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The taxonomist - an endangered race. A practical proposal for its survival

Heike Wägele1*, Annette Klussmann-Kolb2, Michael Kuhlmann3, Gerhard Haszprunar4, David Lindberg5, André Koch1 and J Wolfgang Wägele1

Author Affiliations

1 Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany

2 Institute for Ecology, Evolution and Diversity, Goethe-University, Siesmayerstrasse 70, 60054 Frankfurt am Main, Germany

3 Department of Entomology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK

4 Zoologische Staatssammlung München, Münchhausenstraße 21, 81247 München, Germany

5 Department of Integrative Biology and Museum of Paleontology, University of California, Berkeley, CA 94720-4780, USA

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Frontiers in Zoology 2011, 8:25  doi:10.1186/1742-9994-8-25

The electronic version of this article is the complete one and can be found online at: http://www.frontiersinzoology.com/content/8/1/25


Received:20 May 2011
Accepted:26 October 2011
Published:26 October 2011

© 2011 Wägele et al; licensee BioMed Central Ltd.

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background

Taxonomy or biological systematics is the basic scientific discipline of biology, postulating hypotheses of identity and relationships, on which all other natural sciences dealing with organisms relies. However, the scientific contributions of taxonomists have been largely neglected when using species names in scientific publications by not citing the authority on which they are based.

Discussion

Consequences of this neglect is reduced recognition of the importance of taxonomy, which in turn results in diminished funding, lower interest from journals in publishing taxonomic research, and a reduced number of young scientists entering the field. This has lead to the so-called taxonomic impediment at a time when biodiversity studies are of critical importance.

Here we emphasize a practical and obvious solution to this dilemma. We propose that whenever a species name is used, the author(s) of the species hypothesis be included and the original literature source cited, including taxonomic revisions and identification literature - nothing more than what is done for every other hypothesis or assumption included in a scientific publication. In addition, we postulate that journals primarily publishing taxonomic studies should be indexed in ISISM.

Summary

The proposal outlined above would make visible the true contribution of taxonomists within the scientific community, and would provide a more accurate assessment for funding agencies impact and importance of taxonomy, and help in the recruitment of young scientists into the field, thus helping to alleviate the taxonomic impediment. In addition, it would also make much of the biological literature more robust by reducing or alleviating taxonomic uncertainty.

Keywords:
Taxonomy crisis; taxonomic impediment; impact factor; original species description; citation index; systematics

Background

Taxonomy or biological systematics is the science of discovering, describing, classifying and naming organisms [1]. It dates from Aristotle, and thus is the oldest discipline in biology. It forms the basis for all other scientific disciplines dealing with the study of life, its structure, function and evolution. Taxonomic knowledge is paramount whether studying whole organisms, their organs, their specific bio-molecules or biochemical pathways. Unambiguously identified organisms in the sense of referenced, unique taxonomy are essential to all biological studies, because they are a prerequisite to enable the confirmation or refutation of any scientific study that reports on these taxa or their components. Only if a species' identity is unambiguous, can the study be considered robust enough to discuss species-specific traits or attributes with colleagues or convey them to the scientific community and general public. Identification of a species utilized in a study impacts all subsequent comparisons, predictions, and possible replication of the study. It might be argued that the identification of the study organism is irrelevant when examining basic processes such as membrane transport mechanisms, photosynthetic cycles in plants, etc. However, this is not the case as many pathways of physiological processes are adapted in the organism to the specific environmental conditions and this must be taken into consideration whenever conclusions are generalized beyond the study organism. For example, the eubacterium Thermus aquaticus Brock & Freeze, 1969 [2] is restricted to hot springs and is the only species known (and famous for) possessing the Taq-Polymerase [3]. In addition, medical studies reporting on the leech Hirudo medicinalis Linnaeus, 1758 [4] have been shown to have actually studied several distinct yet morphologically cryptic leech species [5,6]. Given the importance of this species in neurobiology and the study of anticoagulants, it is critical that workers associate leech identifications with a referenced, unique taxonomy rather than use a non-specific, general species name. The identification of the species is the first step in almost any biological or related study.

In many cases species identifications are difficult, and it is not surprising that a staggering number of species remain undescribed [7-10]. Add to this the scarcity of knowledgeable taxonomists [11] (particularly in third world and developing countries [12]), often referred to as the "taxonomic impediment" [1,13-16], and it is understandable why certain biological disciplines have chosen "taxonomy-free" research subjects. In particular, many biodiversity and ecological research programs pursue directions that do not require estimates of the actual (alpha) diversity of ecosystems. Instead proxies such as biomass production, measurements of evaporation, CO2 storage, functional groups, or the focusing on a few selected and well-known taxonomic groups (such as "birds", "bats", or "trees') are substitute for measurements of alpha biodiversity [17]. In addition, funding to include alpha diversity studies across a wide variety of groups making up the community or occurring in the habitat is seldom allocated or made available.

Taxonomy is the discipline in biology where scientists assign to taxa unique identities, and these research products are subsequently used by others to identify further individuals that can be used with confidence by colleagues in other scientific disciplines. Many of these other disciplines often include investigations of smaller components of diversity, such as proteins and genes and larger cell components, but they also include population studies, habitat characterization, environmental monitoring and systemic modelling; investigations that include all types of organisms, from bacteria and protists to vertebrates and plants - the entire Tree of Life. The potential consequences of flawed taxonomy leading to error-cascades affecting scientific hypotheses and ideas are commonly underestimated or ignored, but may have serious ecological and economic implications [18].

The availability of species identifications for life science studies is often taken for granted. Currently, about 1.7 Mio metazoan species have been described and it is assumed that tenfold as many species inhabit our world [8,10,19,20] (but see Castello et al. 2011[21]). Studies of biodiversity are critical [10] and have been mandated by many countries where conservation and sustainable use of natural resources have become matters of scientific and public concern [22-24]. Taxonomy is fundamentally important in ensuring the quality of life of future human generations on the planet.

Discussion

There is no question that taxonomists provide insights into alpha biodiversity, provide names for communication, and are at the forefront documenting the biological richness of our planet. Consequently, they must be recognized for their contributions and should be considered an important resource within biology and the associated life science, as well as by the general public. Moreover, journals and other publication media that convey this taxonomic knowledge should be considered as valuable as journals dedicated to other scientific subjects and findings. However, today we are faced with exactly the opposite scenario. Despite the increasing importance of taxonomists in today's biodiversity crisis, most taxonomists are faced with decreasing funding, as well as editorial resistance to publishing their work in the high impact journals that will secure tenure and promotion and allow them to continue their work and contributions [18,25,26].

Taxonomists are often looked upon by colleagues as bureaucratic accountants and their research programs are not recognized as the intellectually challenging and hypotheses-driven science that it has become [27-29]. Today's taxonomist must have a thorough knowledge of the literature, of theoretical species concepts, phylogenetic and analytical methodology, the application of various phenotypic visualization techniques (e.g., anatomy, histology, fine-structure, imaging, 3-D reconstruction), molecular staining, as well as molecular markers for everything from barcoding to genomics. When taxonomic hypotheses are implemented as published descriptions they are subject to future revisions (i.e., replication) with the possibility of either confirmation or rejection just as any other scientific hypothesis [29]. All this notwithstanding, the work done by the species' author(s) is rarely accredited [26,30,31]. Sometimes the author's name is included with the scientific name, but this citation is rarely included in the publication's references or literature cited. The genetic model organisms Drosophila melanogaster Meigen, 1830 [32] and Arabidopsis thaliana (L.) Heynh. [33], for instance, are among the most prominent species cited in scientific publications (about 352.000 and 232.000 citations, respectively). In sharp contrast, the original scientific descriptions of both these species are cited 0 and 19 times, respectively. Other frequently studied and prominent examples, including more recently described species, are presented in Table 1.

Table 1. Discrepancies between the use of species names in scientific publications and citations of the original authors.

Subsequent taxonomic revisions that consolidate taxa (i.e., synonymization) or split species into different subclades are also usually neglected. Out of the 2270 citations found on Hirudo medicinalis in Google scholar for the year 2010, only 41 mentioned the presence of cryptic species and former misidentifications of H. medicinalis and H. verbena Carena, 1820 [34]. Hence, more than 95% of the analyses published in 2010 that explicitly dealt with H. medicinalis (covering a broad array of subjects, like genomes, proteomes, gene syntheses, medical novelties, etc.) cannot be clearly assigned to this species, nor to either of the two undescribed species within the H. medicinalis species complex [5,6], nor to the frequently misidentified H. verbena. Citing the original publication in which the cryptic species problem had been unravelled would have immediately demonstrated the authors' awareness of this problem and its potential consequences, and would have increased confidence in the author's publication.

Recently, several declarations and suggestions have been published in favour of taxonomy, including arguments for more funding, better education, or recruiting parataxonomists and amateurs [11,16,35]. While these appeals are certainly justified, they will not be effective as long as the work of taxonomists is neglected or viewed as unimportant and self-evident (and therefore not worthy of citation) by colleagues in other natural science disciplines. We therefore here emphasize the need for a fair practice mentioned by Werner in 2006 [30] and Seifert et al. in 2008 [36] that would help to recognize the value of taxonomic work and thus to place taxonomy back into mainstream biology and provide a measure of its impact. This accurate accounting of the value of taxonomic studies will also provide familiar metrics for colleagues and administrators, and will be invaluable in the allocation of funding and the long term recruitment of young taxonomists. We therefore propose the following guidelines:

1. Any study based on a formally named organism should include the citation of the original author(s) and date. We acknowledge that this is already practiced in many, but by no means all journals. In addition, this citation must be included in the literature cited - a practice that is currently extremely rare (e.g., Persoonia; Phytotaxa; Blumea; Organisms, Diversity & Evolution [37], European Journal of Taxonomy) or not obligatory, but encouraged (e.g., Zootaxa).

2. All published taxonomic sources (monographs, identification keys, primary taxonomic literature and revisions) used for identification or as a source of nomenclatural information (e.g., catalogues) should be cited as any other methodological paper would be. The lack of these citations precludes an assessment of quality and reliability of the identification(s) and associated taxonomic information. Thus, independent verification of results and conclusions - the fundament of science - is not possible.

3. Researchers are encouraged to include taxonomists as co-authors when they have made substantial contributions to the research program or where the conclusions of the paper are solely dependent on the accurate identification of the study taxon.

One of the leading journals in ecology, Ecology Letters, follows the proposed guidelines, with the exception of well-established species such as Homo sapiens Linnaeus, 1758 [38], Drosophila melanogaster and Escherichia coli (Migula, 1895) [39]. A most recent suggestion [40] dealt with a solution for special citation of taxonomic work when used in wiki pages by combining both the original non-wiki source and the respective wiki page.

It might be argued that publications that are based on studies of multiple species, such as large phylogenetic analyses of an entire metazoan or plant group (e.g., a phylogenetic analysis of beetles) or monitoring projects, might lead to an inflation of certain citations or journals [30,37]. However, this is no different than the long lists of GenBank entries for sequences or alignments that have come to dominate our publications and associated supplementary materials. Also, arguments that it is difficult to deal with the older literature are becoming increasingly obsolete as the number of online taxonomic databases (e.g., BHL, EoL, Gallica, AnimalBase, and others) rapidly increases. Authors working on projects involving large species data sets would also be more likely to seek out taxonomists for assistance with subsequent co-authorship - already a common practice for bioinformatical or mathematical problems in phylogenetic or statistical analyses. This will increase communication and collaboration as well as the accuracy and usefulness of the vetted work.

It might also be argued that citing old literature is not necessary and that taxonomic hypotheses should be handled as in other disciplines: these hypotheses become "general knowledge" and no longer require citation, such as the seminal discoveries of natural selection published by Wallace in 1855 [41] and Darwin in 1859 [42], or of plate tectonics published by Wegener in 1912 [43]. However, as was shown with the example of Hirudo medicinalis, even "well-established" species can become imprecise, and refined hypotheses with new species names must be formulated. Especially in the time of molecular analyses, we can expect many more surprises with broad implications for various fields, including human welfare. The recent findings [44] of unknown subgroups within the Anopheles gambiae Giles, 1902 [45] complex [46] that exhibit a high susceptibility to infection with wild Plasmodium falciparum (Welch, 1897) [47] must be cited in future analyses to acknowledge one's awareness of sympatric species with different ecological and behavioral strategies within the same strains. The finding of cryptic species in spitting cobras [48], as well as the rearrangement of the large species complex of the Asian pitvipers into distinct genera [49] has a direct implication on categorization of their medical importance, as well as antivenin indication, prescription and research [50]. Results like these are not restricted to small and cryptic living species but also comprise large animals such as turtles, monitor lizards, antelopes or bovids [51-53] with direct implications on conservation biology and related fields [53,54]. Hence it is more important than ever to include all means used for identification, so that the authors' awareness of taxonomic problems that can potentially confound their study, including species concepts applied [10], is obvious to the readers of their published results.

In addition, we would encourage all taxonomists, who are in one way or another responsible for journal administration to ensure that their publications are indexed by ISISM. Based on the situation in molluscan literature (pers. comm. P. Mikkelsen), we assume that more than 90 percent of all taxonomic journals are not indexed so that the overwhelming numbers of taxonomic citations are simply not counted. The inclusion in the ISISM data base will increase the awareness of the journal and guarantee a more accurate calculation of journal and author citation metrics. We estimate that indexing half of all taxonomic journals available today would increase citation indices (CIs) fivefold.

Summary

Taxonomic work has profound implications for all kinds of scientific disciplines. Previous attempts of a few colleagues to encourage citation policies concerning taxonomic descriptions [30,36] have been largely ignored. Therefore, we once again emphatically appeal to colleagues and editors of journals for a much broader acknowledgement of the scientific work of taxonomists. The citation protocol as outlined above would give fair credit and recognition to those scientists who have dedicated their research careers to unveiling the earth's biodiversity and to the journals who have specialized in reporting these results. Currently, neither is recognized for their important contributions irrespective of their geographical location [1]. In addition, citation of species and taxon authorities will validate the taxonomic names used in scientific studies and will increase the robustness and usefulness of their results.

We are well aware of the severe shortcomings and weaknesses of CIs in systematics and taxonomy [16,26,55-57]. However, we cannot ignore the system and its impact; instead we should fully participate to ensure fair and accurate representation of our colleagues and journals. The citation protocol outlined above will require little additional investment by researchers and editors, but would be an important acknowledgement of the vital contributions of taxonomists and hopefully increase the survival rate of this endangered group of scientists.

Competing interests

The authors declare that they have no competing interests.

Authors' contributions

HW initiated and drafted the manuscript, all other authors contributed equally to the manuscript. All authors read and approved the final manuscript.

Author information

1Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany

2Institute for Ecology, Evolution and Diversity, Goethe-University, Siesmayerstrasse 70, 60054 Frankfurt am Main, Germany

3Department of Entomology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK

4Zoologische Staatssammlung München, Münchhausenstraße 21, 81247 München, Germany

5Department of Integrative Biology and Museum of Paleontology, University of California, Berkeley, CA 94720-4780, USA

Acknowledgements

We thank W. Sudhaus (Berlin) for identifying the correct first citation of Caenorhabditis elegans. We also want to thank the reviewers for their valuable comments and suggestions for relevant literature. Lily Wescott (Bonn) helped in polishing the language.

References

  1. Tancoigne E, Bole C, Sigogneau A, Dubois A: Insights from Zootaxa on potential trends in zoological taxonomic activity.

    Front Zoology 2011, 8:5. BioMed Central Full Text OpenURL

  2. Brock TD, Freeze H: Thermus aquaticus gen. n. and sp. n., a nonsporulating extreme thermophile.

    J Bact 1969, 98:289-297. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  3. Saiki RK, Gelfand DH, Stoffel S, Scharf ST, Higuchi R, Horn GT, Mullis KB, Erlich HA: Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase.

    Science 1988, 239:487-491. PubMed Abstract | Publisher Full Text OpenURL

  4. Linnaeus C: Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Editio decima. Holmiæ (= Stockholm): Laurentius Salvius; 1758. OpenURL

  5. Siddall ME, Trontelj P, Utevsky SY, Nkamany M, McDonald KS: Diverse molecular data demonstrate that commercially available medicinal leeches are not Hirudo medicinalis.

    Proc Roy Soc Lond B 2007, 274:1481-1487. Publisher Full Text OpenURL

  6. Phillips AJ, Siddall ME: Poly-paraphyly of Hirudinidae: many lineages of medicinal leeches.

    BMC Evol Biol 2009, 9:246. PubMed Abstract | BioMed Central Full Text | PubMed Central Full Text OpenURL

  7. Pfenninger M, Schwenk K: Cryptic animal species are homogeneously distributed among taxa and biogeographical regions.

    BMC Evol Biol 2007, 7:121. PubMed Abstract | BioMed Central Full Text | PubMed Central Full Text OpenURL

  8. De Broyer C, Danis B: How many species in the Southern Ocean? Towards a dynamic inventory of the Antarctic marine species.

    Deep-Sea Research II 2011, 58:5-17. Publisher Full Text OpenURL

  9. Bebber DP, Carine MA, Wood JRI, Wortley AH, Harris DJ, Prance GT, Davidse G, Paige J, Pennington TD, Robson NKB, Scotland RW: Herbaria are a major frontier for species discovery.

    Proc Natl Acad Sci 2010, 107:22169-22171. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  10. Mora C, Tittensor DP, Adl S, Simpson AGB, Worm B: How many species are there on Earth and in the Ocean.

    PLoS Biology 2011, 9:e1001127. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  11. Pearson DL, Hamilton AL, Erwin TL: Recovery plan for the endangered taxonomy profession.

    BioScience 2011, 61:58-63. Publisher Full Text OpenURL

  12. Global Taxonomy Initiative website (GTI): How many taxonomists are there? [http://www.gti-kontaktstelle.de/english/taxonomy_E.html#brazilNo] webcite

    (last access 10th of May 2011)

  13. De Carvalho MR, Bockmann FA, Amorim DS, de Vivo M, de Toldeo-Piza M, Menezes NA, de Figueiredo JL, Castro RMC, Gill AC, McEachran JD, Compagno LJV, Schelly RC, Britz R, Lundberg JG, Vari RP, Nelson G: Revisiting the taxonomic impediment.

    Science 2005, 307:353. PubMed Abstract OpenURL

  14. De Carvalho MR, Bockmann FA, Amorim DS, Brandão CRF, de Vivo M, de Figueiredo JL, Britski HA, de Pinna MCC, Menezes NA, Marques FPL, Papavero N, Cancello EM, Crisci JV, McEachran JD, Schelly RC, Lundberg JG, Gill AC, Britz R, Wheeler QD, Stiassny MLJ, Parenti LR, Page LM, Wheeler WC, Faivovich J, Vari RP, Grande L, Humphries CJ, DeSalle R, Ebach MC, Nelson G: Taxonomic impediment or impediment to taxonomy? A commentary on systematics and the cybertaxonomic-automation paradigm.

    BMC Evol Biol 2007, 34:140-143. OpenURL

  15. Patterson DJ: Future Taxonomy. In Systema Naturae 250 - the Linnean Ark. Edited by Polaszek A. Boca Raton: CRC Press; 2010:115-124. OpenURL

  16. Ebach MC, Valdecasas AG, Wheeler QD: Impediments to taxonomy and users of taxonomy: accessibility and impact evaluation.

    Cladistics 2011, 27:1-8. Publisher Full Text OpenURL

  17. Moreno CE, Halffter G: Assessing the completeness of bat biodiversity inventories using species accumulation curves.

    J Appl Ecol 2000, 37:149-158. Publisher Full Text OpenURL

  18. Bortolus A: Error cascades in the biological sciences: the unwanted consequences of using bad taxonomy in ecology.

    AMBIO 2008, 37:114-118. PubMed Abstract | Publisher Full Text OpenURL

  19. May RM: How many species are there on earth?

    Science 1998, 241:1441-1449. OpenURL

  20. Chapman AD: Numbers of Living Species in Australia and the World. 2nd edition. Canberra, Australia: Australian Government; 2009. OpenURL

  21. Costello MJ, Wilson S, Houlding B: Predicting total global species richness using rates of species description and estimates of taxonomic effort.

    Syst Biol 2011.

    [Epub ahead of print]

    OpenURL

  22. Heywood VH: The Global Biodiversity Assessment. United Nations Environment Programme. Cambridge: Cambridge University Press; 1995. OpenURL

  23. Groombridge B: Global Biodiversity: Status of the Earth's Living Resources. A Report compiles by the World Conservation Monitoring Centre. London, Glasgow, New York, Tokyo, Melbourne, Madras: Chapman & Hall; 1992. PubMed Abstract | Publisher Full Text OpenURL

  24. McCook LJ, Ayling T, Cappo M, Choate JH, Evans RD, De Freitas DM, Heupel M, Hughes TP, Jones GP, Mapstone B, Marsh H, Mills M, Molloy FJ, Pitcher CR, Pressey RL, Russ GR, Sutton S, Sweatman H, Tobin R, Wachenfeld DR, Williamson DH: Adaptive management of the Great Barrier Reef: A globally significant demonstration of the benefits of networks of marine reserves.

    Proc Natl Acad Sci 2010, 107:18278-18285. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  25. Boero F: The study of species in the era of biodiversity: a tale of stupidity.

    Diversity 2010, 2:115-126. Publisher Full Text OpenURL

  26. Werner YL: The aspiration to be good is bad: The "Impact Factor" hurts both science and society.

    Int J Sci Soc 2009, 1:99-105. OpenURL

  27. Dayrat B: Toward integrative taxonomy.

    Biol J Linn Soc 2005, 85:407-415. Publisher Full Text OpenURL

  28. Padial JM, Miralles A, Riva IDl, Vences M: The integrative future of taxonomy.

    Front Zool 2010, 7:16. PubMed Abstract | BioMed Central Full Text | PubMed Central Full Text OpenURL

  29. Haszprunar G: Species delimitations - not "only descriptive".

    Org Divers Evol 2011, 11:249-252. Publisher Full Text OpenURL

  30. Werner YL: The case of impact factor versus taxonomy: a proposal.

    J Nat Hist 2006, 40:1285-1286. Publisher Full Text OpenURL

  31. Velde van der G: Taxonomists make a name for themselves.

    Nature 2001, 414:148. PubMed Abstract | Publisher Full Text OpenURL

  32. Meigen JW: Systematische Beschreibung der bekannten europäischen zweiflügeligen Insekten, sechster Theil mit 12 Kupfertafeln. Hamm: Schulz; 1830. OpenURL

  33. Linnaeus C: Species plantarum: exhibentes plantas rite cognitas, ad genera relatas, cum differentiis specificis, nominibus trivialibus, synonymis selectis, locis natalibus, secundum systema sexuale digestas. Editio Secunda, Tomus II. Laurentius Salvius: Holmiæ (= Stockholm); 1763. OpenURL

  34. Carena H: Monographie du genre Hirudo ou description des espèces de sangesues qui se trouvent ou qui sont en usage en piémont, avec des observations sur la génération, et sur d'autres points de l'histoire naturelle de quelques unes de ces espèces.

    Mem R Accad Torino 1820, 25:273-316. OpenURL

  35. Mayo SJ, Allkin R, Baker W, Blagoderov V, Brake I, Clark B, Govaerts R, Godfray C, Haigh A, Hand R, Harman K, Jackson M, Kilian N, Kirkup DW, Kitching I, Knapp S, Lewis GP, Malcolm P, von Raab-Straube E, Roberts DM, Scoble M, Simpson DA, Smith C, Smith V, Villalba S, Walley L, Wilkin P: Alpha e-taxonomy: responses from the systematics community to the biodiversity crisis.

    Kew Bull 2008, 63:1-16. Publisher Full Text OpenURL

  36. Seifert KA, Crous PW, Frisvad JC: Correcting the impact factors of taxonomic journals by appropriate citation of taxonomy (ACT).

    Persoonia 2008, 20:105. OpenURL

  37. Bininda-Emonds ORP: Supporting species in ODE: explaining and citing.

    Org Divers Evol 2011, 11:1-2. Publisher Full Text OpenURL

  38. Linnaeus C: Systema naturæ per regna tria naturæ, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Edicio decima. Laurentius Salvius: Holmiæ (= Stockholm); 1758. OpenURL

  39. Migula W: Bacteriaceae (Stäbchenbakterien). In Die Natürlichen Pflanzenfamilien. Edited by Teil I, Abteilung Ia Engler A, Prantl K. Leipzig: W. Engelmann; 1895:20-30. PubMed Abstract | Publisher Full Text OpenURL

  40. Penev L, Hagedorn G, Mietchen D, Georgiev T, Stoev P, Sautter G, Agosti D, Plank A, Balke M, Hendrich L, Erwin T: Interlinking journal and wiki publications through joint citation: Working examples from ZooKeys and Plazi on Species-ID.

    Zookeys 2011, 90:1-12. PubMed Abstract | PubMed Central Full Text OpenURL

  41. Wallace AR: On the law which has regulated the introduction of new species.

    Ann Mag Nat Hist 1855, 16:184-196. Publisher Full Text OpenURL

  42. Darwin C: On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. London: John Murray; 1859. OpenURL

  43. Wegener A: Die Entstehung der Kontinente.

    Peterm Mitt 1912, 81:185-195.

    253-256, 305-309

    OpenURL

  44. Rhiele MM, Guelbeogo WM, Gneme A, Eiglmeier K, Holm I, Bischoff E, Garnier T, Snyder GM, Li X, Markianos K, Sagnon N, Vernick KD: A cryptic subgroup of Anopheles gambiae is highly susceptible to human malaria parasites.

    Science 2011, 331:596-598. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  45. Giles GM: A handbook of the gnats or mosquitoes giving the anatomy and life history of the Culicidae, together with descriptions of all species notices up to the present date. 2nd edition. rewritten and enlarged. London; 1902. OpenURL

  46. White GB, Rosen P: Comparative studies on sibling species of the Anopheles gambiae Giles complex (Dipt., Culicidae). II. Ecology of species A and B in savanna around Kaduna, Nigeria, during transition from wet to dry season.

    Bull Entomol Res 1973, 62:613-625. Publisher Full Text OpenURL

  47. Welch WH: Malaria: definition, synonyms, history, and parasitology. In System of Practical Medicine. Volume 1. Edited by Loomis AL and Thompson WG. New York and Philadelphia: Lea Brothers & Co; 1897::17-76. OpenURL

  48. Wüster W, Thorpe RS: Naja siamensis, a cryptic species of venomous snake revealed by mtDNA sequencing.

    Experientia 1994, 50:75-79. PubMed Abstract | Publisher Full Text OpenURL

  49. Malhotra A, Thorpe RS: A phylogeny of four mitochondrial gene regions suggests a revised taxonomy for Asian pitvipers (Trimeresurus and Ovophis).

    Mol Phyl Evol 2004, 32:83-100. Publisher Full Text OpenURL

  50. WHO Guidelines for the production control and regulation of snake antivenom immunoglobulins. World Health Organization. Geneva: WHO Press; 2010. OpenURL

  51. Stuckas H, Fritz U: Identity of Pelodiscus sinensis revealed by DNA sequences of an approximately 180-year-old type specimen and a taxonomic reappraisal of Pelodiscus species (Testudines: Trionychidae).

    J Zool Syst Evol Res 2011, 49:177-255. Publisher Full Text OpenURL

  52. Koch A, Arida E, Schmitz A, Böhme W, Ziegler T: Refining the polytypic species concept of mangrove monitors (Squamata Varanus indicus group): a new cryptic species from the Talaud Islands, Indonesia, reveals the underestimated diversity of Indo-Australian monitor lizards.

    Austr J Zool 2009, 57:29-40. Publisher Full Text OpenURL

  53. Ceballos G, Ehrlich PR: Discoveries of new mammal species and their implications for conservation and ecosystem services.

    Proc Natl Acad Sci 2009, 106:3841-3846. PubMed Abstract | Publisher Full Text | PubMed Central Full Text OpenURL

  54. Bickford D, Lohmann DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I: Cryptic species as a window on diversity and conservation.

    Trends Ecol Evol 2007, 22:148-155. PubMed Abstract | Publisher Full Text OpenURL

  55. Krell F-T: Why impact factors don't work for taxonomy.

    Nature 2002, 415:957. PubMed Abstract | Publisher Full Text OpenURL

  56. Valdecasas AG, Castroviejo S, Marcus LF: Reliance on the citation index undermines the study of biodiversity.

    Nature 2000, 403:698. PubMed Abstract | Publisher Full Text OpenURL

  57. Lawrence PA: The mismeasurement of science.

    Curr Biol 2007, 17:R583-585. PubMed Abstract | Publisher Full Text OpenURL

  58. Maupas E: La mue et l'enkystement chez les nématodes.

    Arch Zool exp gén, (3e. Série) 1899, 7:563-628. OpenURL

  59. Schulze FE: Trichoplax adhaerens nov. gen., nov. spec.

    Zool Anz 1883, 6:92-97. OpenURL

  60. Hieronymus G: Selaginellaceae. In Die Natürlichen Pflanzenfamilien nebst ihren Gattungen und wichtigeren Arten, insbesondere den Nutzpflanzen, unter Mitwirkung zahlreicher hervorragender Fachgelehrten. Teil 1, Abteilung 4a. Edited by Engler A, Prantl K. Leipzig: W. Engelmann; 1902:621-716. PubMed Abstract | Publisher Full Text OpenURL

  61. Hooper JNA, van Soest RWM: A new species of Amphimedon (Porifera, Demospongiae, Haplosclerida, Niphatidae) from the Capricorn-Bunker Group of Islands, Great Barrier Reef, Australia: target species for the 'sponge genome project'.

    Zootaxa 2006, 1314:31-39. OpenURL

  62. Ladurner P, Schärer L, Salvenmoser W, Rieger R: A new model organism among the lower Bilateria and the use of digital microscopy in taxonomy of meiobenthic Platyhelminthes Macrostomum lignano, n. sp. (Rhabditophora, Macrostomorpha).

    J Zool Syst Evol Res 2005, 43:114-126. Publisher Full Text OpenURL

  63. Longcore JE, Pessier AP, Nichols DK: Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibiens.

    Mycologia 1999, 91:219-227. Publisher Full Text OpenURL

  64. Bechstein JM: Herrn de Lacépède's Naturgeschichte der Amphibien oder der eyerlegenden vierfüssigen Thiere und der Schlangen. Eine Fortsetzung von Buffon's Naturgeschichte aus dem Französischen übersetzt und mit Anmerkungen und Zusätzen versehen. Weimar: Industrie Comptoir; 1802. OpenURL

  65. Thomas R: New species of Antillean Eleutherodactylus.

    Q J Flor Acad Sci 1966, 28:375-391. OpenURL

  66. Deschka G, Dimic N: Cameraria ohridella n. sp. aus Mazedonien, Jugoslawien (Lepidoptera, Lithocolletidae).

    Acta Ent Jug 1986, 22:11-23. OpenURL

  67. Osborn HF: Tyrannosaurus and other Cretaceous carnivorous dinosaurs.

    Bull Am Mus Nat Hist 1905, 21:259-265. OpenURL

  68. Hu HH, Cheng WC: On the new family Metasequoiaceae and on Metasequoia glyptostroboides, a living species of the genus Metasequoia found in Szechuan and Hupeh.

    Bull Fan Mem Inst Biol, new series 1948, 1:153-161. OpenURL

  69. Smith JLB: A living coelacanthid fish from South Africa.

    Nature 1939, 143:748-750. Publisher Full Text OpenURL

  70. Brown P, Sutikna T, Morwood MJ, Soejono RP, Wayhu Saptomo E, Rokus AD: A new small-bodied hominin from the Late Pleistocene of Flores, Indonesia.

    Nature 2004, 431:1055-1061. PubMed Abstract | Publisher Full Text OpenURL

  71. Ouwens PA: On a large Varanus species from the Island of Komodo.

    Bull Jard Bot Buitenzorg 1912, 6:1-3. OpenURL

  72. Reid AL: Review of the Peripatopsidae (Onychophora) in Australia, with comments on peripatopsid relationships.

    Invertebr Taxonomy 1996, 10:663-936. Publisher Full Text OpenURL

  73. Yager J: Cryptocorynetes haptodiscus, a new genus, new species, and Speleonectes benjamini, new species, or remipede crustaceans from achialine caves in the Bahamas, with remarks on distribution and ecology.

    Proc Biol Soc Wash 1987, 100:302-320. OpenURL

  74. Pouyaud L, Wirjoatmodjo S, Rachmatika I, Tjakrawidjaja A, Hadiaty R, Hadie W: Une nouvelle espèce de coelacanthe: preuves génétiques et morphologiques.

    C R Acad Sci III-Vie 1999, 322:261-267. Publisher Full Text OpenURL