What do taxonomists look for in plant populations

The decline in taxonomic expertise substantially compromises rigorous studies in all fields of biodiversity or biogeography, including invasion biology Smith et al. Most regions of the world have been colonized by species from many other parts of the globe, and identifying many of these non-native species is a major challenge. Expertise in taxonomy i. Additionally, resources are required for broad-based public participation in invasive species management and for providing information to horticulturalists, foresters and others who utilize, and often financially benefit from, alien species.

We suggest that a decade after the completion of the first phase of GISP, this prediction has proved correct and the problem has reached critical proportions. More capacity in the taxonomy of plants and animals, both native and alien, is urgently needed Smith et al.

Furthermore, rapid identification of alien specimens can drastically reduce the time taken to respond to new or potential invasions. A fundamental role of taxonomists in both taxonomic and non-taxonomic studies is to provide the correct scientific names by using the best available knowledge of the organisms submitted for identification.

This service is provided to a range of clients—biologists, environmental managers, agronomists and environmental impact assessors—who require a robust framework of names in order to conduct their work accurately Patterson et al. Despite the rapid advances in molecular techniques, classical alpha taxonomy is still useful and necessary in the 21st century.

Additionally, many regions globally are unlikely to have easy access to such genetic data. In ecology, taxonomy is one of the fundamental units of currency Gotelli The reliable identification of taxa native or alien paves the way for the study of organisms, potentially sheds light on many aspects of their biology, allows reference to the same taxa from other localities, and makes comparisons with congeners and other taxa possible.

Incorrect identification of plant invaders as a result of inaccurate taxonomic services could lead to a misunderstanding of the dynamics of biological invasions. Moreover, alien species management is an international and multi-sectoral endeavour that requires accurate scientific names for global information sharing Smith et al.

This paper explores the ongoing and critical role of taxonomy in the study of plant invasions and specifically examines how the lack of taxonomic expertise can impede progress in understanding and managing invasions. The converse is equally true: we argue that taxonomy can also benefit from insights from biological invasions, a perspective that has not been sufficiently explored and emphasized in the literature.

Finally, we suggest that classical taxonomy and modern genetic approaches must work in tandem, not only to improve the accuracy of species identification but also to potentially refine classifications at the levels of organism, population and genotype in the field and laboratory.

Is the current scope of taxonomy and nomenclature facing a crisis? Is the field of taxonomy suffering from a shortage of expertise and declining resources disproportionate relative to other disciplines in biology Agnarsson and Kuntner ? Or, are there now more taxonomists describing more species than ever before, as inferred from new databases showing that the number of taxonomists is increasing faster than the rate of species descriptions Costello et al.

Joppa et al. However, there is a great difference between describing one new species and producing a taxonomic revision for a group of species, the former being a task often undertaken by amateurs whereas the latter demands greater perspective and most usually formal training and long-term employment.

Aside from these issues, it is clear that the field of taxonomy suffers from some systemic problems. Taxonomy is undervalued in current scientometric analyses Krell , ; Valdecasas et al. A primary reason why alpha taxonomy is undervalued in top-ranking journals is that such work is rarely hypothesis driven, is often of more local than global significance, applies standard rather than innovative approaches and has limited immediate impact on policy or management.

Specialist taxonomic journals have relatively low impact factors, due to citation practices that include the convention of not citing original taxonomic descriptions or subsequent taxonomic revisions, the long citation half-life of taxonomic papers, regionality as a typical feature of taxonomic work, and because much important work in taxonomy is published in voluminous and immensely informative monographs rather than as succinct papers in journals.

Furthermore, many authors cite papers that test the validity of taxonomic hypotheses with molecular data or papers that promote or use DNA barcodes, rather than papers based on classical taxonomy Agnarsson and Kuntner The low number of specialists for particular groups of organisms further decreases the chances of taxonomic papers becoming highly cited Krell In the sphere of education, experienced researchers formulate research topics for students and stimulate interest in taxonomy and other fields among future generations.

Data gathered on theses completed from the s to the present from the Department of Botany at Charles University in Prague, Czech Republic, a region where taxonomy has been traditionally very strong, allow us to examine how these trends translate into the interests of students and how research agendas shift over time Fig.

Of particular concern is that the full impact of these trends is delayed as researchers work their way through the academic system. Fewer and fewer senior academics trained in classical taxonomy means fewer voices when it comes to setting institutional research agendas or departmental university priorities. This has the potential to create a negative feedback loop and general downward spiral in the advocacy required to maintain and promote taxonomy as highly relevant.

Taxonomic expertise is rarely required when it comes to securing a job, especially in academia. Agnarsson and Kuntner estimated that as much as half the funding for taxonomic training may be lost due to lack of employer demand. Because the low profile of taxonomy results in serious underfunding in many parts of the world, employment opportunities are reduced for natural scientists, thereby further reducing the profile of taxonomy.

Based on a total sample of theses completed in the examined period, with numbers for decades shown above bars. As in other fields of biology, taxonomic expertise in plant invasion biology is currently underfunded. For example, Europe suffers from a scarcity of experts particularly for insect and plant invasions Hulme et al. This dearth of experts contrasts sharply with the recognition that taxonomists are increasingly needed to address the threats of biological invasions and that training opportunities and employment prospects for these skills are crucial at all career levels Wheeler et al.

Below we discuss problems related to the identification of newly arriving alien species, including the use of molecular tools, and examine how potential biases resulting from misidentification of alien species could impede the progress in ecological research on plant invasions.

The accurate identification of an organism under study is pivotal to all ecological research. Invasion ecologists usually do not have a specific biogeographic focus and require taxonomic information from much larger areas essentially the whole world for many taxa. Taxonomists specializing on a specific area rely on regional literature such as Floras note the capital letter to denote published work and identification keys that they can become well acquainted with during their careers.

Such taxonomists are frequently able to flag taxa as alien i. However, regional taxonomists may prove of little help if their expertise is geographical rather than linked to a particular taxonomic group. An increasing number of online taxonomic databases, such as the Annual Checklist of World Plants www. Current knowledge on biological invasions is geographically and taxonomically biased toward more developed regions, further complicating accurate species identification.

Since research intensity is generally related to economic prosperity Leimu and Koricheva , the same regions are also likely to be taxonomically understudied Stuessy and Lack , which is ironic since they are home to most of the world's biodiversity. Historical information on alien species composition and distribution comes from floristic literature, herbaria and museum collections, seed suppliers and garden catalogues.

Taxonomists are therefore well placed to track the introduction history of alien taxa via the preserved collections that they curate Fuentes et al. Scientific curation by taxonomists in herbaria requires constant and ongoing updating, especially for nomenclature and incorporating taxonomic changes. These collections are indispensable resources to facilitate locating alien species in the exact areas where they were initially collected and the habitats in which they were first described Aikio et al.

As in the case of requiring accurate species identification, expanding preserved collections typically herbaria and natural history museums of alien taxa is important as they provide both temporal-historical and accurate geographical information on such provenances for morphological and genetic data. These data also provide important historical information in cases where the alien population from which a specimen was gathered is subsequently cleared. Identifying the origin of a species, i.

This can be complicated by species being native and alien in different parts of the same country e. Problems also arise from different taxonomic approaches in the native and invaded ranges. For example, the genus Oenothera has a specific reproduction system permanent translocation heterozygosity resulting in rapid formation of new species, which makes it difficult to align taxa invasive in Europe to their native North American counterparts, partly because some of them originated in the invaded range Cleland ; Dietrich et al.

The last decade has seen substantial effort towards consolidating a fragmented taxonomic knowledge base through the use of web-based tools Godfray ; Godfray et al. The plea for web-based unitary taxonomy reflects the threat imposed on classical taxonomy by increasingly classifying biodiversity using available genetic sequence data. This trend therefore suggests that current taxonomy must embrace and absorb new trends rather than set itself in opposition to them Godfray et al. Such is the current prominence of molecular systematics that some journals e.

Phytotaxa strongly discourage authors from attempting to publish papers that recognize classically determined families not accepted as valid by the Angiosperm Phylogeny Group ; the presentation of alternative family concepts otherwise requires a written justification see e.

Taxon identification using standardized DNA gene regions or barcodes, i. A DNA barcode can overcome several limitations of morphology-based taxonomy, including detection of morphologically cryptic species, recognition of species with high phenotypic plasticity, and individuals in early ontogenetic stages or incomplete and poorly developed specimens Valentini et al. Molecular taxonomy can be particularly useful in groups that have received inadequate taxonomic attention e.

The names of organisms are linked to type specimens and the interpretation of these along with the correct nomenclature cannot be replaced by any molecular means. DNA barcoding has recently been successfully applied in plant invasion biology. For example, this methodology has efficiently distinguished invasive aquatic species belonging to the genera Cabomba , Ludwigia , Myriophyllum and to the family Hydrocharitaceae from their non-invasive related counterparts Ghahramanzadeh et al.

Similarly, DNA barcodes proved successful in the identification of invasive Solanum species, with practical implications for plant biomonitoring Zhang et al. Despite these encouraging results, barcoding of terrestrial plants faces several challenges and limitations Chase and Fay , particularly for closely related species in which restricted variation in barcoding markers limits reliable identification; some plant genera have even been found to be refractory to barcoding Piredda et al.

Another limitation of widely used plastid barcodes for taxonomic decision-making stems from their uniparental inheritance maternal in most angiosperms, paternal in the majority of gymnosperms resulting in interspecific crosses remaining unrecognized and identified as their plastid donor parent. This can introduce serious bias in invasion studies because hybrids can show greater invasion potential than their parental species Ellstrand and Schierenbeck , Table 1 ; see also Smith and Figueiredo on a hybrid of Agave species in Portugal.

Biparentally inherited nuclear barcodes might solve the problem and provide more information than organellar DNA. However, their value can be compromised by methodological issues and the presence of multiple divergent copies within a single individual. The risk of misidentification due to paralogy-related problems is particularly high in polyploids and polyploidization is common among invasive plants te Beest et al.

The complex evolutionary history of polyploid species Soltis and Soltis can easily lead to incongruence between morphological and molecular identification that can only be reliably resolved by an experienced taxonomist with a deep understanding of processes shaping the variation of the group under investigation.

Examples of taxonomically challenging genera where ecological studies profited from a detailed taxonomic study. Much of the theory and current knowledge in plant invasion biology has arisen from analyses of secondary data, drawn from regional Floras, floristic literature and distribution atlases. Such analyses have made it possible to explore distribution patterns and invasion dynamics at various scales e.

However, such databases and checklists can be seriously biased in terms of species present in a region and their distribution. Among the many types of errors that can plague occurrence databases, misidentification of species is arguably the most serious Scott and Hallam ; Robertson et al.

Groups for which the taxonomy is contentious or for those whose members are difficult to distinguish from one another are likely to be prone to the greatest bias Ensing et al. An additional problem of invasive species lists is inconsistent terminology Hulme and Weser ; McGeoch et al.

Richardson et al. This strong bias holds even if one accepts that this is a comparison of a specialized regional checklist with a source compiled for a continent several decades ago with no clear focus on alien species.

The discrepancy in the number of naturalized species present in the country for decades is substantial. Such biases seem to be due to insufficient research intensity coupled with a lack of taxonomic expertise. In the dynamic field of plant invasion ecology, focused taxonomic effort results in considerable improvement and almost invariably expansion of knowledge on organisms.

For example, for the Czech Republic, a revision of a national checklist performed a decade after the original study yielded taxa added to the list of alien plant species. These additions were due to detection of newly introduced species, new information due to investigation of sources omitted from the previous catalogue including additional herbarium material , redetermination of previously reported taxa, reassessment of some taxa traditionally considered native and inclusion of intraspecific taxa previously not recognized in the flora.

In addition, names were changed for nomenclatural reasons or changes in taxonomic opinion Danihelka et al. Similarly, 30 taxa were also omitted from the checklist of Belgian alien plants following a thorough taxonomic revision Verloove and Lambinon Such challenges are not restricted to checklists of alien species and the magnitude of the bias usually only becomes obvious when modern monographs are published.

Nevertheless, much has recently been done in Europe to improve the situation with alien species checklists. The research conducted during the building of the DAISIE database illustrates the magnitude of taxonomic work behind any alien species database. With the DAISIE plant data, a merging of checklists of alien floras from the 48 regions considered, yielded 14 different names that had to be manually assigned to alien plant taxa reported for Europe in Lambdon et al.

Although the expertise needed to check and correct synonyms is not directly related to ability to identify species in the field, the above example shows that a huge taxonomic capacity is needed to build these databases and checklists, update and maintain them over time, and incorporate new data. An additional concern is the historical under-representation of alien taxa in some herbaria. Without physical specimens, it is impossible to verify the identity of invaders and update these data in the light of taxonomic changes or to collect DNA samples from archived material.

In the case of South Africa, taxonomists have been appointed and provided with resources to facilitate this process specifically to detect new invaders before they become widespread Wilson et al. Also, given the great differences in species richness across large regions such as Europe, slightly imprecise numbers are unlikely to affect the results of ecological studies significantly. The same is likely to hold for studies that compare the species composition of whole alien floras across a large geographical range Winter et al.

Yet this robustness very much depends on using data that have used a standardized classification of species status. In a comparison of two major databases on alien species distribution in Europe, differences in nomenclature between the databases meant that interpretation of the correlates of alien species richness was dependent on the database used Hulme and Weser These problems would be further accentuated in analyses that incorporate traits if these are incorrectly assigned to a species.

The role of taxonomy therefore becomes explicit when determining the precise identity of species subject to detailed study. Examples of taxa that are taxonomically challenging include apomictic groups e. Crataegus , Pilosella , Rubus , Taraxacum , karyologically variable complexes e.

Centaurea, Fallopia , genera with specific reproduction systems e. Oenothera , or those for which horticulturalists have bred numerous cultivars and varieties e. Cotoneaster Table 1. The reliability of data for ecological studies can be limited in taxonomically or cytologically challenging species or complexes, particularly for historical data reported in the literature.

For Fallopia taxa in the Czech Republic, sites reported in the literature and herbaria were revisited to explore whether the clones still persisted after decades since the first record. The misidentification rate was highest for the hybrid F. For example, these studies documented increased competitive and regenerative ability and faster spread of the hybrid relative to the parents Table 1. Phragmites is an example of a genus where thorough taxonomic research in the last decade has provided insights into the global pattern of its multiple invasions.

Three distinct lineages of Phragmites australis were identified in North America Saltonstall : i native P. The origin of this lineage is unknown and it is therefore considered cryptogenic Saltonstall However, the Phragmites story is further complicated by the hybridization of both the Gulf Coast type and the Eurasian type with other congeners, P. Most recently, a new introduced haplotype of P. Similarly, taxonomic advancement in the genus Bolboschoenus Cyperaceae, formerly included in the genus Scirpus achieved by classical methods during the last few decades has resulted in the reclassification of a taxon previously known as B.

Only then did it become obvious that populations introduced to eastern North America, where they became weedy in rice fields, belong to a distinct taxon, B.

The Fallopia example mentioned above illustrates that identifying hybrids requires considerable taxonomic and karyological experience Suda et al. Spartina anglica , a hybrid taxon that arose through allopolyploidization, is the classic example Thompson ; Ainouche et al.

With the emergence of karyological and molecular methods it has become obvious that invasiveness is often manifested below the species level, for example, at the cytological level e. Centaurea stoebe — Treier et al. Taxonomic uncertainty can also impede the results of ecological studies. For Pilosella glomerata , a European species invasive in North America, ecological niche models yielded varying predictions of its invasion potential depending on which genetic entities are used in training models all records compared with only taxonomically verified records.

Using all records resulted in substantially larger predicted potential ranges in the adventive range Ensing et al. A similar result was reported for the Australian tree Acacia saligna , which is invasive in many parts of the world.

Very different predicted ranges emerged from models trained using different genetic entities tentatively subspecies Thompson et al. These are examples of rare empirical studies showing that vetting occurrence records for taxonomic reliability is crucial for niche modelling—and indeed for ecological research on invasions in general. Records of questionable taxonomic accuracy should be used with caution in ecological studies Jimenez-Valverde et al.

Karyology is a rapidly developing research area and genome characteristics are among the traits that have been recently used in studies explaining species invasiveness. Here as well, the lack of taxonomic expertise could affect the results of ecological studies. Evidence has accumulated in recent years that invasive behaviour can be associated with karyological characteristics, including variation in genome copy number polyploidy and genome size te Beest et al. Polyploidization is one of the few mechanisms of instantaneous speciation and can rapidly alter organisms' traits by a single genetic event Levin In species with multiple cytotypes, the polyploids are usually the ones that become invasive te Beest et al.

Similarly, at the interspecific level, polyploids are overrepresented among invasive aliens relative to native or rare species in local floras Pandit et al. The high incidence of ploidy heterogeneity within plant genera entails the risk of ploidy mismatch: if the samples are not correctly assigned to species, incorrect ploidy levels can be introduced into a data set due to species misidentification, and the results of a study addressing the effects of karyological characteristics on invasiveness can be affected.

We analysed data on ploidy variation from the Index to plant chromosome numbers Goldblatt and Johnson onwards in invasive land plant species of the world as listed by Weber and their non-invasive congeners not included in Weber's checklist. This analysis reveals that the risk of ploidy bias due to species misidentification is likely to be small in 75 of the genera More importantly, the danger of ploidy mismatch between globally invasive and non-invasive species is comparatively high in 35 genera Frequency distribution of risk scores of introducing ploidy bias to ecological studies due to species misidentification, based on chromosome numbers of invasive plant species of the world and their non-invasive congeners see Table 1 for delimitation of risk categories.

Inherently associated with ploidy is the amount of nuclear DNA genome size. Genome size can constrain several characteristics that can underpin invasive success, including minimum generation time, seed mass, growth rate and specific leaf area Leitch and Bennett A negative correlation between invasiveness and genome size was reported, for instance, in pines Grotkopp et al.

Because genome size often varies considerably even among closely related species, accurate species determination is an essential prerequisite for any studies addressing the role of this cytogenetic parameter. Using the same data set as above, we assessed the magnitude of risk that holoploid genome size values taken from the Plant DNA C-values database; Bennett and Leitch would be biased if globally invasive species Weber were misidentified with their non-invasive congeners.

Thus far we have focused on the critical role of taxonomy in studying and managing plant invasions. What is Taxonomy?

Taxonomy is the science of naming, describing and classifying organisms and includes all plants, animals and microorganisms of the world. Using morphological, behavioural, genetic and biochemical observations, taxonomists identify, describe and arrange species into classifications, including those that are new to science.

Taxonomy identifies and enumerates the components of biological diversity providing basic knowledge underpinning management and implementation of the Convention on Biological Diversity. Unfortunately, taxonomic knowledge is far from complete.

In the past years of research, taxonomists have named about 1. Figure 2. Figure 3. Sampling and assessed characters All samples were obtained in Baili in April , during the flowering season of the two species. Figure 4. Table 1. Type specimens Type specimens of five infra-specific taxa for the two study species were examined: i For R.

Statistical analysis All statistical tests were carried out with the statistical software R, version 3. Results Excluded individuals In both species, the style is generally longer than the anthers, and this distance was recorded as a positive number. Figure 5. Table 2. Character R. Re-assignment of individuals to species Using the initial species assignments as prior information, R. Correlation of style and stamen hair-cover with hybrid index Using the co-ordinates along the first MFA dimension to calculate a hybrid index, intermediates showed values in the range of 0.

Figure 6. Table 3. Discussion Morphological characters Because the two study species were not very closely related, many of the qualitative characters were well distinguished Fig. Conclusions It is nowadays evident that hybridization is widespread in certain groups of organisms, and the boundaries between varieties and species can be blurred in complexes of closely related species. Contributions by the Authors T. Conflict of Interest Statement None declared. Supplementary Material Supplementary Data: Click here to view.

Acknowledgements We want to thank our counterparts in Baili, Jiayong Huang and Lingjun Wang for their help with permits and assistance in the field, and David and Maria Chamberlain for valuable support with character measurements. Supporting Information The following additional information is available in the online version of this article — Zip Archive containing morphological scoring data and R scripts used to carry out analysis.

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