Organisms Diversity & Evolution

, Volume 16, Issue 1, pp 1–12 | Cite as

The application of “-omics” technologies for the classification and identification of animals

  • Michael J. Raupach
  • Rudolf Amann
  • Quentin D. Wheeler
  • Christian Roos
Review

Abstract

The correct classification of organisms based on specific rules is essential in biological sciences. Traditionally, morphological characteristics such as size, shape, color, and anatomical structures have been used to identify and classify species. However, as consequence of the tremendous advances in molecular technologies during the last years, new approaches have become available for taxonomic research. Various modern high-throughput technologies allow the detailed characterization of the genome, proteome, metabolome as well as the morphology of an organism. Furthermore, the open access storage of such comprehensive data sets as part of an uprising digital cybertaxonomy enables highly fascinating digital dimensions for modern taxonomy, including the buildup of virtual collections as well as data sets for 3D printing techniques that can be used to replicate complete voucher specimens or at least important diagnostic characters. As a result of these advances, we are now able to document, describe, and identify species much more comprehensively than just a few years ago. In this review we provide an overview about the technical advances in taxonomic research in recent years and discuss their power and limitations.

Keywords

Applied taxonomy Cybertaxonomy Genomics Integrative taxonomy Metabolomics Metazoa Proteomics Transcriptomics 

Notes

Acknowledgments

This review is in part based on the hearings and discussions within the working group “Taxonomic Research in the Era of OMICS Technologies” of the Leopoldina–Nationale Akademie der Wissenschaften (German National Academy of Sciences). We thank all participants of the working group for sharing their views and opinions. The English version of the statement “Challenges and Opportunities of Integrative Taxonomy for Research and Society” can be found here: www.leopoldina.org/en/taxonomy. We thank Terue Cristina Kihara for using the 3D model of the serolid isopod specimen, Karin Pointner for the permission to use the copepod image as well as Ortwin Bleich for his permission to use the ground beetle image taken from www.eurocarabidae.de. We also thank two anonymous reviewers for their helpful comments on the manuscript.

Ethical approval

The authors ensure that accepted principles of ethical and professional conduct have been followed. No potential conflicts of interest are given.

Conflict of interest

The authors have no potential conflict of interest.

References

  1. Akkari, N., Enghoff, H., & Metscher, B.D. (2015). A new dimension in documenting new species: High-detail imaging for myriapod taxonomy and first 3D cybertype of a new millipede species (Diplopoda, Julida, Julidae). Public Library of Science ONE, 10, e0135243. Google Scholar
  2. Andújar, C., Arribas, P., Ruzicka, F., Crampton-Platt, A., Timmermans, M. J., & Vogler, A. (2015). Phylogenetic community ecology of soil biodiversity using mitochondrial metagenomics. Molecular Ecology, 24, 3603–3617.Google Scholar
  3. Arienti, M., Antony, C., Wicker-Thomas, C., Delbecque, J. P., & Jallon, J. M. (2010). Ontogeny of Drosophila melanogaster female sex appeal and cuticular hydrocarbons. Integrative Zoology, 5, 272–282.PubMedCrossRefGoogle Scholar
  4. Asher, R. J., & Hofreiter, M. (2006). Tenrec phylogeny and the noninvasive extraction of nuclear DNA. Systematic Biology, 55, 181–194.PubMedCrossRefGoogle Scholar
  5. Ashton, L., Lau, K., Winder, C. L., & Goodacre, R. (2011). Raman spectroscopy: lighting up the future of microbial identification. Future Microbiology, 6, 991–997.PubMedCrossRefGoogle Scholar
  6. Astrin, J., Zhou, X., & Misof, B. (2013). The importance of biobanking in molecular taxonomy, with proposed definitions for vouchers in a molecular context. ZooKeys, 365, 67–70.PubMedCrossRefGoogle Scholar
  7. Baird, N. A., Etter, P. D., Atwood, T. S., Currey, M. C., Shiver, A. L., Lewis, Z. A., et al. (2008). Rapid SNP discovery and genetic mapping using RAD markers. Public Library of Science ONE, 3, e3376.PubMedPubMedCentralGoogle Scholar
  8. Balke, M., Schmidt, S., Hausmann, A., Toussaint, E. F. A., Bergsten, J., Buffington, M., et al. (2013). Biodiversity into your hands—a call for a virtual global natural history “metacollection”. Frontiers in Zoology, 10, 55.PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bi, K., Linderoth, T., Vanderpool, D., Good, J. M., Nielsen, R., & Moritz, C. (2013). Unlocking the vault: next-generation museum population genomics. Molecular Ecology, 22, 6018–6032.PubMedPubMedCentralCrossRefGoogle Scholar
  10. Blacket, M. J., Semeraro, L., & Malipatil, M. B. (2012). Barcoding Queensland fruit flies (Bactrocera tryoni): impediments and improvements. Molecular Ecology Resources, 12, 428–436.PubMedCrossRefGoogle Scholar
  11. Boistel, R., Swoger, J., Kržic, U., Fernandez, F., Gillet, B., & Reynaud, E. G. (2011). The future of three-dimensional microscopic imaging in marine biology. Marine Ecology, 32, 438–452.CrossRefGoogle Scholar
  12. Brooker, A. J., Shinn, A. P., & Bron, J. E. (2012). Use of laser scanning confocal microscopy for morphological taxonomy and the potential for digital type specimens (e-types). Aquatic Biology, 14, 165–173.CrossRefGoogle Scholar
  13. Bucklin, A., Steinke, D., & Blanco-Bercial, L. (2011). DNA barcoding of marine Metazoa. Annual Review of Marine Science, 3, 471–508.PubMedCrossRefGoogle Scholar
  14. Butcher, B. A., Smith, M. A., Sharkey, M. J., & Quicke, D. L. J. (2012). A turbo-taxonomic study of Thai Aleiodes (Aleiodes) and Aleiodes (Arcaleiodes) (Hymenoptera: Braconidae: Rogadinae) based largely on COI barcoded specimens, with rapid descriptions of 179 new species. Zootaxa, 3457, 1–232.Google Scholar
  15. Cameron, S., Rubinoff, D., & Will, K. (2006). Who will actually use DNA barcoding and what will it cost? Systematic Biology, 55, 844–847.PubMedCrossRefGoogle Scholar
  16. Cappelini, E., Gentry, A., Palkopoulou, E., Ishida, Y., Cram, D., Roos, A.-M., et al. (2014). Resolution of the type material of the Asian elephant, Elephas maximus Linnaeus, 1758 (Proboscidea, Elephantidae). Zoological Journal of the Linnean Society, 170, 222–232.CrossRefGoogle Scholar
  17. Carstens, B. C., Pelletier, T. A., Reid, N. M., & Satler, J. D. (2013). How to fail at species delimitation. Molecular Ecology, 22, 4369–4383.PubMedCrossRefGoogle Scholar
  18. Chang, S. C., Chan, T. Y., & Ahyong, S. T. (2014). Two new species of the rare lobster genus Thaumastocheles Wood-Mason, 1874 (Reptantia: Nephropidae) discovered from recent deep-sea expeditions in the Indo-West Pacific. Journal of Crustacean Biology, 34, 107–122.CrossRefGoogle Scholar
  19. Chen, H.-N., Høeg, J. T., & Chan, B. K. K. (2013). Morphometric and molecular identification of individual barnacle cyprids from wild plankton: an approach to detecting fouling and invasive barnacle species. Biofouling, 29, 133–145.PubMedCrossRefGoogle Scholar
  20. Chun, J., & Rainey, F. A. (2014). Integrating genomics into the taxonomy and systematics of the Bacteria and Archaea. International Journal of Systematic and Evolutionary Microbiology, 64, 316–324.PubMedCrossRefGoogle Scholar
  21. Cochrane, G., Cook, C. E., & Birney, E. (2012). The future of DNA sequence archiving. GigaScience, 1, 2.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Cook, L. G., Edwards, R. D., Crisp, M. D., & Hardy, N. B. (2010). Need morphology always be required for new species descriptions? Invertebrate Systematics, 24, 322–326.CrossRefGoogle Scholar
  23. Correa, M. C. G., Germain, J.-F., Malausa, T., & Zaviezo, T. (2012). Molecular and morphological characterization of mealybugs (Hemiptera: Pseudococcidae) from Chilean vineyards. Bulletin of Entomological Research, 102, 524–530.PubMedCrossRefGoogle Scholar
  24. Corthals, A., & DeSalle, R. (2005). An application of tissue and DNA banking for genomics and conservation: the Ambrose Monell Cryo-Collection (AMCC). Systematic Biology, 54, 819–823.PubMedCrossRefGoogle Scholar
  25. Costa-da-Silva, A., Marinotti, O., Ribeiro, J. M. C., Silva, M. C. P., Lopes, A. R., Barros, M. S., et al. (2014). Transcriptome sequencing and developmental regulation of gene expression in Anopheles aquasalis. Public Library of Science ONE, 8, e3005.Google Scholar
  26. Cozzuol, M. A., Clozato, C. L., Holanda, E. C., Rondrigues, F. H. G., Nienow, S., de Thoisy, B., et al. (2013). A new species of tapir from Amazon. Journal of Mammalogy, 94, 1331–1345.CrossRefGoogle Scholar
  27. Crampton-Platt, A., Timmermans, M. J. T. N., Gimmel, M. L., Kutty, S. N., Cockerill, T. D., Khen, C. V., et al. (2015). Soup to tree: the phylogeny of beetles inferred by mitochondrial metagenomics of a Bornean rainforest sample. Molecular Biology and Evolution, 32, 2302–2316. Google Scholar
  28. Cristescu, M. E. (2014). From barcoding single individuals to metabarcoding biological communities: towards an integrative approach to the study of global biodiversity. Trends in Ecology and Evolution, 29, 566–571.PubMedCrossRefGoogle Scholar
  29. Cvačka, J., Jiroŝ, P., Ŝobotník, J., Hanus, R., & Svatoŝ, A. (2006). Analysis of insect cuticular hydrocarbons using matrix-assisted laser desorption/ionization mass spectrometry. Journal of Chemical Ecology, 32, 409–434.PubMedCrossRefGoogle Scholar
  30. Dayrat, B. (2005). Towards integrative taxonomy. Biological Journal of the Linnean Society, 85, 407–415.CrossRefGoogle Scholar
  31. De Bruyne, K., Slabbinck, B., Waegeman, W., Vauterin, P., De Baets, B., & Vandamme, P. (2011). Bacterial species identification from MALDI-TOF mass spectra through data analysis and machine learning. Systematic and Applied Microbiology, 34, 20–29.PubMedCrossRefGoogle Scholar
  32. Diz, A. P., Martínez-Fernández, M., & Rolán-Alvarez, E. (2012). Proteomics in evolutionary ecology: linking the genotype with the phenotype. Molecular Ecology, 21, 1060–1080.PubMedCrossRefGoogle Scholar
  33. Dufresne, F., & Jeffery, N. (2011). A guided tour of large genome size in animals: what we know and where we are heading. Chromosome Research, 19, 925–938.PubMedCrossRefGoogle Scholar
  34. Dunn, C. W., Hejnol, A., Matus, D. Q., Pang, K., Browne, W. E., Smith, S. A., et al. (2008). Broad phylogenetic sampling improves resolution of the animal tree of life. Nature, 452, 745–749.PubMedCrossRefGoogle Scholar
  35. Dupuis, J. R., Roe, A. R., & Sperling, F. A. H. (2012). Multi-locus species delimitation in closely related animals and fungi: one marker is not enough. Molecular Ecology, 21, 4422–4436.PubMedCrossRefGoogle Scholar
  36. Eaton, M. J., Meyers, G. L., Kolokotronis, S.-O., Leslie, M. S., Martin, A. P., & Amato, G. (2010). Barcoding bushmeat: molecular identification of Central African and South American harvested vertebrates. Conservation Genetics, 11, 1389–1404.CrossRefGoogle Scholar
  37. Eichner, C., Frost, P., Dysvik, B., Jonassen, I., Kristiansen, B., & Nilsen, F. (2011). Salmon louse (Lepeophtheirus salmonis) transcriptomes during post molting maturation and egg production, revealed using EST-sequencing and microarray analysis. BMC Genomics, 9, 126.CrossRefGoogle Scholar
  38. Enghoff, H. (2009). What is taxonomy?—an overview with myriapodological examples. Soil Organisms, 81, 441–451.Google Scholar
  39. Engstrand, R. C., Tovar, J. C., Cibrián-Jaramillo, A., & Kolokotronis, S.-O. (2010). Genetic variation in avocado stem weevils Copturus aguacatae (Coleoptera: Curculionidae) in Mexico. Mitochondrial DNA, 21, 38–43.PubMedCrossRefGoogle Scholar
  40. Erpenbeck, D., Hooper, J. N. A., Bonnard, I., Sutcliffe, P., Chandra, M., Perio, P., et al. (2012). Evolution, radiation and chemotaxonomy of Lamellodysidea, a demosponge genus with anti-plasmodial metabolites. Marine Biology, 159, 1119–1127.CrossRefGoogle Scholar
  41. Faulwetter, S., Vasileiadou, A., Kouratoras, M., Dailianis, T., & Arvanitidis, C. (2013). Micro-computed tomography: introducing new dimensions to taxonomy. ZooKeys, 263, 1–45.PubMedCrossRefGoogle Scholar
  42. Feltens, R., Görner, R., Kalkhof, S., Gröger-Arndt, H., & von Bergen, M. (2010). Discrimination of different species from the genus Drosophila by intact protein profiling using matrix-assisted laser desorption ionization mass spectrometry. BMC Evolutionary Biology, 10, 95.PubMedPubMedCentralCrossRefGoogle Scholar
  43. Ferguson, B., Street, S. L., Wright, H., Pearson, C., Jia, Y., Thompson, S. L., et al. (2007). Single nucleotide polymorphisms (SNPs) distinguish Indian-origin and Chinese-origin rhesus macaques (Macaca mulatta). BMC Genomics, 8, 43.PubMedPubMedCentralCrossRefGoogle Scholar
  44. Fournier, P.-E., Drancourt, M., Colson, P., Rolain, J.-M., La Scola, B., & Raoult, D. (2013). Modern clinical microbiology: new challenges and solutions. Nature Reviews Microbiology, 11, 574–585.PubMedCrossRefGoogle Scholar
  45. Frentiu, F. D., & Chenoweth, S. F. (2010). Clines in cuticular hydrocarbons in two Drosophila species with independent population histories. Evolution, 64, 1784–1794.PubMedCrossRefGoogle Scholar
  46. Frisvad, J. C., Andersen, B., & Thrane, U. (2008). The use of secondary metabolite profiling in chemotaxonomy of filamentous fungi. Mycological Research, 112, 231–240.PubMedCrossRefGoogle Scholar
  47. Fujita, M. K., Leaché, A. D., Burbrink, F. T., McGuire, J. A., & Moritz, C. (2012). Coalescent-based species delimitation in an integrative taxonomy. Trends in Ecology and Evolution, 27, 480–488.PubMedCrossRefGoogle Scholar
  48. Gonçalves, P. F. M., Oliveira-Marques, A. R., Matsumoto, T. E., & Miyaki, C. Y. (2015). DNA barcoding identifies illegal parrot trade. Journal of Heredity, 106, 560–564.PubMedCrossRefGoogle Scholar
  49. Gotelli, N. J., Ellison, A. M., & Ballif, B. A. (2012). Environmental proteomics, biodiversity studies, and food-web structure. Trends in Ecology and Evolution, 27, 436–442.PubMedPubMedCentralCrossRefGoogle Scholar
  50. Guillem, R. M., Drijfhout, F. P., & Martin, S. J. (2012). Using chemo-taxonomy of host ants to help conserve the large blue butterfly. Biological Conservation, 148, 39–43.CrossRefGoogle Scholar
  51. Guschanski, K., Krause, J., Sawyer, S., Valente, L. M., Bailey, S., Finstermeier, K., et al. (2013). Next-generation museomics disentangles one of the largest primate radiations. Systematic Biology, 62, 539–554.PubMedPubMedCentralCrossRefGoogle Scholar
  52. Hanai, T. (1999). HPLC: a practical guide (RSC chromatography monographs). Letchworth: The Royal Society of Chemistry.Google Scholar
  53. Handschuh, S., Baeumler, N., Schwaha, T., & Ruthensteiner, B. (2013). A correlative approach for combining microCT, light and transmission electron microscopy in a single 3D scenario. Frontiers in Zoology, 10, 44.PubMedPubMedCentralCrossRefGoogle Scholar
  54. Haus, T., Akom, E., Agwanda, B., Hofreiter, M., Roos, C., & Zinner, D. (2013). Mitochondrial diversity and distribution of African green monkeys (Chlorocebus Gray, 1870). American Journal of Primatology, 75, 350–360.PubMedPubMedCentralCrossRefGoogle Scholar
  55. Hausmann, A., Godfray, H. C. J., Huemer, P., Mutanen, M., Rougerie, R., van Nieukerken, E. J., et al. (2013). Genetic patterns in European geometrid moths revealed by the Barcode Index Number (BIN system). Public Library of Science ONE, 8, e84518.PubMedPubMedCentralGoogle Scholar
  56. Haye, P. A., Segovia, N. I., Vera, R., Gallardo, M. D. A., & Gallardo-Escárate, C. (2012). Authentication of commercialized crab-meat in Chile using DNA barcoding. Food Control, 25, 239–244.CrossRefGoogle Scholar
  57. Hebert, P. D. N., Ratnasingham, S., & de Waard, J. R. (2003a). Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London, Series B: Biological Sciences, 270, S96–S99.CrossRefGoogle Scholar
  58. Hebert, P. D. N., Cywinska, A., Ball, S. L., & de Waard, J. R. (2003b). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, Series B: Biological Sciences, 270, 313–321.CrossRefGoogle Scholar
  59. Hebert, P. D. N., deWaard, J. R., Zakharov, E. V., Prosser, S. W. J., Sones, J. E., McKeown, J. T. A., et al. (2013). A DNA “Barcode Blitz”: rapid digitization and sequencing of a natural history collection. Public Library of Science ONE, 8, e68535.PubMedPubMedCentralGoogle Scholar
  60. Hendrich, L., Morinière, J., Haszprunar, G., Hebert, P. D. N., Hausmann, A., Köhler, F., et al. (2015). A comprehensive DNA barcode database for Central European beetles with a focus on Germany: adding more than 3500 identified species to BOLD. Molecular Ecology Resources, 15, 795–818.PubMedCrossRefGoogle Scholar
  61. Hrbek, T., da Silva, V. M. F., Dutra, N., Gravena, W., Martin, A. R., & Farias, I. P. (2014). A new species of river dolphin from Brazil or: how little do we know our biodiversity. Public Library of Science ONE, 9, e83623.PubMedPubMedCentralGoogle Scholar
  62. IISE (2011). State of observed species. Tempe, Arizona. International Institute for Species Exploration. Retrieved 2014-09-16 from http://www.esf.edu/species/SOS.htm
  63. Ivanisěvić, J., Thomas, O. P., Lejeusne, C., Chevaldonné, P., & Pérez, T. (2011). Metabolic fingerprinting as an indicator of biodiversity: towards understanding inter-specific relationships among Homoscleromorpha sponges. Metabolomics, 7, 289–304.CrossRefGoogle Scholar
  64. Ji, Y., Ashton, L., Pedley, S. M., Edwards, D. P., Tang, Y., Nakamura, A., et al. (2013). Reliable, verifiable and efficient monitoring of biodiversity via metabarcoding. Ecology Letters, 16, 1245–1257.PubMedCrossRefGoogle Scholar
  65. Jónsson, H., Schubert, M., Seguin-Orlando, A., Ginolhac, A., Peterson, L., Fumagalli, M., et al. (2014). Speciation with gene flow in equids despite extensive chromosomal plasticity. Proceedings of the National Academy of Sciences of the United States of America, 111, 18655–18660.PubMedPubMedCentralCrossRefGoogle Scholar
  66. Karas, M., & Hillenkamp, F. (1988 ). Laser desorption ionization of proteins with molecular masses exceeding 10000 daltons. Analytical Chemistry, 60, 2299–2303.Google Scholar
  67. Karr, T. L. (2008). Application of proteomics to ecology and population biology. Heredity, 100, 200–206.Google Scholar
  68. Kather, R., & Martin, S. J. (2012). Cuticular hydrocarbon profiles as a taxonomic tool: advantages, limitations and technical aspects. Physiological Entomology, 37, 25–32.CrossRefGoogle Scholar
  69. Kather, R., Drijfhout, F. P., & Martin, S. J. (2011). Task group differences in cuticular lipids in the honey bee Apis mellifera. Journal of Chemical Ecology, 37, 205–212.PubMedCrossRefGoogle Scholar
  70. Kaufmann, C., Ziegler, D., Schaffner, F., Carpenter, S., Pflüger, V., & Mathis, A. (2011). Evaluation of matrix-assisted laser desorption/ionization time off flight mass spectrometry for characterization of Culicoides nubeculosus biting midges. Medical and Veterinary Entomology, 25, 32–38.Google Scholar
  71. Khalaji-Pirbalouty, V., & Raupach, M. J. (2014). A new species of Cymodoce Leach, 1814 (Crustacea: Isopoda: Sphaeromatidae) based on morphological and molecular data, with a key to the Northern Indian Ocean species. Zootaxa, 3826, 230–254.PubMedCrossRefGoogle Scholar
  72. Kircher, M., & Kelso, J. (2010). High-throughput DNA sequencing—concepts and limitations. BioEssays, 32, 524–536.PubMedCrossRefGoogle Scholar
  73. Kron, P., Suda, J., & Husband, B. C. (2007). Application of flow cytometry to evolutionary and population biology. Annual Review of Ecology, Evolution, and Systematics, 38, 847–876.CrossRefGoogle Scholar
  74. Laakmann, S., Gerdts, G., Erler, R., Knebelsberger, T., Martínez Arbízu, P., & Raupach, M. J. (2013). Comparison of molecular species identification for North Sea calanoid copepods (Crustacea) using proteome fingerprints and DNA sequences. Molecular Ecology Resources, 13, 862–876.PubMedCrossRefGoogle Scholar
  75. Lamichhaney, S., Berglund, J., Almén, M. S., Maqbool, K., Grabherr, M., Martinez-Barrio, A., et al. (2015). Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature, 518, 371–375.PubMedCrossRefGoogle Scholar
  76. Leaché, A. D., Fujita, M. K., Minin, V. N., & Bouckaert, R. R. (2014). Species delimitation using genome-wide SNP data. Systematic Biology, 63, 534–542.PubMedPubMedCentralCrossRefGoogle Scholar
  77. Lenihan, J., Kvist, S., Fernández, S., Giribret, G., & Ziegler, A. (2014). A dataset comprising four microcomputed tomography scans of freshly fixed and museum earthworm specimens. GigaScience, 3, 6.Google Scholar
  78. Leray, M., & Knowlton, N. (2015). DNA barcoding and metabarcoding of standardized samples reveal patterns of marine benthic diversity. Proceedings of the National Academy of Sciences of the United States of America, 112, 2076–2081.PubMedPubMedCentralCrossRefGoogle Scholar
  79. Liang, D., & Silverman, J. (2000). ‘You are what you eat’: diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile. Naturwissenschaften, 87, 412–416.PubMedCrossRefGoogle Scholar
  80. Liedigk, R., Kolleck, J., Böker, K. O., Meeijard, E., Md-Zain, B. M., Abdul-Latiff, M. A. B., et al. (2015). Mitogenomic phylogeny of the common long-tailed macaque (Macaca fascicularis fascicularis). BMC Genomics, 16, 222.PubMedPubMedCentralCrossRefGoogle Scholar
  81. Lockey, K. H. (1988). Lipids of the insect cuticle: origin, composition and function. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 89, 595–645.CrossRefGoogle Scholar
  82. Lu, G.-H., Chan, K., Liang, Y.-Z., Leung, K., Chan, C.-L., Jiang, Z.-H., et al. (2005). Development of high-performance liquid chromatographic fingerprints for distinguishing Chinese Angelica from related umbelliferae herbs. Journal of Chromatography A, 1073, 383–392.PubMedCrossRefGoogle Scholar
  83. Mardis, E. R. (2013). Next-generation sequencing platforms. Annual Review of Analytical Chemistry, 6, 287–303.PubMedCrossRefGoogle Scholar
  84. Martin, S. J., Helantera, H., & Drijfhout, F. P. (2008). Evolution of species-specific cuticular hydrocarbon patterns in Formica ants. Biological Journal of the Linnean Society, 95, 131–140.CrossRefGoogle Scholar
  85. May, R. R., & Harvey, P. H. (2009). Species uncertainties. Science, 323, 687.PubMedCrossRefGoogle Scholar
  86. Mayagaya, V. S., Michel, K., Benedict, M. Q., Killeen, G. F., Wirtz, R. A., Ferguson, H. M., et al. (2009). Non-destructive determination of age and species of Anopheles gambiae s.l. using near-infrared spectroscopy. The American Journal of Tropical Medicine and Hygiene, 81, 622–630.PubMedCrossRefGoogle Scholar
  87. Mazzeo, M. F., de Giulio, B., Guerriero, G., Ciarcia, G., Malorni, A., Russo, G. L., et al. (2008). Fish authentication by MALDI-TOF mass spectrometry. Journal of Agricultural and Food Chemistry, 56, 11071–11076.PubMedCrossRefGoogle Scholar
  88. Miller, J., Dikow, T., Agosti, D., Sautter, G., Catapano, T., Penev, L., et al. (2012). From taxonomic literature to cybertaxonomic content. BMC Biology, 10, 87.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Miller, J. A., Miller, J. H., Pham, D.-S., & Beentjes, K. K. (2014). Cyberdiversity: Improving the informatic value of diverse tropical arthropod inventories. Public Library of Science ONE, 9, e115750.PubMedPubMedCentralGoogle Scholar
  90. Minelli, A. (2013). Zoological nomenclature in the digital era. Frontiers in Zoology, 10, 4.PubMedPubMedCentralCrossRefGoogle Scholar
  91. Misof, B., Liu, S., Meusemann, K., Peters, R. S., Donath, A., Mayer, C., et al. (2014). Phylogenomics resolves the timing and pattern of insect evolution. Science, 346, 763–767.PubMedCrossRefGoogle Scholar
  92. Mora, C., Tittensor, D. P., Adl, S., Simpson, A. G. B., & Worm, B. (2011). How many species are there on Earth and in the ocean? Public Library of Science Biology, 9, e1001127.Google Scholar
  93. Nadeau, N. J., Martin, S. H., Kozak, K. M., Salazar, C., Dasmahapatra, K., Davey, J. W., et al. (2013). Genome-wide patterns of divergence and gene flow across a butterfly radiation. Molecular Ecology, 22, 814–826.PubMedCrossRefGoogle Scholar
  94. Nagy, Z. T., Sonet, G., Glaw, F., & Vences, M. (2012). First large-scale DNA barcoding assessment of reptiles in the biodiversity hotspot of Madagascar, based on newly designed COI primers. Public Library of Science ONE, 7, e34506.PubMedPubMedCentralGoogle Scholar
  95. Nelson, L. A., Wallman, J. F., & Dowton, M. (2007). Using COI barcodes to identify forensically and medically important blowflies. Medical and Veterinary Entomology, 21, 44–52.PubMedCrossRefGoogle Scholar
  96. Nicholson, S. J., & Puterka, G. J. (2014). Variation in the salivary proteomes of differently virulent green bug (Schizaphis graminum Rondani) biotypes. Journal of Proteomics, 105, 186–203.PubMedCrossRefGoogle Scholar
  97. Oakley, T. H., Wolfe, J. M., Lindgren, A. R., & Zaharoff, A. K. (2012). Phylotranscriptomics to bring the understudied into the fold: monophyletic Ostracoda, fossil placement, and pancrustacean phylogeny. Molecular Biology and Evolution, 30, 215–233.PubMedCrossRefGoogle Scholar
  98. Oetjen, J., Veselkov, K., Watrous, J., McKenzie, J. S., Becker, M., Hauberg-Lotte, L., et al. (2015). Benchmark datasets for 3D MALDI- and DESI-imaging mass spectrometry. GigaScience, 4, 20.PubMedPubMedCentralCrossRefGoogle Scholar
  99. Orgiazzi, A., Dunbar, M. B., Panagos, P., de Groot, G. A., & Lemanceau, P. (2015). Soil biodiversity and DNA barcodes: opportunities and challenges. Soil Biology & Biochemistry, 80, 244–250.CrossRefGoogle Scholar
  100. Padial, J. M., Miralles, A., de la Riva, I., & Vences, M. (2010). The integrative future of taxonomy. Frontiers in Zoology, 7, 16.PubMedPubMedCentralCrossRefGoogle Scholar
  101. Pante, E., Abdelkrim, J., Viricel, A., Gey, D., France, S. C., Boisselier, M. C., et al. (2015). Use of RAD sequencing for delimiting species. Heredity, 114, 450–459.PubMedCrossRefGoogle Scholar
  102. Papadopoulou, A., Taberlet, P., & Zinger, L. (2015). Metagenome skimming for phylogenetic community ecology: a new era in biodiversity research. Molecular Ecology, 24, 3515–3517.PubMedCrossRefGoogle Scholar
  103. Pasquini, C. (2003). Near infrared spectroscopy: fundamentals practical aspects and analytical applications. Journal of the Brazilian Chemical Society, 14, 138–219.CrossRefGoogle Scholar
  104. Perelman, P., Johnson, W. E., Roos, C., Seuanez, H. N., Horvath, J. E., Moreira, M. A. M., et al. (2011). A molecular phylogeny of living primates. Public Library of Science Genetics, 7, e1001342.PubMedPubMedCentralGoogle Scholar
  105. Pettersen, R., Johnsen, G., Bruheim, P., & Andreassen, T. (2014). Development of hyperspectral imaging as a bio-optical taxonomic tool for pigmented marine organisms. Organisms, Diversity and Evolution, 14, 237–246.CrossRefGoogle Scholar
  106. Pilgrim, E. M., & Darling, J. A. (2010). Genetic diversity in two introduced biofouling amphipods (Ampithoe valida & Jassa marmorata) along the Pacific North American coast: investigation into molecular identification and cryptic diversity. Diversity and Distributions, 16, 827–839.CrossRefGoogle Scholar
  107. Poelstra, J. W., Vijay, N., Bossu, C. M., Lantz, H., Ryll, B., Müller, I., et al. (2014). The genomic landscape underlying phenotypic integrity in the face of gene flow in crows. Science, 344, 1410–1414.PubMedCrossRefGoogle Scholar
  108. Polaszek, A., Agosti, D., Alonso-Zarazaga, M., Beccaloni, G., de Place Bjørn, P., Bouchet, P., et al. (2005). A universal register for animal names. Nature, 437, 477.PubMedCrossRefGoogle Scholar
  109. Pop, M., & Salzberg, S. L. (2008). Bioinformatics challenges of new sequencing technology. Trends in Genetics, 24, 142–149.PubMedPubMedCentralCrossRefGoogle Scholar
  110. Puillandre, N., Reto, S., Philippe, F., Estelle, B., Frédéric, P., Audrey, R., et al. (2014). When everything converges: Integrative taxonomy with shell, DNA and venomic data reveals Conus conco, a new species of cone snails (Gastropoda: Conoidea). Molecular Phylogenetics and Evolution, 80, 186–192.PubMedCrossRefGoogle Scholar
  111. Rasmussen, R. S., Morrissey, M. T., & Hebert, P. D. N. (2013). DNA barcoding of commercially important salmon and trout species (Oncorhynchus and Salmo) from North America. Journal of Agricultural and Food Chemistry, 57, 8379–8385.CrossRefGoogle Scholar
  112. Raupach, M. J., Hendrich, L., Küchler, S. M., Deister, F., Morinière, J., & Gossner, M. M. (2014). Building-up of a DNA barcode library for True Bugs (Insecta: Hemiptera: Heteroptera) of Germany reveals taxonomic uncertainties and surprises. Public Library of Sciences ONE, 9, e106940.Google Scholar
  113. Rendón-Anaya, M., Delaye, L., Possani, L. D., & Herrera-Estrella, A. (2012). Global transcriptome analysis of the scorpion Centruroides noxius: new toxin families and evolutionary insights from an ancestral scorpion species. Public Library of Sciences ONE, 7, e43331.Google Scholar
  114. Riccardi, N., Lucini, L., Benagli, C., Welker, M., Wicht, B., & Tonolla, M. (2012). Potential of matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) for the identification of freshwater zooplankton: a pilot study with three Eudiaptomus (Copepoda: Diaptomidae) species. Journal of Plankton Research, 34, 1–9.CrossRefGoogle Scholar
  115. Richter, M., & Rosselló-Móra, R. (2009). Shifting the genomic gold standard for the prokaryotic species definition. Proceedings of the National Academy of Sciences of the United States of America, 106, 19126–19131.PubMedPubMedCentralCrossRefGoogle Scholar
  116. Riedel, A., Sagata, K., Suhardjono, Y. R., Tänzler, R., & Balke, M. (2013a). Integrative taxonomy on the fast track—towards more sustainability in biodiversity research. Frontiers in Zoology, 10, 15.PubMedPubMedCentralCrossRefGoogle Scholar
  117. Riedel, A., Sagata, K., Surbakti, S., Tänzler, R., & Balke, M. (2013b). One hundred and one new species of Trigonopterus weevils from New Guinea. ZooKeys, 280, 1–150.PubMedCrossRefGoogle Scholar
  118. Riesgo, A., Andrade, S. C. S., Sharma, P. P., Novo, M., Pérez-Porro, A. R., Vahtera, V., et al. (2012). Comparative description of ten transcriptomes of newly sequenced invertebrates and efficiency estimation of genomic sampling in non-model taxa. Frontiers in Zoology, 9, 33.PubMedPubMedCentralCrossRefGoogle Scholar
  119. Rodríguez-Fernández, J. I., de Carvalho, C. J. B., Pasquini, C., de Lima, K. M. G., Moura, M. O., & Arízaga, G. G. C. (2011). Barcoding without DNA? Species identification using near infrared spectroscopy. Zootaxa, 2933, 46–54.Google Scholar
  120. Romiguier, J., Gayral, P., Ballenghien, M., Bernard, A., Cahais, A., Chenuil, A., et al. (2014). Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature, 515, 261–263.PubMedCrossRefGoogle Scholar
  121. Roos, C., Nadler, T., & Walter, L. (2008). Mitochondrial phylogeny, taxonomy and biogeography of the silvered langur species group (Trachypithecus cristatus). Molecular Phylogenetics and Evolution, 47, 629–636.PubMedCrossRefGoogle Scholar
  122. Roos, C., Zinner, D., Kubatko, L. S., Schwarz, C., Yang, M., Meyer, D., et al. (2011). Nuclear versus mitochondrial DNA: evidence for hybridization in colobine monkeys. BMC Evolutionary Biology, 11, 77.PubMedPubMedCentralCrossRefGoogle Scholar
  123. Rosenberg, M. S. (2012). Contextual cross-referencing of species names for fiddler crabs (Genus: Uca): an experiment in cyber-taxonomy. Public Library of Science ONE, 9, e101704.Google Scholar
  124. Rowe, K. C., Singhal, S., MacManes, M. D., Ayroles, J. F., Morelli, T. L., Rubidge, E. M., et al. (2011). Museum genomics: low-cast and high accuracy genetic data from historical specimens. Molecular Ecology Resources, 11, 1082–1092.PubMedCrossRefGoogle Scholar
  125. Sauer, S., & Kliem, M. (2010). Mass spectrometry tools for the classification and identification of bacteria. Nature Reviews Microbiology, 8, 74–82.PubMedCrossRefGoogle Scholar
  126. Savolainen, P., & Reeves, G. (2004). A plea for DNA banking. Science, 304, 1445.PubMedCrossRefGoogle Scholar
  127. Schilthuizen, M., Scholte, C., van Wijk, R. E. J., Doimmershuijzen, J., van der Horst, D., Meijer zu Schlochtern, M., et al. (2011). Using DNA-barcoding to make the necrobiont beetle family Cholevidae accessible for forensic entomology. Forensic Science International, 210, 91–95.PubMedCrossRefGoogle Scholar
  128. Schlick-Steiner, B. C., Steiner, F. M., Seifert, B., Stauffer, C., Christian, E., & Crozier, R. H. (2010). Integrative taxonomy: a multisource approach to exploring biodiversity. Annual Review of Entomology, 55, 421–438.PubMedCrossRefGoogle Scholar
  129. Schneider, M. V., & Orchard, S. (2011). Omics technologies, data and bioinformatic principles. Methods in Molecular Biology, 719, 3–30.PubMedCrossRefGoogle Scholar
  130. Schunter, C., Vollmer, S. V., Macpherson, E., & Pascual, M. (2014). Transcriptome analyses and differential gene expression in a non-model fish species with alternative mating tactics. BMC Genomics, 15, 167.PubMedPubMedCentralCrossRefGoogle Scholar
  131. Sehrawat, N., & Gakhar, S. K. (2014). Mosquito proteomics: present and future perspective. Research in Biotechnology, 5, 25–33.Google Scholar
  132. Serrano, W., Amann, R., Rosselló-Mora, R., & Fischer, U. (2010). Evaluation of the use of multilocus sequence analysis (MLSA) to resolve taxonomic conflicts within the genus Marichromatium. Systematic and Applied Microbiology, 33, 116–121.PubMedCrossRefGoogle Scholar
  133. Sherwin, W. B., Frommer, M., Sved, J. A., Raphael, K. A., Oakeshott, J. G., Shearman, D. C. A., et al. (2015). Tracking invasion and invasiveness in Queensland fruit flies: from classical genetics to ‘omics’. Current Zoology, 61, 477–487.CrossRefGoogle Scholar
  134. Shevtsova, E., Hansson, C., Janzen, D. H., & Kjærandsen, J. (2011). Stable structural color patterns displayed on transparent insect wings. Proceedings of the National Academy of Sciences of the United States of America, 108, 668–673.PubMedPubMedCentralCrossRefGoogle Scholar
  135. Shipway, J. R., Borges, L. M. S., Müller, J., & Cragg, S. M. (2014). The broadcast spawning Caribbean shipworm, Teredothyra dominicensis (Bivalvia, Teredinidae), has invaded and become established in the eastern Mediterranean Sea. Biological Invasions, 16, 2037–2048.CrossRefGoogle Scholar
  136. Skoog, D. A., Holler, F. J., & Crouch, S. R. (2006). Principles of Instrumental Analysis. Boston: Cengage Learning.Google Scholar
  137. Soldati, L., Kergoat, G. J., Clamens, A.-L., Jourdan, H., Jabbour-Zahab, R., & Condamine, F. L. (2014). Integrative taxonomy of New Caledonian beetles: species delimitation and definition of the Uloma isoceroides species group (Coleoptera, Tenebrionidae, Ulomini), with the description of four new species. ZooKeys, 415, 133–167.PubMedCrossRefGoogle Scholar
  138. Sombke, A., Lipke, E., Michalik, P., Uhl, G., & Harzsch, S. (2015). Potential and limitations of X-ray micro-computed tomography in arthropod neuroanatomy: a methodological and comparative survey. The Journal of Comparative Neurology, 523, 1281–1295.Google Scholar
  139. Spelda, J., Reip, H. S., Oliveira-Biener, U., & Melzer, R. R. (2011). Barcoding Fauna Bavarica—a contribution to DNA sequence-based identifications of centipedes and millipedes (Chilopoda, Diplopoda). ZooKeys, 156, 123–139.PubMedCrossRefGoogle Scholar
  140. Stoev, P., Komerički, A., Akkari, N., Liu, S., Zhou, X., Weigand, A. M., et al. (2013). Eupolybothrus cavernicolus Komerički & Stoev sp. n. (Chilopoda: Lithobiomorpha: Lithobiidae): the first eukaryotic species description combining transcriptomic, DNA barcoding and micro-CT imaging data. Biodiversity Data Journal, 1, e1013.PubMedCrossRefGoogle Scholar
  141. Struck, T. H., Paul, C., Hill, N., Hartmann, S., Hösel, C., Kube, M., et al. (2011). Phylogenetic analyses unravel annelid evolution. Nature, 471, 95–98.PubMedCrossRefGoogle Scholar
  142. Strutzenberger, P., Brehm, G., & Fiedler, K. (2013). DNA barcode sequencing from old type specimens as a tool in taxonomy: a case study in diverse Eois (Lepidoptera: Geometridae). Public Library of Science ONE, 7, e49710.Google Scholar
  143. Summers, M. M., Al-Hakim, I. I., & Rouse, G. W. (2014). Turbo-taxonomy: 21 new species of Myzostomida (Annelida). Zootaxa, 3873, 301–344.PubMedCrossRefGoogle Scholar
  144. Tang, M., Tan, M., Meng, G., Yang, S., Su, X., Liu, S., et al. (2014). Multiplex sequencing of pooled mitochondrial genomes—a crucial step toward biodiversity analysis using mito-genomics. Nucleic Acids Research, 42, e166.PubMedPubMedCentralCrossRefGoogle Scholar
  145. Tang, M., Hardman, C. J., Ji, Y., Meng, G., Liu, S., Tan, M., et al. (2015). High-throughput monitoring of wild bee diversity and abundance via mitogenomics. Methods in Ecology and Evolution. doi:10.1111/2041-210X.12416.Google Scholar
  146. Taylor, H. R., & Harris, W. E. (2012). An emergent science on the brink of irrelevance: a review of the past 8 years of DNA barcoding. Molecular Ecology Resources, 12, 377–388.PubMedCrossRefGoogle Scholar
  147. Thinh, V. N., Mootnick, A. R., Thanh, V. N., Nadler, T., & Roos, C. (2010). A new species of crested gibbon, from the central Annamite mountain range. Vietnamese Journal of Primatology, 1, 1–12.Google Scholar
  148. Thompson, C. C., Chimetto, L., Edwards, R. A., Swings, J., Stackebrandt, E., & Thompson, F. L. (2014). Microbial genomic taxonomy. BMC Genomics, 14, 913.Google Scholar
  149. Valentini, A., Pompanon, F., & Taberlet, P. (2009). DNA barcoding for ecologists. Trends in Ecology and Evolution, 24, 110–117.PubMedCrossRefGoogle Scholar
  150. van Dijk, E. L., Auger, H., Jaszczyszyn, Y., & Thermes, C. (2014). Ten years of next-generation sequencing technologies. Trends in Genetics, 30, 418–426.PubMedCrossRefGoogle Scholar
  151. van Houdt, J. K. L., Breman, F. C., Virgilio, M., & de Meyer, M. (2010). Recovering full DNA barcodes from natural history collections of Tephritid fruitflies (Tephritidae, Diptera) using mini barcodes. Molecular Ecology Resources, 10, 459–465.CrossRefGoogle Scholar
  152. Villar, M., Popara, M., Mangold, A. J., & de la Fuente, J. (2014). Comparative proteomics for the characterization of the most relevant Amblyomma tick species as vectors of zoonotic pathogens worldwide. Journal of Proteomics, 105, 2014–2216.CrossRefGoogle Scholar
  153. Volta, P., Riccardi, N., Lauceri, R., & Tonolla, M. (2012). Discrimination of freshwater fish species by matrix-assisted laser desorption/ionization-time of flight mass spectrometry (MALDI-TOF MS): a pilot study. Journal of Limnology, 71, 164–169.CrossRefGoogle Scholar
  154. von Reumont, B. M., Jenner, R. A., Wills, M. A., DellÀmpio, E., Pass, G., Ebersberger, I., et al. (2012). Pancrustacean phylogeny in the light of new phylogenomic data: support for Remipedia a possible sister group of Hexapoda. Molecular Biology and Evolution, 29, 1031–1045.CrossRefGoogle Scholar
  155. von Reumont, B. M., Blanke, A., Richter, S., Alvarez, F., Bleidorn, C., & Jenner, R. A. (2014). The first venomous crustacean revealed by transcriptomics and functional morphology: remipede venom glands express a unique toxin cocktail dominated by enzymes and a neurotoxin. Molecular Biology and Evolution, 31, 48–58.CrossRefGoogle Scholar
  156. Wang, X. P., Yu, L., Roos, C., Ting, N., Chen, C. P., Wang, J., et al. (2012). Phylogenetic relationships among the colobine monkeys revisited: new insights from analyses of complete mt genomes and 44 nuclear non-coding markers. Public Library of Science ONE, 7, e36274.PubMedPubMedCentralGoogle Scholar
  157. Weis, A., Meyer, R., Dietz, L., Dömel, J. S., Leese, F., & Melzer, R. R. (2014). Pallenopsis patagonica (Hoek, 1881)—a species complex revealed by morphology and DNA barcoding, with description of a new species of Pallenopsis Wilson, 1881. Zoological Journal of the Linnean Society, 170, 110–131.CrossRefGoogle Scholar
  158. Welker, M., & Moore, E. R. B. (2011). Applications of whole-cell matrix-assisted laser-desorption/ionization time-of-flight mass spectrometry in systematic microbiology. Systematic and Applied Microbiology, 34, 2–11.PubMedCrossRefGoogle Scholar
  159. Wenning, M., & Scherer, S. (2013). Identification of microorganisms by FTIR spectroscopy: perspectives and limitations of the method. Applied Microbiology and Biotechnology, 97, 7111–7120.PubMedCrossRefGoogle Scholar
  160. Wheeler, Q. D., & Valdecasas, A. G. (2010). Cybertaxonomy and ecology. Nature Education Knowledge, 3, 6.Google Scholar
  161. Wheeler, Q. D., Bourgoin, T., Coddington, J., Gostony, T., Hamilton, A., Larimer, R., et al. (2012). Nomenclatural benchmarking: the roles of digital typification and telemicroscopy. ZooKeys, 209, 193–202.PubMedCrossRefGoogle Scholar
  162. Will, K. P., Mishler, P. D., & Wheeler, Q. D. (2005). The perils of DNA barcoding and the need for integrative taxonomy. Systematic Biology, 54, 844–851.PubMedCrossRefGoogle Scholar
  163. Wilson, D., & Alewood, P. F. (2006). Taxonomy of Australian funnel-web spiders using rp-HPLC/ESI-MS profiling techniques. Toxicon, 47, 614–627.PubMedCrossRefGoogle Scholar
  164. Wilson, N. G., Maschek, J. A., & Baker, B. J. (2013). A species flock driven by predation? Secondary metabolites support diversification of slugs in Antarctica. Public Library of Sciences ONE, 8, e80277.Google Scholar
  165. Yan, D., Luo, J. Y., Han, Y. M., Peng, C., Dong, X. P., Chen, S. L., et al. (2013). Forensic DNA barcoding and bio-response studies of animal horn products in traditional medicine. Public Library of Science ONE, 8, e55854.PubMedPubMedCentralGoogle Scholar
  166. Yang, Z., & Rannala, B. (2010). Bayesian species delimitation using multilocus sequence data. Proceedings of the National Academy of Sciences of the United States of America, 107, 9264–9269.PubMedPubMedCentralCrossRefGoogle Scholar
  167. Zapata, M., Jeffrey, S. W., Wright, S. W., Rodríguez, F., Garrido, J. L., & Clementson, L. (2004). Photosynthetic pigments in 37 species (65 strains) of Haptophyta: implications for oceanography and chemotaxonomy. Marine Ecology Progress Series, 270, 83–102.CrossRefGoogle Scholar
  168. Zhou, X., Li, Y., Liu, S., Yang, Q., Su, X., Zhou, L., et al. (2013). Ultra-deep sequencing enables high-fidelity recovery of biodiversity bulk arthropod samples without PCR amplification. GiagaScience, 2, 4.CrossRefGoogle Scholar
  169. Ziegler, A., Ogurreck, M., Steinke, T., Beckmann, F., Prohaska, S., & Ziegler, A. (2010). Opportunities and challenges for digital morphology. Biology Direct, 5, 45.PubMedPubMedCentralCrossRefGoogle Scholar
  170. Ziegler, A., Faber, C., Mueller, S., Nagelmann, N., & Schröder, L. (2014). A data set comprising 141 magnetic resonance imaging scans of 98 extant sea urchin species. GigaScience, 3, 31.CrossRefGoogle Scholar
  171. Zinner, D., Groeneveld, L. F., Keller, C., & Roos, C. (2009a). Mitochondrial phylogeography of baboons (Papio spp.)—indication for introgressive hybridization? BMC Evolutionary Biology, 9, 83.PubMedPubMedCentralCrossRefGoogle Scholar
  172. Zinner, D., Arnold, M. L., & Roos, C. (2009b). Is the new primate genus Rungwecebus a baboon? Public Library of Science ONE, 4, e4859.PubMedPubMedCentralGoogle Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2015

Authors and Affiliations

  • Michael J. Raupach
    • 1
  • Rudolf Amann
    • 2
  • Quentin D. Wheeler
    • 3
  • Christian Roos
    • 4
  1. 1.German Center of Marine Biodiversity ResearchSenckenberg am MeerWilhelmshavenGermany
  2. 2.Max Planck Institute for Marine MicrobiologyBremenGermany
  3. 3.State University of New York College of Environmental Science and ForestrySyracuseUSA
  4. 4.Gene Bank of Primates, Primate Genetics Laboratory, German Primate CenterLeibniz Institute for Primate ResearchGöttingenGermany

Personalised recommendations