Species hypotheses are the basic currency of comparative biology, yet a major portion of global biodiversity remains unnamed and thus in the dark [1]. Remedies for overcoming the taxonomic impediment include the increased development of human resources and new technological approaches [2, 3]. Tools from a taxonomists’ wish list ranging from powerful imaging technologies and DNA sequencing to fast and open internet access are now widely available. Nevertheless, significant progress in terms of formal species descriptions has not been achieved to date. Instead, a decline in taxonomic productivity per author has occurred since World War II [4, 5]. The reasons for this decline are complex, but often the desire to include as many characters as possible in the original description of a new species increases their average length and decreases their number. Nevertheless, issues of quality control could not be addressed sufficiently in traditional taxonomy because morphological descriptions are difficult to standardize. This leads to the problem of synonymy which requires continued efforts to be fixed [6]. Furthermore, lack of standards also means that extremely uninformative descriptions are still being published, which further complicates matters - and does not help to improve the image of the whole discipline.
The practice of taxonomic description
We suggest that the advent of phylogenetic systematics [7] and phenetics [8] had a profound but little-noticed effect on the preparation standards of species descriptions. Since more and more taxonomic revisions incorporated phylogenetic analyses or were at least prepared in parallel with the latter, it was attempted to maximize the number of informative characters. Thus, even characters of little value for species diagnosis were included in the descriptions. Another consequence was that species descriptions within a study were sought to be standardized, best illustrated by the program Delta [9]. Negative character states (i.e. the absence of a character) were often explicitly stated. Thus, the average length of species descriptions increased and their number per author decreased in the past 50 years [4, 5]. Often enough, all this time-consuming procedure did not enhance the usability of descriptions for the purpose of diagnosis, but rather inflated them. After all, standardization among different authors was never achieved not to mention the failure to introduce an urgently needed minimum standard.
Taxonomic impediment or impediment to taxonomy?
The “taxonomic impediment” is known as the situation in which biological studies suffer from shortcomings of the taxonomic basis, i.e. the difficulty in safely identifying many species [10]. We propose that the vast number of undescribed species on Earth [11] may not be the biggest problem in this context. A name and a safe diagnosis for a new species can be provided rapidly and with limited resources. The bigger problem is usually the legacy of earlier taxonomic work, i.e. the interpretation of existing names. Many descriptions are inadequate and to clarify matters, the type specimens have to be examined. The revision of a minor taxonomic group may require extensive travel to museums around the world, without a guarantee that the critical characters are actually found on the types. For example, if a diagnosis based on male characters is state of the art, there is little help if some of the species were described based on unique female specimens. One of the oldest principles of nomenclature, i.e. the Principle of Priority apparently promotes “taxonomic mihilism” (from Latin mihi – belonging to me) [12]: the taxon’s earliest description ensures the name’s use, no matter how low the diagnostic value of the associated description is. Authors with a strong mihi-itch have described new taxa based on inadequate material or data, just to secure authorship of the species; the ensuing problems for identification are left to be sorted out by the community. In orphaned taxa without a sufficient number of experts, taxonomic data of heterogeneous quality become a heavy burden rather than a tool for identification. We suggest that these self-inflicted and system-inherent problems are the main reason for the taxonomic impediment, possibly closely followed by a lack of determination of many biodiversity research projects to include a sufficient budget for taxonomic work.
It appears as a sad irony that a part of the taxonomic community [13, 14] turns a blind eye on these problems while blaming any constructive criticism from end-users [2, 15] as the true impediment to taxonomy. Below we propose that turbo-taxonomy can effectively combine the strengths of both traditional, morphology-based taxonomy and DNA based approaches. We emphasize that a good quality of work always depends on the standards of the persons involved and that the use of DNA sequences is no insurance against over-splitting or other mistakes. But, the combination of morphology and DNA taxonomy will allow to assess and solve such problems more easily than before.
The approach
Examples of turbo-taxonomy
The term “turbo-taxonomy” was coined for an approach combining DNA barcoding with short taxonomic descriptions of morphological characters for hyperdiverse parasitic wasps [16]. We extend this approach by abstaining from laborious, but not necessarily helpful identification keys, and rather adding automated journal-wiki upload (pushing) of data, to reveal and formally describe 101 species of hyperdiverse Trigonopterus weevils. Thus, we combine traditional expert taxonomy with DNA sequencing, subrobotic digital imaging (where a machine takes images of different specimen layers and stacks them automatically) and automated content pushing from a journal into a wiki to show explicitly how to sustainably provide species with the attributes that makes them most visible: names anchored in a framework more rapidly produced than currently the case [17]. Concatenated, versioned species pages using the wiki engine offer a continuous opportunity for subsequent enhancement and community participation (Figure 1).
We established the genus Trigonopterus as our first target for comparative biodiversity studies because it is highly diverse within a region of great biological interest, both genetically and in terms of species. We collected >6,000 specimens of Trigonopterus from across New Guinea and sequenced 1,000 of them, assigned to 279 entities of putative species status [18, 19]. We showed that mitochondrial and nuclear DNA entities were indeed fully congruent or compatible with morphologically delineated groups and argue that such widespread congruence within a taxon is the most important prerequisite for an accelerated framework (Figure 1). The judgment of species status was mainly based on examination of male genital characters. Morphologically delineated species with high cox1 divergence were examined a second time, and nuclear DNA markers sequenced to discover potentially diagnostic nDNA characteristics that suggest the existence of “cryptic” species or reveal overlooked species. The final hypotheses incorporate evidence from both morphology and molecules. After a preliminary screening of known Trigonopterus types, we here avoided the risk of creating synonyms by excluding the few species that could potentially bear a valid name. Species represented only by females were preliminarily excluded, as additional field work may later discover males which we prefer as holotypes. All 279 species are clearly delineated as can be seen in the maximum likelihood tree based on cox1 sequences of 1,002 specimens of Trigonopterus [link to http://www.plosone.org/article/fetchSingleRepresentation.action?uri=info doi/10.1371/journal.pone.0028832.s001] [19]. We formalize our findings by describing the first 101 species new to science [20], introducing a condensed format fully embracing technological advances and in accordance with the International Code of Zoological Nomenclature [21, 22]. As an example, we include this description from the ZooKeys paper.
Trigonopterus phoenix Riedel
Holotype, male (Figure 2A, http://species-id.net/wiki/Trigonopterus_phoenix. Length 2.63 mm. Beetle black; antennae, tarsi and elytra ferruginous. Body subovate; with weak constriction between pronotum and elytron; in profile evenly convex. Rostrum in basal half with distinct median ridge and pair of submedian ridges, furrows with sparse rows of yellowish scales; apically weakly punctate, sparsely setose. Pronotum coarsely punctate-reticulate. Elytra with distinct striae of small punctures; intervals with row of minute punctures; laterally behind humeri with ridge bordered by 4 deep punctures of stria 9. Femora edentate. Mesofemur and metafemur dorsally squamose with silvery scales. Metafemur with weakly denticulate dorsoposterior edge; subapically with stridulatory patch. Metatibia apically with uncus and minute premucro. Abdominal ventrite 5 coarsely punctate, in apical half with round depression fringed with dense erect scales. Aedeagus (Figure 2B) apically weakly pointed, sparsely setose; transfer-apparatus spiniform; ductus ejaculatorius with bulbus. Intraspecific variation. Length 2.53–2.63 mm. Female rostrum in apical half slender, dorsally subglabrous, with sublateral furrows. Female abdominal ventrite 5 densely punctate, with suberect scales, with median ridge.
Material examined. Holotype (SMNK): ARC1153 (EMBL # HE615781), PAPUA NEW GUINEA, Simbu Prov., Karimui Dist., Haia, Supa, S06° 39.815' E145° 03.169' to S06° 39.609' E145° 03.012', 1240–1450 m, 30-IX-2009. Paratype (NAIC): PAPUA NEW GUINEA, Simbu Prov., ARC1132 (EMBL # HE615761), S06° 40.078' E145° 03.207' to S06° 39.609' E145° 03.012', 1220–1450 m, 02-X-2009.
Notes. This species was coded as “Trigonopterus sp. 207” by Tänzler et al. (2012).
Etymology: From the ancient Greek Φοίνιξ, “the reborn”.
This species and 100 additional ones (Figure 3) were described simultaneously in the open-access journal ZooKeys [20]. Holotypes were designated exclusively from sequenced specimens. Photographs of habitus and genitalia were prepared after DNA extraction from holotypes. Thus, potential confusion by type series of mixed species is excluded by providing all relevant data from the holotype.