the Eurasian badger (Meles meles) using faecal DNA. Molecular Ecology 12:1649-1661.

Frantzen, M. A. J., J. B. Silk, J. W. H. Ferguson, R. K. Wayne, and M. H. Kohn. 1998. Empirical evaluation of preservation methods for faecal DNA. Molecular Ecology 7:1423-1428.

Garcia, D. M., M. Marmontel, F. W. Rosas, and F. R. Santos. 2007. Conservation genetics of the giant otter (Pteronura brasiliensis (Zimmerman, 1780)) (Carnivora, Mustelidae). Brazilian Journal of Biolog 67:819–27.

Goossens, B., L. Chikhi, S. S. Utami, J. De Ruiter, and M. W. Bruford. 2000. A multi-samples, multi-extracts approach for microsatellite analysis of faecal samples in an arboreal ape. Conservation genetics 1:157-162.

Guerrero, J., J. P. Gallo-Reynoso, and R. Biek. 2015. Mitochondrial DNA diversity, genetic structure, and demographic history of the Neotropical otter (Lontra longicaudis) in Mexico. Journal of Mammalogy 96:1162-1173.

Guertin, D. A., A. S. Harestad, M. Benâ€David, K. G. Drouillard, and J. E. Elliott. 2010. Fecal genotyping and contaminant analyses reveal variation in individual river otter exposure to localized persistent contaminants. Environmental Toxicology and Chemistry 29:275-284.

Guertin, D. A., M. Benâ€David, A. S. Harestad, and J. E. Elliott. 2012. Fecal genotyping reveals demographic variation in river otters inhabiting a contaminated environment. The Journal of Wildlife Management 76:1540–1550.

Hájková, P., B. Zemanová, J. Bryja, B. Hájek, K. Roche, E. Tkadlec, and J. Zima. 2006. Factors affecting success of PCR amplification of microsatellite loci from otter faeces. Molecular Ecology Notes 6:559–562.

Hansen, H., M. Ben-David, and D.B. Mcdonald. 2008. Effects of genotyping protocols on success and errors in identifying individual river otters (Lontra canadensis) from their faeces. Molecular ecology resources 8:282–9.

Hedrick, P. W. 2001. Conservation genetics: where are we now? Trends in Ecology and Evolution 16:629–636.

Hedrick, P. W. 2004. Recent developments in conservation genetics. Forest Ecology and Management 197:3-19.

Hung, C. M., S. H. Li, and L. L. Lee. 2004. Faecal DNA typing to determine the abundance and spatial organisation of otters (Lutra lutra) along two stream systems in Kinmen. Animal Conservation 7:301–311.

IUCN. 2015. The IUCN Red List of Threatened Species 2015. www.iucnredlist.org. Downloaded on 10 June 2016.

Johnson, C .J., D. P. Hodder, and S. Crowley. 2013. Assessing noninvasive hair and fecal sampling for monitoring the distribution and abundance of river otter. Ecological Research 28:881–892.

Kalz, B., K. Jewgenow, and J. Fickel. 2006. Structure of an otter (Lutra lutra) population in Germany – results of DNA and hormone analyses from faecal samples. Mammalian Biology 71:321–335.

Koelewijn, H. P., M. Pérez-Haro, H. A. H. Jansman, M. C. Boerwinkel, J. Bovenschen, D. R. Lammertsma, and A.T. Kuiters. 2010. The reintroduction of the Eurasian otter (Lutra lutra) into the Netherlands: hidden life revealed by noninvasive genetic monitoring. Conservation Genetics 11:601–614.

Kohn, M., and E. York. 1999. Estimating population size by genotyping faeces. Proceedings of the Royal Society of London 266:657-663.

Kruuk, H. 2006. Otters: ecology, behaviour and conservation. Oxford University Press. Oxford, United Kindom.

Lampa, S., B. Gruber, K. Henle, and M. Hoehn. 2008. An optimisation approach to increase DNA amplification success of otter faeces. Conservation Genetics 9:201–210.

Lanszki, J., A. Hidas, K. Szentes, T. Révay, I. Lehoczky, Z. Jeney, and S. Weiss. 2010. Genetic structure of otter (Lutra lutra) populations from two fishpond systems in Hungary. Mammalian Biology 75:447–450.

Lanszki, J., A. Hidas, K. Szentes, T. Révay, I. Lehoczky, and S. Weiss. 2008. Relative spraint density and genetic structure of otter (Lutra lutra) along the Drava River in Hungary. Mammalian Biology 73:40–47.

Lerone, L., C. Mengoni, G. M. Carpaneto, E. Randi, and A. Loy. 2014. Procedures to genotype problematic non-invasive otter (Lutra lutra) samples. Acta Theriologica 59:511–520.

Longmire, J. L., M. Maltbie, and R. J. Baker. 1997. Use of ‘‘Lysis Buffer’’ in DNA isolation and its implication for museum collections. Occasional papers, The Museum of Texas Tech University 163:1–3.

Lynch, M. 1996. A quantitative-genetic perspective on conservation issues. Pp. 471–501 in Conservation Genetics: Case Histories from Nature (Avise, J. C., and J. L. Hamrick, eds.). Chapman y Hall. New York, U. S. A.

Lynch, M., and W. Gabriel. 1990. Mutation load and the survival of small populations. Evolution 44:1725–1737.

Macdonald, S., and C. Mason. 1990. Action plan for European otters. Pp. 29-40 in Otters: An Action Plan for their Conservation (Foster-Turley, P., S. Macdonald, and C. F. Mason eds). IUCN otter specialist group. Gland, Suiza.

Márquez, A., and J. Maldonado. 2006. Phylogeography and Pleistocene demographic history of the endangered marsh deer (Blastocerus dichotomus) from the Río de la Plata Basin. Conservation Genetics 7:563-575.

Mason, C., and S. Macdonald. 2004. Growth in otter (Lutra lutra) populations in the UK as shown by long-term monitoring. A Journal of the Human Environment 33:148-152.

Möller, L. 2001. Alliance membership and kinship in wild male bottlenose dolphins (Tursiops aduncus) of southeastern Australia. Proceedings of the Royal Society of London. Series B: Biological Sciences 268:1941-1947.

Montoyaâ€Burgos, J. 2003. Historical biogeography of the catfish genus Hypostomus (Siluriformes: Loricariidae), with implications on the diversification of Neotropical ichthyofauna. Molecular Ecology 12:1855-1867.

Moritz, C. 2002. Strategies to protect biological diversity and the evolutionary processes that sustain it. Systematic Biology 51:238-254.

Mowry, R. A., M. E. Gompper, J. Beringer, and L. S. Eggert. 2011. River otter population size estimation using noninvasive latrine surveys. The Journal of Wildlife Management 75:1625–1636.

Mowry, R. A., T. M. Schneider, E. K. Latch, M. E. Gompper, J. Beringer, and L. S. Eggert. 2015. Genetics and the successful reintroduction of the Missouri river otter. Animal Conservation 18:196-206.

Mucci, N., C. Pertoldi, A. B Madsen, V. Loeschcke, and E. Randi. 1999. Extremely Low Mitochondrial DNA Controlâ€Region Sequence Variation in the Otter Lutra lutra Population of Denmark. Hereditas 130:331-336.

Murphy, M. A., L. P. Waits, K. C. Kendall, S. K. Wasser, J. A. Higbee y R. Bogden. 2002. An evaluation of long-term preservation methods for brown bear (Ursus arctos) faecal DNA samples. Conservation genetics 3:435-440.

Murphy, M. A., L. P. Waits, and K. C. Kendall. 2003. The influence of diet on faecal DNA amplification and sex identification in brown bears (Ursus arctos). Molecular Ecology 12:2261-2265.

Oliveira De, L. R., R. Loizaga De Castro, S. Cárdenasâ€Alayza, and S. L. Bonatto. 2012. Conservation genetics of South American aquatic mammals: an overview of gene diversity, population structure, phylogeography, non-invasive methods and forensics. Mammal Review 42:275–303.

O’Neill, D., P. D. Turner, D. B. O’Meara, E. A. Chadwick, L. Coffey, and C. O’Reilly. 2013. Development of novel realâ€time TaqMan® PCR assays for the species and sex identification of otter (Lutra lutra) and their application to noninvasive genetic monitoring. Molecular ecology resources 13:877-883.

Ortega J., D. Navarrete, and J. E. Maldonado. 2012. Non-invasive sampling of endangered neotropical river otters reveals high levels of dispersion in the Lacantun River System of Chiapas, Mexico. Animal Biodiversity and Conservation 35:59-69.

Parera, A. 1996. Las “nutrias verdaderas†de la Argentina. Fundación Vida Silvestre Argentina. Buenos Aires, Argentina.

Parera, A. 1993. The neotropical river otter Lutra longicaudis in Iberá lagoon, Argentina. IUCN Otter Spec Group Bull 8:13-16.

Park, H. C., T. Y. Han, D. C. Kim, M. S. Min, S. Y. Han, K. S. Kim, and H. Lee. 2011. Individual identification and sex determination of Eurasian otters (Lutra lutra) in Daegu city based on genetic analysis of otter spraint. Genes and Genomics 33:653–657.

Panasci, M., W. B. Ballard, S. Breck, D. Rodriguez, L. D. Densmore, D. B. Wester, and R. J. Baker. 2011. Evaluation of fecal DNA preservation techniques and effects of sample age and diet on genotyping success. The Journal of wildlife management 75:1616-1624.

Pearse, D., and C. Eckerman. 2001. A genetic analogue of “mark–recaptureâ€methods for estimating population size: an approach based on molecular parentage assessments. Molecular Ecology 10:2711-2718.

Pickles, R. S., J. J. Groombridge, V. D. Z. Rojas, and W. C. Jordan. 2009. Cross-species characterisation of polymorphic microsatellite loci in the giant otter (Pteronura brasiliensis). Molecular ecology resources 9:415–417.

Pickles, R. S., J. J. Groombridge, V. Z. Rojas, P. Van Damme, D. Gottelli, S. Kundu, and W. C. Jordan. 2011a. Evolutionary history and identification of conservation units in the giant otter, Pteronura brasiliensis. Molecular phylogenetics and evolution 61:616–627.

Pickles, R. S., J. J. Groombridge, V. Z. Rojas, P. Van Damme, D. Gottelli, C. V. Ariani, and W. C. Jordan. 2011b. Genetic diversity and population structure in the endangered giant otter, Pteronura brasiliensis. Conservation Genetics 13:235–245.

Pompanon, F., A. Bonin, E. Bellemain, and P. Taberlet. 2005. Genotyping errors: causes,consequences and solutions. Natural Revision in Genetics 6:847–849.

Prigioni, C. L., L. U. Remonti, and A. L. Balestrieri. 2006. Otter Lutra lutra movements assessed by genotyped spraints in southern Italy. Hystrix, the Italian Journal of Mammalogy 17:91–96.

Rheingantz, M .L., and C. S. Trinca. 2015. Lontra longicaudis. The IUCN Red List of Threatened Species 2015:e.T12304A21937379. http://dx.doi.org/10.2305/IUCN.UK.2015- 2.RLTS.T12304A21937379.

Roeder, A. D., F. I. Archer, H. N. Poinar, and P. A. Morin. 2004. A novel method for collection and preservation of faeces for genetic studies. Molecular Ecology Notes 4:761–764.

Rosas, F., and E. Colares. 1991. Mamíferos aquáticos da Amazônia brasileira. Pp 405-411 in Bases científicas para o estabelecimento de estratégias de preservação e desenvolvimento da Amazônia: fatos e perspectivas (Val, A. L., R. Figliuolo, and E. Feldsberg, eds.). Manaus. Brasil.

Smith, D. A., K. Ralls, A. Hurt, B. Adams, M. Parker, and J. E. Maldonado. 2006. Assessing reliability of microsatellite genotypes from kit fox faecal samples using genetic and GIS analyses. Molecular Ecology 15:387-406.

Spinola-Parallada, R., and C. Vaughan-Dickhaut. 1995. Abundancia relativa y actividad de marcaje de la nutria neotropical (Lutra longicaudis) en Costa Rica. Vida Silvestre Neotropical 4:38-45.

Taberlet, P., and S. Griffin. 1996. Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids 24:3189-3194.

Taberlet, P., and G. Luikart. 1999. Non-invasive genetic sampling and individual identification. Biological Journal of the Linnean Society 68:41–55.

Tchaicka, L., E. Eizirik, T. G. De Oliveira, J. F. Cândido, and T. R. Freitas. 2007. Phylogeography and population history of the crab-eating fox (Cerdocyon thous). Molecular Ecology 16:819–38.

Trigila, A. P., J. J. Gómez, M. H. Cassini, and J. I. Túnez. 2016. Genetic diversity in the Neotropical river otter, Lontra longicaudis (Mammalia, Mustelidae), in the Lower Delta of Parana River, Argentina and its relation with habitat suitability. Hydrobiologia 768:287-298.

Trinca, C. S., B. De Thoisy, F. C. Rosas, H. F. Waldemarin, K. P. Koepfli, J. A. Vianna, and E. Eizirik. 2012. Phylogeography and demographic history of the neotropical otter (Lontra longicaudis). The Journal of heredity 103:479–92.

Trinca, C. S., C. F. Jaeger, and E. Eizirik. 2013. Molecular ecology of the Neotropical otter (Lontra longicaudis): non-invasive sampling yields insights into local population dynamics. Biological Journal of the Linnean Society 109:932–948.

Trinca, C. S., H. F. Waldemarin, and E. Eizirik. 2007. Genetic diversity of the Neotropical otter (Lontra longicaudis Olfers, 1818) in Southern and Southeastern Brazil. Brazilian Journal of Biology 67:813–8.

Valqui, J., G. B. Hartl, and F. E. Zachos. 2010. Non-invasive genetic analysis reveals high levels of mtDNA variability in the endangered South-American marine otter (Lontra felina). Conservation Genetics 11:2067–2072.

Vergara, M., A. Ruiz-González, J. L. De Luzuriaga, and B. J. Gómez-Moliner. 2014. Individual identification and distribution assessment of otters (Lutra lutra) through non-invasive genetic sampling: Recovery of an endangered species in the Basque Country (Northern Spain). Mammalian Biology 79:259-267.

Vianna, J. A., P. Ayerdi, G. Medina-Vogel, J. C. Mangel, H. Zeballos, M. Apaza, and S. Faugeron. 2010. Phylogeography of the Marine Otter (Lontra felina): historical and contemporary factors determining its distribution. The Journal of heredity 101:676–689.

Vianna, J. A., G. Medina-Vogel, C. Chehébar, W. Sielfeld, C. Olavarría, and S. Faugeron. 2011. Phylogeography of the Patagonian otter Lontra provocax: adaptive divergence to marine habitat or signature of southern glacial refugia? BMC evolutionary biology 11:53

Waits, L., and D. Paetkau. 2005. Noninvasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection. Journal of Wildlife Management 69:1419-1433.

Waldemarin, H., and R. Alvares. 2008. Lontra longicaudis. IUCN 2010. Lista Roja de Especies Amenazadas IUCN. Versión 2010.1.

Wasser, S. K., C. S. Houston, G. M. Koehler, G. G. Cadd, and S. R. Fain. 1997. Techniques for application of faecal DNA methods to field studies of ursids. Molecular Ecology 6:1091–1097.

Weber, L. I., C. G. Hildebrand, A. Ferreira, G. Pedarassi, J. A. Levy, and E. P. Colares. 2009. Microsatellite genotyping from faeces of Lontra longicaudis from southern Brazil. REVISTA, 99:5–11.

White, S., D. D. B. O’meara, C. Shores, C. O. R. A. P Harrington, G. Weyman, and D. Sleeman. 2013. A non-invasive genetic survey of otters (Lutra lutra) in an urban environment : A pilot study with citizen scientists. IUCN Otter Specialist Group Bulletin 30:103–111.

Wilson, G., and A. Frantz. 2003. Estimation of badger abundance using faecal DNA typing. Journal of Applied Ecology 40:658-666.

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2018-01-26

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