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

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 ISI^SM.

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.     

The unknown northern green: evaluation of a national forest biodiversity research program

The taxonomic knowledge gap and lack of knowledge on species-level diversity has been a global concern within conservation biology through the recent two decades. As a national response, Finland has funded a Research Program of Poorly Known and Threatened Forest Species from the year 2003. The program is an essential part of the knowledge base applied in Finnish forest policy. The present paper evaluates the outcomes of the program, covering scientific publication, training, taxonomic coverage, increased knowledge on boreal forest biodiversity and awareness rising. The ongoing program has been funded by 6.5 million Euros to date including 59 projects. The program has produced 19 master’s theses and six doctoral theses. Due to their expertise the graduated biologists have been employed in environmental administration or become researchers. The program has produced 163 refereed scientific articles, 104 of which are recognized by the Web of Science; with an average impact factor of 1.81. The results of the program include 15 genera and 348 species new to science, and 60 genera and 1,664 species to Finland’s list of known species. Due to new knowledge gathered in the program 3,000–4,000 species could be included in the most recent National Red List assessment. The publishing of identification books on local language has proved as the most effective way of advancing general species knowledge among the public and end-users. The high number of new species to science from a biodiversity-poor boreal country describes the scale of the huge work still be done in describing the global species-level diversity. The program has achieved its goals in many ways, but the program leaves out a large part of the species that do not occur in forest biotopes. Moreover, the funding has decreased through the years despite the international goal of halting the world’s biodiversity loss has not been met.     

Biodiversity inventory and informatics in Southeast Asia

Rapidly changing land use in Southeast Asia threatens plant diversity, and reduces the time we have left to document it. Despite over 200 years of scientific plant exploration, many plant species have yet to be discovered. Moreover, we still have a very poor understanding of the distribution of known taxa in this biogeographically complex region. We review the current state of biodiversity exploration, using plants in Indonesia as an example. Traditional methods of collecting and describing species have provided a solid foundation for our understanding of plant biodiversity, but are insufficient for the pragmatic task of rapidly discovering and documenting today’s biodiversity before it is gone, because general collecting expeditions tend to be infrequent, and documentation of most new species must await taxonomic revisions many years in the future. Solutions to this exploration and documentation crisis (i) could use the abundant resource of enthusiastic, networked, national biology students, (ii) should employ biodiversity informatics tools to efficiently engage both specialists and parataxonomists, and (iii) might require adoption of new types of α-taxonomy, utilizing increasingly low-cost molecular methods and high resolution photographs. We describe emerging technologies that will facilitate this taxonomic development. We believe that a new golden age of biodiversity exploration may be dawning, just as biodiversity itself is most threatened, and are hopeful that increasing knowledge of biodiversity will be a positive force to slow its loss.     

A return-on-investment approach for prioritization of rigorous taxonomic research needed to inform responses to the biodiversity crisis

Global biodiversity loss is a profound consequence of human activity. Disturbingly, biodiversity loss is greater than realized because of the unknown number of undocumented species. Conservation fundamentally relies on taxonomic recognition of species, but only a fraction of biodiversity is described. Here, we provide a new quantitative approach for prioritizing rigorous taxonomic research for conservation. We implement this approach in a highly diverse vertebrate group—Australian lizards and snakes. Of 870 species assessed, we identified 282 (32.4%) with taxonomic uncertainty, of which 17.6% likely comprise undescribed species of conservation concern. We identify 24 species in need of immediate taxonomic attention to facilitate conservation. Using a broadly applicable return-on-investment framework, we demonstrate the importance of prioritizing the fundamental work of identifying species before they are lost.

In order to inform conservation effort, there is urgent need for rigorous taxonomic research to describe species under threat of extinction. Implementation of a new prioritization method identified 282 Australian reptile species needing taxonomic research, of which 17.6% represent undescribed species of conservation concern; this approach could be readily implemented across many faunal groups.     

Ecometagenetics confirm high tropical rainforest nematode diversity

The general patterns of increasing biodiversity from the poles to the equator have been well documented for large terrestrial organisms such as plants and vertebrates but are largely unknown for microbiota. In contrast to macrobiota, microbiota have long been assumed to exhibit cosmopolitan, random distributions and a lack of spatial patterns. To evaluate the assumption, we conducted a survey of nematode diversity within the soil, litter and canopy habitats of the humid lowland tropical rainforest of Costa Rica using an ultrasequencing ecometagenetic approach at a species-equivalent taxonomic level. Our data indicate that both richness and diversity of nematode communities in the tropical rainforests of Costa Rica are high and exceed observed values from temperate ecosystems. The majority of nematode species were unknown to science, providing evidence for the presence of highly endemic (not cosmopolitan) species of still completely undiscovered biodiversity. Most importantly, the greater taxonomic resolution used here allowed us to reveal predictable habitat associations for specific taxa and thus gain insights into their nonrandom distribution patterns.     

A review of the relationships between human population density and biodiversity

To explore the impacts of increasing human numbers on nature, many studies have examined relationships between human population density (HPD) and biodiversity change. The implicit assumption in many of these studies is that as population density increases so does the threat to biodiversity. The implications of this assumption are compounded by recent research showing that species richness for many taxonomic groups is often highest in areas with high HPD. If increasing HPD is a threat to conservation, this threat may be magnified owing to the spatial congruence between people and species richness. Here, I review the relationships between HPD and measures of biodiversity status focussing in particular on evidence for the spatial congruence between people and species richness and the threat that increasing HPD may pose to biodiversity conservation. The review is split into two major sections: (i) a quantitative assessment of 85 studies covering 401 analyses, including meta-analyses on discrete relationships; and (ii) a discussion of the implications of the quantitative analyses and major issues raised in the literature. Our understanding of the relationships between HPD and biodiversity is skewed by geographic and taxonomic biases in the literature. Most research has been conducted in the Northern Hemisphere and focussed primarily on birds and mammals, largely ignoring relationships with other taxonomic groups. A total of 127 analyses compared HPD with the species richness of particular taxonomic groups. A meta-analysis of these results found a significant positive population correlation indicating that, on average, species-rich regions and human settlements co-occur. However, there was substantial unexplained heterogeneity in these data. Some of this heterogeneity was explained by the size of the sampling unit used by researchers - as this increased so did the strength of the correlation between HPD and species richness. The most convincing result for a taxonomic group was a significant positive population correlation between HPD and bird species richness. Significant positive population correlations were also found for HPD versus the richness of threatened and geographically restricted species. Hence, there is reasonably good evidence for spatial congruence between people and species-rich regions. The reasons for this congruence are only just beginning to be explored, but key mutual drivers appear to include available energy and elevation. The evidence for increasing HPD as a threat to conservation was weak, owing primarily to the extreme heterogeneity in the approaches used to address this issue. There was some suggestion of a positive relationship between HPD and species extinction, but this result should be interpreted with caution owing to the wide diversity of approaches used to measure extinction. Identifying strong links between human development and species extinction is hampered in part by the difficulty of recording extinction events. The most convincing indication of the negative impact of increasing HPD was a significant negative population correlation between density and the size of protected areas. The magnitude and implications of spatial congruence between people and biodiversity are now being explored using the principles of complementarity and irreplaceability. Human development as a threat to conservation is usually assessed within a complex, interdisciplinary modelling framework, although population size is still considered a key factor. Future population growth and expansion of human settlements will present increasing challenges for conserving species-rich regions and maximising the benefits humans gain from nature.     

How many species of flowering plants are there?

We estimate the probable number of flowering plants. First, we apply a model that explicitly incorporates taxonomic effort over time to estimate the number of as-yet-unknown species. Second, we ask taxonomic experts their opinions on how many species are likely to be missing, on a family-by-family basis. The results are broadly comparable. We show that the current number of species should grow by between 10 and 20 per cent. There are, however, interesting discrepancies between expert and model estimates for some families, suggesting that our model does not always completely capture patterns of taxonomic activity. The as-yet-unknown species are probably similar to those taxonomists have described recently—overwhelmingly rare and local, and disproportionately in biodiversity hotspots, where there are high levels of habitat destruction.     

The Diversity of Coral Reefs: What Are We Missing?

Tropical reefs shelter one quarter to one third of all marine species but one third of the coral species that construct reefs are now at risk of extinction. Because traditional methods for assessing reef diversity are extremely time consuming, taxonomic expertise for many groups is lacking, and marine organisms are thought to be less vulnerable to extinction, most discussions of reef conservation focus on maintenance of ecosystem services rather than biodiversity loss. In this study involving the three major oceans with reef growth, we provide new biodiversity estimates based on quantitative sampling and DNA barcoding. We focus on crustaceans, which are the second most diverse group of marine metazoans. We show exceptionally high numbers of crustacean species associated with coral reefs relative to sampling effort (525 species from a combined, globally distributed sample area of 6.3 m(2)). The high prevalence of rare species (38% encountered only once), the low level of spatial overlap (81% found in only one locality) and the biogeographic patterns of diversity detected (Indo-West Pacific>Central Pacific>Caribbean) are consistent with results from traditional survey methods, making this approach a reliable and efficient method for assessing and monitoring biodiversity. The finding of such large numbers of species in a small total area suggests that coral reef diversity is seriously under-detected using traditional survey methods, and by implication, underestimated.     

Do biodiversity hotspots match with rodent conservation hotspots?

Biodiversity hotspots are used widely to designate priority regions for conservation efforts. It is unknown, however, whether the current network of hotspots adequately represents globally threatened taxonomic diversity for whole plant and animal groups. We used a mammalian group traditionally neglected in terms of conservation efforts, the rodents, in order to test whether biodiversity hotspots match the current distribution of threatened taxa (genera and species). Significantly higher numbers of threatened rodent genera and species fell within biodiversity hotspots; nonetheless over 25% of the total threatened genera and species did not occur in any biodiversity hotspot. This was particularly true for the Australian region, where 100% of the threatened genera and species fell outside biodiversity hotspots, with many threatened taxa found in Papua-New Guinea. We suggest to officially including Papua New Guinea among biodiversity hotspots for rodents, and also the steppic/semidesert areas of central Asia.     

20 years since the introduction of DNA barcoding: from theory to application

Traditionally, taxonomic identification has relied upon morphological characters. In the last two decades, molecular tools based on DNA sequences of short standardised gene fragments, termed DNA barcodes, have been developed for species discrimination. The most common DNA barcode used in animals is a fragment of the cytochrome c oxidase (COI) mitochondrial gene, while for plants, two chloroplast gene fragments from the RuBisCo large subunit (rbcL) and maturase K (matK) genes are widely used. Information gathered from DNA barcodes can be used beyond taxonomic studies and will have far-reaching implications across many fields of biology, including ecology (rapid biodiversity assessment and food chain analysis), conservation biology (monitoring of protected species), biosecurity (early identification of invasive pest species), medicine (identification of medically important pathogens and their vectors) and pharmacology (identification of active compounds). However, it is important that the limitations of DNA barcoding are understood and techniques continually adapted and improved as this young science matures.     

Application of DNA barcoding in biodiversity studies of shallow-water octocorals: molecular proxies agree with morphological estimates of species richness in Palau

The application of DNA barcoding to anthozoan cnidarians has been hindered by their slow rates of mitochondrial gene evolution and the failure to identify alternative molecular markers that distinguish species reliably. Among octocorals, however, multilocus barcodes can distinguish up to 70 % of morphospecies, thereby facilitating the identification of species that are ecologically important but still very poorly known taxonomically. We tested the ability of these imperfect DNA barcodes to estimate species richness in a biodiversity survey of the shallow-water octocoral fauna of Palau using multilocus (COI, mtMutS, 28S rDNA) sequences obtained from 305 specimens representing 38 genera of octocorals. Numbers and identities of species were estimated independently (1) by a taxonomic expert using morphological criteria and (2) by assigning sequences to molecular operational taxonomic units (MOTUs) using predefined genetic distance thresholds. Estimated numbers of MOTUs ranged from 73 to 128 depending on the barcode and distance threshold applied, bracketing the estimated number of 118 morphospecies. Concordance between morphospecies identifications and MOTUs ranged from 71 to 75 % and differed little among barcodes. For the speciose and ecologically dominant genus Sinularia, however, we were able to identify 95 % of specimens correctly simply by comparing mtMutS sequences and in situ photographs of colonies to an existing vouchered database. Because we lack a clear understanding of species boundaries in most of these taxa, numbers of morphospecies and MOTUs are both estimates of the true species diversity, and we cannot currently determine which is more accurate. Our results suggest, however, that the two methods provide comparable estimates of species richness for shallow-water Indo-Pacific octocorals. Use of molecular barcodes in biodiversity surveys will facilitate comparisons of species richness and composition among localities and over time, data that do not currently exist for any octocoral community.     

Nematode chromosomes

The nematode Caenorhabditis elegans has shed light on many aspects of eukaryotic biology, including genetics, development, cell biology, and genomics. A major factor in the success of C. elegans as a model organism has been the availability, since the late 1990s, of an essentially gap-free and well-annotated nuclear genome sequence, divided among 6 chromosomes. In this review, we discuss the structure, function, and biology of C. elegans chromosomes and then provide a general perspective on chromosome biology in other diverse nematode species. We highlight malleable chromosome features including centromeres, telomeres, and repetitive elements, as well as the remarkable process of programmed DNA elimination (historically described as chromatin diminution) that induces loss of portions of the genome in somatic cells of a handful of nematode species. An exciting future prospect is that nematode species may enable experimental approaches to study chromosome features and to test models of chromosome evolution. In the long term, fundamental insights regarding how speciation is integrated with chromosome biology may be revealed.     

Biodiversity loss and the taxonomic bottleneck: emerging biodiversity science

Human domination of the Earth has resulted in dramatic changes to global and local patterns of biodiversity. Biodiversity is critical to human sustainability because it drives the ecosystem services that provide the core of our life-support system. As we, the human species, are the primary factor leading to the decline in biodiversity, we need detailed information about the biodiversity and species composition of specific locations in order to understand how different species contribute to ecosystem services and how humans can sustainably conserve and manage biodiversity. Taxonomy and ecology, two fundamental sciences that generate the knowledge about biodiversity, are associated with a number of limitations that prevent them from providing the information needed to fully understand the relevance of biodiversity in its entirety for human sustainability: (1) biodiversity conservation strategies that tend to be overly focused on research and policy on a global scale with little impact on local biodiversity; (2) the small knowledge base of extant global biodiversity; (3) a lack of much-needed site-specific data on the species composition of communities in human-dominated landscapes, which hinders ecosystem management and biodiversity conservation; (4) biodiversity studies with a lack of taxonomic precision; (5) a lack of taxonomic expertise and trained taxonomists; (6) a taxonomic bottleneck in biodiversity inventory and assessment; and (7) neglect of taxonomic resources and a lack of taxonomic service infrastructure for biodiversity science. These limitations are directly related to contemporary trends in research, conservation strategies, environmental stewardship, environmental education, sustainable development, and local site-specific conservation. Today’s biological knowledge is built on the known global biodiversity, which represents barely 20% of what is currently extant (commonly accepted estimate of 10 million species) on planet Earth. Much remains unexplored and unknown, particularly in hotspots regions of Africa, South Eastern Asia, and South and Central America, including many developing or underdeveloped countries, where localized biodiversity is scarcely studied or described. "Backyard biodiversity", defined as local biodiversity near human habitation, refers to the natural resources and capital for ecosystem services at the grassroots level, which urgently needs to be explored, documented, and conserved as it is the backbone of sustainable economic development in these countries. Beginning with early identification and documentation of local flora and fauna, taxonomy has documented global biodiversity and natural history based on the collection of "backyard biodiversity" specimens worldwide. However, this branch of science suffered a continuous decline in the latter half of the twentieth century, and has now reached a point of potential demise. At present there are very few professional taxonomists and trained local parataxonomists worldwide, while the need for, and demands on, taxonomic services by conservation and resource management communities are rapidly increasing. Systematic collections, the material basis of biodiversity information, have been neglected and abandoned, particularly at institutions of higher learning. Considering the rapid increase in the human population and urbanization, human sustainability requires new conceptual and practical approaches to refocusing and energizing the study of the biodiversity that is the core of natural resources for sustainable development and biotic capital for sustaining our life-support system. In this paper we aim to document and extrapolate the essence of biodiversity, discuss the state and nature of taxonomic demise, the trends of recent biodiversity studies, and suggest reasonable approaches to a biodiversity science to facilitate the expansion of global biodiversity knowledge and to create useful data on backyard biodiversity worldwide towards human sustainability.     

A warning for ecologists and conservation biologists using species checklists: How the European marine fauna ‘lost’ all of its 16 <Emphasis Type="Italic">Discodoris</Emphasis> species (Mollusca: Gastropoda)

The European marine fauna used to be considered to include 16 species of Discodoris sea slugs until a recent worldwide revision demonstrated that there is not a single Discodoris species in European waters. This exemplary case illustrates the fact that species checklists do not accurately represent biodiversity unless they are based on sound taxonomic work in which (1) the status of every available species name has been addressed, i.e. whether it is valid, synonymous, or of doubtful application, and (2) classification reflects phylogenetic relationships. It is argued that taxonomic revisions are critically needed, because the status of species names can only be addressed properly through revisions. It is discussed that fields which depend on taxonomic data, such as conservation biology and ecology, might be affected deeply if problematic species names (synonyms and nomina dubia) have not been recognized. Consequently, it is proposed that a taxon that has not been revised be red-flagged in checklists, so that non-taxonomists will know which species names should be applied with caution or not at all.     

Taxonomic inflation: its influence on macroecology and conservation

Species numbers are increasing rapidly. This is due mostly to taxonomic inflation, where known subspecies are raised to species as a result in a change in species concept, rather than to new discoveries. Yet macroecologists and conservation biologists depend heavily on species lists, treating them as accurate and stable measures of biodiversity. Deciding on a standardized, universal species list might ameliorate the mismatch between taxonomy and the uses to which it is put. However, taxonomic uncertainty is ultimately due to the evolutionary nature of species, and is unlikely to be solved completely by standardization. For the moment, at least, users must acknowledge the limitations of taxonomic species and avoid unrealistic expectations of species lists.     

Buried treasure: soil biodiversity and conservation

Soils are incredibly biodiverse habitats, yet soil-dwelling organisms have received little attention within the field of conservation biology. Due to difficulties involved in studying soil biota, and to taxonomic biases in conservation research, the full extent of soil biodiversity is not well understood, and soil-dwelling organisms are rarely candidates for conservation. The biogeography of soil biota differs significantly from that of plants or animals aboveground, and the taxonomic and functional diversity of soil-dwellers allows them to have a multitude of ecological effects on aboveground organisms. Soil organisms exhibit levels of biodiversity several orders of magnitude greater than those found in their aboveground counterparts on a per-area basis. The biodiversity of soils underpins many crucial ecosystem services which support the plants and animals typically targeted by conservation efforts. Strategies detailed in this paper provide practitioners with the ability to address many of the challenges related to incorporating soils and soil organisms into conservation planning.     

我国植物种级水平分类学研究刍议

对洪德元先生最近在《生物多样性》(2016年第24卷第3期)发表的《关于提高物种划分合理性的意见》一文中的部分观点进行了进一步阐述。强调我国植物确实还存在大量种级水平的分类学问题有待解决, 我国植物分类学研究在一些重要发展阶段(如系统阶段和物种生物学阶段)上存在明显缺失, 需要弥补。指出分类学发展到今天, 不宜再强调“经典分类学”和“实验分类学”之分, 应采用多学科手段解决分类学问题; 我国应加强植物分类专著水平的研究工作, 注意培养年轻一辈植物分类学专著工作者; 在分类处理中应用居群概念和统计学方法时应特别谨慎; 在系统植物学中接受物种概念的多元性是必要的, 但要向达到广义的生物学种概念努力, 不宜以有所谓的“归并派”和“细分派”之分为借口而完全主观地划分物种。     

Haplotype diversity of the nematode Pristionchus pacificus on Réunion in the Indian Ocean suggests multiple independent invasions

Pristionchus pacificus has been established as a nematode model system in evolutionary developmental biology and evolutionary ecology. Field studies in North and South America, Asia, Africa and Europe indicated that nematodes of the genus Pristionchus live in association with scarab beetles. Here, we describe the first account of soil‐ and beetle‐associated nematodes on an island setting by investigating the island of Réunion in the Indian Ocean. Réunion has high numbers of endemic insects and is one among several attractive islands for biodiversity studies. Being of volcanic origin, Réunion is 2–3 million years old, making it the youngest of the Mascareigne islands. We show that beetle‐ and soil‐derived nematodes on Réunion are nearly exclusively hermaphroditic, suggesting that selfing is favoured over gonochorism (outcrossing) during island colonization. Among members of four nematode genera observed on Réunion, Pristionchus pacificus was the most prevalent species. A total of 76 isolates, in association with five different scarab beetles, has been obtained for this cosmopolitan nematode. A detailed mitochondrial haplotype analysis indicates that the Réunion isolates of P. pacificus cover all four worldwide clades of the species. This extraordinary haplotype diversity suggests multiple independent invasions, most likely in association with different scarab beetles. Together, we establish Réunion as a case study for nematode island biogeography, in which the analysis of nematode population genetics and population dynamics can provide insight into evolutionary and ecological processes. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 170–179.     

Arthropod biodiversity after forest fires: winners and losers in the winter fire regime of the southern Alps

Since prehistoric times, natural and man made fires have been important factors of natural disturbance in many forest ecosystems, like those on the southern slopes of the Alps. Their effect on scarce, endangered or stenotopic species and on the diversity of invertebrate species assemblages which depend on a mosaic of successional habitat stages, is controversially discussed. In southern Switzerland, in a region affected by regular winter fires, we investigated the effect of the fire frequency on a large spectrum of taxonomic groups. We focussed on total biodiversity, taxonomic groups specific to certain habitat types, and on scarce and endangered species. Overall species richness was significantly higher in plots with repeated fires than in the unburnt control sites. Plots with only one fire in the last 30 yr harboured intermediate species numbers. Fire frequency had a significantly positive effect on species richness of the guilds of interior forest species and forest edge specialists. Species of open landscape, open forests and interior forests were not influenced by fire frequency. A positive effect of fire on species richness was observed for ground beetles (Carabidae), hoverflies (Syrphidae), bees and wasps (Hymenoptera aculeata, without Formicidae), and spiders (Araneae). True bugs (Heteroptera), lacewings (Neuroptera) and the saproxylic beetle families Cerambycidae, Buprestidae and Lucanidae showed positive trends, but no statistically significant effects of fire on species numbers or/and abundances. Negative effects of fire on species numbers or/and abundances were found only for isopods and weevils (Curculionidae). A compromise for forest management is suggested, which considers the risk of damage by fire to people and goods, while avoiding the risk of damage to biodiversity by imitating the effects of sporadic fires and providing a mosaic forest with open gaps of different successional stages.