No CrossRef data available.
Article contents
Conservation implications of genetic structure in the Critically Endangered Hooded Grebe Podiceps gallardoi
Published online by Cambridge University Press: 22 August 2025
Summary
The Critically Endangered Hooded Grebe Podiceps gallardoi has suffered a population decline of 80% since the 1980s. The evolutionary history and its critical conservation status place it 20th in the EDGE of Existence Bird List (EDGE-ZSL) among the more than 10,000 bird species of the world. The identification of demographically independent units (“management units”) is essential to address appropriate conservation and management strategies for threatened species. Genetic markers can be used to infer isolated populations without the need for logistically expensive banding and recapture. We used blood samples of 71 Hooded Grebes (c.10% of the global population) from three reproductive populations located at different plateaus that hold over 90% of the species’ global population. We analysed genetic population structure using a 353-bp fragment of mtDNA control region and 1,886 RAD loci to study whether Hooded Grebes are philopatric or not. We did not find differences in genetic structure of populations between plateaus indicating that Hooded Grebes do not consistently return to their plateau of origin. Our results are critical to understanding the connection of populations throughout the full annual movement cycle and propose management actions accordingly.
Information
- Type
- Research Article
- Information
- Copyright
- © The Author(s), 2025. Published by Cambridge University Press on behalf of BirdLife International
References
Allendorf, F.W. and Luikart, G. (2007). Conservation and the Genetics of Populations. Oxford: Blackwell.Google Scholar
Arantes, L.S., Caccavo, J.A., Sullivan, J.K., Sparmann, S., Mbedi, S., Höner, O.P. et al. (2023). Scaling‐up RADseq methods for large datasets of non‐invasive samples: Lessons for library construction and data preprocessing. Molecular Ecology Resources 25, e13859. https://doi.org/10.1111/1755-0998.13859CrossRefGoogle ScholarPubMed
Battey, C.J., Linck, E.B., Epperly, K.L., French, C., Slager, D.L., Sykes, P.W. Jr et al. (2018). A migratory divide in the Painted Bunting (Passerina ciris). The American Naturalist 191, 259–268.CrossRefGoogle ScholarPubMed
Beltrán, J., Bertonatti, C., Johnson, A., Serret, A. and Sutton, P. (1992). Actualizaciones sobre la distribución, biología y estado de conservación del maca tobiano (Podiceps gallardoi). Hornero 13, 193–199.CrossRefGoogle Scholar
Berthold, P. (2001). Bird Migration: A General Survey. Oxford: Oxford University Press.CrossRefGoogle Scholar
Berthold, P. and Querner, U. (1981). Genetic basis of migratory behavior in European warblers. Science 212, 77–79.CrossRefGoogle ScholarPubMed
BirdLife International (2023). Species Factsheet: Hooded Grebe Podiceps gallardoi. Available at http://datazone.birdlife.org/species/factsheet/hooded-grebe-podiceps-gallardoi (accessed July 2023).Google Scholar
Brown, L.L., Singer, B.S. and Gorring, M.L. (2004). Paleomagnetism and 40 Ar/ 39 Ar chronology of lavas from Meseta del Lago Buenos Aires, Patagonia. Geochemistry, Geophysics, Geosystems 5, 1–21.10.1029/2003GC000526CrossRefGoogle Scholar
Catchen, J., Hohenlohe, P.A., Bassham, S., Amores, A. and Cresko, W.A. (2013). Stacks: an analysis tool set for population genomics. Molecular Ecology 22, 3124–3140.CrossRefGoogle ScholarPubMed
Chang, C.C., Chow, C.C., Tellier, L.C., Vattikuti, S., Purcell, S.M. and Lee, J.J. (2015). Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience 4, s13742–015.10.1186/s13742-015-0047-8CrossRefGoogle Scholar
Clausen, K.K., Madsen, J., Cottaar, F., Kuijken, E. and Verscheure, C. (2018). Highly dynamic wintering strategies in migratory geese: Coping with environmental change. Global Change Biology 24, 3214–3225.CrossRefGoogle ScholarPubMed
de Jong, M.J., de Jong, J.F., Hoelzel, A.R. and Janke, A. (2021). SambaR: An R package for fast, easy and reproducible population‐genetic analyses of biallelic SNP data sets. Molecular Ecology Resources 21, 1369–1379.Google Scholar
DeSaix, M.G., Bulluck, L.P., Eckert, A.J., Viverette, C.B., Boves, T.J., Reese, J.A. et al. (2019). Population assignment reveals low migratory connectivity in a weakly structured songbird. Molecular Ecology 28, 2122–2135.CrossRefGoogle Scholar
Díaz, S., Settele, J., Brondízio, E.S., Ngo, H.T., Agard, J., Arneth, A. et al. (2019). Pervasive human-driven decline of life on Earth points to the need for transformative change. Science 366, eaax3100.CrossRefGoogle Scholar
Driller, M., Arantes, L.S., Vilaça, S.T., Carrasco-Valenzuela, T., Heeger, F., Mbedi, S. et al. (2021). Achieving high-quality ddRAD-like reference catalogs for non-model species: the power of overlapping paired-end reads. BioRxiv p. 2020.04.03.024331.Google Scholar
Earl, D.A. and von Holdt, B.M. (2012). STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.Google Scholar
EDGE of Existence (EDGE-ZSL) (2023). Hooded Grebe Podiceps gallardoi. Zoological Society of London. Available at http://www.edgeofexistence.org/species/hooded-grebe/ (accessed 10 July 2023).Google Scholar
Ellegren, H. (2013). The evolutionary genomics of birds. Annual Review of Ecology, Evolution, and Systematics 44, 239–259.Google Scholar
Esler, D. (2000). Applying metapopulation theory to conservation of migratory birds. Conservation Biology 14, 366–372.CrossRefGoogle Scholar
Fasola, L. and Roesler, I. (2018). A familiar face with a novel behavior raises challenges for conservation: American mink in arid Patagonia and a critically endangered bird. Biological Conservation 218, 217–222.CrossRefGoogle Scholar
Faaborg, J., Holmes, R.T., Anders, A.D., Bildstein, K.L., Dugger, K.M., Gauthreaux, S.A. Jr et al. (2010). Recent advances in understanding migration systems of New World land birds. Ecological Monographs 80, 3–48.10.1890/09-0395.1CrossRefGoogle Scholar
Fjeldså, J. (1986). Feeding ecology and possible life history tactics of the Hooded Grebe Podiceps gallardoi. Ardea 74, 40–58.Google Scholar
Fjeldså, J. (2004). Bird Families of the World: The Grebes. Oxford: Oxford University Press.Google Scholar
Fraser, D.J. and Bernatchez, L. (2001). Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Molecular Ecology 10, 2741–2752.CrossRefGoogle ScholarPubMed
Gordon, A. and Hannon, G.J. (2010). Fastx-toolkit. FASTQ/A Short-reads Preprocessing Tools. Available at http://hannonlab.cshl.edu/fastx_toolkit/ (accessed 15 November 2023).Google Scholar
Hall, T.A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Helbig, A.J. (1991). Inheritance of migratory direction in a bird species: a cross-breeding experiment with SE- and SW-migrating blackcaps (Sylvia atricapilla). Behavioral Ecology and Sociobiology 28, 9–12.CrossRefGoogle Scholar
Hoffberg, S.L., Kieran, T.J., Catchen, J.M., Devault, A., Faircloth, B.C., Mauricio, R. et al. (2016). RAD cap: sequence capture of dual‐digest RAD seq libraries with identifiable duplicates and reduced missing data. Molecular Ecology Resources 16, 1264–1278.CrossRefGoogle Scholar
Jakobsson, M. and Rosenberg, N.A. (2007). CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806.10.1093/bioinformatics/btm233CrossRefGoogle ScholarPubMed
Johnson, A.E. (1997). Distribución Geográfica del Macá Tobiano (Podiceps gallardoi). Technical Report. Buenos Aires: Fundación Vida Silvestre Argentina.Google Scholar
Johnson, A.E. and Serret, A. (1994). Búsqueda del Paradero Invernal del Macá Tobiano (Podiceps gallardoi). Technical Report. Buenos Aires: Fundación Vida Silvestre Argentina.Google Scholar
Jonker, R.M., Kraus, R.H., Zhang, Q., van Hooft, P., Larsson, K., van der Jeugd, H.P. et al. (2013). Genetic consequences of breaking migratory traditions in barnacle geese Branta leucopsis. Molecular Ecology 22, 5835–5847.CrossRefGoogle ScholarPubMed
Konter, A. and Konter, M. (2006). Migration patterns and site fidelity of European Grebes Podicipedidae. Regulus 21, 1–17.Google Scholar
Kramer, G.R., Andersen, D.E., Buehler, D.A., Wood, P.B., Peterson, S.M., Lehman, J.A. et al. (2018). Population trends in Vermivora warblers are linked to strong migratory connectivity. Proceedings of the National Academy of Sciences of the USA – PNAS 115, E3192–E3200.Google ScholarPubMed
Krueger, F. (2021). Trimgalore. GitHub Repository. https://github.com/FelixKrueger/TrimGaloreGoogle Scholar
Lancelotti, J., Marinone, M.C. and Roesler, I. (2016). Rainbow trout effects on zooplankton in the reproductive area of the critically endangered hooded grebe. Aquatic Conservation: Marine and Freshwater Ecosystems 27, 128–136.CrossRefGoogle Scholar
Lancelotti, J.L. (2009). Caracterización Limnológica de Lagunas de La Provincia de Santa Cruz y Efectos de La Introducción de Trucha Arco Iris (Oncorhynchus mykiss) Sobre Las Comunidades Receptoras. PhD dissertation, Comahue National University, Bariloche.Google Scholar
Lancelotti, J.L., Pessacg, N.L., Roesler, I. and Pascual, M.A. (2020). Climate variability and trends in the reproductive habitat of the critically endangered hooded grebe. Aquatic Conservation: Marine and Freshwater Ecosystems 30, 554–564.10.1002/aqc.3240CrossRefGoogle Scholar
Lange, C.E. (1981). A season of observations on Podiceps gallardoi (Aves Podicipediformes). Ecology and ethology. Neotropica 27, 39–56.Google Scholar
Langmead, B. and Salzberg, S.L. (2012). Fast gapped-read alignment with Bowtie 2. Nature Methods 9, 357–359.10.1038/nmeth.1923CrossRefGoogle ScholarPubMed
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N. et al. (2009). The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079.10.1093/bioinformatics/btp352CrossRefGoogle ScholarPubMed
Lischer, H.E. and Excoffier, L. (2012). PGDSpider: an automated data conversion tool for connecting population genetics and genomics programs. Bioinformatics 28, 298–299.10.1093/bioinformatics/btr642CrossRefGoogle ScholarPubMed
Madsen, J. (2001). Spring migration strategies in Pink-footed Geese Anser brachyrhynchus and consequences for spring fattening and fecundity. Ardea 89, 43–55.Google Scholar
Marra, P.P., Cohen, E.B., Loss, S.R., Rutter, J.E. and Tonra, C.M. (2015). A call for full annual cycle research in animal ecology. Biology Letters 11, 20150552.CrossRefGoogle Scholar
Mazzoni, E. and Rabassa, J. (2018). Volcanic Landscapes and Associated Wetlands of Lowland Patagonia. The Latin American Book Series. Heidelberg: Springer Nature.CrossRefGoogle Scholar
Merlin, C. and Liedvogel, M. (2019). The genetics and epigenetics of animal migration and orientation: birds, butterflies and beyond. Journal of Experimental Biology 222, jeb191890.10.1242/jeb.191890CrossRefGoogle ScholarPubMed
Møller, A.P., Jokimäki, J., Skorka, P. and Tryjanowski, P. (2014). Loss of migration and urbanization in birds: a case study of the blackbird (Turdus merula). Oecologia 175, 1019–1027.10.1007/s00442-014-2953-3CrossRefGoogle ScholarPubMed
Moritz, C. (1994). Defining ‘Evolutionarily Significant Units’ for conservation. Trends in Ecology & Evolution 9, 373–375.Google ScholarPubMed
Mueller, T., O’Hara, R.B., Converse, S.J., Urbanek, R.P. and Fagan, W.F. (2013). Social learning of migratory performance. Science 341, 999–1002.10.1126/science.1237139CrossRefGoogle ScholarPubMed
Norris, D.R. and Taylor, C.M. (2006). Predicting the consequences of carry-over effects for migratory populations. Biology Letters 2, 148–151.10.1098/rsbl.2005.0397CrossRefGoogle ScholarPubMed
Ogawa, L.M., Pulgarin, P.C., Vance, D.A., Fjeldså, J. and van Tuinen, M. (2015). Opposing demographic histories reveal rapid evolution in grebes (Aves: Podicipedidae). The Auk: Ornithological Advances 132, 771–786.CrossRefGoogle Scholar
Palsbøll, P.J., Berube, M. and Allendorf, F.W. (2007). Identification of management units using population genetic data. Trends in Ecology & Evolution 22, 11–16.10.1016/j.tree.2006.09.003CrossRefGoogle ScholarPubMed
Paradis, E. (2010). pegas: an R package for population genetics with an integrated–modular approach. Bioinformatics 26, 419–420.CrossRefGoogle Scholar
Paradis, E., Baillie, S.R., Sutherland, W.J. and Gregory, R.D. (1998). Patterns of natal and breeding dispersal in birds. Journal of Animal Ecology 67, 518–536.CrossRefGoogle Scholar
Paris, J.R., Stevens, J.R. and Catchen, J.M. (2017). Lost in parameter space: a road map for stacks. Methods in Ecology and Evolution 8, 1360–1373.10.1111/2041-210X.12775CrossRefGoogle Scholar
Parmesan, C. and Yohe, G. (2003). A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42.CrossRefGoogle ScholarPubMed
Porcel, S., Fogel, M.L., Izaguirre, I., Roesler, I. and Lancelotti, J.L. (2022). Effect of rainbow trout introductions on food webs in lakes of the arid Patagonia. Hydrobiologia 849, 2057–2075.10.1007/s10750-022-04848-2CrossRefGoogle Scholar
Pritchard, J.K., Stephens, M. and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.10.1093/genetics/155.2.945CrossRefGoogle ScholarPubMed
Prugnolle, F. and De Meeus, T. (2002). Inferring sex-biased dispersal from population genetic tools: a review. Heredity 88(3), 161–165.10.1038/sj.hdy.6800060CrossRefGoogle ScholarPubMed
R Core Team (2017). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. www.r-project.orgGoogle Scholar
Roesler, I. (2015). The status of Hooded Grebe (Podiceps gallardoi) in Chile. Ornitologia Neotropical 26, 255–263.CrossRefGoogle Scholar
Roesler, I. (2016). Conservación del Macá Tobiano (Podiceps gallardoi): Factores que Afectan la Viabilidad de sus Poblaciones. PhD dissertation, Buenos Aires University.Google Scholar
Roesler, I., Fasola, L., Casañas, H., Hernández, P.M., De Miguel, A., Giusti, M.E. et al. (2016). Colony guardian programme improves recruitment in the critically endangered hooded grebe Podiceps gallardoi in Austral Patagonia, Argentina. Conservation Evidences 13, 62–66.Google Scholar
Roesler, I., Imberti, S., Casañas, H., Mahler, B. and Reboreda, J.C. (2012a). Hooded Grebe Podiceps gallardoi population decreased by eighty per cent in the last twenty-five years. Bird Conservation International 22, 371–382.CrossRefGoogle Scholar
Roesler, I., Imberti, S., Casañas, H. and Volpe, N. (2012b). A new threat for the globally Endangered Hooded Grebe Podiceps gallardoi: the American mink Neovison vison. Bird Conservation International. 22, 383–388.CrossRefGoogle Scholar
Roesler, I., Lancelotti, J.L., Gabarain, G.T., Buchanan, P.I., Hernández, P.M. and Fasola, L. (2025). Hooded Grebe (Podiceps gallardoi), version 2.0. In Schulenberg, T.S. (ed.) Birds of the World. Ithaca: Cornell Lab of Ornithology. Available at https://birdsoftheworld.org/bow/species/hoogre1/cur/introduction (accessed 29 July 2023).Google Scholar
Rolshausen, G., Segelbacher, G., Hobson, K.A. and Schaefer, H.M. (2009). Contemporary evolution of reproductive isolation and phenotypic divergence in sympatry along a migratory divide. Current Biology 19, 2097–2101.10.1016/j.cub.2009.10.061CrossRefGoogle ScholarPubMed
Root, T.L., Price, J.T., Hall, K.R., Schneider, S.H., Rosenzweig, C. and Pounds, J.A. (2003). Fingerprints of global warming on wild animals and plants. Nature 421, 57–60.10.1038/nature01333CrossRefGoogle ScholarPubMed
Ruegg, K.C., Anderson, E.C., Paxton, K.L., Apkenas, V., Lao, S., Siegel, R.B. et al. (2014). Mapping migration in a songbird using high-resolution genetic markers. Molecular Ecology 23, 5726–5739.10.1111/mec.12977CrossRefGoogle Scholar
Rumboll, M.A.E. (1974). Una nueva especie de Macá (Podicipitidae). Revista del Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’ 4, 33–35.Google Scholar
Runge, C.A., Martin, T.G., Possingham, H.P., Willis, S.G. and Fuller, R.A. (2014). Conserving mobile species. Frontiers in Ecology and the Environment 12, 395–402.CrossRefGoogle Scholar
Sherry, T.W. (2018). Identifying migratory birds’ population bottlenecks in time and space. Proceedings of the National Academy of Sciences of the USA – PNAS 115, 3515–3517.10.1073/pnas.1802174115CrossRefGoogle ScholarPubMed
Sutherland, W.J. (1998). Evidence for flexibility and constraint in migration systems. Journal of Avian Biology 29, 441–446.10.2307/3677163CrossRefGoogle Scholar
Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.10.1093/nar/22.22.4673CrossRefGoogle ScholarPubMed
Vilaça, S.T., Maroso, F., Lara, P., de Thoisy, B., Chevallier, D., Arantes, L.S. et al. (2023). Evidence of backcross inviability and mitochondrial DNA paternal leakage in sea turtle hybrids. Molecular Ecology 32, 628–643.10.1111/mec.16773CrossRefGoogle ScholarPubMed
Visser, M.E. and Both, C. (2005). Shifts in phenology due to global climate change: the need for a yardstick. Proceedings of the Royal Society B: Biological Sciences 272, 2561–2569.10.1098/rspb.2005.3356CrossRefGoogle ScholarPubMed
Visser, M.E., Perdeck, A.C., Van Balen, J.H. and Both, C. (2009). Climate change leads to decreasing bird migration distances. Global Change Biology 15, 1859–1865.CrossRefGoogle Scholar
Wright, S. (1943). Isolation by distance. Genetics 28, 114–138.10.1093/genetics/28.2.114CrossRefGoogle ScholarPubMed
Roesler et al. supplementary material 1
Roesler et al. supplementary material
File
14 KB
Roesler et al. supplementary material 2
Roesler et al. supplementary material
File
17.1 KB