Skip to main content

Estimating genetic and demographic parameters relevant for the conservation of the Neotropical otter, Lontra longicaudis, in Mexico

Conservation Genetics volume 21, pages 719–734 (2020)Cite this article

Abstract

Habitat deterioration and fragmentation increase the risk of wildlife extirpation as they have strong impacts on population size, genetic diversity and gene flow. Small populations are more susceptible to these factors because the loss of genetic diversity by drift and inbreeding occurs at faster rates. Therefore, estimates of genetic diversity and population sizes of threatened and small wildlife populations in deteriorated landscapes are critical for managing and conservation. Here, we used a non-invasive sampling approach in combination with eleven microsatellite loci to evaluate genetic diversity, genetic structure, and demographic parameters of the Neotropical otter (Lontra longicaudis) in three river basins (Actopan, La Antigua and Jamapa), which are priority conservation areas for Veracruz, Mexico. Our results revealed moderate genetic diversity and genetic structure among river basins. However, we detected first-generation migrants among basins, suggesting current gene flow. Effective population size for each basin was considerably lower than the value (Ne < 100) suggested to maintain genetic variation of populations in the short-term. Similarly, census population size was lower than estimates reported for L. longicaudis in a conserved region in Mexico. We did not find evidence of recent genetic bottlenecks for any basin. Our genetic and demographic results suggest that L. longicaudis in the three river basins could be experiencing genetic isolation and erosion, with La Antigua being the most vulnerable basin. Natural fragmentation and habitat deterioration seem to be shaping the observed patterns of genetic variation in the Neotropical otter.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Allendorf FW, Luikart G, Aitken S (2013) Conservation and the genetics of populations. Blackwell Publishing, Massachusetts

    Google Scholar 

  • Amos W, Wilmer JW, Fullard K et al (2001) The influence of parental relatedness on reproductive success. Proc Biol Sci 268:2021–2027

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aparicio JM, Ortego J, Cordero PJ (2006) What should we weigh to estimate heterozygosity, alleles or loci? Mol Ecol 15:4659–4665

    CAS  PubMed  Google Scholar 

  • Arellano E, Sánchez Nuñez E, Mosquera MA (2012) Distribución y abundancia de la nutria neotropical (Lontra longicaudis annectens) en Tlacotalpan, Veracruz, México. Acta Zool Mex 28:270–279

    Google Scholar 

  • Aristizábal Duque SL, Orozco-Jiménez LY, Zapata-Escobar C, Palacio-Baena JA (2018) Conservation genetics of otters: review about the use of non-invasive samples. Therya 9:85–93

    Google Scholar 

  • Arrendal J, Vilà C, Björklund M (2007) Reliability of noninvasive genetic census of otters compared to field censuses. Conserv Genet 8:1097–1107

    Google Scholar 

  • Beichman AC et al (2019) Aquatic adaptation and depleted diversity: a deep dive into the genomes of the sea otter and giant otter. Mol Biol Evol. https://doi.org/10.1093/molbev/msz101

    Article  PubMed  PubMed Central  Google Scholar 

  • Beheler A, Fike S, Rhodes G, Serfass OE, Thomas L (2004) Development of polymorphic microsatellite loci for North American river otters (Lontra canadensis) and amplification in related Mustelids. Mol Ecol Notes 4:56–58

    CAS  Google Scholar 

  • Beheler A, Fike S, Dharmarajan JA, Rhodes G, Serfass OE, Thomas L (2005) Ten new polymorphic microsatellite loci for North American river otters (Lontra canadensis) and their utility in related mustelids. Mol Ecol Notes 5:602–604

    CAS  Google Scholar 

  • Biaffi D, Williams DA (2017) Use of non-invasive techniques to determine population size of the marine otter in two regions of Peru. Mammal biol 84:12–19

    Google Scholar 

  • Bouzat JL (2010) Conservation genetics of population bottlenecks: the role of chance, selection, and history. Conserv Genet 11:463–478

    Google Scholar 

  • Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225

    PubMed  Google Scholar 

  • Byrne MS, Quintana RD, Bolkovic MA, Cassini MH, Túnez JI (2015) The role of river drainages in shaping the genetic structure of capybara populations. Genetica 6:645–656

    Google Scholar 

  • Carranza ML et al (2012) Connectivity providers for semi-aquatic vertebrates: the case of the endangered otter in Italy. Landsc Ecol 27:281–290

    Google Scholar 

  • Chapman JR, Nakagawa S, Coltman DW, Slate J, Sheldon BC (2009) A quantitative review of heterozygosity–fitness correlations in animal populations. Mol Ecol 18:2746–2765

    CAS  PubMed  Google Scholar 

  • Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 243:621–631

    Google Scholar 

  • Cianfrani C, Broennimann O, Loy A, Guisan A (2018) More than range exposure: global otter vulnerability to climate change. Biol Conserv 221:103–113

    Google Scholar 

  • Cotler-Ávalos H, Garrido A, Bunge V, Cuevas ML (2010) Las cuencas hidrográficas de México: priorización y toma de decisiones. In: Cotler-Ávalos H, et al. (eds) Las cuencas hidrográficas de México. Diagnóstico y priorización. Pluralia Ediciones e Impresiones, Mexico City

    Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Crawford JC, Liu Z, Nelson TA, Nielsen CK, Bloomquist CK (2009) genetic population structure within and between beaver (Castor canadensis) populations in Illinois. J Mammal 90:373–379

    Google Scholar 

  • Crow JF, Kimura M (1970) An introduction in population genetics theory. Harper and Row, New York

    Google Scholar 

  • Cushman SA, McRae B, Adriaensen F, Beier P, Shirley M, Zeller K (2013) Biological corridors and connectivity. In: Macdonald DW, Willis KJ (eds) Key topics in conservation biology 2. Wiley, Oxford, pp 384–404

    Google Scholar 

  • Di Fonzo MMI, Pelletier F, Clutton-Brock TH, Pemberton JM, Coulson T (2011) The population growth consequences of variation in individual heterozygosity. PLoS ONE 6:e19667. https://doi.org/10.1371/journal.pone.0019667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Do C, Waples RS, Peel D, Macbeth GM, Tillett BF, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214

    CAS  PubMed  Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genets Resour 4:359–361

    Google Scholar 

  • Environmental Systems Research Institute (ESRI) (2013) ArcGIS Desktop: Release 10.2.1. Redlands, CA

  • Epperson BK (2005) Estimating dispersal from short distance spatial autocorrelation. Heredity 95:7–15

    CAS  PubMed  Google Scholar 

  • Epps CW, Keyghobadi N (2015) Landscape genetics in a changing world: disentangling historical and contemporary influences and inferring change. Mol Ecol 24:6021–6040

    PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    CAS  PubMed  Google Scholar 

  • Ferreira CM, Sabino-Marques H, Barbosa S (2018) Genetic non-invasive sampling (GNIS) as a cost-effective tool for monitoring elusive small mammals. Eur J Wildl Res. https://doi.org/10.1007/s10344-018-1188-8

    Article  Google Scholar 

  • Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508

    Google Scholar 

  • Frankham R (2010) Where are we in conservation genetics and where do we need to go? Conserv Genet 11:661–663

    Google Scholar 

  • Frankham R (2015) Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Mol Ecol 24:2610–2618

    PubMed  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Google Scholar 

  • Frankham R, Bradshaw CJA, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conserv 170:56–63

    Google Scholar 

  • Frankham JD, Ralls RK, Eldridge MDB et al (2017) Genetic management of fragmented animal and plant populations. Oxford University Press, Oxford

    Google Scholar 

  • Franklin IR (1980) Evolutionary change in small populations. In: Soule ME, Wilcox BA (eds) Conservation biology: an evolutionary-ecological perspective. Sinauer Associate, Sunderland, pp 135–149

    Google Scholar 

  • Franklin IR, Frankham R (1998) How large must populations be to retain evolutionary potential? Anim Conserv 1:69–73

    Google Scholar 

  • Gagne RB, Tinker MT, Gustafson KD (2018) Measures of effective population size in sea otters reveal special considerations for wide-ranging species. Evol Appl 11:1779–1790

    PubMed  PubMed Central  Google Scholar 

  • Gallo-Reynoso JP (1997) Situación y distribución de las nutrias en México, en énfasis en Lontra longicaudis annectens MAJOR, 1897. Rev Mex Mastozool 2:10–32

    Google Scholar 

  • Gallo-Reynoso (2007) Evaluación del riesgo de extinción de Lontra longicaudis de acuerdo al numeral 5–7 de la NOM-059-ECOL-2001. In: Sánchez O et al. Método de Evaluación del Riesgo de Extinción de las Especies Silvestres en México (MER). INE-SEMARNAT CONABIO, Mexico City

  • Galpern P, Manseau M, Hettinga P, Smith K, Wilson P (2012) Allelematch: an R package for identifying unique multilocus genotypes where genotyping error and missing data may be present. Mol Ecol Resour 12:771–778

    PubMed  Google Scholar 

  • Gerlach G, Jueterbock A, Kraemer P, Deppermann J, Harmand P (2010) Calculations of population differentiation based on G(ST) and D: Forget G(ST) but not all of statistics! Mol Ecol 19:3845–3852

    PubMed  Google Scholar 

  • Gilbert KJ, Whitlock MC (2015) Evaluating methods for estimating local effective population size with and without migration. Evolution 69:2154–2166

    PubMed  Google Scholar 

  • González-Chisten A, Delfín-Alfonso CA, Sosa-Martínez A (2013) Distribución y abundancia de la nutria neotropical (Lontra longicaudis annectens Major, 1897) en el lago de Catemaco Veracruz, México. Therya 4:201–217

    Google Scholar 

  • Goudet J (2001) FSTAT, version 2.9. 3, A program to estimate and test gene diversities and fixation indices. Lausanne University, Lausanne

    Google Scholar 

  • Goossens B et al (2005) Patterns of genetic diversity and migration in increasingly fragmented and declining orangutan (Pongo pygmaeus) populations from Sabah, Malaysia. Mol Ecol 14:441–456

    CAS  PubMed  Google Scholar 

  • Guerrero J, Gallo-reynoso JP, Biek R (2015) Mitochondrial DNA diversity, genetic structure, and demographic history of the Neotropical otter (Lontra longicaudis) in Mexico. J Mammal 96:1162–1173

    Google Scholar 

  • Hague MT, Routman EJ (2016) Does population size affect genetic diversity? A test with sympatric lizard species. Heredity 116:92–98

    CAS  PubMed  Google Scholar 

  • Hedrick PW (2005) Genetics of populations. Jones and Bartlett publishers, Massachusetts

    Google Scholar 

  • Hernández-Romero PC, Gutiérrez-Rodríguez C, Valdespino C, Prieto-Torres DA (2017) The role of geographical and ecological factors on population divergence of the neotropical otter Lontra longicaudis (Carnivora, Mustelidae). Evol Biol 45:37–55

    Google Scholar 

  • Hernández-Romero PC, Botello-López FJ, Hernández-García N, Espinosa-Rodríguez J (2018) New Altitudinal Record of Neotropical Otter (Lontra longicaudis Olfers, 1818) and Conflict with Fish Farmers in Mexico. Otter Spec Group Bull 35:193–197

    Google Scholar 

  • Higgins K, Lynch M (2001) Metapopulation extinction caused by mutation accumulation. PNAS 98:2928–2933

    CAS  PubMed  PubMed Central  Google Scholar 

  • Honorato R, Crouzeilles R, Ferreira MS, Grelle CEV (2015) The effects of habitat availability and quality on small mammals abundance in the Brazilian Atlantic Forest. Natureza & Conservação 13:133–138

    Google Scholar 

  • Huang AC et al (2018) River otters (Lontra canadensis) “trapped” in a coastal environment contaminated with persistent organic pollutants: demographic and physiological consequences. Environ Pollut 238:306–316

    CAS  PubMed  Google Scholar 

  • Hughes JM, Schmidt DJ, Finn DS (2009) Genes in Streams: using dna to understand the movement of freshwater fauna and their riverine habitat. Bioscience 59:573–583

    Google Scholar 

  • Instituto Nacional de Estadística, Geografía e Informática - INEGI (2016) Continuo De Elevación Mexicano, CEM 3.0. https://www.inegi.org.mx/app/geo2/elevacionesmex/. Accessed 27 Jan 2016

  • Instituto Nacional de Estadística y Geografía (INEGI) (2011) Sistema de consultas de las cuencas hidrográficas de México. Disponible en. https://cuencas.ine.gob.mx/cuenca/

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    CAS  PubMed  Google Scholar 

  • Janssens X, Fontaine MC, Michaux JR, Libois R, De Kermabon J, Defourny P, Baret PV (2008) Genetic pattern of the recent recovery of European otters in southern France. Ecography 31:176–186

    Google Scholar 

  • Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    CAS  PubMed  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 94:1471–2156

    Google Scholar 

  • Jost L (2008) Gst and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    PubMed  Google Scholar 

  • Kalinowski ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conserv Genet 5:539–543

    CAS  Google Scholar 

  • Kalinowski ST (2005) HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:187–189

    CAS  Google Scholar 

  • Keyghobadi N (2007) The genetic implications of habitat fragmentation for animals. Can J Zool 85:1049–1064

    Google Scholar 

  • Knaepkens G, Bervoets L, Verheyen E, Eens M (2004) Relationship between population size and genetic diversity in endangered populations of the European bullhead (Cottus gobio): implications for conservation. Biol Conserv 115:403–410

    Google Scholar 

  • Kretzmann M, Mentzer L, DiGiovanni R, Leslie MS, Amato G (2006) Microsatellite diversity and fitness in stranded juvenile harp seals (Phoca groenlandica). J Hered 97:555–560

    CAS  PubMed  Google Scholar 

  • Kruuk H (2006) Otters: ecology, behaviour and conservation. Oxford University Press, Oxford

    Google Scholar 

  • Lariviére S (1999) Lontra longicaudis. Mamm Species 609:1–5

    Google Scholar 

  • Larson S, Jameson R, EtnierM FM, Bentzen P (2002) Loss of genetic diversity in sea otters (Enhydra lutris) associated with the fur trade of the 18th and 19th centuries. Mol Ecol 11:1899–1903

    CAS  PubMed  Google Scholar 

  • Larson S, Jameson R, Etnier M, Jones T, Hall R (2012) Genetic diversity and population parameters of sea otters, Enhydra lutris, before Fur Trade Extirpation from 1741–1911. PLoS ONE 7(3):e32205. https://doi.org/10.1371/journal.pone.0032205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Latorre-Cardenas MC, Gutiérrez Rodríguez C, Lance S (2020) Isolation and characterization of 13 microsatellite loci for the Neotropical otter, Lontra longicaudis, by next generation sequencing. Mol Biol Rep 47:731–736

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Luikart G, Sherwin WB, Steele BM, Allendorf FW (1998) Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Mol Ecol 7:963–974

    CAS  PubMed  Google Scholar 

  • Luikart G et al (2010) Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conserv Genet 11:355–373

    CAS  Google Scholar 

  • Mable BK (2019) Conservation of adaptive potential and functional diversity: integrating old and new approaches. Conserv Genet 20:89. https://doi.org/10.1007/s10592-018-1129-9

    Article  CAS  Google Scholar 

  • Macías-Sánchez S, Aranda M (1999) Análisis de la alimentación de la nutria Lontra longicaudis (Mammalia: Carnivora) en un sector del Río Los Pescados, Veracruz, México. Acta Zoologica Mexicana 76:49–57. https://doi.org/10.21829/azm.1999.76761699

    Article  Google Scholar 

  • Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197

    Google Scholar 

  • Markert JA, Grant PR, Grant BR, Keller LF, Coombs JL, Petren K (2004) Neutral locus heterozygosity, inbreeding, and survival in Darwin's ground finches (Geospiza fortis and G. scandeus). Heredity 92:306–315

    CAS  PubMed  Google Scholar 

  • Markert JA, Champlin DM, Gutjahr-Gobell R et al (2010) Population genetic diversity and fitness in multiple environments. BMC Evol Biol. https://doi.org/10.1186/1471-2148-10-205

    Article  PubMed  PubMed Central  Google Scholar 

  • Meffe GK, Vrijenhoek RC (1988) Conservation genetics in the management of desert fishes. Conserv Biol 2:157–169

    Google Scholar 

  • Miller CR, Joyce P, Waits LP (2005) A new method for estimating the size of small populations from genetic mark-recapture data. Mol Ecol 14:1991–2005

    CAS  PubMed  Google Scholar 

  • Morris DW, Clark R, Boyce MS (2008) Habitat and habitat selection: theory, tests, and implications. Isr J Ecol Evol 54:287–294

    Google Scholar 

  • Mowry RA et al (2015) Genetics and the successful reintroduction of the Missouri river otter. Anim Conserv 18:196–206

    Google Scholar 

  • Mumma MA, Zieminski C, Fuller TK, Mahoney SP, Waits LP (2015) Evaluating non-invasive genetic sampling techniques to estimate large carnivore abundance. Mol Ecol Resour 15:1133–1144. https://doi.org/10.1111/1755-0998.12390

    Article  PubMed  Google Scholar 

  • Ortega J, Navarrete D, Maldonado JE (2012) Non-invasive sampling of endangered neotropical river otters reveals high levels of dispersion in the Lacantun River System of Chiapas, Mexico. Anim Biodiv Conserv 35:59–69

    Google Scholar 

  • Pacifici M, Santini L, Di Marco M, Baisero D et al (2013) Generation length for mammals. Nat Conserv 5:89–94. https://doi.org/10.3897/natureconservation.5.5734

    Article  Google Scholar 

  • Pagacz S (2016) The effect of a major drainage divide on the gene flow of a semiaquatic carnivore, the Eurasian otter. J Mamm 97:1164–1176

    Google Scholar 

  • Palstra FP, Ruzzante DE (2008) Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Mol Ecol 17:3428–3447

    PubMed  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peery MZ, Kirby R, Reid BN, Stoelting R, Doucet-Beer E, Robinson S, Vásquez-Carrillo C, Palsbøll PJN (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418

    PubMed  Google Scholar 

  • Pennell MW, Stansbury CR, Waits LP, Miller CR (2013) Capwire: a R package for estimating population census size from non-invasive genetic sampling. Mol Ecol Resour 13:154–157

    PubMed  Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (2008) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Google Scholar 

  • Pflüger FJ, Signer J, Balkenhol N (2019) Habitat loss causes non-linear genetic erosion in specialist species. Glob Ecol Conserv 17:e00507

    Google Scholar 

  • Pickles RSA, Groombridge JJ, Rojas VDZ et al (2012) Genetic diversity and population structure in the endangered giant otter, Pteronura brasiliensis. Conserv Genet 13:235–245

    Google Scholar 

  • Pigneur LM, Caublot G, Fournier-Chambrillon C et al (2019) Current genetic admixture between relictual populations might enhance the recovery of an elusive carnivore. Conserv Genet 20:1133. https://doi.org/10.1007/s10592-019-01199-9

    Article  Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J Hered 90:502–503

    Google Scholar 

  • Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    CAS  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev 6:847–859

    CAS  Google Scholar 

  • Quaglietta L, Fonseca VC, Hájková P, Mira A, Boitani L (2013) Fine-scale population genetic structure and short-range sex-biased dispersal in a solitary carnivore, Lutra lutra. J Mammal 94:561–571

    Google Scholar 

  • R Core Team (2017) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/

  • Ramos-Rosas NN, Valdespino C, García-Hernández J, Gallo-Reynoso JP, Olguín EJ (2012) Heavy metals in the habitat and throughout the food chain of the Neotropical otter, Lontra longicaudis, in protected Mexican wetlands. Environ Monit Assess 185:1163–1173

    PubMed  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using microsatellite genotypes. Proc Natl Acad Sci USA 94:9197–9201

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reed-Smith J (2008) North American river otter husbandry notebook. John Ball Zoological Garden, Grand Rapids

    Google Scholar 

  • Reed-Smith J (2012) North American river otter husbandry notebook. Grand Rapids Press, Michigan

    Google Scholar 

  • Rémy A, Le Galliard J, Gundersen G, Steen H, Andreassen HP (2011) Effects of individual condition and habitat quality on natal dispersal behaviour in a small rodent. J Anim Ecol 80:929–937

    PubMed  Google Scholar 

  • Rheingantz ML, Trinca CS (2015) Lontra longicaudis. The IUCN Red List of Threatened Species. https://doi.org/10.2305/IUCN.UK.2015-2.RLTS.T12304A21937379.en

    Article  Google Scholar 

  • Rheingantz ML, Trinca S-P (2017) The Neotropical otter Lontra longicaudis: a comprehensive update on the current knowledge and conservation status of this semiaquatic carnivore. Mamm Rev 47:291–305

    Google Scholar 

  • Rheingantz ML, de Menezes JFS, de Thoisy B (2014) Defining neotropical Otter Lontra Longicaudis distribution, conservation priorities and ecological frontiers. Trop Conserv Sci 7:214–229

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    PubMed  Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Google Scholar 

  • SEMARNAT (2010) NORMA Oficial Mexicana NOM-059-SEMARNAT-2010, Protección ambiental-Especies nativas de México de flora y fauna silvestres-Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-Lista de especies en riesgo. https://www.biodiversidad.gob.mx/especies/pdf/NOM_059_SEMARNAT_2010.pdf. Accessed 28 oct 2017

  • Selkoe KA, Scribner KT, Galindo HM (2015) Waterscape genetics——applications of landscape genetics to Rivers, Lakes, and Seas. In: Balkenhol N, Cushman S, Storfer AT, Waits L (eds) Landscape genetics. Wiley, Chichester, pp 220–246

    Google Scholar 

  • Smouse P, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573

    PubMed  Google Scholar 

  • Smouse PE, Peakall R, Gonzales E (2008) A heterogeneity test for fine-scale genetic structure. Mol Ecol 17:3389–3400

    PubMed  Google Scholar 

  • Soulé M (1976) Allozyme variation: its determinants in space and time. In: Ayala F (ed) Molecular evolution. Sinauer Associates, Sunderland, pp 60–77

    Google Scholar 

  • Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101:15261–15264

    CAS  PubMed  PubMed Central  Google Scholar 

  • Taberlet P, Griffin S, Goossens B, Questiau S et al (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 24:3189–3194

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tallmon DA, Koyuk A, Luikart G, Beaumont MA (2008) ONeSAMP: a program to estimate effective population size using approximate Bayesian computation. Mol Ecol Res 8:299–301

    Google Scholar 

  • Tison JL, Blennow V, Palkopoulou E et al (2015) Population structure and recent temporal changes in genetic variation in Eurasian otters from Sweden. Conserv Genet 16:371–384

    Google Scholar 

  • Townsend AK, Taffs CC, Wheeler SS et al (2018) Low heterozygosity is associated with vector-borne disease in crows. Ecosphere 9:e02407. https://doi.org/10.1002/ecs2.2407

    Article  Google Scholar 

  • Trigila AP, Gómez JJ, Cassini MH, Túnez JI (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

    Google Scholar 

  • Trinca CS, Jaeger CF, Eizirik E (2013) Molecular ecology of the Neotropical otter (Lontra longicaudis): non-invasive sampling yields insights into local population dynamics. Biol J Linn Soc 109:932–948

    Google Scholar 

  • Valière N (2002) GIMLET: a computer program for analyzing genetic individual identification data. Mol Ecol Notes 2:377–379

    Google Scholar 

  • van Oosterhout C, Hutchinson WF, Willis DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Google Scholar 

  • Vergeer P, Rengelink R, Copal A, Ouborg NJ (2003) The interacting effects of genetic variation, habitat quality and population size on performance of Succisa pratensis. J Ecol 91:18–26

    CAS  Google Scholar 

  • Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256

    CAS  PubMed  Google Scholar 

  • Wang J (2009) A new method for estimating effective population sizes from a single sample of multilocus genotypes. Mol Ecol 18:2148–2164

    PubMed  Google Scholar 

  • Wang J (2016) A comparison of single-sample estimators of effective population sizes from genetic marker data. Mol Ecol 25:4692–4711

    PubMed  Google Scholar 

  • Waples RS (1991) Genetic methods for estimating the effective size of cetacean populations. Rep Int Whal Commn 13:279–300

    Google Scholar 

  • Waples RS (2008) ldne: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 4:753–756

    Google Scholar 

  • Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–262

    PubMed  Google Scholar 

  • Waples RS, Yokota M (2007) Temporal estimates of effective population size in species with overlapping generations. Genetics 175:219–233

    PubMed  PubMed Central  Google Scholar 

  • Weber L, Hildebrand C, Ferreira A, Pedarass G, Levy J, Colares EP (2009) Microsatellite genotyping from faeces of Lontra longicaudis from southern Brazil. Iheringia Sér Zool 99:5–11

    Google Scholar 

  • Willoughby JR, Sundaram M, Wijayawardena BK, Kimble SJA et al (2015) The reduction of genetic diversity in threatened vertebrates and new recommendations regarding IUCN conservation rankings. Biol Conserv 191:495–503

    Google Scholar 

  • Wozney KM, Haxton TJ, Kjartanson S et al (2011) Genetic assessment of lake sturgeon (Acipenser fulvescens) population structure in the Ottawa River. Environ Biol Fish 90:183

    Google Scholar 

  • Wright S (1940) Breeding Structure of Populations in Relation to Speciation. Am Nat 74:232–248

    Google Scholar 

Download references

Acknowledgements

This work was partially supported by the National Geographic Society Early Career Grant (Grant No. # WW-185ER-17), by the Rufford Small Grants Foundation (Grant No. ID-19592-2) and by research funds from the Instituto de Ecología, A.C. (Grant No. 20012-11-080). María Camila Latorre-Cardenas is grateful with the Posgrado en Ciencias Biológicas of the Universidad Nacional Autónoma de México for the academic support provided during her doctoral studies and with the Consejo Nacional de Ciencia y Tecnología (CONACyT) for the Doctoral scholarship (#414864). This research constitutes a requirement for obtaining the doctoral degree of Latorre-Cardenas. The “Acuario de Veracruz, A.C.” donated blood from six individuals. Pablo C. Hernández-Romero, Tarcisio Solis and Luz Magali Sánchez Méndez provided field assistance; and Luz Magali Sánchez Méndez, Denisse Maldonado Sánchez and Cristina Bárcenas laboratory assistance.

Author information

Authors and Affiliations

  1. Red de Biología Evolutiva, Instituto de Ecología A.C., 91070, Xalapa, Veracruz, Mexico

    María Camila Latorre-Cardenas & Carla Gutiérrez-Rodríguez

  2. Posgrado Ciencias Biológicas, Universidad Nacional Autónoma de México, 04510, Mexico City, Mexico

    María Camila Latorre-Cardenas

  3. Red de Diversidad Biológica del Occidente Mexicano, Instituto de Ecología A.C., 61600, Pátzcuaro, Michoacán, Mexico

    Yessica Rico

  4. CONACyT, 03940, Mexico City, Mexico

    Yessica Rico

Authors
  1. María Camila Latorre-Cardenas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carla Gutiérrez-Rodríguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yessica Rico
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to María Camila Latorre-Cardenas.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

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

Verify currency and authenticity via CrossMark

Cite this article

Latorre-Cardenas, M.C., Gutiérrez-Rodríguez, C. & Rico, Y. Estimating genetic and demographic parameters relevant for the conservation of the Neotropical otter, Lontra longicaudis, in Mexico. Conserv Genet 21, 719–734 (2020). https://doi.org/10.1007/s10592-020-01283-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-020-01283-5

Keywords

  • Lontra longicaudis
  • Effective population size
  • Genetic structure
  • Gene flow
  • Freshwater ecosystems
  • Non-invasive genetic sampling