Abstract
The taxonomic assignment of the Artemia from Qinghai-Xizang Plateau has been argued. In the present paper, the morphology of frontal knobs and gonopods of five Artemia populations from Qinghai-Xizang Plateau (Lagkor Co, Cam Co, Dagdong Co and Jibu Caka, Tibet; Jingyu Hu, Xinjiang) and three populations from North China (Badain Jaran and Yimeng, Inner Mongolia; Xiechi Lake, Shanxi) is described and compared with four non-Chinese species, the results of cross-breeding tests between the eight Chinese populations are documented and the taxonomic assignment of these Artemia populations is discussed. Morphological observations show that gonopods of the Chinese populations are significantly longer than those of the other species; distal gonopods of the Chinese populations possess spines that can be classified into three groups (posterior spines, exolateral spines and orthostichous spines). In the four non-Chinese species, however, orthostichous spines are absent (thus providing a morphological separation between A. urmiana and A. tibetiana) and the number of spines is much smaller than those of the Chinese populations. Discriminant analysis on numerical characters showed that three North China populations were divergent from four Tibetan populations, with Jingyu Hu population intermediate. Compared with the North China populations, the Tibetan populations possess a longer gonopod (longer gonopod, longer distal gonopod and longer finger-like tip), larger basal gonopod spine, larger percent of frontal knob spines that emerge by 2 spines from the same region and smaller percent of frontal knob spines that emerge by 4 and 5 spines from the same region. The Artemia from Jingyu Hu is morphometrically close to the Tibetan populations by possessing a larger basal gonopod spine, larger percent of frontal knob spines emerging by 2 spines from the same region and smaller percent of frontal knob spines emerging by 4 and 5 spines from the same region, but different from the latter by having a shorter gonopod (shorter gonopod, shorter distal gonopod and shorter finger-like tip), fewer frontal knob spines, more distal gonopod spines and more posterior spines. The results of cross-breeding tests showed that isolating barrier did not exist among the three North China populations or among the five Qinghai-Xizang Plateau populations, while they might exist between A. urmiana and the populations of Xiechi Lake (type locality of A. sinica) and Lagkor Co (type locality of A. tibetiana) and between the Qinghai-Xizang Plateau populations and A. sinica. The present results thus support the validity of A. tibetiana. Among the eight Chinese populations, the five populations from Qinghai-Tibet Plateau belong in A. tibetiana, whereas three populations from North China belong in A. sinica.References
Abatzopoulos, T. J., 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.
Abatzopoulos, T. J., Kappas, I., Bossier, P., Sorgeloos, P. & Beardmore, J. A. (2002) Genetic characterization of Artemia tibetiana (Crustacea: Anostraca). Biological Journal of the Linnean Society, 75, 333–344.
Abatzopoulos, T. J., Baxevanis, A. D., Triantaphyllidis, G. V., Criel, G., Pador, E. L., Van Stappen, G. & Sorgeloos, P. (2006) Quality evaluation of Artemia urmiana Günther (Urmia Lake, Iran) with special emphasis on its particular cyst characteristics (International Study on Artemia LXIX). Aquaculture, 254, 442–454.
An, M., Jiang, Z.-N., Liu, H.-T., Zhang, J.-H., Bao, L.-B., Yuan, M.-C., Zhang, L., Zhu, Y.-G., Liu, P.-B. & Liang, K.-Q. (2003) Study on the biological character of the Artemia sp. lived in both Wenzi and Naoeree saltine lake. Chinese Journal of Fisheries, 16, 27–31 (in Chinese with English abstract).
Baratelli, L., Badaracco, G., Varotto, V., Mura, G., Barigozzi, C. & Battaglia, B. (1988) Heteroploidy and diploidy in bisexual Artemia living in the salterns of S. Antioco and Carloforte (Sardinia). Atti della Accademia Nazionale dei Lincei Memorie, 82, 577–580.
Baratelli, L., Varotto, V., Badaracco, G., Mura, G., Battaglia, B. & Barigozzi, C. (1990) Biological data on the brine shrimp Artemia living in the Italian saltworks. Atti della Accademia Nazionale dei Lincei Memorie, 1, 45–53.
Barigozzi, C. (1972) Problems of speciation in the genus Artemia. In: Battaglia, B. (ed.), Proceedings of the Fifth European Marine Biology Symposium. Piccini Editors, Padua, 61–66.
Barigozzi, C. (1974) Artemia: A survey of its significance in genetic problems. Evolutionary Biology, 7, 221–252.
Baxevanis, A. D., Triantaphyllidis, G. V., Kappas, I., Triantafyllidis, A., Triantaphyllidis, C. D. & Abatzopoulos, T. J. (2005) Evolutionary assessment of Artemia tibetiana (Crustacea, Anostraca) based on morphometry and 16S rRNA RFLP analysis. Journal of Zoological Systematics and Evolutionary Research, 43, 189–198.
Baxevanis, A. D., Kappas, I. & Abatzopoulos, T. J. (2006) Molecular phylogenetics and asexuality in the brine shrimp Artemia. Molecular Phylogenetics and Evolution, 40, 724-738.
Benesch, R. (1969) Zur Ontogenie und Morphologie von Artemia salina L. Zoologische Jahrbücher, Abteilung für Anatomie und Ontogenie der Tiere, 86, 307–458.
Browne, R. A. & Bowen, S. T. (1991) Taxonomy and population genetics of Artemia. In: Browne, R., Sorgeloos, P. & Trotman, N. A. (eds), Artemia Biology. CRC Press, Boca Raton, pp. 221-235.
Bossier, P., Van Stappen, G., Yu, H.-Y., Wang, X.-M., Xin, N.-H., Deloof, D., Delbare, D. & Sorgeloos, P. (2004) Evaluation of mixed status of Asian Artemia populations through RFLP-analysis. Regional Workshop on Artemia Biodiversity (INCO Concerted Action). Urmia, Iran.
Cai, Y.-N. (1989) A redescription of the brine shrimp (Artemia sinica). Wasmann Journal of Biology, 47, 105–110.
Cai, Y.-N. & Gao, L. (1992) Comparative study of the male clasper and its frontal knob of four species of Artemia. Journal of Ocean University of Qingdao, 22, 90–96 (In Chinese with English abstract).
Clark, L. S. & Bowen, S. T. (1976) The genetics of Artemia salina. VII.. Reproductive isolation. The Journal of Heredity, 67, 385–388.
Guan, Y.-Q., Zhang, D.-C. & Yin, X.-C. (2003) Species composition and reproductive traits of Artemia in the Haifeng Saltworks, Bohai Bay. Marine Environmental Science, 22, 1–4 (In Chinese with English abstract).
Hontoria, F. & Amat, F. (1992a) Morphological characterization of adult Artemia (Crustacea, Branchiopoda) from different geographical origin. Mediterranean populations. Journal of Plankton Research, 14, 949–959.
Hontoria, F.. & Amat, F. (1992b) Morphological characterization of adult Artemia (Crustacea, Branchiopoda) from different geographical origin. American populations. Journal of Plankton Research, 14, 1461–1471.
Hou, L., Cai, H.-J. & Zou, X.-Y. (1993) A study on isozymes of ten Artemia strains from China. Acta Zoologica Sinica, 39, 30–37 (In Chinese with English abstract).
Hou, L., Cai, H.-J., Zou, X.-Y. & Yang, G. (1997a) Expression of isozyme genes and taxonomic status of bisexual Artemia from China. Acta Zoologica Sinica, 43, 184–191 (In Chinese with English abstract).
Hou, L., Yang, G. & Cai, H.-J. (1997b) The reproductive isolation among 11 bisexual Artemia strains from China. Transactions of Oceanology and Limnology, (1), 48–52 (In Chinese with English abstract).
Hou, L., Qu, R.-Z., Zou, X. & Zheng, Y.-J. (2003) The analysis of four bisexual Artemia strains by ISSR DNA finger prints. Journal of Liaoning Normal University, 26, 174–177 (In Chinese with English abstract).
Hou, L., Bi, X.-D., Zou, X.-Y., He, C.-B., Yang, L., Qu, R.-Z. & Liu, Z.-J. (2006) Molecular systematics of bisexual Artemia populations. Aquaculture Research, 37, 671–680.
Ma, Z.-Z. (1993) A studies (sic) on the biogeography of brine shrimp, Artemia spp. in China. Modern Fisheries Information, 8, 19-26 (In Chinese with English title).
Mayer, R. J. (2002) Morpholgy and biometry of three populations of Artemia (Branchiopoda: Anostraca) from the Dominican Republic and Puerto Rico. Hydrobiologia, 486, 29–38.
Montgomery, D. C. (1991) Design and Analysis of Experiments. 3rd edition. John Wiley & Sons, Inc., New York. Chinese edition translated by Wang, R. & Cheng, R. (1998). China Statistical Press, Beijing.
Mura, G. (1990) Artemia salina (Linnaeus, 1758) from Lymington, England: frontal knob morphology by scanning electron microscopy. Journal of Crustacean Biology, 10, 364–368.
Mura, G. & Brecciaroli, B. (2004) Use of morphological characters for species separation within the genus Artemia (Crustacea, Branchiopoda). Hydrobiologia, 520, 179–188.
Mura, G., Del Caldo, L. & Fanfani, A. (1989a) Sibling species of Artemia: a light and electron microscopic survey of the morphology of the frontal knobs. Part I. Journal of Crustacean Biology, 9, 414–419.
Mura, G., Fanfani, A. & Del Caldo, L. (1989b) Sibling species of Artemia: a light and electron microscopic survey of the morphology of the frontal knobs. Part II. Journal of Crustacean Biology, 9, 420–424.
Piccinelli, M. & Prosdocimi, T. (1968) Descrizione tassonomica delle due specie Artemia salina L. e Artemia persimilis n. sp. Rendiconti dell’Istituto Lombardo di Scienze e Lettere, 102, 113–118.
Pilla, E. & Beardmore, J. A. (1994) Genetic and morphometric differentiation in Old World bisexual species of Artemia (the brine shrimp). Heredity, 73, 47–56.
Ren, M.-L. & Ren, B. (1996) Biology of Artemia in inland salt lakes of Xinjiang, Qinghai, and Nei Monggol. In: Ren, M.-L., Guo, Y., Wang, J.-L., Su, R., Li, H. & Ren, B. (eds), Survey of Artemia Ecology and Resources in Inland Salt Lakes in Northwest China. Heilongjiang Science and Technology Press, Harbin, pp. 31-43 (In Chinese).
Rogers, D. C., Timms, B. V., Jocquè, M. & Brendonck, L. (2007) A new genus and species of branchipodid fairy shrimp (Crustacea: Branchiopoda: Anostraca) from Australia. Zootaxa, 1551, 49–59.
Rosner, B. (2000) Fundamentals of Biostatistics. 5th edition. Duxbury Press, Belmont, CA. Chinese edition translated by Sun, S. (2004). Science Press, Beijing.
Sun, Y., Song, W.-Q., Zhong, Y.-C., Zhang, R.-S., Abatzopoulos, T. J. & Chen, R.-Y. (1999) Diversity and genetic differentiation in Artemia species and populations detected by AFLP markers. International Journal of Salt Lake Research, 8, 341–350.
Torrentera, L. & Dodson, S. I. (1995) Morphological diversity of populations of Artemia (Branchiopoda) in Yucatan. Journal of Crustacean Biology, 15, 86–102.
Torrentera, L. & Belk, D. (2002) New penis characters to distinguish between two American Artemia species. Hydrobiologia, 470, 149–156.
Triantaphyllidis, G. V., Criel, G. R. J., Abatzopoulos, T. J., Thomas, K. M., Peleman, J., Beardmore, J. A. & Sorgeloos, P. (1997a) International study on Artemia. LVII. Morphological and molecular characters suggest conspecificity of all bisexual European and North African Artemia populations. Marine Biology, 129, 477–487.
Triantaphyllidis, G. V., Criel, G. R. J., Abatzopoulos, T. J. & Sorgeloos, P. (1997b) International study on Artemia. LIII. Morphological study of Artemia with emphasis to Old World strains. I. Bisexual populations. Hydrobiologia, 357, 139–153.
Triantaphyllidis, G. V., Criel, G. R. J., Abatzopoulos, T. J. & Sorgeloos, P. (1997c) International study on Artemia. LIII. Morphological study of Artemia with emphasis to Old World strains. II.. Parthenogenetic populations. Hydrobiologia, 357, 155–163.
Van Stappen, G. (1996) Introduction, biology and ecology of Artemia. In: Lavens, P. & Sorgeloos, P. (eds), Manual on the Production and Use of Live Food for Aquaculture. FAO Fisheries Technical Paper No. 361. FAO, Rome, 79–106.
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.
Wolfe, A. F. (1971) A histological and histochemical study of the male reproductive system of Artemia (Crustacea, Branchiopoda). Journal of Morphology, 135, 51–70.
Wang, S.-F. & Sun, S.-C. (2007) Comparative observations on the cyst shells of seven Artemia strains from China. Microscopy Research and Technique, 70: 663–670.
Xin, N.-H., Sun, J.-J., Zhang, B., Triantaphyllidis, G. V., Van Stappen, G. & Sorgeloos, P. (1994) International Study on Artemia. LI. New survey of Artemia resources in the People’s Republic of China. International Journal of Salt Lake Research, 3, 105–112.
Xin, N.-H., Audenaert, E., Vanoverbeke, J., Brendonck, L., Sorgeloos, P. & De Meester, L. (2000) Low among-population genetic differentiation in Chinese bisexual Artemia populations. Heredity, 84, 238–243.
Yang, G., Cai, H.-J. & Hou, L. (1995) Study on the biological characteristics of Artemia strains from six salt lakes in China. Transactions of Oceanology and Limnology, (3), 39–47 (In Chinese with English abstract).
Zheng, B., Sun, S.-C. & Ma, L. (2004) The occurrence of an exotic bisexual Artemia species, Artemia franciscana, in two coastal salterns of Shandong Province, China. Journal of Ocean University of China, 3, 171–174.
Zhou, K.-X., Xu, M.-Q. & Yin, X.-C. (2003a) Morphological characterization of sexual Artemia (Branchiopoda) from China. Crustaceana, 76, 1331–1346.
Zhou, K.-X., Xu, M.-Q., Guan, Y.-Q. & Yin, X.-C. (2003b) Numeric taxonomy using cysts and nauplii of bisexual Artemia from China. Journal of Lake Sciences, 15, 153–159 (In Chinese with English abstract).
Zhou, K.-X., Xu, M.-Q. & Yin, X.-C. (2006) Constitution of Artemia strains in coastal salterns of Hebei Province. Chinese Journal of Zoology, 41, 1–5 (In Chinese with English abstract).
Zuñiga, O., Wilson, R., Amat, F. & Hontoria, F. (1999) Distribution and characterization of Chilean populations of the brine shrimp Artemia (Crustacea, Branchiopoda, Anostraca). International Journal of Salt Lake Research, 8, 23–40.