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The genus Artemia Leach, 1819 (Crustacea: Branchiopoda). I. True and false taxonomical descriptions/El genero Artemia Leach, 1819 (Crustacea: Branchiopoda). I. Descripciones taxonomicas verdaderas y falsas.

The brine shrimp Artemia is one of the most important aquatic animals used in aquaculture industry. It was first reported from Urmia Lake in 982 by an unknown Iranian geographer (Asem, 2008), and then in 1756 Schlosser pictured both sexes clearly. Linnaeus (1758) described it as Cancer salinus but 61 years later, Leach (1819) transferred it to Artemia salina.

The taxonomic status of the genus Artemia is as follows (Martin & Davis, 2001):

Subphylum: Crustacea Brunnich, 1772

Class: Branchiopoda Latreille, 1817

Subclass: Sarsostraca Tasch, 1969

Order: Anostraca Sars, 1867

Family: Artemiidae Grochowski, 1896

Genus: Artemia Leach, 1819

--A. salina (Linnaeus, 1758): Mediterranean area

--A. monica Verrill, 1869: USA (Mono Lake; California)

--A. urmiana Gunther, 1899: Iran (Urmia Lake; West Azerbaijan Province)

--A. franciscana Kellogg, 1906: America, Caribbean and Pacific islands

--A. persimilis Piccinelli & Prosdocimi, 1968: South America

--A. sinica Cai, 1989: Central and Eastern Asia

--A. tibetiana Abatzopoulos, Zhang & Sorgeloos, 1998: China (Tibet)

--Artemia sp. Pilla & Beardmore, 1994: Kazakhstan

--Parthenogenetic population(s) of Artemia: Europe, Africa, Asia and Australia

Taxonomists are still confused about the systematic and phylogenetic relationships of the Artemia species (Triantaphyllidis et al., 1997) and there are different opinions about its biosystematics. For example, there are two views for A. franciscana and A. monica. Artemia monica, from Mono Lake, cannot be crossed with A. franciscana because of the inability of the two species to tolerate the same water ionic composition (Mono Lake has a mix of [Cl.sup.-], S[O.sub.4.sup.2-] and C[O.sub.3.sup.-] ions). A. monica is therefore thought to be effectively debarred from exchanging gene with A. franciscana so these two sPecies are known as two different "biological species" (Clark & Bowen, 1976). According to others (Abreu-Grobois & Beardmore, 1982; Triantaphyllidis et al., 1998), A. monica may be ecologically seParated from A. franciscana, but the genetic distance between these two taxa is less than the distance between other Artemia taxa; therefore they can be described as sibling species. Furthermore, there are no taxonomic identification keys for the genus due to a lack of reliable morPhological characters, so different methods have been used for species characterization. The most relevant methods are comParison of biometric characteristics, electrophoretic patterns of different allozymes, cross-fertility tests and microscopic survey of the morphology such as frontal knob and gonopod (Abreu-Grobois & Beardmore, 1982; Mura, 1990; Hontoria & Amat, 1992; Triantaphyllidis et al., 1997; De los Rios & Zuniga, 2000; Torrentera & Belk, 2002; De los Rios & Asem, 2008).

Seeing that Artemia was an economically important species this has led to a decline of basic studies on this taxon, with wide use of "Artemia salina" as a trade name. There are numerous published data on biochemical, mutational, toxicological and others aspects of Artemia, all using the name Artemia salina for any population in this genus (Abreu-Grobois & Beardmore, 1982; Gajardo et al., 2002). As a result, the brine shrimp Artemia is used in many aquaculture studies and for experimental models but its basic taxonomy is not considered by many authors resulting in taxonomical confusion (Table 1), with the mistakes and respective corrections about systematic nomenclature.

DOI: 10.3856/vol38-issue3-fulltext-14

ACKNOWLEDGEMENTS

Dr. D. Christopher Rogers (EcoAnalysts Inc., California, U.S.A.) is thanked for the scientific comments and English text.

REFERENCES

Abatzopoulos, T.J., B. Zhang & P. Sorgeloos. 1998. International study on Artemia: 59. Artemia tibetiana: preliminary characterization of a new Artemia species found in Tibet (People's Republic of China). Int. J. Salt Lake Res., 7: 41-44.

Abatzopoulos, T.J., J.A. Beardmore, J.S. Clegg & P. Sorgeloos. 2002. Artemia: basic and applied biology. Kluwer Academic Publishers, Dordrecht, pp. 171-224.

Abreu-Grobois, F.A. & J.A. Beardmore. 1982. Genetic differentiation and speciation in the brine shrimp Artemia. In: C. Barigozzi (ed.). Mechanisms of speciation. Alan R. Liss, New York, pp. 345-376.

Asem, A. 2008. Historical record on brine shrimp Artemia more than one thousand years ago from Urmia Lake, Iran. J. Biol. Res., 9: 113-114.

Barigozzi, C. 1974. Artemia: A survey of its significance in genetic problems. Evol. Biol., 7: 221.

Browne, R.A., & S.T. Bowen. 1991. Taxonomy and population genetics of Artemia. In: R.A. Browne, P. Sorgeloos & C.A.N. Trotman (eds.). Artemia Biology CRC Press, Boca Raton, pp. 221-253.

Cai, Y. 1989. New Artemia sibling species from PR China. Artemia Newslett., 11: 40-41.

Clark, L.S. & S.T. Bowen. 1976. The genetics of Artemia salina. VII. Reproductive isolation. J. Hered., 67: 385-388.

De los Rios, P. & A. Asem. 2008. The comparison of diameter of the frontal knobs in Artemia urmiana Gunther, 1899 (Anostraca): possible similarities with new world populations. Crustaceana, 81: 1281-1228.

De los Rios, P. & O. Zuniga. 2000. Comparacion biometrica del lobulo frontal en poblaciones de Artemia (Anostraca, Artemiidae). Rev. Chil. Hist. Nat., 73: 31-38.

Gajardo, G., T.J. Abatzopoulos, I. Kappas & J.A. Beardmore. 2002. Evolution and speciation. In: T.J. Abatzopoulos, J.A. Beardmore, J.S. Clegg & P. Sorgeloos (eds.). Artemia basic and applied biology. Kluwer Academic Publishers, Dordrecht, pp. 225-250.

Gunther, R.T. 1899. Crustacea. pp. 394-399. In: R.T Gunther (ed.). Contributions to the natural history of Lake Urmi, N.W-Persia, and its neighbourhood. J. Linnean Soc. (Zool.), 27(177): 345-453.

Hontoria, F. & F. Amat. 1992. Morphological characterization of adult Artemia (Crustacea, Branchiopoda) from different geographical origins. Mediterranean population, J. Plankton Res., 14: 949-956.

International Commission on Zoological Nomenclature (ICZN). 2000. International Code of Zoological Nomenclature (ICZN). Tipografia La Garangola.

Kellogg, V.L. 1906. A new Artemia and its life condition. Science, 24: 594-596.

Leach, W.E. 1819. Entomostraca, Dictionaire des Science Naturelles, 14, pag. 524.

Linnaeus, C. 1758. Systema naturae. Hofniae, 1: 634.

Martin, J.W. & G.E. Davis. 2001. An updated classification of the Recent Crustacea. Nat. Hist. Mus. Los Angeles County. Sci. Ser., 39: 1-124.

Mura, G. 1990. Artemia salina (Linnaeus, 1758) from Lymington, England: frontal knob morphology by scanning electron microscopy. J. Crust. Biol., 10: 364-368

Piccinelli, M. & T. Prosdocimi. 1968. Descrizione tassonomica delle due species Artemia salina L. e. Artemia persimilis n.sp. Genetica, 102: 113-118.

Pilla, E.J.S. & J.A. Beardmore. 1994. Genetic and morphometric differentiation in Old World bisexual species of Artemia (the brine shrimp). Heredity, 73: 47-56.

Schlosser, D. 1756. Extrait d'une lettre de M. le Docteur Schlosser concernant un insecte peu connu. Observation periodique sur la physique, l'histoire naturille et les beaux arts, de Gautier, pp. 58-60.

Torrentera, L. & D. Belk. 2002. New penis characters to distinguish between two American Artemia species. Hydrobiologia, 470: 149-156.

Triantaphyllidis, G., G.R. Criel, T.J. Abatzopoulos, K.M. Thomas, J. Peleman, J.A. Beardmore & P. Sorgeloos. 1997. International study on Artemia: 57. Morphological and molecular characters suggest conspecificity of all bisexual European and North African Artemia populations. Mar. Biol., 129: 477487.

Triantaphyllidis, G.V., T.J. Abatzopoulos & P. Sorgeloos. 1998. Review of the biogeography of the genus Artemia (Crustacea, Anostraca). J. Biogeogr., 25: 213-226.

Verrill, A.E. 1869. Contributions to zoology from the Museum of Yale College. III. Descriptions of some new America Phyllopod Crustacea. Am. J. Sci. Arts, 142: 244-254.

Zhou, K., M. Xu & X. Yin. 2003. Morphological characterization of sexual Artemia (Branchiopoda) from China. Crustaceana, 76(11): 1331-1346.

Received: 27 October 2009; Accepted: 17 August 2010

Alireza Asem (1), Nasrullah Rastegar-Pouyani (2) & Patricio De Los Rios-Escalante (3)

(1) Protectors of Urmia Lake National Park Society (NGO), Urmia, Iran

(2) Department of Biology, Faculty of Science, Razi University, 67149 Kermanshah, Iran

(3) Escuela de Ciencias Ambientales, Facultad de Recursos Naturales, Universidad Catolica de Temuco Casilla 15-D, Temuco, Chile

Corresponding author: Alireza Asem (alireza_1218@yahoo.com)
Table 1. True and false taxonomic expression on the genus Artemia.

Tabla 1. Expresion verdadera y falsa taxonomica sobre el genero
Artemia.

Taxon                 Status        False decision         Comment

Artemia               Genus         Artemia L., 1758          1
                                    Artemia (L., 1758)        2
                                    Artemia Linnaeus,         3
                                    1758
                                    Artemia (Linnaeus,        4
                                    1758)
                                    Artemia (Leach,           5
                                    1819)
Artemia salina        Species       Artemia salina L.,        7
                                    1758
                                    Artemia salina            8
                                    Linnaeus, 1758
                                    Artemia salina            9
                                    Leach, 1819
                                    Artemia salina           10
                                    (Leach, 1819)
Aremia monica         Species       Aremia monica            13
                                    (Verrill, 1869)
Aremia monica         Sibling       Artemia franciscana      14
                      species       monica
                                    Artemia urmiana          17
                                    (Gunther, 1900)
                                    Artemia urmiana          18
                                    (Gunther, 1890)
Artemia urmiana       Species       Artemia urmiana          19
                                    (Gunther, 1899)
                                    Artemia urmiana          20
                                    Gunther, 1900
                                    Artemia urmiana          21
                                    Gunther, 1890
Artemia franciscana   Species       Artemia franciscana      23
                                    (Kellogg, 1906)
Artemia franciscana   Sibling       Artemia franciscana      24
                      species       franciscana
Partenogenetic        population    Artemia                  27
  population(s)                     parthenogenetica
Artemia persimilis    Species       Artemia persimilis       29
                                    (Piccinelli &
                                    Prosdocimi, 1968)
                                    Artemia sinica           31
                                    (Cai, 1989)
Artemia sinica        Species       Artemia sinica           32
                                    (Yaneng, 1989)
                                    Artemia sinica
                                    Yaneng, 1989
Artemia sinica        Sub-          Artemia sinica           34
  sinica              species       sinica Zhou et
                                    al., 2003
                                    Artemia sinica
                                    sinica Zhou,
                                    et al, 2003
Artemia tibetiana     Species       Artemia tibetiana        36
                                    (Abatzopoulos et
                                    al., 1998)
Artemia sinica                      Artemia sinica
  tibetiana                         tibetiana Zhou
                                    et al., 2003
                      Sub-species   Artemia sinica           38
                                    tibetiana Zhou,
                                    et al, 2003

Taxon                 True decision         Comment

Artemia               Artemia                  6
                      Leach, 1819
Artemia salina        Artemia                 11
                      salina (L., 1758)
                      Artemia salina          12
                      (Linnaeus, 1758)
Aremia monica         Aremia monica           15
                      Verrill, 1869
Aremia monica         Aremia monica           16
                      Verrill, 1869
Artemia urmiana       Artemia urmiana         22
                      Gunther, 1899
Artemia franciscana   Artemia franciscana     25
                      Kellogg, 1906
Artemia franciscana   Artemia franciscana     26
                      Kellogg, 1906
Partenogenetic        parthenogenetic         28
  population(s)       population(s) of
                      Artemia
Artemia persimilis    Artemia persimilis      30
                      Piccinelli &
                      Prosdocimi, 1968
Artemia sinica        Artemia sinica          33
                      Cai, 1989
Artemia sinica        Artemia sinica          35
  sinica              sinica Cai,
                      1989
Artemia tibetiana     Artemia tibetiana       37
                      Abatzopoulos,
                      et al, 1998
                      Artemia tibetiana
                      Abatzopoulos
                      et al., 1998
Artemia sinica        Artemia sinica
  tibetiana           tibetiana
                      Abatzopoulos
                      et al., 1998
                      Artemia sinica          39
                      tibetiana
                      Abatzopoulos,
                      et al., 1998

Comments:

NOTE: The "comma" must be used between the name of the author and
date [Art. 22; (ICZN, 2000)].

--1, 2, 3, 4: The genus Artemia was described by Leach in 1819 not
Linnaeus. Linnaeus, C. 1758  Systema naturae. Hofniae, 1: 634.

--5: Leach described Artemia so parentheses should not be used.

--6: Leach had described the genus Artemia in 1819 so it should be
depicted as: Artemia Leach, 1819

--Leach, W.E. 1819. Entomostraca, Dictionaire des Science
Naturelles, 14, 524.

--7, 8: Although Linnaeus (1758) described the brine shrimp as
Cancer salinus and Leach has corrected its status as Artemia salina
in 1819, according to Article 22: 22A.3. (ICZN 2000) the only true
status will be: Artemia salina (L. 1758) or Artemia salina (Linnaeus,
1758). Use of parentheses around author's name shows Linnaeus had
described this species in a different genus in 1758 and then it has
been changed into Artemia salina.

NOTE: Article 22: 22A.3. Date in a changed combination (ICZN, 2000).
When the original date of publication of a species-group name is
cited with the name in a changed combination, the date should be
enclosed within the same parentheses as the name of the original
author [Art. 51.3; (ICZN 2000)].

--9, 10: Although the rule of Article 22: 22A.3. (ICZN, 2000) is
respected but punctuation mark "()" is absent. Because Linnaeus had
used a different name for Artemia therefore according to Article 22:
22A.3. (ICZN, 2000), Linnaeus and its date must be put in parenthesis.

--11, 12: These two expressions conform that Linnaeus had considered
Artemia salina in another genus and was corrected afterward. So, use
of parentheses around author name and date is necessary.

--13: Verrill is the original describer of Artemia monica therefore
use of parentheses is incorrect.

--14: Verrill is the original describer of Artemia monica therefore
the name is: Artemia monica Verrill, 1869

--Verrill, A.E. 1869. Contributions to zoology from the museum of
Yale College. III. Descriptions of some new America Phyllopod
Crustacea, Am. J. Sci. Arts, 142: 244-254.

--15, 16: Although there is debate about Artemia in Mono Lake being
a biological or sibling species, trinomial nomenclature is used only
for subspecies (see Article 4.; ICZN, 2000). So the proper name is:
Artemia monica Verrill, 1869

--17, 18, 19, 20, 21, 22: Gunther (1899, not 1900) is the original
describer of Artemia urmiana so use of parentheses around author name
and date is incorrect.

NOTE: Gunther's manuscript has been published in The Journal of the
Linnean Society (Zoology) in volume 27. The date of publication is
1899. Gunther's article has been printed in issue 177 with actual
publication date in December 1899. Gunther described Artemia urmiana
in page 395. The correct reference for this manuscript is:

--Gunther, R.T. (1899) Crustacea. pp: 394-399. In: R.T. Gunther
(ed.). Contributions to the Natural History of Lake Urmi, N.W-Persia,
and its Neighbourhood. The Journal of Linnean Society (Zoology), 27
(177): 345-453.

--23: Kellogg had reported and described Artemia franciscana from
San Francisco Bay in 1906 so there is no need for parentheses.

--24: Kellogg is the original describer of therefore the proper name
is: Artemia franciscana Kellogg, 1906

--Kellogg, V.L. 1906. A new Artemia and its life condition. Science,
24: 594-596.

--25: Though even Artemia from San Francisco Bay is accepted as
sibling species its name will be: Artemia franciscana Kellogg, 1906
because "Trinomial Nomenclature" used only for subspecies (see
Article 4; ICZN, 2000).

--26: Sibling spices are defined under the "Binomial Nomenclature"
system (see Article 4.; ICZN, 2000).

--27, 28: The asexual populations had been named such as biological
species; Artemiaparthenogenetica by Barigozzi in 1974 (Browne &
Bowen, 1991). Since their reproductive mechanism is via
parthenogenesis and the males seldom are produced in these
populations. Therefore, they are introduced as "parthenogenetic
Artemia populations" (Abatzopoulos et al., 2002)

--29: Piccinelli & Prosdocimi are the original describers of Artemia
persimilis in 1968 so parentheses are not needed.

--Piccinelli, M. & T. Prosdocimi. 1968. Descrizione tassonomica delle
due species Artemia salina L. e. Artemia persimilis n.sp. Genetica,
102: 113-118.

--30: The proper name is: Artemia persimilis Piccinelli & Prosdocimi,
1968

--31: Cai is original describer of Artemia sinica in 1989 from China
so parentheses are not needed.

--Cai, Y. 1989. New Artemia sibling species from PR China. Artemia
Newslett., 11: 40-41.

--32: Yaneng is the first name of Cai; but sometimes Artemia sinica
is cited and referred by Yaneng which it will be false.

--33: The proper name is: Artemia sinica Cai, 1989

--34, 35: Artemia sinica had been described by Cai and Zhou et al.
has been introduced as two subspecies. New subspecies must be
expressed as: Artemia sinica sinica Cai, 1989, because Zhou et al.,
2003 has done nothing but change the rank.

--36, 37: Abatzopoulos et al. have introduced Artemia tibetiana
in 1998 from Tibet so use of parentheses around author name and
date won't be true status. Its right status only will be: Artemia
tibetiana Abatzopoulos et al., 1998 or Artemia
tibetiana Abatzopoulos, Zhang & Sorgeloos, 1998 (See also
Recommendation 51C; ICZN, 2000)

--Abatzopoulos, T.J., B. Zhang & P. Sorgeloos. 1998. International
study on Artemia: 59. Artemia tibetiana: preliminary characterization
of a new Artemia species found in Tibet (People's Republic of China).
Int. J.Salt Lake Res., 7: 41-44.

--38, 39: Abatzopoulos et al. (1998) described Artemia tibetiana and
later Zhou et al. (2003) described the subspecies Artemia sinica
tibetiana. New subspecies must be ex-pressed: Artemia sinica tibetiana
Abatzopoulos et al., 1998 or Artemia sinica tibetiana Abatzopoulos,
Zhang & Sorgeloos, 1998. Because Zhou et al., 2003 has only changed
the rank (See also Recommendation 51C; ICZN, 2000).
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Author:Asem, Alireza; Rastegar-Pouyani, Nasrullah; De Los Rios-Escalante, Patricio
Publication:Latin American Journal of Aquatic Research
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Date:Nov 1, 2010
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