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Conservation Genetics

, Volume 18, Issue 5, pp 1037–1046 | Cite as

The application of non-invasive genetic tagging reveals new insights into the clay lick use by macaws in the Peruvian Amazon

  • George OlahEmail author
  • Robert G. Heinsohn
  • Donald J. Brightsmith
  • Rod Peakall
Research Article

Abstract

Genetic tagging, the unique identification of individuals by their DNA profile, has proven to be an effective method for research on several animal species. In this study we apply non-invasive genetic tagging from feather samples to reveal the genetic structure and estimate local population size of red-and-green macaws (Ara chloropterus) without the need to capture these animals. The study was centered in the Tambopata region of the Peruvian Amazon. Here macaws frequently visit clay licks and their naturally molted feathers provide a unique source of non-invasively sampled DNA. We analyzed 249 feathers using nine microsatellite loci and identified 221 unique genotypes. The remainder revealed 21 individuals which were ‘recaptured’ one or more times. Using a capture-mark-recapture model the average number of different individuals visiting clay licks within one breeding season was estimated to fall between 84 and 316 individuals per clay lick. Analysis of population genetic structure revealed only small genetic differences among regions and clay licks, suggesting a single red-and-green macaw genetic population. Our study confirms the utility of non-invasive genetic tagging in harsh tropical environment to obtain crucial population parameters about an abundant parrot species that is very difficult to capture in the wild.

Keywords

Parrot Ara chloropterus Clay lick Feather Genetic tagging Microsatellite CMR 

Notes

Acknowledgements

This research was supported by funds from the Rufford Small Grants Foundation, Loro Parque Foundation, Idea Wild, and The Australian National University. Thanks to the Peruvian crew of this project for their enormous help with sample collection and field logistics: Braulio Poje Mishaja, Andres Veras, Jerico Solis, Crissel Vargas, Lizzie Ortiz, Gabriela Vigo, Nancy Carlos, Mabe Aguirre, Gustavo Martinez, the full staff and guides of Rainforest Expeditions, and the volunteers of the Tambopata Macaw Project. Thanks to George Powell and the WWF for providing some extra feather samples from Peru. Thanks for laboratory technical support to Christine Hayes and Cintia Garai. We thank for the laboratory space provided by the Unidad de Biotecnología Molecular, Laboratorio de Investigación y Desarrollo, Universidad Peruana Cayetano Heredia in Lima, Peru. Samples were collected under research permits from the Servicio Nacional de Areas Naturales Protegidas (SERNANP) in Peru. Genetic access to the samples was granted by the Servicio Nacional Forestal y de Fauna Silvestre (SERFOR) in Peru. CITES permits were provided by the Peruvian and Australian authorities (No 15PE000448/SP, No PWS2015-AU-001508). We thank to the anonymous reviewers whose constructive suggestions and comments improved the quality of this paper.

Supplementary material

10592_2017_954_MOESM1_ESM.pdf (204 kb)
Supplementary material 1 (pdf 204 KB)

References

  1. Andreou D, Vacquie-Garcia J, Cucherousset J, Blanchet S, Gozlan RE, Loot G (2012) Individual genetic tagging for teleosts: an empirical validation and a guideline for ecologists. J Fish Biol 80:181–194. doi: 10.1111/j.1095-8649.2011.03165.x CrossRefPubMedGoogle Scholar
  2. Baraloto C et al (2015) Effects of road infrastructure on forest value across a tri-national Amazonian frontier. Biol Conserv 191:674–681. doi: 10.1016/j.biocon.2015.08.024 CrossRefGoogle Scholar
  3. Beck NR, Peakall R, Heinsohn R (2008) Social constraint and an absence of sex-biased dispersal drive fine-scale genetic structure in white-winged choughs. Mol Ecol 17:4346–4358. doi: 10.1111/j.1365-294X.2008.03906.x CrossRefPubMedGoogle Scholar
  4. Bridge ES et al (2011) Technology on the move: recent and forthcoming innovations for tracking migratory birds. Bioscience 61:689–698. doi: 10.1525/bio.2011.61.9.7 CrossRefGoogle Scholar
  5. Brightsmith DJ (2004) Effects of weather on parrot geophagy in Tambopata, Peru. Wilson Bull 116:134–145CrossRefGoogle Scholar
  6. Brightsmith DJ (2005) Parrot nesting in Southeastern Peru: seasonal patterns and keystone trees. Wilson Bull 117:296–305CrossRefGoogle Scholar
  7. Brightsmith DJ, Aramburú Muñoz-Najar R (2004) Avian Geophagy and soil characteristics in Southeastern Peru. Biotropica 36:534–543Google Scholar
  8. Brightsmith DJ, Villalobos EM (2011) Parrot behavior at a Peruvian clay lick. Wilson Journal of Ornithology 123:595–602CrossRefGoogle Scholar
  9. Brightsmith DJ, Taylor J, Phillips TD (2008) The roles of soil characteristics and toxin adsorption in Avian Geophagy. Biotropica 40:766–774CrossRefGoogle Scholar
  10. Brouwer K, Jones ML, King CE, Schifter H (2000) Longevity records for Psittaciformes in captivity. Int Zoo Yearb 37:299–316CrossRefGoogle Scholar
  11. Bulut Z, Bragin EA, DeWoody JA, Braham MA, Katzner TE, Doyle JM (2016) Use of non-invasive genetics to assess nest and space use by White-tailed Eagles. J Raptor Res 50:351–362CrossRefGoogle Scholar
  12. Burger J, Gochfeld M (2003) Parrot behavior at a Rio Manu (Peru) clay lick: temporal patterns, associations and antipredator responses. Acta Ethol 6:23–34Google Scholar
  13. Bush KL et al (2011) Population structure and genetic diversity of greater sage-grouse (Centrocercus urophasianus) in fragmented landscapes at the northern edge of their range. Conserv Genet 12:527–542. doi: 10.1007/s10592-010-0159-8 CrossRefGoogle Scholar
  14. Caparroz R, Miyaki CY, Bampi MI, Wajntal A (2001) Analysis of the genetic variability in a sample of the remaining group of Spix’s Macaw (Cyanopsitta spixii, Psittaciformes: Aves) by DNA fingerprinting. Biol Conserv 99:307–311CrossRefGoogle Scholar
  15. Conover T (2003) Perú’s long haul: highway to riches, or ruin? Natl Geogr 203:80–100Google Scholar
  16. Dalén L, Götherström A, Meijer T, Shapiro B (2007) Recovery of DNA from Footprints in the Snow. Can Field-Nat 121:321–324CrossRefGoogle Scholar
  17. Forshaw JM (2011) Parrots of the world. vol Accessed from http://nla.gov.au/nla.cat-vn4839547. CSIRO Publishing, Collingwood
  18. Frankham R, Ballou JD, Briscoe DA (2004) A primer of conservation genetics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  19. Gebhardt KJ, Brightsmith D, Powell G, Waits LP (2009) Molted feathers from clay licks in Peru provide DNA for three large macaws (Ara ararauna, A. chloropterus, and A. macao). J Field Ornithol 80:183–192CrossRefGoogle Scholar
  20. Groom C, Warren K, Le Souef A, Dawson R (2015) Attachment and performance of Argos satellite tracking devices fitted to black cockatoos (Calyptorhynchus spp.). Wildlife Research 41:571–583. doi: 10.1071/WR14138 CrossRefGoogle Scholar
  21. Hoffman JI, Trathan PN, Amos W (2006) Genetic tagging reveals extreme site fidelity in territorial male Antarctic fur seals Arctocephalus gazella. Mol Ecol 15:3841–3847. doi: 10.1111/j.1365-294X.2006.03053.x CrossRefPubMedGoogle Scholar
  22. Horváth MB, Martínez-Cruz B, Negro JJ, Kalmár L, Godoy JA (2005) An overlooked DNA source for non-invasive genetic analysis in birds. J Avian Biol 36:84–88. doi: 10.1111/j.0908-8857.2005.03370.x CrossRefGoogle Scholar
  23. IUCN (2014) The IUCN Red List of Threatened Species. Version 2014.2. http://www.iucnredlist.org/.
  24. Jacob G, Debrunner R, Gugerli F, Schmid B, Bollmann K (2009) Field surveys of capercaillie (Tetrao urogallus) in the Swiss Alps underestimated local abundance of the species as revealed by genetic analyses of non-invasive samples. Conserv Genet 11:33–44. doi: 10.1007/s10592-008-9794-8 CrossRefGoogle Scholar
  25. Lee ATK, Kumar S, Brightsmith DJ, Marsden SJ (2010) Parrot claylick distribution in South America: do patterns of “where” help answer the question “why”? Ecography 33:1–4CrossRefGoogle Scholar
  26. Limiñana R, Arroyo B, Terraube J, McGrady M, Mougeot F (2015) Using satellite telemetry and environmental niche modelling to inform conservation targets for a long-distance migratory raptor in its wintering grounds. Oryx 49:329–337. doi: 10.1017/S0030605313001075 CrossRefGoogle Scholar
  27. Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766PubMedPubMedCentralGoogle Scholar
  28. Mantel N (1967) The Detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  29. Marques ARdO (2010) Caracterização da estrutura genética populacional das araras vermelhas Ara chloropterus e Ara macao (Psittaciformes, Aves). University of São Paulo, São PauloGoogle Scholar
  30. May DL (2001) Grey parrots of the Congo basin forest. PsittaScene 13:8–10Google Scholar
  31. Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evol Int J Org Evol 60:2399–2402. doi: 10.1111/j.0014-3820.2006.tb01874.x CrossRefGoogle Scholar
  32. Meirmans PG, Hedrick PW (2011) Assessing population structure: FST and related measures. Mol Ecol Resour 11:5–18. doi: 10.1111/j.1755-0998.2010.02927.x CrossRefPubMedGoogle Scholar
  33. 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. doi: 10.1111/j.1365-294X.2005.02577.x CrossRefPubMedGoogle Scholar
  34. Mollet P, Kéry M, Gardner B, Pasinelli G, Royle JA (2015) Estimating population size for capercaillie (Tetrao urogallus L.) with spatial capture-recapture models based on genotypes from one field sample. PLoS ONE 10:e0129020. doi: 10.1371/journal.pone.0129020 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Moran-Luis M et al (2014) Demographic status and genetic tagging of endangered capercaillie in NW Spain. PLoS ONE 9:e99799. doi: 10.1371/journal.pone.0099799 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Munn CA (1992) Macaw biology and ecotourism, or “When a bird in the bush is worth two in the hand”. In: Beissinger SR, Snyder NFR, Munn CA (eds) New world parrots in crisis: solutions from conservation biology. Smithsonian Institution Press, Washington, DC, pp 47–72Google Scholar
  37. Nycander E, Blanco DH, Holle KM, del Campo A, Munn CA, Moscoso JI, Ricalde DG (1995) Manu and Tambopata: nesting success and techniques for increasing reproduction in wild macaws in southeastern Peru. In: Abramson J, Spear BL, Thomsen JB (eds) The large macaws: their care, breeding and conservation. Raintree Publications, Fort Bragg, California, pp 423–443Google Scholar
  38. Olah G, Heinsohn RG, Espinoza JR, Brightsmith DJ, Peakall R (2015) An evaluation of primers for microsatellite markers in Scarlet Macaw (Ara macao) and their performance in a Peruvian wild population. Conserv Genet Resour 7:157–159. doi: 10.1007/s12686-014-0317-2 CrossRefGoogle Scholar
  39. Olah G, Butchart SHM, Symes A, Guzmán IM, Cunningham R, Brightsmith DJ, Heinsohn R (2016a) Ecological and socio-economic factors affecting extinction risk in parrots. Biodivers Conserv 25:205–223. doi: 10.1007/s10531-015-1036-z CrossRefGoogle Scholar
  40. Olah G, Heinsohn RG, Brightsmith DJ, Espinoza JR, Peakall R (2016b) Validation of non-invasive genetic tagging in two large macaw species (Ara macao and A. chloropterus) of the Peruvian Amazon. Conserv Genet Resour 8:499–509. doi: 10.1007/s12686-016-0573-4 CrossRefGoogle Scholar
  41. Owens IPF, Bennett PM (2000) Ecological basis of extinction risk in birds: Habitat loss versus human persecution and introduced predators. Proc Natl Acad Sci 97:12144–12148. doi: 10.1073/pnas.200223397 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Palsboll PJ et al (1997) Genetic tagging of humpback whales. Nature 388:767–769CrossRefPubMedGoogle Scholar
  43. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. doi: 10.1111/j.1471-8286.2005.01155.x CrossRefGoogle Scholar
  44. 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. doi: 10.1093/bioinformatics/bts460 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Peakall R, Ebert D, Cunningham R, Lindenmayer D (2006) Mark–recapture by genetic tagging reveals restricted movements by bush rats (Rattus fuscipes) in a fragmented landscape. J Zool 268:207–216. doi: 10.1111/j.1469-7998.2005.00011.x CrossRefGoogle Scholar
  46. Petit E, Valiere N (2006) Estimating population size with noninvasive capture-mark-recapture data. Conserv Biol 20:1062–1073. doi: 10.1111/j.1523-1739.2006.00417.x CrossRefPubMedGoogle Scholar
  47. Pires SF (2012) The illegal parrot trade: a literature review. Glob Crime 13:176–190CrossRefGoogle Scholar
  48. Pollock KH, Nichols JD, Simons TR, Farnsworth GL, Bailey LL, Sauer JR (2002) Large scale wildlife monitoring studies: statistical methods for design and analysis. Environmetrics 13:105–119 doi: 10.1002/env.514 CrossRefGoogle Scholar
  49. Powell LL, Powell TU, Powell GVN, Brightsmith DJ (2009) Parrots Take it with a Grain of Salt: Available Sodium Content May Drive Collpa (Clay Lick) Selection in Southeastern Peru. Biotropica 41:279–282CrossRefGoogle Scholar
  50. Prugnolle F, de Meeus T (2002) Inferring sex-biased dispersal from population genetic tools: a review. Heredity 88:161–165CrossRefPubMedGoogle Scholar
  51. Puechmaille SJ, Petit EJ (2007) Empirical evaluation of non-invasive capture–mark–recapture estimation of population size based on a single sampling session. J Appl Ecol 44:843–852. doi: 10.1111/j.1365-2664.2007.01321.x CrossRefGoogle Scholar
  52. Renton K, Brightsmith DJ (2009) Cavity use and reproductive success of nesting macaws in lowland forest of southeast Peru. J Field Ornithol 80:1–8CrossRefGoogle Scholar
  53. Ringler E, Mangione R, Ringler M (2015) Where have all the tadpoles gone? Individual genetic tracking of amphibian larvae until adulthood. Mol Ecol Resour 15:737–746. doi: 10.1111/1755-0998.12345 CrossRefPubMedGoogle Scholar
  54. Rudnick JA, Katzner TE, Bragin EA, Rhodes OE, Dewoody JA (2005) Using naturally shed feathers for individual identification, genetic parentage analyses, and population monitoring in an endangered Eastern imperial eagle (Aquila heliaca) population from Kazakhstan. Mol Ecol 14:2959–2967. doi: 10.1111/j.1365-294X.2005.02641.x CrossRefPubMedGoogle Scholar
  55. Rudnick JA, Katzner TE, Bragin EA, DeWoody (2008) A non-invasive genetic evaluation of population size, natal philopatry, and roosting behavior of non-breeding eastern imperial eagles (Aquila heliaca) in central Asia. Conserv Genet 9:667. doi: 10.1007/s10592-007-9397-9 CrossRefGoogle Scholar
  56. Ruegg KC et al (2014) Mapping migration in a songbird using high-resolution genetic markers. Mol Ecol 23:5726–5739. doi: 10.1111/mec.12977 CrossRefPubMedGoogle Scholar
  57. Ruibal M, Peakall R, Claridge A, Murray A, Firestone K (2010) Advancement to hair-sampling surveys of a medium-sized mammal: DNA-based individual identification and population estimation of a rare Australian marsupial, the spotted-tailed quoll (Dasyurus maculatus). Wildlife Research 37:27–38. doi: 10.1071/WR09087 CrossRefGoogle Scholar
  58. Schmidt KL (2013) Spatial and temporal patterns of genetic variation in scarlet macaws (Ara macao): implications for population management in La Selva Maya, Central America. Columbia University, New YorkGoogle Scholar
  59. Seabury CM et al. (2013) A multi-platform draft de novo genome assembly and comparative analysis for the Scarlet Macaw (Ara macao). PloS ONE 8:e62415–e62415CrossRefPubMedPubMedCentralGoogle Scholar
  60. Segelbacher G (2002) Noninvasive genetic analysis in birds: testing reliability of feather samples. Mol Ecol Notes 2:367–369. doi: 10.1046/j.1471-8286.2002.00180.x-i2 Google Scholar
  61. Sekino M, Saitoh K, Yamada T, Hara M, Yamashita Y (2005) Genetic tagging of released Japanese flounder (Paralichthys olivaceus) based on polymorphic DNA markers. Aquaculture 244:49–61. doi: 10.1016/j.aquaculture.2004.11.006 CrossRefGoogle Scholar
  62. Smith AL, Landguth EL, Bull CM, Banks SC, Gardner MG, Driscoll DA (2016) Dispersal responses override density effects on genetic diversity during post-disturbance succession. Proc R Soc Lond B. doi: 10.1098/rspb.2015.2934 Google Scholar
  63. Smouse PE, Long JC (1992) Matrix correlation analysis in anthropology and genetics. Am J Phys Anthropol 35:187–213. doi: 10.1002/ajpa.1330350608 CrossRefGoogle Scholar
  64. Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573CrossRefPubMedGoogle Scholar
  65. Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extensions of the mantel test of matrix correspondence. Syst Zool 35:627–632. doi: 10.2307/2413122 CrossRefGoogle Scholar
  66. Symes CT, Hughes JC, Mack AL, Marsden SJ (2006) Geophagy in birds of Crater Mountain Wildlife Management Area, Papua New Guinea. J Zool 268:87–96. doi: 10.1111/j.1469-7998.2005.00002.x CrossRefGoogle Scholar
  67. Valdéz-Peña RA, Ortiz-Maciel SG, Valdez Juarez SO, Enkerlin Hoeflich EC, Snyder NFR (2008) Use of clay licks by Maroon-fronted Parrots (Rhynchopsitta terrisi) in Northern Mexico. Wilson J Ornithol 120:176–180CrossRefGoogle Scholar
  68. Webster MS, Marra PP, Haig SM, Bensch S, Holmes RT (2002) Links between worlds: unraveling migratory connectivity. Trends in Ecol Evol 17:76–83. doi: 10.1016/S0169-5347(01)02380-1 CrossRefGoogle Scholar
  69. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:S120–S139 doi: 10.1080/00063659909477239 CrossRefGoogle Scholar
  70. Woods JG, Paetkau D, Lewis D, McLellan BN, Proctor M, Strobeck C (1999) Genetic tagging of free-ranging black and brown bears. Wildl Soc Bull 27:616–627 doi: 10.2307/3784082 Google Scholar
  71. Wright TF, Rodriguez AM, Fleischer RC (2005) Vocal dialects, sex-biased dispersal, and microsatellite population structure in the parrot Amazona auropalliata. Mol Ecol 14:1197–1205. doi: 10.1111/j.1365-294X.2005.02466.x CrossRefPubMedGoogle Scholar
  72. Wunderle JM Jr (1999) Pre- and post-hurricane fruit availability: implications for Puerto Rican Parrots in the Luquillo Mountains. Carib J Sci 35:249–264Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  1. 1.Fenner School of Environment and SocietyThe Australian National UniversityCanberraAustralia
  2. 2.Research School of BiologyThe Australian National UniversityCanberraAustralia
  3. 3.Department of Veterinary Pathobiology, Schubot Exotic Bird Health CenterTexas A&M UniversityCollege StationUSA

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