Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-05T02:59:15.820Z Has data issue: false hasContentIssue false
  • English
  • Français

Influence of historical and contemporary habitat changes on the population genetics of the endemic South African parrot Poicephalus robustus

Published online by Cambridge University Press:  22 August 2019

WILLEM G. COETZER Open the ORCID record for WILLEM G. COETZER [Opens in a new window] ,
COLLEEN T. DOWNS ,
MIKE R. PERRIN  and
SANDI WILLOWS-MUNRO Open the ORCID record for SANDI WILLOWS-MUNRO [Opens in a new window]
WILLEM G. COETZER
Affiliation:
School of Life Sciences, University of KwaZulu-Natal, P/Bag X01, Scottsville, Pietermaritzburg3209, South Africa.
COLLEEN T. DOWNS
Affiliation:
School of Life Sciences, University of KwaZulu-Natal, P/Bag X01, Scottsville, Pietermaritzburg3209, South Africa.
MIKE R. PERRIN
Affiliation:
School of Life Sciences, University of KwaZulu-Natal, P/Bag X01, Scottsville, Pietermaritzburg3209, South Africa.
SANDI WILLOWS-MUNRO*
Affiliation:
School of Life Sciences, University of KwaZulu-Natal, P/Bag X01, Scottsville, Pietermaritzburg3209, South Africa.
*
*Author for correspondence; e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The Cape Parrot Poicephalus robustus is a habitat specialist, restricted to forest patches in the Eastern Cape (EC), KwaZulu-Natal (KZN) and Limpopo provinces of South Africa. Recent census estimates suggest that there are less than 1,600 parrots left in the wild, although historical data suggest that the species was once more numerous. Fragmentation of the forest biome is strongly linked to climate change and exploitation of the forest by the timber industry. We examine the subpopulation structure and connectivity between fragmented populations across the distribution of the species. Differences in historical and contemporary genetic structure of Cape Parrots is examined by including both modern samples, collected from 1951 to 2014, and historical samples, collected from 1870 to 1946. A total of 114 individuals (historical = 29; contemporary = 85) were genotyped using 16 microsatellite loci. We tested for evidence of partitioning of genotypes at both a temporal and spatial scales by comparing shifts in allelic frequencies of historical (1870–1946) and contemporary (1951–2014) samples across the distribution of the species. Tests for population bottlenecks were also conducted to determine if anthropogenic causes are the main driver of population decline in this species. Analyses identified three geographically correlated genetic clusters. A southern group restricted to forest patches in the EC, a central group including birds from KZN and a genetically distinct northern Limpopo cluster. Results suggest that Cape Parrots have experienced at least two population bottlenecks. An ancient decline during the mid-Holocene (∼ 1,800-3,000 years before present) linked to climate change, and a more recent bottleneck, associated with logging of forests during the early 1900s. This study highlights the effects of climate change and human activities on an endangered species associated with the naturally fragmented forests of eastern South Africa. These results will aid conservation authorities with the planning and implementation of future conservation initiatives. In particular, this study emphasises the Eastern Cape mistbelt forests as an important source population for the species and calls for stronger conservation of forest patches in South Africa to promote connectivity of forest taxa.

Type
Research Article
Information
Bird Conservation International , Volume 30 , Issue 2 , June 2020 , pp. 236 - 259
Copyright
© BirdLife International, 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arif, I. A. and Khan, H. A. (2009) Molecular markers for biodiversity analysis of wildlife animals: a brief review. Anim. Biodivers. Conserv. 32: 9–17.Google Scholar
Beaumont, M. A. (1999) Detecting population expansion and decline using microsatellites. Genetics 153: 2013–2029.Google Scholar
Bickham, J. W., Sandhu, S., Hebert, P. D. N., Chikhi, L. and Athwal, R. (2000) Effects of chemical contaminants on genetic diversity in natural populations: implications for biomonitoring and ecotoxicology. Mutat. Res. Mutat. Res. 463: 33–51.Google Scholar
Bouzat, J. L. (2010) Conservation genetics of population bottlenecks: the role of chance, selection, and history. Conserv. Genet. 11: 463–478.Google Scholar
Bouzat, J. L., Paige, K. N. and Lewin, H. A. (1998) The ghost of genetic diversity past: Historical DNA analysis of the Greater Prairie Chicken. Am. Nat. 152: 1–6.Google Scholar
Brightsmith, D. J. (2005) Parrot nesting in southeastern Peru: seasonal patterns and keystone trees. Wilson Bull . 117: 296–305.Google Scholar
Brook, B. W., Sodhi, N. S. and Bradshaw, C. J. A. (2008) Synergies among extinction drivers under global change. Trends Ecol. Evol. 23: 453–460.Google Scholar
Bruggeman, D. J., Wiegand, T. and Fernández, N. (2010) The relative effects of habitat loss and fragmentation on population genetic variation in the red-cockaded woodpecker (Picoides borealis). Mol. Ecol. 19: 3679–3691.Google Scholar
Bruton, M. N., Smith, M. and Taylor, R. H. (1980) A brief history of human evolvement in Maputaland. Pp. 432–459 in Bruton, M. N. and Cooper, K. H., eds. Studies on the ecology of Maputaland. Durban, South Africa: Rhodes University and the Natal Branch of the Wildlife Society of Southern AfricaGoogle Scholar
Callens, T., Galbusera, P., Matthysen, E., Durand, E. Y., Githiru, M., Huyghe, J. R. and Lens, L. (2011) Genetic signature of population fragmentation varies with mobility in seven bird species of a fragmented Kenyan cloud forest. Mol. Ecol. 20: 1829–1844.Google Scholar
Campos, P. F., Willerslev, E., Sher, A., Orlando, L., Axelsson, E., Tikhonov, A., Aaris-Sørensen, K., Greenwood, A. D., Kahlke, R.-D., Kosintsev, P., Krakhmalnaya, T., Kuznetsova, T., Lemey, P., MacPhee, R., Norris, C. A., Shepherd, K., Suchard, M. A., Zazula, G. D., Shapiro, B. and Gilbert, M. T. P. (2010) Ancient DNA analyses exclude humans as the driving force behind late Pleistocene musk ox (Ovibos moschatus) population dynamics. Proc. Natl. Acad. Sci. 107: 5675–5680.Google Scholar
Chapuis, M.-P. and Estoup, A. (2007) Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 24: 621–631.Google Scholar
Chase, B. M., Meadows, M. E., Scott, L., Thomas, D. S. G., Marais, E., Sealy, J. and Reimer, P. J. (2009) A record of rapid Holocene climate change preserved in hyrax middens from southwestern Africa. Geology 37: 703–706.Google Scholar
Chen, C., Durand, E., Forbes, F. and François, O. (2007) Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Mol. Ecol. Notes 7: 747–756.Google Scholar
Coetzer, W. G., Downs, C. T., Perrin, M. R. and Willows-Munro, S. (2015) Molecular systematics of the cape parrot (Poicephalus robustus): Implications for taxonomy and conservation. PLoS One 10: e0133376.Google Scholar
Collar, N. J. (2000) Globally threatened parrots: criteria, characteristics and cures. Int. Zoo Yearb. 37: 21–35.Google Scholar
Collazo, J. A., Fackler, P. L., Pacifici, K., White, T. H. Jr., Llerandi-Roman, I. and Dinsmore, S. J. (2013) Optimal allocation of captive-reared Puerto Rican parrots: Decisions when divergent dynamics characterize managed populations. J. Wildl. Manage. 77: 1124–1134.Google Scholar
Cooper, T. J. G., Wannenburgh, A. M. and Cherry, M. I. (2017) Atlas data indicate forest dependent bird species declines in South Africa. Bird Conserv. Internatn. 27: 337–354.Google Scholar
Cornuet, J. M. and Luikart, G. (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144: 2001–2014.Google Scholar
Couvet, D. (2002) Deleterious effects of restricted gene flow in fragmented populations. Conserv. Biol. 16: 369–376.Google Scholar
Dakin, E. E. and Avise, J. C. (2004) Microsatellite null alleles in parentage analysis. Heredity 93: 504–509.Google Scholar
Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2000) Emerging infectious diseases of wildlife - Threats to biodiversity and human health. Science (80- ) 287: 443–449.Google Scholar
DeSalle, R. and Amato, G. (2004) The expansion of conservation genetics. Nat. Rev. Genet. 5: 702–712.Google Scholar
Do, C., Waples, R. S., Peel, D., Macbeth, G. M., Tillett, B. J. and Ovenden, J. R. (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.Google Scholar
Di Rienzo, A., Peterson, A. C., Garza, J. C., Valdes, A. M., Slatkin, M. and Freimer, N. B. (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc. Natl. Acad. Sci. 91: 3166–3170.Google Scholar
dos Anjos, L., Collins, C. D., Holt, R. D., Volpato, G. H., Mendonça, L. B., Lopes, E. V, Boçon, R., Bisheimer, M. V, Serafini, P. P. and Carvalho, J. (2011) Bird species abundance–occupancy patterns and sensitivity to forest fragmentation: Implications for conservation in the Brazilian Atlantic forest. Biol. Conserv. 144: 2213–2222.Google Scholar
Downs, C. T. (2005a) Abundance of the endangered Cape parrot, Poicephalus robustus, in South Africa: implications for its survival. African Zool . 40: 15–24.Google Scholar
Downs, C. T. (2005b) Artificial nest boxes and wild Cape Parrots Poicephalus robustus: persistence pays off. Ostrich - J. African Ornithol. 76: 222–224.Google Scholar
Downs, C. T., Pfeiffer, M. and Hart, L. A. (2014) Fifteen years of annual Cape Parrot Poicephalus robustus censuses: current population trends and conservation contributions. Ostrich 85: 273–280.Google Scholar
Downs, C. T. and Symes, C. T. (2004) Snag dynamics and forest structure in Afromontane forests in KwaZulu-Natal, South Africa: implications for the conservation of cavity-nesting avifauna. South African J. Bot . 70: 265–276.Google Scholar
Dray, S. and Dufour, A.-B. (2007) The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22: 1–20.Google Scholar
Durand, E., Jay, F., Gaggiotti, O. E. and François, O. (2009) Spatial inference of admixture proportions and secondary contact zones. Mol. Biol. Evol. 26: 1963–1973.Google Scholar
Dussex, N., Rawlence, N. J. and Robertson, B. C. (2015) Ancient and contemporary DNA reveal a pre-human decline but no population bottleneck associated with recent human persecution in the Kea (Nestor notabilis). PLoS One 10: e0118522.Google Scholar
Earl, D. A. and vonHoldt, B. M. (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4: 359–361.Google Scholar
Edwards, C. J., Soulsbury, C. D., Statham, M. J., Ho, S. Y. W., Wall, D., Dolf, G., Iossa, G., Baker, P. J., Harris, S., Sacks, B. N. and Bradley, D. G. (2012) Temporal genetic variation of the red fox, Vulpes vulpes, across western Europe and the British Isles. Quat. Sci. Rev. 57: 95–104.Google Scholar
Eeley, H. A. C., Lawes, M. J. and Piper, S. E. (1999) The influence of climate change on the distribution of indigenous forest in KwaZulu-Natal, South Africa. J. Biogeogr. 26: 595–617.Google Scholar
Eick, G. N., Jacobs, D. S. and Matthee, C. A. (2005) A nuclear DNA phylogenetic perspective on the evolution of echolocation and historical biogeography of extant bats (Chiroptera). Mol. Biol. Evol. 22: 1869–1886.Google Scholar
Evanno, G., Regnaut, S. and Goudet, J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14: 2611–2620.Google Scholar
Evers, T. M. (1975) Recent Iron Age research in the eastern Transvaal, South Africa. South African Archaeol. Bull. 30: 71–83.Google Scholar
Fisher, E. C., Albert, R.-M., Botha, G., Cawthra, H. C., Esteban, I., Harris, J., Jacobs, Z., Jerardino, A., Marean, C. W. and Neumann, F. H. (2013) Archaeological reconnaissance for middle stone age sites along the Pondoland Coast, South Africa. PaleoAnthropology 1: 104–137.Google Scholar
Garza, J. C. and Williamson, E. G. (2001) Detection of reduction in population size using data from microsatellite loci. Mol. Ecol. 10: 305–318.Google Scholar
Geldenhuys, C. J. (1989) Biogeography of the mixed evergreen forests of southern Africa. Pretoria, South Africa: Foundation for Research Development.Google Scholar
Goldstein, P. Z. and Desalle, R. (2003) Calibrating phylogenetic species formation in a threatened insect using DNA from historical specimens. Mol. Ecol. 12: 1993–1998.Google Scholar
Gottelli, D., Sillero-Zubiri, C., Marino, J., Funk, S. M. and Wang, J. (2013) Genetic structure and patterns of gene flow among populations of the endangered Ethiopian wolf. Anim. Conserv. 16: 234–247.Google Scholar
Goudet, J. (2001) FSTAT, a program to estimate and test gene diversities and fixation indices, version 2.9. 3. Available at: http://www2.unil.ch/popgen/softwares/fstat.htm [Accessed June 22, 2015].Google Scholar
Greenbaum, G., Templeton, A. R., Zarmi, Y. and Bar-David, S. (2014) Allelic richness following population founding events – A stochastic modeling framework incorporating gene flow and genetic drift. PLoS One 9: e115203.Google Scholar
Groombridge, J. J., Jones, C. G., Bruford, M. W. and Nichols, R. A. (2000) ‘Ghost’ alleles of the Mauritius kestrel. Nature 403: 616.Google Scholar
Hansson, B., Bensch, S., Hasselquist, D., Lillandt, B.-G., Wennerberg, L. and Von Schantz, T. (2000) Increase of genetic variation over time in a recently founded population of great reed warblers (Acrocephalus arundinaceus) revealed by microsatellites and DNA fingerprinting. Mol. Ecol. 9: 1529–1538.Google Scholar
Hart, L. A., Grieve, G. R. H. and Downs, C. T. (2013) Fruiting phenology and implications of fruit availability in the fragmented Ngele Forest Complex, KwaZulu-Natal, South Africa. South African J. Bot . 88: 296–305.Google Scholar
Hastings, A. (1993) Complex interactions between dispersal and dynamics: lessons from coupled logistic equations. Ecology 74: 1362–1372.Google Scholar
Herron, M. D., Waterman, J. M. and Parkinson, C. L. (2005) Phylogeny and historical biogeography of African ground squirrels: the role of climate change in the evolution of Xerus. Mol. Ecol. 14: 2773–2788.Google Scholar
Hubisz, M. J., Falush, D., Stephens, M. and Pritchard, J. K. (2009) Inferring weak population structure with the assistance of sample group information. Mol. Ecol. Resour. 9: 1322–1332.Google 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.Google Scholar
Kalinowski, S. T. (2011) The computer program STRUCTURE does not reliably identify the main genetic clusters within species: Simulations and implications for human population structure. Heredity 106: 625–632.Google Scholar
Kalinowski, S. T. and Taper, M. L. (2006) Maximum likelihood estimation of the frequency of null alleles at microsatellite loci. Conserv. Genet. 7: 991995.Google Scholar
King, N. L. (1941) The exploitation of the indigenous forests of South Africa. J. South African For. Assoc. 6: 26–48.Google Scholar
Klapwijk, M. (1974) A preliminary report on pottery from the north-eastern Transvaal, South Africa. South African Archaeol. Bull. 29: 19–23.Google Scholar
Kopelman, N. M., Mayzel, J., Jakobsson, M., Rosenberg, N. A. and Mayrose, I. (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol. Ecol. Resour. 15: 1179–1191.Google Scholar
Kotlík, P., Marková, S., Vojtek, L., Stratil, A., Šlechta, V., Hyršl, P. and Searle, J. B. (2014) Adaptive phylogeography: functional divergence between haemoglobins derived from different glacial refugia in the bank vole. Proc. R. Soc. B Biol. Sci. 281: 20140021.Google Scholar
Lacy, R. C. (1987) Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv. Biol. 1: 143–158.Google Scholar
Lawes, M. J., Griffiths, M. E. and Boudreau, S. (2007) Colonial logging and recent subsistence harvesting affect the composition and physiognomy of a podocarp dominated Afrotemperate forest. For. Ecol. Manage. 247: 48–60.Google Scholar
Lee-Thorp, J. A., Holmgren, K., Lauritzen, S.-E., Linge, H., Moberg, A., Partridge, T. C., Stevenson, C. and Tyson, P. D. (2001) Rapid climate shifts in the southern African interior throughout the Mid to Late Holocene. Geophys. Res. Lett. 28: 4507–4510.Google Scholar
Leonard, J. A., Wayne, R. K. and Cooper, A. (2000) Population genetics of Ice Age brown bears. Proc. Natl. Acad. Sci. 97: 1651–1654.Google Scholar
Lorenzen, E. D., Nogués-Bravo, D., Orlando, L., Weinstock, J., Binladen, J., Marske, K. A., Ugan, A., Borregaard, M. K., Gilbert, M. T. P., Nielsen, R., Ho, S. Y. W., Goebel, T., Graf, K. E., Byers, D., Stenderup, J. T., Rasmussen, M., Campos, P. F., Leonard, J. A., Koepfli, K.-P., Froese, D., Zazula, G., Stafford, T. W., Aaris-Sørensen, K., Batra, P., Haywood, A. M., Singarayer, J. S., Valdes, P. J., Boeskorov, G., Burns, J. A., Davydov, S. P., Haile, J., Jenkins, D. L., Kosintsev, P., Kuznetsova, T., Lai, X., Martin, L. D., McDonald, H. G., Mol, D., Meldgaard, M., Munch, K., Stephan, E., Sablin, M., Sommer, R. S., Sipko, T., Scott, E., Suchard, M. A., Tikhonov, A., Willerslev, R., Wayne, R. K., Cooper, A., Hofreiter, M., Sher, A., Shapiro, B., Rahbek, C. and Willerslev, E. (2011) Species-specific responses of Late Quaternary megafauna to climate and humans. Nature 479: 359.Google Scholar
Luikart, G. and Cornuet, J.-M. (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv. Biol. 12: 228–237.Google Scholar
Luikart, G, Allendorf, F. W., Cornuet, J.-M. and Sherwin, W. B. (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J. Hered. 89: 238–247.Google Scholar
Maggs, T. (1984) The Iron Age south of the Zambezi. P. 404 in Klein, R. G., ed. Southern African Prehistory and Paleoenvironments. Rotterdam: BalkemaGoogle Scholar
Makokha, J. S., Bauer, A. M., Mayer, W. and Matthee, C. A. (2007) Nuclear and mtDNA-based phylogeny of southern African sand lizards, Pedioplanis (Sauria: Lacertidae). Mol. Phylogenet. Evol. 44: 622–633.Google Scholar
Mantel, N. (1967) The detection of disease clustering and a generalized regression approach. Cancer Res . 27: 209–220.Google Scholar
Mazus, H. (2000) Clues on the history of Podocarpus forest in Maputaland, South Africa, during the Quaternary, based on pollen analysis. Africa Geosci. Rev. 7: 75–82.Google Scholar
McCracken, D. P. (1986) The indigenous forests of Colonial Natal and Zululand. Natalia 16: 19–38.Google Scholar
McNeely, J. A., Miller, K. R., Reid, W. V., Mittermeier, R. A. and Werner, T. B. (1990) Conserving the world’s biological diversity. Gland, Switzerland: IUCN and Washington DC: WRI, Conservation International, WWF-US, World Bank.Google Scholar
Mende, M. B. and Hundsdoerfer, A. K. (2013) Mitochondrial lineage sorting in action – historical biogeography of the Hyles euphorbiae complex (Sphingidae, Lepidoptera) in Italy. BMC Evol. Biol. 13: 83.Google Scholar
Metwally, A. A., Scott, L., Neumann, F. H., Bamford, M. K. and Oberhänsli, H. (2014) Holocene palynology and palaeoenvironments in the Savanna Biome at Tswaing Crater, central South Africa. Palaeogeogr. Palaeoclimatol. Palaeoecol. 402: 125–135.Google Scholar
Miller, C. S. and Gosling, W. D. (2014) Quaternary forest associations in lowland tropical West Africa. Quat. Sci. Rev. 84: 7–25.Google Scholar
Minister of Environmental Affairs and Tourism (2007) National Environmental Management: Biodiversity Act (ACT 10 of 2004): Publication of Lists of Critically Endangered, Endangered. Gov. Gaz.: 467: 26436.Google Scholar
Mucina, L. and Rutherford, M. C. (2006) The vegetation of South Africa, Lesotho and Swaziland. Pretoria, South Africa: South African National Biodiversity Institute.Google Scholar
Neumann, F. H., Scott, L., Bousman, C. B. and van As, L. (2010) A Holocene sequence of vegetation change at Lake Eteza, coastal KwaZulu-Natal, South Africa. Rev. Palaeobot. Palynol. 162: 39–53.Google Scholar
Neumann, F. H., Stager, J. C., Scott, L., Venter, H. J. T. and Weyhenmeyer, C. (2008) Holocene vegetation and climate records from Lake Sibaya, KwaZulu-Natal (South Africa). Rev. Palaeobot. Palynol. 152: 113–128.Google Scholar
Oehler, D. A., Boodoo, D., Plair, B., Kuchinski, K., Campbell, M., Lutchmedial, G., Ramsubage, S., Maruska, E. J. and Malowski, S. (2001) Translocation of Blue and Gold Macaw Ara ararauna into its historical range on Trinidad. Bird Conserv. Internatn. 11: 129–141.Google Scholar
Ortiz-Catedral, L., Adams, L., Hauber, M. E. and Brunton, D. H. (2010) Conservation translocations of red-fronted parakeets on Matiu/Somes Island and Motuihe Island, New Zealand. Abu Dhabi, UAE.Google Scholar
Pain, D. J., Martins, T. L. F., Boussekey, M., Diaz, S. H., Downs, C. T., Ekstrom, J. M. M., Garnett, S., Gilardi, J. D., McNiven, D., Primot, P., Rouys, S., Saoumoé, M., Symes, C. T., Tamungang, S. A., Theuerkauf, J., Villafuerte, D., Verfailles, L., Widmann, P. and Widmann, I. D. (2006) Impact of protection on nest take and nesting success of parrots in Africa, Asia and Australasia. Anim. Conserv. 9: 322–330.Google Scholar
Peakall, R. and Smouse, P. (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28: 2537–2539.Google Scholar
Peakall, R., Smouse, P. E. and Huff, D. R. (1995) Evolutionary implications of allozyme and RAPD variation in diploid populations of dioecious buffalograss Buchloë dactyloides. Mol. Ecol. 4: 135–148.Google Scholar
Peery, M. Z., Kirby, R., Reid, B. N., Stoelting, R., Doucet-Bëer, E., Robinson, S., Vásquez-Carrillo, C., Pauli, J. N. and Palsbøll, P. E. R. J. (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol. Ecol. 21: 3403–3418.Google Scholar
Pergams, O. R. W., Barnes, W. M. and Nyberg, D. (2003) Rapid change in mouse mitochondrial DNA. Nature 423: 397.Google Scholar
Perrin, M. R. (2009) Niche separation in African parrots. Pp. 29–37 in Harebottle, D. M., Craig, A. J. F. K., Anderson, M. D., Rakotomanana, H. and & Muchai, M., eds. Proceedings of the 12th Pan-African Ornithological Congress, 2008. Rawsonville, South Africa: Cape Town, Animal Demography UnitGoogle Scholar
Pillay, K., Dawson, D. A., Horsburgh, G. J., Perrin, M. R., Burke, T. and Taylor, T. D. (2010) Twenty-two polymorphic microsatellite loci aimed at detecting illegal trade in the Cape parrot, Poicephalus robustus (Psittacidae, AVES). Mol. Ecol. Resour. 10: 142–149.Google Scholar
Piry, S., Luikart, G. and Cornuet, J. M. (1999) BOTTLENECK: A computer program for detecting recent reductions in the effective population size using allele frequency data. J. Hered. 90: 502–503.Google Scholar
Pritchard, J. K., Wen, X. and Falush, D. (2010) Structure, version 2.3. Available at: http://pritch.bsd.uchicago.edu/software [Accessed March 25, 2015].Google Scholar
R Core Team. (2015) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available at: http://www.r-project.org.Google Scholar
Radespiel, U. and Bruford, M. W. (2014) Fragmentation genetics of rainforest animals: Insights from recent studies. Conserv. Genet. 15: 245–260.Google Scholar
Rambaut, A. and Drummond, A. J. (2007) Molecular evolution, phylogenetics and epidemiology, Tracer v.1.5.Google Scholar
Rice, W. R. (1989) Analysing tables of statistical tests. Evolution (N. Y). 43: 223–225.Google Scholar
Rivera-Ortíz, F. A., Solórzano, S., Arizmendi, M. del C., Dávila-Aranda, P. and Oyama, K. (2017) Genetic diversity and structure of the Military Macaw (Ara militaris) in Mexico: Implications for conservation. Trop. Conserv. Sci. 10: 1–12.Google Scholar
Rosenberg, N. A. (2004) Distruct: A program for the graphical display of population structure. Mol. Ecol. Notes 4: 137–138.Google Scholar
Rousset, F. (2008) Genepop’007: a complete re-implementation of the Genepop software for Windows and Linux. Mol. Ecol. Resour. 8: 103–6.Google Scholar
Rycroft, H. B. (1942) The plant ecology of the Karkloof forest, Natal. J. South African For. Assoc. 11: 14–25.Google Scholar
Schultz, S., Bradbury, R. B., Evans, K. L., Gregory, R. D. and Blackburn, T. M. (2005) Brain size and resource specialization predict long-term population trends in British birds. Proc. R. Soc. B Biol. Sci. 272: 2305–2311.Google Scholar
Scott, L. (1987) Late quaternary forest history in Venda, Southern Africa. Rev. Palaeobot. Palynol. 53: 1–10.Google Scholar
Scott, L. (1999) Vegetation history and climate in the Savanna biome South Africa since 190,000 ka: a comparison of pollen data from the Tswaing Crater (the Pretoria Saltpan) and Wonderkrater. Quat. Int. 57–58: 215–223.Google Scholar
Scott, L., Anderson, H. M. and Anderson, J. M. (1997) Vegetation history. Pp. 62–84 in Cowling, R. M., Richardson, D. M. and Pierce, S. M., eds. Vegetation of Southern Africa. Cambridge: Cambridge University Press.Google Scholar
Scott, L., Holmgren, K., Talma, A. S., Woodborne, S. and Vogel, J. C. (2003) Age interpretation of the Wonderkrater spring sediments and vegetation change in the Savanna Biome, Limpopo province, South Africa. S. Afr. J. Sci. 99: 484–488.Google Scholar
Scott, L. and Vogel, J. C. (2000) Evidence for environmental conditions during the last 20000 years in Southern Africa from 13C in fossil hyrax dung. Glob. Planet. Change 26: 207–215.Google Scholar
Shaffer, M. L. (1981) Minimum population sizes for species conservation. Bioscience 31: 131–134.Google Scholar
Spielman, D., Brook, B. W. and Frankham, R. (2004) Most species are not driven to extinction before genetic factors impact them. Proc. Natl. Acad. Sci. U. S. A. 101: 15261–15264.Google Scholar
Storz, J. F. and Beaumont, M. A. (2002) Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite dna variation using a hierarchical bayesian model. Evolution (N. Y). 56: 154–166.Google Scholar
Swart, B. L., Tolley, K. A. and Matthee, C. A. (2009) Climate change drives speciation in the southern rock agama (Agama atra) in the Cape Floristic Region, South Africa. J. Biogeogr. 36: 78–87.Google Scholar
Symes, C., Brown, M., Warburton, L., Perrin, M. and Downs, C. (2004) Observations of Cape Parrot, Poicephalus robustus, nesting in the wild. Ostrich 75: 106–109.Google Scholar
Symes, C. T. (2010) Growing up with Cape Parrots. In Papousči. PIPress.Google Scholar
Taberlet, P., Fumagalli, L., Wust-Saucy, A.-G. and Cosson, J.-F. (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol. Ecol. 7: 453–464.Google Scholar
Taylor, M. (2014) Eskom Red book of birds of South Africa, Lesotho and Swaziland. Johannesburg, South Africa: BirdLife South Africa.Google Scholar
Taylor, T. D. and Parkin, D. Y. (2010) Preliminary insights into the level of genetic variation retained in the endangered echo parakeet (Psittacula eques) towards assisting its conservation management. African Zool . 45: 189–194.Google Scholar
Teacher, A. G. F., Thomas, J. A. and Barnes, I. (2011) Modern and ancient red fox (Vulpes vulpes) in Europe show an unusual lack of geographical and temporal structuring, and differing responses within the carnivores to historical climatic change. BMC Evol. Biol. 11: 214.Google Scholar
Thomas, W. K., Pääbo, S., Villablanca, F. X. and Wilson, A. C. (1990) Spatial and temporal continuity of kangaroo rat populations shown by sequencing mitochondrial DNA from museum specimens. J. Mol. Evol. 31: 101–112.Google Scholar
Tolley, K. A., Burger, M., Turner, A. A. and Matthee, C. A. (2006) Biogeographic patterns and phylogeography of dwarf chameleons (Bradypodion) in an African biodiversity hotspot. Mol. Ecol. 15: 781–793.Google Scholar
Tolley, K. A., Chase, B. M. and Forest, F. (2008) Speciation and radiations track climate transitions since the Miocene Climatic Optimum: a case study of southern African chameleons. J. Biogeogr. 35: 1402–1414.Google Scholar
Tolley, K. A., Makokha, J. S., Houniet, D. T., Swart, B. L. and Matthee, C. A. (2009) The potential for predicted climate shifts to impact genetic landscapes of lizards in the South African Cape Floristic Region. Mol. Phylogenet. Evol. 51: 120–130.Google Scholar
Tucker, J. M., Schwartz, M. K., Truex, R. L., Pilgrim, K. L. and Allendorf, F. W. (2012) Historical and contemporary DNA indicate fisher decline and isolation occurred prior to the European settlement of California. PLoS One 7: e52803.Google Scholar
Wandeler, P., Hoeck, P. E. A. and Keller, L. F. (2007) Back to the future: museum specimens in population genetics. Trends Ecol. Evol. 22: 634–642.Google Scholar
Wang, J. (2005) Estimation of effective population sizes from data on genetic markers. Philos. Trans. R. Soc. B Biol. Sci. 360: 1395–1409.Google Scholar
Welch, A. J., Wiley, A. E., James, H. F., Ostrom, P. H., Stafford, T. W. Jr and Fleischer, R. C. (2012) Ancient DNA reveals genetic stability despite demographic decline: 3,000 years of population history in the endemic Hawaiian Petrel. Mol. Biol. Evol. 29: 3729–3740.Google Scholar
Williamson-Natesan, E. G. (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv. Genet. 6: 551–562.Google Scholar
Wilson, G. A. and Rannala, B. (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163: 1177–1191.Google Scholar
Wirminghaus, J. O. (1997) Cape Parrot Poicephalus robustus. In Harrison, J. A., Alan, D. G., Underhill, L. L., Herremans, M., Tree, A. J., Parker, V. and Brown, C. J., eds. The atlas of Southern African Birds, Johannesburg, South Africa: BirdLife South Africa.Google Scholar
Wirminghaus, J. D., Downs, C. T., Symes, C. T. and Perrin, M. R. (1999) Conservation of the Cape Parrot in southern Africa. South African J. Wildl. Res. 29: 118–129.Google Scholar
Wirminghaus, J. O., Downs, C. T., Symes, C. T. and Perrin, M. R. (2000) Abundance of the Cape parrot in South Africa. South African J. Wildl. Res. 30: 43–52.Google Scholar
Wirminghaus, J. O., Downs, C. T., Perrin, M. R. and Symes, C. T. (2001a) Breeding biology of the Cape Parrot, Poicephalus robustus. Ostrich 72: 159–164.Google Scholar
Wirminghaus, J. O, Downs, C. T., Symes, C. T. and Perrin, M. R. (2001b) Fruiting in two afromontane forests in KwaZulu-Natal, South Africa: the habitat type of the endangered Cape Parrot Poicephalus robustus. South African J. Bot . 67: 325–332.Google Scholar
Wirminghaus, J. O., Downs, C. T., Symes, C. T. and Perrin, M. R. (2002) Diet of the Cape Parrot, Poicephalus robustus, in Afromontane forests in KwaZulu-Natal, South Africa. Ostrich 73: 20–25.Google Scholar
Wright, T. F., Rodrigues, A. M. and Fleischer, R. C. (2005) Vocal dialects, sex-biased dispersal, and microsatellite population structure in the parrot Amazona auropalliata. Mol. Ecol. 14: 1197–1205.Google Scholar
Supplementary material: File

Coetzer et al. supplementary material

Figures S1-S5

Download Coetzer et al. supplementary material(File)
File 413.1 KB
Supplementary material: File

Coetzer et al. supplementary material

Tables S1-S5

Download Coetzer et al. supplementary material(File)
File 27.3 KB