How Big Is Our Knowledge Gap in Taxonomy and Systematics? A Decade Long Aphidiinae Story

: Knowledge gaps in taxonomy and systematics are present in all insect groups, differing just in size. Generally, size of the gap is negatively correlated with body size and positively with number of species within the group. As an example, we present the size of the knowledge gap within the subfamily Aphidiinae (Hymenoptera: Braconidae). As solitary koinobiont endoparasi-toids of aphids, Aphidiinae are widely used as biocontrol agents and consequently one of the best studied parasitoid groups. In the last decade, taxonomical studies on Aphidiinae have been focused on an integrative approach which resulted in numerous new findings: description of new species, detection of alien species, resolving the taxonomical status of genera and species groups, proposition of new classification schemes, etc. All those findings are critically summarized. Availability of different types of data is discussed and propositions for future studies and optimal research practices are given.

The biodiversity crisis has been known for decades, but it just recently started getting the public attention it deserves [1].There is an urgent need to mitigate the crisis by exploring, managing and conserving biodiversity.The very first step is to overcome the ignorance and realize that the most important unfinished job in biology is discovering and describing biodiversity [2,3].This brings us to the vital role of taxonomy in today's biology.As a biological discipline with the task to identify, name and describe organisms [4], taxonomy represents a bridge between morphology and systematics.Unfortunately, at this moment, taxonomy is not a highway bridge that we need.It is more like an old, decrepit bridge which is still standing on a good foundation, but full of gaps, holes, and obstacles.These difficulties associated with taxonomy are: gaps in taxonomic knowledge, lack of taxonomic infrastructure and an insufficient number of taxonomic experts; and are called "taxonomic impediment".With more than 1 million described species, insects comprise more than half of all known species [5], and with an estimate of 5.5 million living species [6] they represent the biggest proportion of the taxonomic impediment.
Knowledge gaps in taxonomy and consequently in systematics are present in all insect groups, differing just in size.Generally, size of the gap is negatively correlated with body size and positively with number of species within the group.Families of small Diptera and parasitoid wasps (Hymenoptera) are recognized as groups with highest proportions of dark taxa (little-known and unknown species).
In order to present the size of the knowledge gap in taxonomy and systematics I chose the subfamily Aphidiinae (Hymenoptera: Braconidae) as an example.Aphidiinae are solitary koinobiont endoparasitoids of aphids and as such, a single specimen completes its development inside the living aphid host, which continues to feed and grow [7].Among Aphidiinae there are several species which are widely used as biocontrol agents.Primarily because of their economic importance, Aphidiinae are one of the best studied parasitoid groups.Taxonomy and systematics of Aphidiinae is especially well studied in Europe, with over 70 years of continuous research [8].History of Aphidiinae taxonomy goes back to the dawn of nomenclature and taxonomy, with the first species described in the 10 th edition of Systema Naturae (Aphidius rosae Haliday, 1834 described as Ichneumon aphidum L. 1758) [9].In the last 263 years, many notable entomologists have contributed to Aphidiinae taxonomy (e.g.Christian Gottfried Daniel Nees von Esenbeck, Alexander Henry Haliday, Thomas Ansell Marshall, William Harris Ashmead and many others), but the real pioneers are our contemporaries: professor Manfred Mackauer and Dr. Petr Starý.More than six decades ago they started their research on Aphidiinae, and since then published numerous papers concerning taxonomy, systematics and all other aspects of Aphidiinae biology.Dr. Petr Starý, with more than 500 published papers dealing with Aphidiinae, can undoubtedly be labeled as a man who made a difference.One may ask where that knowledge gap is if one man performed so much research.Well, the answer would be that taxonomy is a never ending story, so here we present taxonomical studies on Aphidiinae conducted in the period 01.01.2010-01.06.2020.as a proxy of knowledge gap size.

Chapters that have been told in the last decade
The first problem that emerges when someone starts reading about the subfamily Aphidiinae is the number of described species and genera.Those numbers differ as much as 33% in various sources, starting with 400 species in 50 genera in Boivin et al. [8], then 505 species in 38 genera according to Žikić et al. [10], up to more than 600 species in 65 genera according to Tian et al. [11].There are two reasons for this discrepancy: 1) lack of an updated world checklist of Aphidiinae (last comprehensive list was published in late 1960s [8,12]) and 2) uncritical use of World Ichneumonoidea database in Taxapad [13].Determination of the exact number of Aphidiinae species is beyond the subject of this paper but according to available data our best estimate is that there were about 500 living species classified in 52 genera prior to year 2010.

New taxa in the Old World and all other 'Worlds'
The subfamily Aphidiinae is an excellent model to emphasize the 'taxonomic impediment'.We estimate that in the last 12 years (2010-2021) about 1800 papers (2770 results in Google scholar search minus double results) which deal with Aphidiinae were published.A vast majority of studies have been done on various applied aspects of Aphidiinae biology (life history, demography, functional response, host preference, foraging behavior), and to a lesser extent on local faunas, all with the aim of using those parasitoids in biological control.To the best of our knowledge, among those papers there are less than 60 papers focusing on Aphidiinae taxonomy and systematics, and only 37 in which new Aphidiinae taxa are described .This discrepancy between applicative and taxonomical studies (30:1) is a real proxy of the "taxonomic impediment".In total, three new genera (Choreopraon Mackauer, 2012; Sergeyoxys Davidian, 2016; and Astigmapraon Tian et Chen, 2017) [25,32,35] and 55 new species were described from around the world.Newly described taxa represent 6% and 10 % of all known Aphidiinae genera and species, respectively (Figure 1).Those numbers alone indicate that the knowledge gap in Aphidiinae taxonomy is very big, despite the long research history and economic importance.Further analysis of data about taxa described since 2010 provides us an insight to other aspects of the 'taxonomic impediment'.Two out of three genera were described from the Palaearctic (Sergeyoxys -Russia, Astigmapraon -China) while Choreopraon was discovered in New Zealand (Australasia).Dominance of discoveries in Palaearctic is much more expressed on species level with 67% of them being described from this region, while none of the species were discovered in Afrotropical and Neotropical regions (Figure 2).This is a clear indicator of the fact that there is an insufficient number of taxonomic experts and that they are unevenly distributed in the world.Uneven distribution of experts is even more obvious when species authors were analyzed.Fifty five Aphidiinae species described between 2010 and 2021 were named by 19 researchers (up to 3 authors per species) from which four were from USA (Nearctic), one from India (Oriental), and 14 from Palaearctic (two from China, one from Iran and 11 from Europe).Only seven species were described without authors from Europe.

Foreigners in Europe (New alien species in Europe)
Species descriptions and rate of species description are often used as sole indicator of taxonomic activity, but taxonomy is much more than just naming a species, and various indicators can and should be used to assess the current state of taxonomy and systematics [51].One such indicator, which is widely underestimated, is the crucial role of taxonomists in identification of alien species.In European Aphidiinae fauna only five species were marked as alien ( [54], while Aphidius ericaphidis was described in 2011 from USA and was detected in samples from Serbia and Scotland collected in 2014 and 2015, respectively [55].Additional revision of collections determined that both species were present in Europe long before their formal descriptions (L.orientalis back in 1995, and A. ericaphidis in 1965).Trioxys liui was first collected in Spain in 2017 [55].All three alien species were identified by an integrative taxonomic approach using molecular, morphological and ecological data, which became the standard in Aphidiinae taxonomical studies in the last decade.Using all available types of data is the only way which will lead to shrinking the knowledge gap in taxonomy and systematics.

Revising the unrevised
A single description of a species is of inestimable importance, but sometimes alpha-taxonomy can be in discrepancy with beta-taxonomy because of "superficial description taxonomic impediment" (older descriptions often can be too superficial by today's standards) [3].In such cases revision of a whole group of organisms (species group, genus, tribe...) is necessary in order to reduce the knowledge gap [51].
The majority of Aphidiinae tribes, subtribes and genera were revised 30-50 years ago and those revisions are mainly outdated.In the last decade a lot of effort has been put into the improvement of Aphidiinae taxonomy and systematics and into clarification of species status.Revision of the world Monoctonina is the only revision on the subtribe level and it included all available species [43,47].Several genera with smaller number of species were also reviewed: Monoctonia Starý, 1962 [31], Lipolexis Foerster, 1862 [31], Areopraon Mackauer, 1959 [39], Pseudopraon Starý, 1975 [39], Paralipsis Foerster, 1862 [33,41], Acanthocaudus Smith, 1944 [37], Euaphidius Mackauer, 1961 [57], Remaudierea Starý, 1973 [57].Most of those revisions resulted in a higher nuber of species within the genus, while genera Euaphidius and Remaudierea were determined as junior synonyms of Aphidius [57].European species of the genera Adialytus Foerster, 1862 and Lysiphlebus Foerster, 1862 were also revised [40,58], and new subgeneric classification of European Ephedrus Haliday, 1833 species was proposed [42].Lysiphlebus revision [40] can serve as a classical example of importance of revisions in taxonomy and consequently in biodiversity research.Prior to revision there were 15 Lysiphlebus species known from Europe.With this study the number of European Lysiphlebus species is reduced to 13; four species were synonymized and two new species were described.Although this quantitative taxonomic information is very important, even more important is the quality of taxonomic information [51].Within this study Tomanović et al. determined that only two descriptions of Lysiphlebus species match today's standards in Aphidiinae taxonomy and redescribed all other species [40].In addition, remarks about species biology and distribution were also provided.
There are several published studies dealing with taxonomic status of Aphidiinae species groups [26,29,30,53,[59][60][61][62] among which the most important are those about taxonomy of biocontrol agents belonging to Aphidius colemani and A. eadyi species groups [53,61].It was determined that Aphidius colemani species group is consisted of three species -A.colemani, A. transcaspicus Telenga, 1958 and almost forgotten A. platensis Brethes, 1913 [61].At the time when this study was conducted, parasitoids within global commercially distributed materials were a mixture of all three species [61], and most likely the situation is the same at this moment.Interestingly, similar results were obtained within the A. eadyi species group [53].Three species of biocontrol agents against Acyrthosiphon pisum (Harris) were identified (A.smithi, A. eadyi Stary, Gonzalez & Hall, 1980 and A. banksae Kittel, 2016).Aphidius banksae, which was previously known only from Israel and Turkey, was identified as a widely distributed species with a range that covers most of the western Palaearctic [53].Such huge knowledge gaps in taxonomy of economically very important biocontrol agents raise numerous questions about the taxonomic status of many other Aphdiinae species, especially those which parasitize aphids on nonagricultural plants.

Epilogue
The bridge from the beginning of the story looks a bit different after a decade of research.Some holes are filled and some obstacles are removed.Now we can see further.We can see some new holes, obstacles and gaps that need to be fixed.
Even with the tremendous work that has been done so far, the knowledge gap in Aphidiinae taxonomy is still very big and all aspects of the taxonomic impediment are more than obvious.
Although there is no meaningful research in biology without reliable taxonomy [53], its importance in the modern world is far from being fully acknowledged [63].Recently Swiss Re concluded that 55% of global GDP is dependent on biodiversity and ecosystem service [64], but we are still lacking large research grants (and even small ones) for taxonomy which is considered only as a cost [63].Until institutions, governments and the world realize the importance of this kind of research, taxonomists need to be more clever and utilize data from all available resources such as museum collections, as well as cybertaxonomy and molecular data.In the last two years 10 Aphidiinae species were described thanks to cooperation between taxonomists and the Barcode of life initiative [43,45,47].
The one who would like to take this interesting walk over the bridge called taxonomy should be aware that in Aphidiinae taxonomy barcodes are not enough, and must be used only as a part of integrative taxonomy.Similar situation is in most other taxa, and using just one type of information can make our knowledge gaps even bigger.
It seems appropriate to finish with a citation of a song by Jonathan Coulton adapted for taxonomy:

Citation:
Petrović, A. How Big Is Our Knowledge Gap in Taxonomy and Systematics?A Decade Long Aphidiinae Story, in Proceedings of the 1st International Electronic Conference on Entomology, 1-15 July 2021, MDPI: Basel, Switzerland, doi:10.3390/IECE-10534Published: 1 July 2021 Publisher's Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.Copyright: © 2021 by the authors.Submitted for possible open access publication under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses /by/4.0/).

Figure 1 .
Figure 1.Percentage of described Aphidiinae species before and after year 2010.

Figure 2 .
Figure 2. Number and percentage (lower left corner) of described Aphidiinae species in different ecoregions in the period 01.01.2010-01.06.2021.

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We've experiments to runThere is research to be done On the species who are Still alive."Funding: This research was funded by the Ministry of Education, Science and Technological Development of the Republic of Serbia (Grant number 451-03-9/2021-14/ 200178).