Using DNA to assess errors in tropical tree identifications: How often are ecologists wrong and when does it matter?

Ecological Monographs

Volumn 80, Issue 2, 2010, Pages 267-286

  Dexter, Kyle G ^a   Pennington, Terence D ^b   Cunningham, Clifford W ^c  

^a École Nationale de Formation Agronomique   (France)

^b DUKE UNIVERSITY   (United States)

^c ROYAL BOTANIC GARDENS   (United Kingdom)

Author keywords

Biodiversity; DNA barcoding; Genealogical species concept; Inga (Fabaceae); Madre de Dios; Neutral ecological theory; Southern Peru; Species delimitation; Species identification; Tropical trees

Indexed keywords

CHLOROPLAST; COMMUNITY COMPOSITION; ECOLOGICAL THEORY; FLORAL TRAIT; FRUIT; GENEALOGY; GENETIC ANALYSIS; LEGUME; MORPHOLOGY; PHYLOGENY; SPECIES CONCEPT; TAXONOMY;

AMAZONIA; PERU;

FABACEAE; INGA;

EID: 77951729649     PISSN: 00129615     EISSN: 15577015     Source Type: Journal    
DOI: 10.1890/09-0267.1     Document Type: Article

References (104)

1. Alvarez, I., and J. F. Wendel, 2003. Ribosomal ITS sequences and plant phylogenetic inference. Molecular Phylogenetics and Evolution 29: 417-434. (Pubitemid 37491888)
2. Archaux, F., F. Gosselin, L. Berges, and R. Chevalier. 2006. Effects of sampling time, species richness and observer on the exhaustiveness of plant censuses. Journal of Vegetation Science 17: 299-306. (Pubitemid 44197062)
3. Avise, J. C., and R. M. Ball, 1990. Principles of genealogical concordance in species concepts and biological taxonomy. Pages 45-67 in D. Futuyama and J. Antonovics, editors. Oxford surveys in evolutionary biology. Oxford University Press, Oxford, UK.
4. Barra, B. I. P., J. G. B. Derraik, C. G. Rufaut, A. J. Goodman, and K. J. M. Dickinson. 2003. Morphospecies as a substitute for Coleoptera species identification, and the value of experience in improving accuracy. Journal of the Royal Society of New Zealand 33: 583-590.
5. Baum, D. A., and K. L. Shaw. 1995. Genealogical perspectives on the species problem. Pages 289-303 in P. C. Hoch and A. G. Stephenson, editors. Experimental and molecular approaches to plant biosystematics. Missouri Botanical Garden, St. Louis, Missouri, USA.
6. Bickford, D., D. J. Lohman, N. S. Sodhi, P. K. L. Ng, R. Meier, K. Winker, K. K. Ingram, and I. Das. 2007. Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22: 148-155. (Pubitemid 46273824)
7. Blanchet, F. G., P. Legendre, and D. Borcard. 2008. Forward selection of explanatory variables. Ecology 89: 2623-2632.
8. Borcard, D., and P. Legendre. 2004. SpaceMaker2. 〈www.bio umontreal.ca/casgrain/en/labo/sp acemaker.html〉
9. Bortolus, A. 2008. Error cascades in the biological sciences: the unwanted consequences of using bad taxonomy in ecology. Ambio 37: 114-118. (Pubitemid 351656229)
10. Brown, B., R. M. Emberson, and A. M. Paterson. 1999. Mitochondrial COI and II provide useful markers for Wiseana (Lepidoptera: Hepialidae) species identification. Bulletin of Entomological Research 89: 287-293. (Pubitemid 29475565)
11. Burger, W. C. 1975. The species concept in Quercus. Taxon 24: 45-50.
12. Caesar, R. M., M. Sorensson, and A. I. Cognato. 2006. Integrating DNA data and traditional taxonomy to streamline biodiversity assessment: an example from edaphic beetles in the Klamath ecoregion, California, USA. Diversity and Distributions 12: 483-489.
13. Chase, M. W., N. Salamin, M. Wilkinson, J. M. Dunwell, R. P. Kesanakurthi, N. Haidar, and V. Savolainen. 2005. Land plants and DNA barcodes: short-term and long-term goals. Philosophical Transactions of the Royal Society B 360: 1889-1895.
14. Chave, J., and E. G. Leigh, 2002. A. spatially explicit neutral model of beta-diversity in tropical forests. Theoretical Population Biology 62: 153-168. (Pubitemid 38051032)
15. Clement, M., D. Posada, and K. A. Crandall. 2000. TCS: a computer program, to estimate gene genealogies. Molecular Ecology 9: 1657-1659.
16. Coley, P. D., et al. 2005. Divergent defensive strategies of young leaves in two species of Inga. Ecology 86: 2633-2643.
17. Colwell, R. K. 2006. Estimates: statistical estimation of species richness and shared species from, samples. University of Connecticut, Storrs, Connecticut, USA.
18. Condit, R. 1998. Tropical forest census plots: methods and results from Barro Colorado Island, Panama and comparison with other plots. Springer-Verlag, Berlin, Germany.
19. Condit, R., et al. 2002. Beta-diversity in tropical forest trees. Science 295: 666-669.
20. Connell, J. H. 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. Pages 289-312 in P. J. den Boer and G. R. Gradweli, editors. Dynamics of numbers in populations. Center for Agricultural Publication and Documentation, Wageningen, The Netherlands.
21. Connell, J. H. 1978. Diversity in tropical rainforests and coral reefs: high diversity of trees and corals is maintained only in a non-equilibrium state. Science 199: 1302-1310.
22. Cowan, R. S., M. W. Chase, W. J. Kress, and V. Savolainen. 2006. 300,000 species to identify: problems, progress, and prospects in DNA barcoding of land plants. Taxon 55: 611-616.
23. Davis, J. I., and K. C. Nixon. 1992. Populations, genetic variation, and the delimitation of phylogenetic species. Systematic Biology 41: 421-435.
24. Demesure, B., N. Sodzi, and R. J. Petit. 1995. A set of universal primers for amplification of polymorphic noncoding regions of mitochondrial and chloroplast DNA in plants. Molecular Ecology 4: 129-131.
25. Denslow, J. S. 1987. Tropical rainforest gaps and tree species diversity. Annual Review of Ecology and Systematics 18: 431-451.
26. Derraik, J. G. B., G. P. Closs, K. J. M. Dickinson, P. Sirvid, B. I. P. Barratt, and B. H. Patrick. 2002. Arthropod morphospecies versus taxonomic species: a case study with Araneae, Coleoptera, and Lepidoptera. Conservation Biology 16: 1015-1023.
27. Doyle, J. J., and J. L. Doyle. 1990. Isolation of plant DNA from, fresh, tissue. Focus 12: 13-15.
28. Dray, S. 2007. Packfor: an R package for forward selection. 〈http://www.bio.umontreal.ca/legendre/ 〉
29. Duivenvoorden, J. F., J. C. Svenning, and S. J. Wright. 2002. Ecology-beta diversity in tropical forests. Science 295: 636-637.
30. Gilbert, B., and M. J. Lechowicz. 2004. Neutrality, niches, and dispersal, in a temperate forest understory. Proceedings of the National Academy of Sciences USA 101: 7651-7656. (Pubitemid 38658084)
31. Goldstein, P. Z. 1997. How many things are there? A reply to Oliver and Beattie, Beattie and Oliver, Oliver and Beattie, and Oliver and Beattie. Conservation Biology 11: 571-574.
32. Gurevitch, J., S. M, Scheiner, and G. A, Fox. 2006. The ecology of plants. Sinnauer, Sunderland, Massachusetts, USA.
33. Hart, M. W., and J. Sunday. 2007. Things fall apart: biological species form unconnected parsimony networks. Biology Letters 3: 509-512.
34. Hebert, P. D. N., A. Cywinska, S. L. Ball, and J. R, DeWaard, 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society B 270: 313-321.
35. Hebert, P. D. N., M. Y. Stoeckle, T. S. Zemlak, and C. M. Francis. 2004. Identification of birds through DNA barcodes. PLoS Biology 2: 1657-1663.
36. Hickerson, M. J., C. P. Meyer, and C. Moritz. 2006. DNA barcoding will often fail to discover new animal species over broad parameter space. Systematic Biology 55: 729-739.
37. Hubbell, S. P. 1979. Tree dispersion, abundance, and diversity in a tropical dry forest. Science 203: 1299-1309.
38. Hubbell, S. P. 2001. The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton, New Jersey, USA.
39. Hubbell, S. P., R. B. Foster, S. T. O'Brien, K. E. Harms, R. Condit, B. Wechsler, S. J. Wright, and S. L. de Lao. 1999. Light-gap disturbances, recruitment limitation, and tree diversity in a neotropical forest. Science 283: 554-557. (Pubitemid 129504625)
40. Jabot, F., R. S. Etienne, and J. Chave. 2008. Reconciling neutral community models and environmental filtering: theory and an empirical test. Oikos 117: 1308-1320.
41. Janzen, D. H. 1970. Herbivores and the number of tree species in tropical, forests. American Naturalist 104: 501-528.
42. Janzen, D. H., M. Hajibabaei, J. M. Burns, W. Hallwachs, E. Remigio, and P. D. N. Hebert. 2005. Wedding biodiversity inventory of a large and complex Lepidoptera fauna with DNA barcoding. Philosophical Transactions of the Royal Society B 360: 1835-1845.
43. Jobson, R. W., and M. Luckow. 2007. Phylogenetic study of the genus Piptadenia (Mimosoideae: Leguminosae) using plastid trnL-F and trnK/matK sequence data. Systematic Botany 32: 569-575.
44. John, R., J. W. Dalling, K. E. Harms, J. B. Yavitt, R. F. Stallard, M. Mirabello, S. P. Hubbell, R. Valencia, H. Navarrete, M. Vallejo, and R. B. Foster. 2007. Soil nutrients influence spatial distributions of tropical tree species. Proceedings of the National Academy of Sciences USA 104: 864-869. (Pubitemid 46154702)
45. Jones, M. M., H. Tuomisto, D. Borcard, P. Legendre, D. B. Clark, and P. C. Olivas. 2008. Explaining variation in tropical plant community composition: influence of environmental and spatial data quality. Oecologia 155: 593-604.
46. Kalliola, R., J. Salo, M. Puhakka, and M. Rajasilta. 1991. New site formation and colonizing vegetation in primary succession on the western Amazon floodplains. Journal of Ecology 79: 877-901.
47. Killeen, T. J., M. Douglas, T. Consiglio, P. M. Jorgensen, and J. Mejia. 2007. Dry spots and wet spots in the Andean hotspot. Journal of Biogeography 34: 1357-1373.
48. Knowl.es L. L., and B. C. Carstens. 2007. Delimiting species without monophyletic gene trees. Systematic Biology 56: 887895.
49. Knowlton, N., E. Weil, L. A. Weigt, and H. M. Guzman. 1992. Sibling species in Montastraea annularis, coral bleaching, and the coral climate record. Science 255: 330-333.
50. Koptur, S. 1984. Outcrossing and pollinator limitation of fruit set: breeding systems of neotropical Inga trees (Fabaceae: Mimosoideae). Evolution 38: 1130-1143.
51. Kress, W. J., K. J. Wurdack, E. A. Zimmer, L. A. Weigt, and D. H. Janzen. 2005. Use of DNA barcodes to identify flowering plants. Proceedings of the National Academy of Sciences USA 102: 8369-8374. (Pubitemid 40803501)
52. Lahaye, R., M. Van der Bank, D. Bogarin, J. Warner, F. Pupulin, G. Gigot, O. Maurin, S. Duthoit, T. G. Barraclough, and V. Savolainen. 2008. DNA barcoding the floras of biodiversity hotspots. Proceedings of the National Academy of Sciences USA 105: 2923-2928. (Pubitemid 351723645)
53. Lavin, M. 2006. Floristic and geographic stability of discontinuous seasonally dry tropical forests explains patterns of plant phylogeny and endemism. Pages 433-447 in R. T. Pennington, J. A. Ratter, and G. P. Lewis, editors. Neotropical savannas and seasonally dry forests: plant biodiversity, biogeographic patterns, and conservation. CRC Press, Boca Raton, Florida, USA.
54. Legendre, P., D. Borcard, and P. R. Peres-Neto. 2005. Analyzing beta diversity: partitioning the spatial variation of community composition data. Ecological Monographs 75: 435-450. (Pubitemid 41476777)
55. Legendre, P., D. Borcard, and P. R. Peres-Neto. 2008. Analyzing or explaining beta diversity? Comment. Ecology 89: 3238-3244.
56. Legendre, P., X. Mi, H. Ren, K. Ma, M. Yu, I.-F. Sun, and F. He. 2009. Partitioning beta diversity in a subtropical broadleaved forest of China. Ecology 90: 663-674.
57. Maddison, D. R., and W. P. Maddison. 2003. MacClade. Sinauer, Sunderland, Massachusetts, USA.
58. McGiIl, B. J. 2003. A test of the unified neutral theory of biodiversity. Nature 422: 881-885. (Pubitemid 36520038)
59. McGill, B. J., B. A. Maurer, and M. D. Weiser. 2006. Empirical evaluation of neutral theory. Ecology 87: 1411-1423.
60. Meyer, C. P., and G Paulay. 2005. DNA barcoding: error rates based on comprehensive sampling. PLoS Biology 3: 2229-2238.
61. Moritz, C. 1994. Defining evolutionarily significant units for conservation. Trends in Ecology and Evolution 9: 373-375. (Pubitemid 2130029)
62. Morion, H., G. Chuyong, R. Condit, S. Hubbell, D. Kenfack, D. Thomas, R. Valencia, and J. L. Green. 2008. A general framework for the distance-decay of similarity in ecological communities. Ecology Letters 11: 1-14.
63. Nanney, D. L. 1982. Genes and phenes in Tetrahymena. BioScience 32: 783-788.
64. Nekola, J. C., and P. S. White. 1999. The distance decay of similarity in biogeography and ecology. Journal of Biogeography 26: 867-878.
65. Newmaster, S. G., A. J. Fazekas, and S. Ragupathy. 2006. DNA barcoding in land plants: evaluation of rbcL in a multigene tiered approach. Canadian Journal of Botany 84: 335-341.
66. Nielsen, R., and M. Matz. 2006. Statistical approaches for DNA barcoding. Systematic Biology 55: 162-169.
67. Norden, N., J. Chave, A. Caubere, P. Chatelet, N. Ferroni, P. M. Forget, and C. Thebaud. 2007. Is temporal variation of seedling communities determined by environment or by seed arrival? A test in a neotropical forest. Journal of Ecology 95: 507-516. (Pubitemid 46624079)
68. Oh, S. H., and D. Potter. 2003. Phylogenese utility of the second intron of LEAFY in Neillia and Stephanandra (Rosaceae) and implications for the origin of Stephanandra. Molecular Phylogenetics and Evolution 29: 203-215.
69. Oksanen, J., R. Kindt, P. Legendre, B. O'Hara, G. L. Simpson, T. Solymos, M. H. H. Stevens, and H. Wagner. 2008. Vegan: community ecology package, 〈 http://cc.oulu.fi/̃~jarioksa/softhelp/vegan.html〉
70. Oliver, I., and A. J. Beattie. 1993. A possible methods for the rapid assessment of biodiversity. Conservation Biology 7: 562-568. (Pubitemid 24410141)
71. Pace, N. R. 1997. A molecular view of microbial diversity and the biosphere. Science 276: 734-740.
72. Pennington, T. D. 1997. The genus Inga: botany. Royal Botanic Gardens, Kew, UK.
73. Peres-Neto, P. R., P. Legendre, S. Dray, and D. Borcard. 2006. Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87: 2614-2625.
74. Phillips, O. L., P. N. Vargas, A. L. Monteagudo, A. P. Cruz, M. E. C. Zans, W. G. Sanchez, M. Yli-Halla, and S. Rose. 2003. Habitat association among Amazonian tree species: a landscape-scale approach. Journal of Ecology 91: 757-775.
75. Pitman, N. C. A., J. Terborgh, M. R. Silman, and P. Nuñez V. 1999. Tree species distributions in an upper Amazonian forest. Ecology 80: 2651-2661. (Pubitemid 30001011)
76. Pitman, N. C. A., J. W. Terborgh, M. R. Silman, P. Nunez V., D. A. Neill, C. E. Ceron, W. A. Palacios, and M. Aulestia. 2001. Dominance and distribution of tree species in upper Amazonian terra firme forests. Ecology 82: 2101-2117.
77. Pons, J., T. G. Barraclough, J. Gomez-Zurita, A. Cardoso, D. P. Duran, S. Hazell, S. Kamoun, W. D. Sumlin, and A. P. Vogler. 2006. Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55: 595-609.
78. Posada, D. 2006. Collapse: Describing haplotypes from, sequence alignment, 〈http://darwin.uvigo.es/software/collapse. html〉
79. Posada, D., and K. A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818. (Pubitemid 28552116)
80. Preston, F. W. 1962. Canonical distribution of commonness and rarity. Ecology 43: 185-215.
81. Queenborough, S. A., D. Burslem, N. C. Garwood, and R. Valencia. 2007. Habitat niche partitioning by 16 species of Myristicaceae in Amazonian Ecuador. Plant Ecology 192: 193-207.
82. R Development Core Team. 2008. R: a language and environment for statistical computing. R Foundation for Statistical. Computing, Vienna, Austria.
83. Rach, J., R. DeSalle, I. N. Sarkar, B. Schierwater, and H. Hadrys. 2008. Character-based DNA barcoding allows discrimination of genera, species and populations in Odonata. Proceedings of the Royal Society B 275: 237-247. (Pubitemid 350295712)
84. Raxworthy, C. J., C. M. Ingram, N. Rabibisoa, and R. G. Pearson. 2007. Applications of ecological niche modeling for species delimitation: a review and empirical evaluation using day geckos (Phelsuma) from Madagascar. Systematic Biology 56:907-923.
85. Richardson, J. E., R. T. Pennington, T. D. Pennington, and P. M. Hollingsworth. 2001, Rapid diversification of a speciesrich genus of neotropical rain forest trees. Science 293: 2242-2245.
86. Rissler, L. J., and J. J. Apodaca. 2007. Adding more ecology into species delimitation: ecological niche models and phylogeography help define cryptic species in the black salamander (Aneides flavipunctatus). Systematic Biology 56: 924-942.
87. Ronquist, F., and J. P. Huelsenbeck. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574. (Pubitemid 37038874)
88. Scott, W. A., and C. J. Hallam. 2002. Assessing species misidentification rates through quality assurance of vegetation monitoring. Plant Ecology 165: 101-115.
89. Sheil, D. 1995. A critique of permanent plot methods and analysis with examples from Budongo Forest, Uganda. Forest Ecology and Management 77: 11-34. (Pubitemid 26469706)
90. Stanford, A, M., R. Harden, and C. R. Parks. 2000. Phytogeny and biogeography of Juglans (Juglandaceae) based on matK and ITS sequence data. American Journal of Botany 87: 872-882.
91. Stuart, B. L., and U. Fritz. 2008. Historical DNA from museum type specimens clarifies diversity of Asian leaf turtles (Cyclemys). Biological Journal of the Linnean Society 94: 131-141.
92. Swofford, D. L. 2002. PAUP. Sinauer, Sunderland, Massachusetts, USA
93. Turnan, D. 1994. Competition and biodiversity in spatially structured habitats. Ecology 75: 2-16. (Pubitemid 2031809)
94. Tuomisto, H., and K. Ruokolainen. 2006. Analyzing or explaining beta diversity? Understanding the targets of different methods of analysis. Ecology 87: 2697-2708. (Pubitemid 44904855)
95. Tuomisto, H., K. Ruokolainen, and M. Yli-Halla. 2003. Dispersal, environment, and floristic variation of western Amazonian forests. Science 299: 241-244. (Pubitemid 36125208)
96. Valencia, R., R. B. Foster, G. Villa, R. Condit, J. C. Svenning, C. Hernandez, K. Romoleroux, E. Losos, E. Magard, and H. Balslev. 2004. Tree species distributions and local habitat variation in the Amazon: large forest plot in eastern Ecuador. Journal of Ecology 92: 214-229. (Pubitemid 38448459)
97. Vecchione, M., W. F. Mickevich, K. Fauchald, B. B. Collette, A. B. Williams, T. A. Munroe, and R. E. Young. 2000. Importance of assessing taxonomic adequacy in determining fishing effects on marine biodiversity. ICES Journal of Murine Science 57: 677-681.
98. Volkov, I., J. R. Banavar, S. P. Hubbell, and A. Maritan. 2003. Neutral theory and relative species abundance in ecology. Nature 424: 1035-1037. (Pubitemid 37064300)
99. Webb, C. O. 2000. Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. American Naturalist 156: 145-155.
100. White, T. J., T. Bruns, S. Lee, and J. Taylor. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogeneties
101. Wiens, J. J., and T. A. Penkrot. 2002. Delimiting species using DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Systematic Biology 51: 6991.
102. Wills, C., R. Condit, R. B. Foster, and S. P. Hubbell. 1997. Strong density- and diversity-related effects help to maintain tree species diversity in a neotropical forest. Proceedings of the National Academy of Sciences USA 94: 1252-1257. (Pubitemid 27087837)
103. Zillio, T., and R. Condit. 2007. The impact of neutrality, niche differentiation and species input on diversity and abundance distributions. Oikos 116: 931-940. (Pubitemid 46743909)
104. Zwickl, D. J. 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological datasets under the maximum likelihood criterion. University of Texas, Austin, Texas, USA.