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An overview on the nomenclatural and phylogenetic problems of native Asian brine shrimps of the genus Artemia Leach, 1819 (Crustacea, Anostraca)
expand article infoAlireza Asem§, Amin Eimanifar|, Nasrullah Rastegar-Pouyani, Francisco Hontoria#, Stephanie De Vos¤, Gilbert Van Stappen¤, Shi-Chun Sun
‡ Ocean University of China, Qingdao, China
§ Hainan Tropical Ocean University, Sanya, China
| Unaffiliated, Maryland, United States of America
¶ Razi University, Kermanshah, Iran
# Instituto de Acuicultura de Torre de la Sal, Castellón, Spain
¤ Ghent University, Gent, Belgium
Open Access

Abstract

The genus Artemia Leach, 1819 is a cosmopolitan halophilic crustacean, consisting of bisexual species and obligate parthenogenetic populations. Asia is rich in Artemia biodiversity. More than 530 Artemia sites have been recorded from this area and more than 20 species/subspecies/variety names have been used for them. There exist various problems in the nomenclature, identification, and phylogenetic status of Artemia native to Asia, which are discussed in this paper.

Keywords

Artemia, phylogeny, nomenclature, taxonomy, Asia

The brine shrimp Artemia Leach, 1819 is a halophilic zooplankton, distributed in saline habitats worldwide, with the exception of Antarctica (Van Stappen 2002). The genus consists of several bisexual species and a large number of polyphyletic obligate parthenogenetic populations including di-, tri-, tetra-, and pentaploid (Asem et al. 2016). Asia is rich in Artemia biodiversity, where more than 530 Artemia sites have been recorded (count based on Walter 1888; Sars 1901; Bond 1934; Van Stappen 2002; John et al. 2004; Mura and Nagorskaya 2005; Abatzopoulos et al. 2006; Shadrin and Anufriieva 2012; Salman et al. 2012; Vikas et al. 2012; Zheng and Sun 2013; Naganawa and Mura 2017). Many of the sites are now inhabited by the invasive species Artemia franciscana Kellogg, 1906 (in some cases, co-existing with other bisexual species or parthenogenetic populations), whose identification were mostly confirmed by molecular analyses (e.g., Van Stappen et al. 2007; Vikas et al. 2012; Eimanifar et al. 2014). For Artemia native to Asia, more than 20 binomial/trinomial names have been used by different authors (see below). Several problems emerged in the past related to the nomenclature, identification or the phylogenetic status of Artemia species. Some of these issues have found a solution and scientific consensus, whereas others still persist.

As far as we are aware, 14 binomens (including the one questionably reported as a species of Branchinecta Verrill, 1869) and nine trinomens, as well as unidentified species/subspecies/varieties, have appeared in the form of scientific names (combined with a genus name and typeset in italics) in literature relating to native Asian brine shrimps. As shown in Table 1, almost all of the names have some kind of nomenclatural problem. Among the 13 binomens proposed for Artemia, eleven fulfil the availability requirements of International Code of Zoological Nomenclature (ICZN, 4th edition) and are considered to be available species names [Artemia salina (Linnaeus, 1758); Artemia asiatica Walter, 1887; Artemia urmiana Günther, 1899; Artemia parthenogenetica Bowen & Sterling, 1978; Artemia sinica Cai, 1989; Artemia barkolica Qian and Wang in Qian et al. 1992; Artemia urumuqinica Qian and Wang in Qian et al. 1992; Artemia ebinurica Qian and Wang in Qian et al. 1992; Artemia tibetiana Abatzopoulos, Zhang & Sorgeloos, 1998; Artemia frameshifta Naganawa & Mura, 2017; Artemia murae Naganawa in Naganawa and Mura 2017], and the other two are unavailable [Artemia kazakhastan Vikas et al., 2012; Artemia china Vikas et al., 2012]. Branchinecta orientalis Sars, 1901 sensu Chiang, 1983 is supposed to be a misuse for brine shrimp (vide post). Three trinomens (Artemia sinica sinica Cai, 1989; Artemia sinica tibetiana Abatzopoulos, Zhang & Sorgeloos, 1998; Artemia salina arietina Fischer, 1851) are available subspecies names, with all their subspecific names first proposed as (available) specific names. The other six trinomens are unavailable names.

Table 1.

Names that have ever been used for native brine shrimps Artemia of Asia, their availability, information of type specimens and nomenclatural problems

Taxon names Availability Type specimens Type locality Comments and/or references
A. salina (Linnaeus, 1758) Available Not mentioned in original description Salt works at Lymington, England Linnaeus 1758
A. asiatica Walter, 1887 Available Syntypes. Number of specimens and deposit place not mentioned in original description Murgab, Tajikistan This species is known only from type locality (Walter 1887, 1888). It was considered to be a nomen dubium (Belk and Brtek 1995)
A. urmiana Günther, 1899 Available Syntypes. Number of specimens and deposit place not mentioned in original description Urmia Lake, Iran Günther 1899
A. parthenogenetica Bowen & Sterling, 1978 Available Syntypes, containing cysts from five localities. Deposit place not mentioned in original description Madras and Kutch, India; Port Hedland, Australia; Sète, France; Yamaguchi-ken, Japan Though the term “parthenogenetica” was used by earlier authors, Belk and Brtek (1995) clarified its authorship should be Bowen and Sterling (1978). Type specimens should include all specimens that Bowen and Sterling (1978) studied, and type localities include all 5 sites collecting the specimens (ICZN Articles 73.2.3, 76.1). Rogers (2013) listed this name as a nomen dubium.
A. sinica Cai, 1989 Available Syntypes, probably containing cysts and laboratory cultured adults, which are believed to have been lost (Yaneng Cai, pers. comm.) Yun Cheng Salt Lake, Shanxi, China Artemia sinica was referred to Cai (1989b) in some publications (e.g., Abatzopoulos et al. 1998; Hou et al. 2006; Van Stappen et al. 2009; Zheng and Sun 2013). However, Cai (1989a; an abridged version of Cai 1989b) has nomenclatural priority because it was published earlier (January 1989) than Cai (1989b; spring and fall 1989 / mailed 17 July 1990). Cai (1989a) described only the morphology of adults, but according to Cai (1989b), the type series of this species might contain cysts and laboratory cultured adults (ICZN Article 72.4)
A. barkolica Qian & Wang in Qian et al. 1992 Available “Holotypes” 5♀♀, 5♂♂; paratypes 56♀♀, 4♂♂. Deposited at Xinjiang August First Agricultural College (now Xinjiang Agricultural University), Xinjiang, China Barkol Lake, Xinjiang, China Multiple specimens were designated as ‘holotype’ in the original description (Qian et al. 1992). All type specimens may be regarded as syntypes, with original authors’ “holotypes” having the priority in designating as a lectotype when necessary
A. urumuqinica Qian & Wang in Qian et al. 1992 Available “Holotypes” 5♀♀; paratypes 60♀♀. Deposited at Xinjiang Agricultural University Urumqi Caiwuo Pu Yan Hu (= Dabancheng Salt Lake / Dabancheng Dong Salt Lake), Xinjiang, China Ibid
A. ebinurica Qian & Wang in Qian et al. 1992 Available “Holotypes” 6♀♀, 2♂♂; paratypes 60♀♀. Deposited at Xinjiang Agricultural University Ebinur (=Aibi Lake used in many publications), Xinjiang, China Ibid
A. tibetiana Abatzopoulos, Zhang & Sorgeloos, 1998 Available Syntypes, probably consisting of cysts (two batches collected in different time), nauplii and adults. Deposit place not mentioned in original description Lagkor Co, Tibet, China Abatzopoulos et al. (1998) studied adults, nauplii and cysts, all should be components of type series (ICZN Article 72.4). Later studies showed Lagkor Co population was a mixture of bisexual and parthenogenetic Artemia (Van Stappen et al. 2003; Maccari et al. 2013). So the type series may contain specimens of more than one species, given that samples studied by Abatzopoulos et al. (1998) were not contaminated after collection and parthenogens were not introduced to the lake after harvesting of type samples
A. kazakhastan Vikas et al. 2012 Unavailable N/A N/A This name appeared in Vikas et al. (2012: 135, 138) in the form of binomen, which seemed to refer to “Artemia sp. Kazakhstan” mentioned in the same paper. It is obvious that the authors did not intend to establish any new taxa, therefore is unavailable (ICZN Article 16)
A. china Vikas et al. 2012 Unavailable N/A N/A Same as the last name, but this name seemed to refer to “Artemia sp. China” (Kyêbxang Co population)
A. frameshifta Naganawa & Mura, 2017 Available Holotype ♀; Deposited at Kyoto University Museum Bajan-Onjul, Tov aimag, Mongolia Naganawa and Mura 2017
A. murae Naganawa in Naganawa & Mura, 2017 Available Holotype ♂; allotype ♀. Deposited at Kyoto University Museum Tonkhil nuur (Tonkhil Lake), Gobi-Altai, Mongolia In addition to the type specimens, Naganawa and Mura (2017) observed 232 other specimens including 124 ♂♂ and 108 ♀♀
? Branchinecta orientalis Sars, 1901 sensu Chiang, 1983 N/A N/A N/A Sars (1901) described this anostracan based on specimens from Lake Chuntu-nor, Dornod, Mongolia. Chiang’s (1983) record from Kyêbxang Co, Tibet, China might be Artemia (see text)
A. urmiana parthenogenetica Barigozzi, 1980 non A. parthenogenetica Bowen & Sterling, 1978 Unavailable N/A N/A Barigozzi (1980) used this trinomen as an example to discuss the nomenclature of parthenogenetic Artemia. It is unavailable because of no description or diagnosis (ICZN Article 13)
A. parthenogenetica urmiana Barigozzi, 1980 non A. urmiana Günther, 1899 Unavailable N/A N/A Ibid
A. sinica sinica Cai, 1989 See A. sinica See A. sinica See A. sinica Zhou et al. (2003b)
A. sinica tibetiana Abatzopoulos, Zhang & Sorgeloos, 1998 See A. tibetiana See A. tibetiana See A. tibetiana Zhou et al. (2003b)
A. sinica jingyuhuensis Yin, Zhang & You, 2013 Unavailable N/A N/A Referring to the bisexual population from Jingyu Lake, Xinjiang, China, this name appeared first in the MSc degree thesis of Zhou (2001), and then in Yin et al. (2013). The former was an unpublished work, the later did not describe it as a new taxon and designate name-bearing type(s), thus the name is unavailable (ICZN Articles 13 and 16)
A. sinica xiaochaidanensis Yin, Zhang & You, 2013 Unavailable N/A N/A Same as the last name, but referring to the bisexual population from Xiao Qaidam Lake, Qinghai, China
A. sinica gahaiensis Yin, Zhang & You, 2013 Unavailable N/A N/A Yin et al. (2013) used this name for the parthenogenetic Artemia population from Ga Hai, Qinghai, China. It is unavailable because these authors did not describe it as a new taxon and designate name-bearing type(s) (ICZN Articles 13 and 16)
A. sinica aibihuensis Yin, Zhang & You, 2013 Unavailable N/A N/A Same as the last name, but referring to the parthenogenetic Artemia population from Ebinur, Xinjiang, China
A. salina var. arietina Fischer, 1851 Available Syntypes, including several specimens. Deposit place not mentioned in original description Odessa, Ukraine Fischer (1851) described Artemia arietina, which might be bisexual because both sexes were mentioned. The name is now thought to be a nomen dubium (Belk and Brtek 1995). Gurney (1921) reported the Amara (Iraq) population as A. salina var. arietina
Artemia sp. N/A N/A N/A Many Asian Artemia populations were reported as Artemia sp.
Artemia s. subsp. (=A. sinica subsp.) N/A N/A N/A Yin et al. (2011) reported the Artemia from Jingyu Lake (Xinjiang, China) and Xiao Qaidam Lake (Qinghai, China) as A. s. subsp.
A. salina var. N/A N/A N/A Walter (1888) reported Molla-kary population (Turkmenistan) as “Artemia salina L. var.” and considered it a variety between A. salina and Artemia milhausenii (Fischer, 1834) [“in die Reihe der von Artemia salina L. (Milne Edw.) zur Artemia milhausenii Fisch.”]. The name A. milhausenii was established for Artemia from Crimmea (Fischer, 1834) and is now considered a nomen dubium or nomen nodum (Belk and Brtek 1995; Rogers 2013)

Many Asian Artemia populations were reported as A. salina in earlier publications but most of these records were later revealed to be parthenogenetic Artemia, A. tibetiana, A. sinica or unidentified bisexual populations (Mura and Nagorskaya 2005; Salman et al. 2012; Shadrin and Anufriieva 2012; Zheng and Sun 2013; Eimanifar et al. 2014; Litvinenko et al. 2016). Even so, the inadequate use of the name still appeared in very recent papers, e.g., Alas et al. (2017) identified the Salt Lake (= Tuz Lake, Turkey) population as A. salina although they have been aware that Başbuğ (1999) already documented the population reproducing parthenogenetically.

Padhye and Lazo-Wasem (2018) indicated that the Sambhar Lake (Rajasthan, India) population was a valid report of A. salina, whereas the several hundred specimens from this lake at the Indian Museum seem to be all females (Belk and Esparza 1995). Confirmed distribution of this species in Asian countries is restricted to Cyprus, an island in the eastern Mediterranean (Baxevanis et al. 2006).

Bond (1934) reported A. salina from Tso Kar, Ladakh, Jammu & Kashmir. Padhye and Lazo-Wasem (2018) studied Bond’s specimens deposited in the Yale Peabody Natural History Museum, and referred them as an Artemia sp. that is morphologically close to A. sinica. However, this study made a mistake in citing literature and erroneously stated that A. tibetiana does not have a basal spine on the male gonopod, even though it is well developed in this species (Mura and Brecciaroli 2004; Zheng and Sun 2008). Given that Tso Kar is closer to the sites of A. tibetiana (than those of A. sinica), and that they live in similar high altitude habitats, this population awaits a (molecular) comparison with A. tibetiana, as well as with other bisexual phylogenetic lineages from adjacent areas such as the “Kazakhstan” and “Kyêbxang Co” population (vide post).

Two varieties of A. salina were reported from Asia. Gurney (1921) identified the Amara (Iraq) population as Artemia salina var. arietina Fischer 1851. Since the Amara population is parthenogenetic (Salman et al. 2012), the population is by no means assignable to A. salina. Walter (1888) identified his specimens from Molla-kary (Turkmenistan) as “Artemia salina L. var.” and thought it to be a variety between A. salina and Artemia milhausenii (Fischer, 1834). Because Walter’s specimens contained only females, the Molla-kary population may also be parthenogenetic and is not assignable to any bisexual species.

Artemia urmiana was originally described as a bisexual species based on specimens from Urmia Lake, Iran (Günther 1899), but Barigozzi and Baratelli (1989) documented that all samples collected from Urmia Lake in 1987 were parthenogenetic and contained di-, tetra-, and pentaploid individuals. Azari Takami (1989) reported that bisexual and parthenogenetic populations coexisted in the Lake. Agh et al. (2007) concluded that parthenogenetic samples had likely been collected from lagoons neighbouring Urmia Lake or its coastal areas, whereas bisexual A. urmiana dominated in the main body of the lake. However, a later study documented the existence of parthenogenetic populations in both the lagoons and the main body of Urmia Lake, with significant morphometric differentiation (Asem et al. 2009). In addition to Iran, several populations in Altai (Russia) may belong to this species (Shadrin and Anufriieva 2012), Turkey and Turkmenistan (Eimanifar et al. 2014). The record of this species from Basrah (Iraq) should be A. franciscana (see Salman et al. 2012). Outside Asia, Abatzopoulos et al. (2009) identified A. urmiana from Lake Koyashskoe (Crimea). Another study based on sequence variation of the mitochondrial COI marker suggested the occurrence of A. urmiana in Bulgaria, China, Greece, Crimea, Turkey, and Turkmenistan (Eimanifar et al. 2015). However, these populations need to be further explored with special emphases on the status of reproductive mode (bisexual or parthenogenetic) to confirm the coexistence of A. urmiana and parthenogenetic populations in these localities or/and existence of shared COI haplotype(s) between A. urmiana and parthenogenetic gene pools.

For two decades, Tibetan bisexual populations have been considered as belonging to a single species, A. tibetiana, originally described as a bisexual species from Lagkor Co, Tibet, China (Abatzopoulos et al. 1998). However, as that in Urmia Lake, a parthenogenetic population was also documented from this lake (Van Stappen et al. 2003; Maccari et al. 2013; see Table 1). Wang et al. (2008) documented four Tibetan bisexual populations clustering in two different clades using the mitochondrial COI marker, with one clade only hosting the type locality population (Lagkor Co) and a second distinct clade hosting the others (Kyêbxang Co (=Qixiang Lake or Qi Xiang Cuo), Nima, and Yangnapeng Co). Two other studies have shown that the Tibetan populations clustered in two different groups in a phylogenetic tree based on the COI marker, while all of them represented a single clade based on the nuclear marker ITS1 (Maccari et al. 2013; Eimanifar et al. 2014). Thus, the taxonomic status of these populations awaits to be clarified by future investigations. Chiang (1983) reported Branchinecta orientalis from Kyêbxang Co, whereas later studies showed that the anostracan in this lake was Artemia (e.g., Zhou et al. 2003a, 2003b; Hou et al. 2006; Yu and Xin 2006; Wang et al. 2008). We suppose that Chiang (1983) might have confused his specimens (no Tb-76-2012) for two reasons: 1) Chiang (1983: 451) reported the altitude of the lake as 4740 m, while it was listed as 4660 m in the chapter “General Account” of the same book (Chiang et al. 1983: 29); and 2) during the time (1976) he collected specimens, the salinity of this lake was as high as 63.27 g/L (Zheng et al. 2002), salinity that is not suitable for B. orientalis.

The validity of Artemia sinica, described based on specimens from Yuncheng Salt Lake, China (Cai 1989a) has rarely been questioned, and nearly 30 bisexual populations from China (see review of Zheng and Sun 2013), and several populations from Russia (Shadrin and Anufriieva 2012; Litvinenko et al. 2016), and Mongolia (Gajardo and Beardmore 2012; Eimanifar et al. 2014) have been identified as this species so far. The molecular clock divergence analysis indicated that A. sinica had already diverged in the late Miocene (19.99 Mya), whereas A. urmiana, A. tibetiana, and “Eurasian Haplotype Complex” (EHC refer to group of parthenogenetic Artemia lineages) shared a common ancestor in the late Pliocene (5.41 Mya) (Eimanifar et al. 2015).

Another controversial topic in taxonomy of Artemia relates to a batch of bisexual Artemia cysts from Kazakhstan (KAZ; ARC no. 1039), supplied by Catvis Co. (s-Hertogenbosch, The Netherlands) in 1988. However, no information about the exact origin(s) of the sample (Pilla and Beardmore 1994; Ben Cattel, pers. comm. 2017) was provided. An earlier study documented morphological differentiations between this bisexual sample and other Asian species (Pilla and Beardmore 1994). In molecular analyses, this population was located in a separate phylogenetic clade in the mitochondrial COI tree (Maccari et al. 2013), but was clustered together with A. urmiana and A. tibetiana using ITS1 nuclear marker (Vikas et al. 2012). Under these circumstances, the systematic position and geographical origin of this sample remains a source of debate. So far only one site, the salt lake Margen-sor (district of Atbassar), was reported to be inhabited by bisexual Artemia in Kazakhstan (Sars 1901: reported as A. salina). Future sampling in Margen-sor may help to elucidate if KAZ and the Margen-sor population belong to the same species/lineage.

Qian et al. (1992) described three species based on specimens from three different salt lakes in Xinjiang, China, namely Artemia barkolica Qian & Wang, 1992, Artemia urumuqinica Qian & Wang, 1992 and Artemia ebinurica Qian & Wang, 1992 (Table 1). Except for 12 papers in the special Chinese-language issue “Studies on Artemia of Barkol Lake” (Journal of August 1st Agriculture College, 1994, Vol. 17 no. 2) and Qian et al. (1993), which used the names A. barkolica and A. urumuqinica, respectively, these three species have not been recognised by other researchers. As commented by Zheng and Sun (2013), the very biased sex ratios in the original description, as well as the results of many other studies, have indicated that all three populations were parthenogenetic. Since all these populations consist of strains of different ploidies (for reference review see Zheng and Sun 2013), and diploid/triploids and tetraploid/pentaploids are assumed to have originated separately (Maniatsi et al. 2011; Asem et al. 2016); each of the three nominal species may represent more than one phylogenetic clade (or species) or they may be synonyms.

Recently, in Mongolia, two new species have been described: A. frameshifta and A. murae (see Naganawa and Mura 2017). These species have been described using primary morphological characters and a single COI sequence, whereas morphometric differentiation and population genetic analysis have not been studied. Although both species were said to reproduce bisexually in the original descriptions, males have not been observed in A. frameshifta. Considering the ‘sex ratio’ (125 males and 109 females were observed), phylogenetic position (sister to A. sinica) and genetic distance (p-distance between A. murae and A. sinica is 4.8%) (Naganawa and Mura 2017), A. murae may represent a lineage close to A. sinica. Moreover, no sequences of parthenogenetic Artemia were included in the phylogenetic analysis of Naganawa and Mura (2017). Therefore, the taxonomic status of these species also needs to be re-confirmed by future multidisciplinary studies on their biology and phylogeny.

Artemia asiatica was described according to only female specimens from Murgab, Tadjikistan (Walter 1887). It may be a parthenogenetic population, and the name is now treated as a nomen dubium (Belk and Brtek 1995).

Theoretically, the ability of interfertility and producing offspring able to reproduce is a common criterion to confirm subspecies status (Mayr 1969). In nature however, subspecies populations mostly have an allopatric distribution. Due to geographical isolation, proof of natural interbreeding is practically impossible except in rare cases. The results of cross-breeding tests with different Asian bisexual Artemia were inconsistent among different studies. Pilla and Beardmore (1994) documented complete interfertility among Artemia sp. (the KAZ sample), A. urmiana, and A. sinica. Zhou et al. (2003b) showed interfertility between A. sinica and A. tibetiana, and considered them as subspecies (Artemia sinica sinica and Artemia sinica tibetiana). In other studies, however, an isolating barrier was found between A. urmiana and A. sinica (see Zheng and Sun 2008), and between A. sinica and A. tibetiana (see Abatzopoulos et al. 2002b; Zheng and Sun 2008). Due to the possible effect of laboratory rearing conditions (ionic composition of the medium, salinity and temperature) on the reproductive potential of Artemia (Abatzopoulos et al. 2003; Velasco et al. 2016, 2018), it seems that a fertility test is not suitable as a single biological tool to determine Artemia population/species ranks. Although reproductive isolation in captivity/laboratory circumstances might refer to a lack of gene flow in nature, laboratory cross-fertility even for F1 and later generations cannot evidence that such cross-fertility would occur under natural conditions if there is no hybrid zone (Helbig et al. 2002).

Two other bisexual populations, the Jingyu Lake (Xinjiang, China) population and the Xiao Qaidam Lake (Qinghai, China) population, were considered to represent different subspecies of A. sinica. The subspecies names Artemia sinica jingyuhuensis Yin, Zhang & You, 2013 and Artemia sinica xiaochaidanensis Yin, Zhang & You, 2013 were proposed for them, respectively, though they are not available (Table 1). Zheng and Sun (2008) documented some morphological differences between Jingyu Lake and Lagkor Co populations though they identified the former population as A. tibetiana. In phylogenetic analyses the Jingyu Lake population located in a clade containing A. tibetiana (Wang et al. 2008; Yin et al. 2011, 2013), while the Xiao Qaidam Lake population is clustered together with A. sinica (Yin et al. 2011, 2013).

In addition, there are also a number of allegedly bisexual populations, generally based on visual observation and personal communication, in Asian saline habitats, especially in Siberia and China, which have not been identified to any nominal species (Van Stappen et al. 2009; Zheng and Sun 2013). The phylogenetic status of these populations still needs to be determined.

The nomenclatural and taxonomic status of Artemia parthenogenetica have been discussed by previous authors (Barigozzi 1980; Belk and Brtek 1995; Baxevanis et al. 2006; see also Table 1). Since Bowen and Sterling (1978), this name has been used in numerous publications (sometimes followed by a population site), whereas some authors preferred to refer parthenogenetic Artemia as “populations” (Abatzopoulos et al. 2002a; Baxevanis et al. 2006; Asem et al. 2010). Recent molecular analyses have shown that parthenogenetic Artemia is a polyphyletic group, with diploids/triploids being evolutionally close to A. urmiana while tetraploids/pentaploids sharing a common ancestor with A. sinica (Asem et al. 2016). In another molecular analysis conducted by Eimanifar et al. (2015), the parthenogenetic Artemia has been named as “Eurasian Haplotype Complex” comprising a group of putative parthenogenetic Artemia lineages which were genetically close to two bisexual species, A. urmiana and A. tibetiana. The molecular divergence analysis has indicated that a recent population expansion in A. urmiana and “Eurasian Haplotype Complex” occurred in the Pleistocene (1.72 Mya) and Holocene (0.84 Mya), respectively. Males of parthenogenetic Artemia (produced only by diploids; Saleem Chang et al. 2017) are fertile when mating with bisexual A. sinica, A. tibetiana, A. urmiana and KAZ (Cai 1993; Liu et al. 2007; Maccari et al. 2014), but not fertile when mating with the female of the other bisexual species (MacDonald and Browne 1987). Parthenogenetic females mating with males produce only parthenogenetic offspring (Barigozzi 1974). These results suggest that parthenogenetic Artemia may originate from bisexual species native to Asia; the gene pool of bisexual Artemia may be affected by diploid parthenogenetic Artemia but not vice versa; gene exchange can hardly happen among parthenogenetic individuals of different ploidies. In other words, parthenogenetic individuals cannot readily be considered as belonging to a single species as commented by Abatzopoulos et al. (2002a), and can be assigned to taxa different from bisexuals. There are already some available names referring to parthenogenetic Artemia, e.g., Artemia bivalens Artom, 1912 (Artom 1912 proposed this name for a tetraploid parthenogenetic population from Capo d’ Istria; also as Artemia salina bivalens), and the aforementioned A. asiatica, A. barkolica, A. urumuqinica, A. ebinurica, and A. frameshifta (?). These names could be candidates to be assigned to parthenogenetic populations, but this requires the type specimens to be re-examined, or/and topotypes to be studied using multidisciplinary methods.

Artemia is a taxon of difficult classification because of the lack of discernible characters. Some morphological characters are documented to be useful in delimitate species. For instance, the conical frontal knob on male antenna and the absence of basal spine on gonopod can segregate A. salina from the other bisexual species (e.g., Mura and Brecciaroli 2004; Zheng and Sun 2008), the “orthostichous spines” on gonopod are present only in species from China (A. sinica, A. tibetiana) (Zheng and Sun 2008). Molecular analyses based on genetic markers, like mitochondrial COI and 16SrRNA, and nuclear ITS1 sequences, have successfully resolved the phylogenetic relationships of different populations and are useful to assign a population to a known species/clade (e.g., Baxevanis et al. 2006; Wang et al. 2008; Yin et al. 2011, 2013; Eimanifar et al. 2014, 2015; Asem et al. 2016). However, these methods cannot resolve all taxonomic problems existing in Asian Artemia, particularly they cannot tell the taxonomic rank (species/subspecies) of a certain morphological group or phylogenetic clade. As discussed earlier, the test of reproductive isolation, though theoretically supposed to be a gold criterion for diagnosing species, cannot resolve these problems, either. Therefore, based on present knowledge it is hard to tell an exact number of valid species of Artemia living in Asia.

As far as we know, there are three ongoing comprehensive projects related to Artemia genomics, including the Artemia genome project, in which the full nuclear genome of inbred A. franciscana from Great Salt Lake was assembled and annotated (Ghent University, Belgium), also a study involving the creation of whole-genome SNP-based second-generation genetic maps (Ocean University of China, China), and a study devoted to complete the mitochondrial genomes of all described bisexual species (including both bisexual clades from Tibet) and parthenogenetic Artemia with different ploidy degrees (Hainan Tropical Ocean University, China). We believe that the final results of these studies will further contribute to deciphering the phylogenetic relationships in the genus Artemia.

Acknowledgements

This study was supported by the Fundamental Research Funds for the Central Universities (201762017), and Science and Technology Research Funds of Tibet Autonomous Region (XZ201703-GB-04). We thank Professor Alexei V. Chernyshev (National Scientific Center of Marine Biology, Russian Academy of Sciences) for explaining some questions regarding the literature.

References

  • Abatzopoulos TJ, Agh N, Van Stappen G, Razavi Rouhani SM, Sorgeloos P (2006) Artemia sites in Iran. Journal of the Marine Biological Association of the United Kingdom 86: 299–307. https://doi.org/10.1017/S0025315406013154
  • Abatzopoulos TJ, Amat F, Baxevanis AD, Belmonte G, Hontoria F, Maniatsi S, Moscatello S, Mura G, Shadrin NV (2009) Updating geographic distribution of Artemia urmiana Günther, 1890 (Branchiopoda: Anostraca) in Europe: An integrated and interdisciplinary approach. International Review of Hydrobiology 94: 560–579. https://doi.org/10.1002/iroh.200911147
  • Abatzopoulos TJ, El-Bermawi N, Vasdekis C, Baxevanis AD, Sorgeloos P (2003) Effects of salinity and temperature on reproductive and life span characteristics of clonal Artemia. (International Study on Artemia. LXVI). Hydrobiologia 492: 191–199. https://doi.org/10.1023/A:1024826702830
  • Abatzopoulos TJ, Kappas I, Bossier P, Sorgeloos P, Beardmore JA (2002b) Genetic characterization of Artemia tibetiana (Crustacea: Anostraca). Biological Journal of the Linnean Society 75: 333–344. https://doi.org/10.1046/j.1095-8312.2002.00023.x
  • Abatzopoulos TJ, Zhang B, Sorgeloos P (1998) Artemia tibetiana: preliminary characterization of a new Artemia species found in Tibet (People’s Republic of China). International study on Artemia. LIX. International Journal of Salt Lake Research 7: 41–44. https://doi.org/10.1007/BF02449923
  • Agh N, Abatzopoulos TJ, Kappas I, Van Stappen G, Razavi Rouhani SM, Sorgeloos P (2007) Coexistence of sexual and parthenogenetic Artemia populations in Lake Urmia and neighbouring lagoons. International Review of Hydrobiology 92: 48–60. https://doi.org/10.1002/iroh.200610909
  • Alas A, Kaya M, 0ktener A (2017) Distribution and abundance of Artemia salina in the Salt Lake Basin (Central Anatolia, Turkey). Transylvanian Review of Systematical and Ecological Research 19: 37–44. https://doi.org/10.1515/trser-2017-0011
  • Artom C (1912) Le basi citologiche di una nuova sistematica del genere Artemia. Sulla dipendeiiza tra il numero dei cromosomi delle cellule germinative, e la graiidezza dei nuclei delle cellule somatiche dell’ Artemia salina univalens di Cagliari, e dell’ Artemia saliiia bivalens di Capo d’ Istria. Archiv für Zellforschung 9: 87–113.
  • Asem A, Eimanifar A, Sun S-C (2016) Genetic variation and evolutionary origins of parthenogenetic Artemia (Crustacea: Anostraca) with different ploidies. Zoologica Scripta 45: 421–436. https://doi.org/10.1111/zsc.12162
  • Asem A, Atashbar B, Rastegar-Pouyani N, Agh N (2009) Biometric comparison of two parthenogenetic populations of Artemia Leach, 1819 from the Urmia Lake basin, Iran (Anostraca: Artemiidae). Zoology in the Middle East 47: 117–120. https://doi.org/10.1080/09397140.2009.10638358
  • Asem A, Rastegar-Pouyani N, De los Rios P (2010) The genus Artemia Leach, 1819 (Crustacea: Branchiopoda): true and false taxonomical descriptions. Latin American Journal of Aquatic Research 38: 501–506.
  • Azari Takami G (1989) Two strains of Artemia in Urmia Lake (Iran). Artemia Newsletter 13: 5 pp.
  • Barigozzi C (1980) Genus Anemia: problems of systematics. In: Persoone G, Sorgeloos P, Roels O, Jaspers E (Eds) The Brine Shrimp Anemia, Vol. 1, Morphology, Genetics, Radiobiology, Toxicology. Universa Press, Wetteren, 147–153.
  • Barigozzi C, Baratelli L (1989) The problem of Artemia urmiana. Artemia Newsletter 14: 14 pp.
  • Başbuğ Y (1999) Reproduction characteristics of Artemia salina (L., 1758) in Salt Lake. Turkish Journal of Zoology 23: 635–640.
  • Bond RM (1934) Report of phyllopod Crustacea (Anostraca, Notostraca and Conchostraca) including a revision of the Anostraca of the Indian Empire. Memoirs of the Connecticut Academy of Arts and Sciences 10: 29–62.
  • Bowen ST, Sterling G (1978) Esterase and malate dehydrogenase isozyme polymorphisms in 15 Artemia populations. Comparative Biochemistry and Physiology. B, Comparative Biochemistry 61: 593–595. https://doi.org/10.1016/0305-0491(78)90055-X
  • Cai Y (1989a) New Artemia sibling species from PR China. Artemia Newsletter, 11: 40–41.
  • Cai Y (1989b) A redescription of the brine shrimp (Artemia sinica). Wasmann Journal of Biology 47: 105–110.
  • Cai Y (1993) Artemia and its crossing experiments. Journal of Ocean University of Qingdao 23: 52–57. [in Chinese with English summary]
  • Chiang S-C (1983) The branchiopod crustaceans from Xizang Plateau. In: Chiang S-C, Shen Y-F, Gong X-J (Eds) The Series of the Scientific Expedition to Qinghai-Xizang Plateau: Aquatic Invertebrates of the Tibetan Plateau. Science Press, Beijing, 443–466. [In Chinese]
  • Chiang S-C, Shen Y-F, Gong X-J (1983) General Account. In: Chiang S-C, Shen Y-F, Gong X-J (Eds) The Series of the Scientific Expedition to Qinghai-Xizang Plateau: Aquatic Invertebrates of the Tibetan Plateau. Science Press, Beijing, 1–38. [In Chinese]
  • Eimanifar A, Van Stappen G, Marden B, Wink M (2014) Artemia biodiversity in Asia with the focus on the phylogeography of the introduced American species Artemia franciscana Kellogg, 1906. Molecular Phylogenetics and Evolution 79: 392–403. https://doi.org/10.1016/j.ympev.2014.06.027
  • Eimanifar A, Van Stappen G, Wink M (2015) Geographical distribution and evolutionary divergence times of Asian populations of the brine shrimp Artemia (Crustacea, Anostraca). Zoological Journal of the Linnean Society 174: 447–458. https://doi.org/10.1111/zoj.12242
  • Fischer GW (1834) Notice sur une nouvelle espèce de Branchipus de Latreille. Bulletin de la Société Impériale des Naturalistes de Moscou 7: 452–461.
  • Fischer GW (1851) Branchiopoden und Entomostracen. In: Middendorff AT (Ed.) Reise in den äussersten Norden und Osten Sibiriens während der Jahre 1843 und 1844 mit Allerhöchster Genehmigung auf Veranstaltung der Kaiserlichen Akademie der Wissenschaften zu St. Petersburg ausgeführt und in Verbindung mit vielen Gelehrten, Bd. 2., T. 1. Kaiserlichen Akademie der Wissenschaften, St. Petersburg, 149–162.
  • Gurney R (1921) Freshwater crustacean collected by Dr. P.A. Buxton in Mesoptamia and Persia. The Bombay Natural History Society 27: 835–843.
  • John CJA, Abatzopoulos TJ, Marian PM (2004) Characterization of a new parthenogenetic Artemia population from Thamaraikulam, India. Journal of Biological Research 2: 63–74.
  • Linnaeus C (1758) Systema Naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis, Vol. 1. Laurentii Salvii, Holmiae, 823 pp. https://doi.org/10.5962/bhl.title.542
  • Litvinenko LI, Litvinenko AI, Boyko EG (2016) Brine Shrimp Artemia in Western Siberia Lakes. Siberian Publishing Company “Nauka”, Novosibirsk, 295 pp.
  • Liu F-Q, Xiang J-H, Liu G-M, Bu W-J, Ji B-C, Liu A-X (2007) Rare male culture from Artemia parthenogenetica of Gahai and its cross breeding with Artemia sinica. Acta Scientiarum Naturalium Universitatis Nankaiensis 40: 24–27. [in Chinese with English summary]
  • Maccari M, Amat F, Hontoria F, Gomez A (2014) Laboratory generation of new parthenogenetic lineages supports contagious parthenogenesis in Artemia. PeerJ 2: e439. https://doi.org/10.7717/peerj.439
  • MacDonald GH, Browne RA (1987) Inheritance and reproductive role of rare males in a parthenogenetic population of the brine shrimp, Artemia parthenogenetica. Genetica 75: 47–53. https://doi.org/10.1007/BF00056032
  • Maniatsi S, Baxevanis AD, Kappas I, Deligiannidis P, Triantafyllidis A, Papakostas S, Bougiouklis D, Abatzopoulos TJ (2011) Is polyploidy a persevering accident or an adaptive evolutionary pattern? The case of the brine shrimp Artemia. Molecular Phylogenetics and Evolution 58: 353–364. https://doi.org/10.1016/j.ympev.2010.11.029
  • Mayr E (1969) Principles of Systematic Zoology. McGraw Hill, New York (& London), xiv + 434 pp.
  • Mura G, Nagorskaya L (2005) Notes on the distribution of the genus Artemia in the former USSR countries (Russia and adjacent regions). Journal of Biological Research 4: 139–150.
  • Naganawa H, Mura G (2017) Two new cryptic species of Artemia (Branchiopoda, Anostraca) from Mongolia and the possibility of invasion and disturbance by the aquaculture industry in East Asia. Crustaceana 90: 1679–1698. https://doi.org/10.1163/15685403-00003744
  • Padhye SM, Lazo-Wasem EA (2018) An updated and detailed taxonomical account of the large Branchiopoda (Crustacea: Branchiopoda: Anostraca, Notostraca, Spinicaudata) from the Yale North India Expedition deposited in the Yale Peabody Natural History Museum. Zootaxa 4394(2): 207–218. https://doi.org/10.11646/zootaxa.4394.2.3
  • Pilla EJS, Beardmore JA (1994) Genetic and morphometric differentiation in Old World bisexual species of Artemia (the brine shrimp). Heredity 73: 47–56. https://doi.org/10.1038/hdy.1994.97
  • Qian Y, Zhang Q, Yang C-Z, Cai X-L, Fan Y, Wang G-X (1992) Description of three new species of the genus Artemia in Xinjiang, China. Journal of August 1st Agriculture College 15(1): 41–47. [in Chinese with English summary]
  • Qian Y, Zhang Q, Yang C-Z, Wang G-Y (1993) Studies on growing behavior of A. urumuqinica. Journal of August 1st Agriculture College 16: 55–58. [in Chinese with English summary]
  • Rogers DC (2013) Anostraca catalogus (Crustacea: Branchiopoda). The Raffles Bulletin of Zoology 61: 525–546.
  • Saleem Chang M, Asem A, Sun SC (2017) The incidence of rare males in seven parthenogenetic Artemia (Crustacea: Anostraca) populations. Turkish Journal of Zoology, 41: 138–143. https://doi.org/10.3906/zoo-1512-67
  • Salman SD, Mohammed DS, Ali MH (2012) Review of the biogeography of Artemia Leach, 1819 (Crustacea: Anostraca) in Iraq. International Journal of Artemia Biology, 2: 62–73.
  • Sars GO (1901) On the crustacean fauna of central Asia. Part I, Amphipoda and Phyllopoda. Annuaire du Musée Zoologique de l’Académie Impériale des Sciences de St. Pétersbourg, 6: 130–164.
  • Shadrin N, Anufriieva E (2012) Review of the biogeography of Artemia Leach, 1819 (Crustacea: Anostraca) in Russia. International Journal of Artemia Biology 2: 51–61.
  • Van Stappen G (2002) Zoogeography. In: Abatzopoulos TJ, Beardmore JA, Clegg JS, Sorgeloos P (Eds) Biology of Aquatic Organisms. Artemia Basic and Applied Biology. Dordrecht, 171–224. https://doi.org/10.1007/978-94-017-0791-6_4
  • Van Stappen G, Litvinenko LI, Litvinenko AI, Boyko EG, Marden B, Sorgeloos P (2009) A survey of Artemia resources of Southwest Siberia (Russian Federation). Reviews in Fisheries Science 17: 116–148. https://doi.org/10.1080/10641260802590095
  • Van Stappen G, Sui L-Y, Xin N-H, Sorgeloos P (2003) Characterisation of high-altitude Artemia populations from the Qinghai-Tibet Plateau, PR China. Hydrobiologia 500: 179–192. https://doi.org/10.1023/A:1024658604530
  • Van Stappen G, Yu H-Y, Wang X-M, Hoffman S, Cooreman K, Bossier P, Sorgeloos P (2007) Occurrence of allochthonous Artemia species in the Bohai Bay area, PR China, as confirmed by RFLP analysis and laboratory culture tests. Fundamental and Applied Limnology 170: 21–28. https://doi.org/10.1127/1863-9135/2007/0170-0021
  • Velasco SJ, Retana OD, Castro MJ, Castro MG, Castro CAE (2018) Effect of different salinities on the survival and reproductive characteristics of populations of Artemia franciscana Kellogg, 1906 from coastal and inland waters of Mexico. Journal of Entomology and Zoology Studies 6(2): 1090–1096.
  • Velasco SJ, Retana ODA, Castro MJ, Castro MG, Monroy DMC, Ocampo CJA, Cruz CI, Becerril CD (2016) Salinity effect on reproductive potential of four Artemia franciscana (Kellogg, 1906) Mexican populations grown in laboratory. International Journal of Fisheries and Aquatic Studies 4(3): 247–253.
  • Vikas PA, Sajeshkumar NK, Thomas PC, Chakraborty K, Vijayan KK (2012) Aquaculture related invasion of the exotic Artemia franciscana and displacement of the autochthonous Artemia populations from the hypersaline habitats of India. Hydrobiologia, 684: 129–142. https://doi.org/10.1007/s10750-011-0976-x
  • Walter A (1887) Vorläufige Diagnose und Beschreibung zweier neuer Branchiopoden aus Transkaspien. Bulletin de la Societe Imperiale des Naturalistes de Moscou, no. 4. 924–927.
  • Walter A (1888) Transkaspische Binnencrustaceen. Zoologische Jahrbücher, Abtheilung für Systematik, Geographie und Biologie der Thiere 3: 987–1014.
  • Wang W, Luo Q, Guo H, Bossier P, Van Stappen G, Sorgeloos P, Xin N, Sun Q, Hu S, Yu J (2008) Phylogenetic analysis of brine shrimp (Artemia) in China using DNA barcoding. Genomics, Proteomics and Bioinformatics 6: 155–162. https://doi.org/10.1016/S1672-0229(09)60003-6
  • Yin H, Guan N, Fu Y-T (2011) Molecular phylogeny of bisexual Artemia based on 16S rDNA. Agricultural Science &Technology 12: 659–662.
  • Yin Z, Zhang X-X, You T (2013) Molecular phylogeny of different geographic Artemia populations based on 16S rDNA mark. Heilongjiang Animal Science and Veterinary Medicine (7–1): 135–137. [in Chinese]
  • Yu X-L, Xin N-H (2006) The characterization of Artemia cysts from 4 salt lakes of Tibet. Sea-Lake Salt and Chemical Industry 35(1): 25–26. [in Chinese with English summary]
  • Zheng B, Sun S-C (2008) Taxonomic consideration of eight Chinese bisexual Artemia populations, based on the morphology of frontal knob and gonopod and the result of cross-breeding tests. Zootaxa 1919: 25–44. https://doi.org/10.11646/zootaxa.1919.1.2
  • Zheng B, Sun S-C (2013) Review of the biogeography of Artemia Leach, 1819 (Crustacea: Anostraca) in China. International Journal of Artemia Biology 3(1): 20–50.
  • Zheng X-Y, Zhang M-G, Xu C, Li B-X (2002) An Overview of Salt Lakes in China. Science Press, Beijing, 415 pp. [In Chinese]
  • Zhou K-X (2001) Studies on the Taxonomy and Biological Features of Bisexual Artemia from Plateau Salt Lakes of China. M. Sci. thesis. Hebei University, Baoding. [in Chinese with English summary]
  • Zhou K-X, Xu M-Q, Guan Y-Q, Yin X-C (2003a) Numeric taxonomy using cysts and nauplii of bisexual Artemia from China. Journal of Lake Sciences 15(2): 153–159. [in Chinese with English summary] https://doi.org/10.18307/2003.0209
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