Continental diatom biodiversity discovery and description in China: 1848 through 2019

Abstract In this paper we inventory the continental diatom taxa described from inland waters in China, from the first species descriptions dating back to 1848 through 2019. China’s geography and hydrography are complex, including the world’s highest mountains, many large rivers, salty lakes, and large karst regions. From this area, a total of 1128 taxa have been described from China over this time period. We examine the number of taxa described in ca. 20-year intervals and note the periods of time of no to few descriptions, versus time intervals with many taxon descriptions. Early on, taxon descriptions of freshwater diatoms from China were done by mostly by Europeans working alone, and the time frame of 1948 to 1967 had few descriptions, as a devasting famine and the cultural revolution impacted scientific work and productivity. B.V. Skvortzov produced a large number of taxon descriptions, during his time in residence in Harbin, later while in Sao Paulo, Brazil, and even posthumously. More recently, a wide range of labs and collaborations across China, and with a diverse array of international partners, is ushering in a new, robust era of research on the biodiversity of continental diatoms. A few areas of research and work for the future are discussed.


introduction
Asia has received considerable attention in the context of biodiversity discovery, biogeography and resolving the evolutionary history of a variety of lineages (Gower et al. 2012). It is an area harboring many endemic species and broader lineages (López-Pujol et al. 2011;Lu et al. 2018), relicts (Wu et al. 2007López-Pujol and Ren 2009;Li et al. 2012a) as well as extinct taxa (Fu et al. 2019;Proust et al. 2020;Zhang 2020). Many diverse lineages have originated, radiated and gone extinct in China. This is true for many groups of organisms, including continental diatoms (see Skvortzov 1937;Hustedt 1938aHustedt , b, 1939Williams 2004;Williams and Reid 2006;Kulikovskiy et al. , 2015Hamsher et al. 2014;Kociolek 2019).
Within China, there has been a long history and much recent attention on the description of many new species and even genera from continental ecosystems across the country. Interest in continental diatoms of China extends beyond biodiversity discovery to a rich array of work related to water quality and bioassessment (e.g. Ouyang et al. 2015), impacts of eutrophication and the creation of dams (Wang and Zhang 2004;Shen et al. 2018), paleoenvironmental reconstructions (Rioual and Wang 2009) and the development of many products with diatoms (Zhang et al. 2012;Wang and Seibert 2017;Zhang 2019).
The work on biodiversity discovery, as well as ecological work and more applied studies, depends on a working knowledge of the flora that has already been documented. We have compiled and present here a listing of the continental diatoms described from China to provide these descriptive and practical projects with a historical context and a baseline against future work can be compared. This compilation of new taxa described from China, and the publications in which they were presented, can also help interpret the history and development of diatom studies in China, from the middle of the 19 th century to the present.

Methods
In our work developing this compilation of names of the continental diatoms described from China, we used the current geo-political circumscription of the country recognized by the United Nations. Our definition of "continental" refers to a variety of inland waters bodies, including freshwaters as well as those with high conductivity and, to some extent, 'salty' waters. But we have excluded taxa described from estuaries and marine localities from our review.
The bases of this compilation are the major resources for diatom nomenclature, including Catalogue of Diatom Names (Fourtanier and Kociolek 2011), DiatomBase (Kociolek et al. 2020) and AlgaeBase (Guiry and Guiry 2020). In addition, we reviewed several of the compilations of diatoms of China ("Flora Algarum Sinicarum Aquae Dulcis") and some primary literature that escaped the notice of these comprehensive works and summative projects. An important reference for this work is Jin (1951), in which the knowledge of diatoms reported from China from 1848 to 1946, noting over 1000 taxa had been reported from marine and freshwater ecosystems, is summarized. The paper lists the taxa described from China (mostly by Skvortzov up to 1946). Although Jin (1951) did not document most of the other descriptions by European authors, both prior to and concurrent with Skvortzov, and his list obviously does not include post-1946 names, it is a great (but under cited) reference from which to develop a list of diatoms from China. The Skvortzov names were checked against the check list of his taxa compiled by Gololobova (2012). All of the names documented in this work have been included in DiatomBase.

Continental diatoms described from China: An overview
In the 170-year history of continental diatom discovery in China, 1128 taxa have been described at the level of species and below (Table 1). This was not a smooth, equal accumulation of species over time, and if we examine the overall time period in groups of 20-year intervals, we can see there were times when significant numbers of taxa were described. For example, the time interval of 1928 to 1947 there were 355 taxa described in 16 publications, and between 1968 and 1987, 189 taxa were described in only 13 publications. In both instances, most of the publications were by a single author (See Appendices 1 and 2). On the other hand, in the more recent period of 2000 to 2019, the highest number of taxa were described (421), and published in 99 separate publications. Many of these papers were multi-authored. Periods of low publication of new species can be found in the earliest periods  and in the period 1948-1967 (Fig. 1).
The initial period:  Studies on the continental diatoms of China date back to the mid 1800's, to the work of Ehrenberg. From these initial works through ¾ of the 20 th century, there were many studies that documented continental diatom taxa in China, with a few genera and many species and subspecific taxa being proposed. The majority of taxa described was at the subspecific level. In Appendix 1 we document the new genera, species and subspecific continental diatoms described from China in this time period. This list, based on more than 50 publications only, shows that there were 2 genera described from continentals of China (Amphiraphia Zhu 1983 andPorosularia Skvortzov 1976b). Neither of these genera have been reported since they were first described, and neither of these names are in use today. Table 1 and Appendix 1 show that from 1848 until 1999, a total of 707 taxa were described from continental in China. Of these, 218 were recognized as separate species, while 489 were described as varieties and forms. These taxa were included across 48 genera. Genera with the most taxa described include Pinnularia (138), Navicula sensu lato (98), Cymbella sensu lato (56) and Nitzschia (43) and Gomphonema (39).
The data for this period were organized into 20-year intervals (except the last period) and show some interesting trends. The first works in which new taxa were described were penned by Europeans working alone. This included Ehrenberg being the first in 1848 and then again in 1854, but after that more than 50 years went by before another publication that included a new species described was produced. In 1906 Mereschkowsky studies diatoms from Tibet, and in 1922 Hustedt worked on diatoms from Tibet and the northwestern part of China. Starting in the late 1920's, through the 1940's, the description of continental diatom taxa was dominated by Boris V. Skvortzov. Williams et al. (2016) have provided insights into the life and work of Skvortzov, and Gololobova (2012) has created a checklist of the taxa described by him. Unlike his predecessors who described continental diatoms from China, Skvortzov actually lived and worked in China (though he studied from many parts of Asia, from the Philippines, Russia and to India, and further afield, and received samples from many individuals). His base was in Harbin, in Heilongjiang Province, in the northeastern part of the country. Thus, while species he described were from many areas and diverse ecosystems across China, many of the taxa described were from the northeastern part of the country. Skvortzov trained students in Harbin, and later work on diatom taxonomy in China has been carried out by three generations of scientists who can trace their academic lineages back to him. During the same time period as Skvortzov was describing many taxa, some Europeans also contributed to our knowledge of new continental diatoms, such as Skuja (1937) and Voigt (1942a, b).
In the period following Skvortzov's large work published in 1946, only one other publication appeared (in which 8 taxa were described), until another large work on the continental diatoms of China was published by Skvortzov in 1976. From 1950to 1976 Taxa  Cumulative  Publications  1848-1867  9  9  2  1868-1887  0  9  0  1888-1907  28  37  1  1908-1927  57  94  2  1928-1947  355  449  16  1948-1967  8  457  2  1968-1987  189  646  13  1988-1999  61  707  17  2000-2019  421  1128  99 was a period of dramatic challenges and cultural change in China. The first occurred with the severe famine that hit the country in 1950, lasting three years. The impacts of that famine led to the deaths of tens of millions of people, and this had lasting impacts on society for many years afterwards. In addition, the Cultural Revolution, in part a reaction to the great famine, also had negative impacts on life in China, and those impacts on academics are well-documented. Thus, with the few publications produced in this time period within the narrow discipline of diatom taxonomy and biodiversity discovery, we can see the impacts of natural disasters, economic decline and political and cultural change on the output and continuation of scientific research and training. Skvortzov left China during the cultural revolution, and ended up in Sao Paulo, Brazil. While there, he published two large works in which nearly 140 taxa were described from Chinese continental (Skvortzov 1976a, b). These were to be his last works on the topic of continental diatoms from China while he was alive. His collections have never been found (See Williams et al. 2016). Despite his death, and the uncertainty regarding his collections, Skvortzov's legacy lives on with the works of his students, especially Professor Bao (who is currently in Harbin) and Professor Qi (who is currently in Guangzhou), both of whom are officially retired, as well as Professor Zhang, previously of Jinan University in Guangzhou (now deceased). All of these scientists ended up forming collaborations with scientists in the USA, with C.W. Reimer at the Academy of Natural Sciences of Philadelphia (who visited Harbin and hosted Bao, Qi and Zhang in Philadelphia) and E.F. Stoermer at the University of Michigan. Professor Qi visited Reimer at the Academy in Philadelphia while attending the International Diatom Symposium there in 1982 and stayed with Stoermer at his home in Ann Arbor, while on an extended trip to the USA in 1984. These connections yielded published collaborative works (Qi et al. 1984;Stoermer et al. 1986;Bao and Reimer 1992).

Number of
In the latter part of the 20 th century, we see important floristic works being published on the diatoms from Tibet, Yunnan and other localities, and some emphasis on freshwater fossil diatoms by Chinese researchers. In these books and papers, a new generation of scientists had come on the scene, and there was the initiation of an important series focused on documenting the freshwater diatom flora of the country ("Flora Algarum Sinicarum Aquae Dulcis" Qi 1995; Qi and Li 2004;Li and Qi 2010;Shi 2004Shi , 2013.
There is also great geographic breadth represented in these studies, with taxa being described in the northwestern portion of the country, Tibet and Yunnan, across the biodiverse regions of the karst belt extending from Yunnan to Guizhou, the central part of China, and from Hainan to the extreme Northeast.
Since 2000, there have been floristic studies that have yielded description of new taxa, such as Zhu and Chen's (2000) tome on the diatoms of Tibet, as well as revisionary work, such as Shi's (2004) study on gomphonemoid diatoms. While these were published in Chinese, the trend has been in more recent years for works to be published in English-language journals, such as Phytotaxa, Phycologia, Fottea, Cryptogamie: Algologie, Nova Hedwigia, and Diatom Research. Some research continues to be published in several Chinese-language journals as well.
In 2012, Kulikovskiy et al. included a paper offered by Gololobova and Kulikovskiy where they traced a manuscript submitted in the 1960's by Skvortzov to Dr. Proschkina-Lavrenko in Moscow for publication. but the paper was, for unknown reasons, never published. In this paper, which has been published in the 23 rd volume of Iconographia Diatomologica, Skvortzov presents 445 taxa, that represent either new names, transfers or new taxon descriptions. This work includes taxa from India, China, Philippines, Japan, Korea, Australia and even Cuba. For the purposes of the current work, 208 of the taxa were newly described from China, and recorded for the year of publication (2012) even though the work was submitted 4 decades previously. These new taxon descriptions were not validly published (they lacked designation of type specimens) but are included here since they represent the identification and publication of new taxa in China. In total, since 2000, the 421 described taxa were included in nearly 100 published books and papers (Table 2), nearly twice the number of publications than was published in the preceding 150 years. In some of the recent studies, observations have verified the continued presence of endemics described in earlier works (e.g. Gomphonema eminens Skuja in Yunnan; Liu et al. 2020; several species of Pinnularia from the Great A'er Mountains; Liu et al. 2018; and species of centric diatoms from Yunnan), though the population sizes of these endemic taxa are reported to be declining (Li et al. 2012b).
The degree of collaboration between Chinese researchers within and between institutions, and the inclusion of students in these works, are both striking and a demonstration that this area of research will have a fruitful period of work ahead. Amongst the senior and corresponding authors of these papers we see the impact of Skvortzov, whose academic grandchildren and great-grandchildren working on freshwater diatoms are now in Shanghai, Taiyuan, and Harbin. There are also well-established labs in Beijing, Shanghai, Kunming, Nanjing, and Jishou, whose focus may include the study of ecological and palaeoecological interpretation, as well as biodiversity discovery and description. Collaborations with non-Chinese scientists is also hallmark of this most recent era, with partners joining in these works from the U.K., Spain, Macedonia, Germany, Luxembourg, Belgium, Canada, and the USA.

Discussion: A look ahead
While there has been a tremendous amount of work done to document the freshwater diatom flora of China, there are still many areas across the country that await initial or additional in-depth study. Some of these areas include, Yunnan Province, the vast karst region across Yunnan/Guangxi/Guizhou provinces, the subtropical southern part of the country, Xinjiang Autonomous Region, and Tibet, to name a few. In these regions are the two biodiversity hotspots the are fully in China (Myers et al. 2000;CEPF 2019). Also, the two longest rivers in China, The Yangtze River and Yellow River, have had isolated studies, but not comprehensive analyses. There exist specialized habitats such as also high mountain ranges, waterfalls, and hot springs, to name a few, where more intensive studies are warranted.
Perhaps one of the most challenging projects, with the potential of having the least "impact" (in the way most universities or state labs would assess that notion), but the greatest impact on the discipline, would be the typification of the diatom taxa described by Skvortzov. With the location of his collection uncertain (several generations of curators have attempted to track the collection to universities and institutes in China, Russia, Brazil, and Scandanavia), it seems likely that the collection has been lost. The challenge would not only be the large number of taxa he described. There would be a huge challenge to find specimens to designate as neotypes for his taxa, or to designate illustrations of his as epitypes. If neotypification was chosen, it would present many challenges, especially in situations where several varieties or forms were dissected from the same species, or for the large number of taxa described in his 1976 and 2012 papers, where the illustrations are of a quality that might not facilitate making positive identifications. It also appears that the collections of Chen and Zhu have been lost, and typification of their taxa will also be an important activity for taxonomists.
The loss of several important collections in China is not restricted to that country. Collections have been discarded by many universities and research institutes across the world. Currently, China does not have a national diatom collection. Such a repository might be useful in the future, as the significant, current activities of collection-building and biodiversity discovery and description, which appears to still be in a log growth phase (see Fig. 1). The fate of the collections that have been established and blossomed in a single generation in Shanghai, Harbin, Taiyuan, Beijing and other labs will always be tenuous. Having a national collection would potentially provide a repository for the country to serve future generations of scientists.
Although there is tremendous described diversity in the continental diatom flora of China, and it is likely that there is still much to do to achieve a more comprehensive knowledge of that flora, the number of strains of continental diatoms in GenBank traceable to a source in China is modest. In fact, this is all the more surprising since some groups of continental diatoms have a tremendous diversity in China, and some endemic genera in Asia have representatives in the Chinese flora (Kociolek 2019). Some of these groups include the Thalassiosiraceae and Cymbellales. In the latter group, the only endemic genera known for that lineage worldwide are from Asia and include species from China (e.g. Zhang et al. 2018). Workflows and resources will need to be developed so that the number of molecular sequences generated from Chinese taxa are commensurate with the diversity and unique nature of the flora. Gong  Compere (Bacillariophyta) from China, with reference to the fine structure of their valvocopula. Cryptogamie. Algologie 40 (11) Skvortzov (1896Skvortzov ( -1980