Abstract
A survey and analysis of fungal taxa introduced over seven decades is presented. The numbers of introduced taxa were collated from ten editions of the Dictionary of the Fungi as well as from the Index of Fungi. In total, around 9100 genera and 108,000 species had been introduced by 2014. Between 1943 and 2008, the average numbers of introduced novel genera increased annually by 73 and species by 950. However, between 2008 and 2012, the average numbers of introduced novel genera increased annually by 110 and species by 1430. There were 1203 novel genera and 16,912 novel species described between 2001 and 2012, with an average of 100 new genera and 1397 new species published annually during the period. Advances in molecular techniques have accelerated the discovery of novel taxa; it therefore seems likely that many more novel taxa will be described in the future. Between 2001 and 2012, 1529 novel species were described from China, accounting for 9.2 % of all novel species descriptions worldwide. Around 17,000 fungal species had been recorded in China by 2014 with 5700 basidiomycete species, and 6700 species from important fungal groups being documented in Flora Fungorum Sinicorum with detailed descriptions, microscopic drawings and lists of voucher collections. An overview of studies on fungal diversity in China is presented.
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Introduction
According to the ratio of vascular plants and fungi in different regions, Hawksworth (1991) conservatively estimated that there were 1,500,000 fungal species worldwide, with about 69,000 species known at that time. Two decades later, with 97,861 known species, fungal species numbers were estimated to be as high as 5,100,000 (Blackwell 2011). However, the number currently accepted by many mycologists is between 1,500,000 and 3,000,000 (Hawksworth 2012), with the former being an acceptable working figure. Schmit and Mueller (2007) estimated there to be at least 712,000 fungal species, explaining that this figure could be revised upwards, as more pertinent information became available.
These revised estimates partially result from an increase in specialized knowledge, made available by new techniques. For example, high-throughput sequencing of soil samples from two forest plots yielded a much higher ratio of fungi to plants than that used by Hawksworth (1991); extrapolations from this new ratio resulted in a much higher estimate of fungal species numbers (O’Brien et al. 2005). Because the number of known fungal species forms the basis of estimates (Hawksworth 1991; O’Brien et al. 2005), it is important that the known species number is precise when estimating total fungal numbers.
Although several papers have estimated global fungal species numbers (Hawksworth 1991, 2001, 2012; O’Brien et al. 2005; Schmit and Mueller 2007; Blackwell 2011), there is no documentation summarizing the numbers of fungal genera and species introduced at different times. One way to provide data for estimating the extent of fungal diversity is to add up the numbers of introduced genera and species listed in the Dictionary of the Fungi and the Index of Fungi. In this paper, we collate the taxa at the generic and species levels from the Dictionary of the Fungi, from the first edition of 1943 through to the tenth edition in 2008 (Ainsworth and Bisby 1943, 1945, 1950, 1954; Ainsworth 1961, 1971; Hawksworth et al. 1983, 1995; Kirk et al. 2001, 2008), as well as listing novel genera and species listed in Index of Fungi from 2002 to 2014 (Anonymous 2002a, b, 2003a, b, 2004a, b, 2005a, b, 2006a, b, 2007a, b, 2008a, b, 2009a, b, 2010a, b, 2011a, b, 2012a, b, 2013a, b, 2014). The Dictionary of the Fungi lists known numbers of genera and species, while the Index of Fungi provides lists that include novel genera and species published annually from 2001 to 2012. The estimated number of known fungal species at the end of 2014 is provided. In addition, data on studies of fungal diversity in China are presented.
Dynamics of introduced fungal taxa
The number of introduced fungal taxa has generally increased (Fig. 1). The number of genera increased from 3503 in 1943 to 8283 in 2008, i.e., an increase of around 73 genera annually, while the number of species increased from 36,100 in 1943 to 97,861 in 2008, corresponding to an increase of 950 annually during the period. One exception is that the number of fungal species decreases from 50,000 in 1961 to 45,000 in 1971, suggesting that 1961 was an unusual year for fungal introductions. This unusual phenomenon might be partially caused by the names of both perfect and imperfect states being simultaneously used for a single deuteromycetes species in the fifth edition of the Dictionary of the Fungi published in 1961, where one-third of 15,000 imperfect fungal species also have names of perfect states (Ainsworth 1961). The International Code of Nomenclature in 1956 sanctioned the use of different names applied to the perfect and imperfect states of a single species; however, certain names of imperfect states were excluded from Deuteromycotina in the sixth edition of the Dictionary of the Fungi (Ainsworth 1971), because the names of the perfect state take precedence. Another possible reason is that the species number was overestimated in the fifth edition of the Dictionary of the Fungi, published 1961. For example, Basidiomycetes was introduced to accommodate 15,000 species belonging to nine orders, viz. Agaricales, Hymenogastrales, Lycoperdales, Nidulariales, Phallales, Sclerodermatales, Tremellales, Uredinales and Ustilaginales, but the sum of species numbers introduced in these nine orders was actually 13,145 (Ainsworth 1961).
Ascomycetes and basidiomycetes are the main groups of Fungi, and their generic numbers increased in each edition of the Dictionary of the Fungi (Tables 1 and 2). Similar to all fungal groups, the species numbers of ascomycetes and basidiomycetes both decreased in 1971 (Tables 1 and 2). The number of ascomycetes as a percentage of all known fungi almost doubled from 1943 to 2008 (Table 1), whereas the number of basidiomycetes as a percentage of all fungi was approximately constant (Table 2).
There was an increase in the number of introduced genera (3217) and species (33,024) from 2001 to 2008, as extracted from the Dictionary of the Fungi (Fig. 1). However, according to the Index of Fungi, 654 novel genera and 9494 novel species were published during the same period (Table 3). So most of the increased genera and species in the Dictionary of the Fungi from 2001 to 2008 are not novel.
When combining the data from the tenth edition of the Dictionary of the Fungi and the Index of Fungi, the total number of fungal genera known by 2012 is 8283 + 550 (the number of novel genera reported from 2008 to 2012, Table 4) = 8833, and the total number of fungal species known by 2012 is 97,861 + 7148 (the number of novel species reported from 2008 to 2012, Table 4) = 105,009.
The numbers of novel genera introduced from 2008 to 2012 was 550 and species was 7148; around 110 genera and 1430 species were described annually during this period (Table 4). Thus, a greater number of novel genera and species were described per year between 2008 and 2012 than between 1943 and 2008. These increases can be accounted for by the large increase in investigations in tropical areas (Hawksworth 2012), and, more importantly, by the application of molecular techniques (Yang 2011; Du et al. 2012a; Dai et al. 2014; Liu et al. 2014; Wu et al. 2015; Zhou et al. 2015a), especially in the pathogenic genera (Maharachchikumbura et al. 2011, 2012; Hyde et al. 2014). High-throughput sequencing of environmental samples also indicates there are a greater number of fungi than the traditional techniques reveal (Lindahl et al. 2013; Peršoh 2015). With advanced techniques used to discover fungal diversity, the rate of introducing novel taxa could increase sharply in the future (Yang 2013).
At the time of writing, the Index of Fungi Volume 8 (issue 7), provides details of novel taxa published before 2013 (Anonymous 2014), and data on novel taxa published after this issue are not included in the data. However, we estimate the numbers of novel genera and species published in 2013 and 2014 to be around 220 and 2860, based on the average numbers of new genera and species per year, that is, 110 and 1430, respectively, from 2008 to 2012. Therefore, we estimate that by the end of 2014, the numbers of known fungal genera will be around 9100 and species to be 108,000.
Fungal diversity studies in China
Publications dealing with Chinese fungal species were systematically reviewed in 2010, by which time, 16,046 species and 297 varieties, including 300 species of Chromista and 340 of Protozoa, had been recorded in the Chinese territories (Dai and Zhuang 2010). However, 10 % of these species were synonyms; thus, the number of known Chinese fungal species was estimated to be around 14,700 (Dai and Zhuang 2010). Most of the descriptions of these species were morphology based. Recently, phylogenetic studies have demonstrated that many morphologically similar taxa might represent distinct lineages, and numerous well-known species are in fact species complexes (Li et al. 2009; Du et al. 2012a, b; Chen et al. 2015); many plant pathogen species comprise cryptic species (Hyde et al. 2009; Cui et al. 2015). Therefore, the assumption that 10 % of Chinese fungal species are synonyms is probably unrealistic and the fungal diversity in China was in fact underestimated. From 2010 to 2014, details of 912 novel species and 614 new records were introduced for China, based on Chinese materials. Given the above, by the end of 2014, the number of known Fungi in China was approximately 17,000 (16,046 − 300–340 + 912 + 614), accounting for approximately 16 % of known species worldwide. Among the 17,000 Chinese species, around 5700 species, accounting for around 33.7 % of the total, are basidiomycetes; this ratio is almost the same as that found globally in 2008 (32.2 %, Table 2). A total of 50 volumes of Flora Fungorum Sinicorum have been published, and 6700 species were documented with detailed descriptions, drawings of microscopy and lists of voucher collections (Table 5).
There are many universities and institutes working on fungal diversity in China. Among them, the State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences (HMAS), Kunming Institute of Botany, Chinese Academy of Sciences (HKAS), Institute of Applied Ecology, Chinese Academy of Sciences (IFP), Guizhou Academy of Agricultural Science, Beijing Academy of Agriculture and Forestry Sciences, Beijing Forestry University (BJFC), Jilin Agricultural University (HMJAU), Guangdong Institute of Microbiology (GDGM), Shandong Agricultural University (SDAU), Guizhou University (GACP), Hunan Normal University (HNNU), Shanxi University (SXU), Capital Normal University (BJTC), Anhui Agricultural University (AAUB), Yunnan University (PYU), Qingdao Agricultural University (LYAC), and National Museum of Natural Science in Taichung (TNM) have made major contributions to the understanding of the diversity of Fungi in China, and their herbaria (acronyms given in brackets after host names) conserve most of available Chinese fungal collections and cultures. The University of Hong Kong previously had an active research group, but this was not continued when K.D. Hyde retired and the herbarium at the university, HKU (M), was moved to IFRDC in Kunming (Chen et al. 2010).
Mycosystema, the first official journal of the Mycological Society of China (MSC), was first published quarterly in 1982 as Acta Mycologica Sinica, and then bimonthly since 2008. This journal accepts both Chinese and English papers. Mycosystema paper numbers increased from 48 in 1983 to 136 in 2014. Moreover, the Journal of Fungal Research in 2002 and Mycology—an International Journal on Fungal Biology in 2010 are published by MSC; the latter is an exclusively English journal. The English language journal Fungal Diversity, with a good reputation worldwide, also became the journal of Kunming Institute of Botany, Chinese Academy of Sciences in 2011, while Mycosphere has recently become the journal of Guizhou Academy of Agricultural Science. In addition, studies on fungal diversity and related studies are scattered in other journals, such as Fungal Science, Acta Edulis Fungi, Edible and Medicinal Mushrooms and Edible Fungi of China. These journals play an essential role in reporting the advances in fungal diversity research in China. In addition, Fungal Names (http://www.fungalinfo.net/fungalname/fungalname.html), one of the three repositories for new fungal names, is located in China. This database together with the Chinese version of MycoBank (http://cn.mycobank.org/) indicate the importance of the Chinese contribution to fungal biodiversity.
Compared to other countries, the Chinese government has increased funding for exploring fungal diversity in recent years. For example, the National Natural Science Foundation of China provided 25,280,000 RMB for 36 projects in 2012, while the numbers were 240,000 RMB for two projects in 1999; the funds increased more than 100 times in 13 years.
More and more new taxa have been described from China, and there were almost twice as many newly introduced species in 2014 (208) as in 2004 (109). Accordingly, many more publications reporting on Chinese fungal diversity have been published in recent years. For example, around 210 papers related to fungal diversity research were published from 1950 to 1980, with most being published in the Chinese journals, while the number in 2014 was not less than 220, with more than half published in the international journals (Table 6).
With the accumulation of knowledge of fungal diversity, other research fields have also benefitted. Thirty-seven species, most belonging to Mucorales, are aetiological agents of rhino-orbital-cerebral mycosis (Li et al. 2014); 24 are involved in cerebral phaeohyphomycosis, and most are from Chaetothyriales (Li and de Hoog 2009). The identification of aetiological agents is important for treatment of disease. Grape is one of the most important agricultural crops in China, but yields may be affected by grape disease. Anthracnose is a serious disease of grapes caused by Colletotrichum Corda species and has been reported by Yan et al. (2013, 2015). Other grape diseases have also been surveyed and published, and these data may help in disease control (Dissanayake et al. 2015; Jayawardena et al. 2015). Dai et al. (2007) recorded 102 potential forest pathogens as a result of field surveys throughout China, which are important for protection of forest resources. The genus Amanita Pers. comprises valued edible mushrooms, but also deadly poisonous species, and their morphological delimitation is ambiguous even for specialists (Yang 2005b); thus, several poisoning cases caused by lethal amanitas occur annually (Chen et al. 2014). Cai et al. (2014) identified the diversity and found some cryptic species of lethal amanitas, which undoubtedly helps to reduce cases of fungal poisoning. The true morels (Morchella Dill. ex Pers.) are prized edible mushrooms, which are delicious, but produce small amounts of fruiting bodies. Du et al. (2012a) elucidated the phylogeny of Morchella and identified several new lineages from China. This information will be helpful in advancing morel conservation and commercial harvests. Zhou et al. (2015a, b) clarified the global diversity of two important medicinal fungal complexes, ‘sanghuang’ and ‘lingzhi’, and provided insights for further utilization of these genera of medicinal mushrooms.
More than 1800 macrofungal resources, including many edible and medicinal species, were recently documented for China, with colour photographs and descriptions (Li et al. 2015), and many have the potential to be cultivated (Thawthong et al. 2014). Around 20 species have been commercially cultivated in China, and the Chinese production of edible mushrooms in 2013 is about 32 million tons, which accounted for more than 75 % of the world production; the direct product value is 170.7 billion RMB (=28 billion $). The most important cultivated species are Agaricus bisporus (J.E. Lange) Imbach, Agrocybe cylindracea (DC.) Maire, Auricularia cornea Ehrenb., A. heimuer F. Wu, B.K. Cui & Y.C. Dai, Coprinus comatus (O.F. Müll.) Pers., Flammulina velutipes (Curtis) Singer, Hericium erinaceus (Bull.) Pers., Lentinula edodes (Berk.) Pegler, Pholiota microspora (Berk.) Sacc., Pleurotus eryngii (DC.) Quél., P. eryngii var. tuoliensis C.J. Mou, P. ostreatus (Jacq.) P. Kumm., Tremella fuciformis Berk. and Volvariella volvacea (Bull.) Singer (Zhang et al. 2015). Among 540 medicinal fungi recorded from China (Dai et al. 2009), the most important species are Ganoderma lingzhi Sheng H. Wu, Y. Cao & Y.C. Dai, Ophiocordyceps sinensis (Berk.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora and Taiwanofungus camphoratus (M. Zang & C.H. Su) Sheng H. Wu, Z.H. Yu, Y.C. Dai & C.H. Su, and the biogeographical centre of these species is in East Asia (Wu et al. 2004; Cao et al. 2012; Zhang et al. 2013).
Although having contributed to the understanding of global diversity of Fungi, Chinese mycologists have much work to do. China possesses large land areas, with numerous ecological niches, where almost all fungal groups can be found (Yang 2005a). However, many of these niches have been poorly or never studied. Many groups of fungi, such as the Ascomycota, have also been poorly investigated, and studies will likely result in the discovery of numerous new taxa. There is a strong need to explore unique ecological niches to fully understand Chinese fungal diversity and utilize these resources. For some hotspots of biodiversity, certain groups of fungi might be extensively surveyed, but a joint field trip for collecting most, or all, fungal groups would be better to understand fungal diversity in a special ecological region. Funding for such joint surveys has been initiated by National Science and Technology Foundation Project, now focusing on the Qinghai-Tibet Plateau and the Xinjiang Region, Greater and Lesser Khingan Mountains, and Karst regions in southwestern China. We can expect further contributions from China that will help to improve the understanding of fungal diversity worldwide, with the efforts of Chinese mycologists and Chinese government financial support.
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Acknowledgments
Kevin D. Hyde thanks the Chinese Academy of Sciences, project number 2013T2S0030, for the award of Visiting Professorship for Senior International Scientists at Kunming Institute of Botany.
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Dai, YC., Cui, BK., Si, J. et al. Dynamics of the worldwide number of fungi with emphasis on fungal diversity in China. Mycol Progress 14, 62 (2015). https://doi.org/10.1007/s11557-015-1084-5
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DOI: https://doi.org/10.1007/s11557-015-1084-5