Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-18T19:06:11.567Z Has data issue: false hasContentIssue false
  • English
  • Français

Genetic identification of South African Artemia species: invasion, replacement and co-occurrence

Published online by Cambridge University Press:  12 March 2014

Athanasios D. Baxevanis ,
Stefania Maniatsi ,
Dimitrios Kouroupis ,
Konstantinos Marathiotis ,
Ilias Kappas ,
Horst Kaiser  and
Theodore J. Abatzopoulos
Athanasios D. Baxevanis
Affiliation:
Department of Genetics, Development and Molecular Biology, School of Biology, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
Stefania Maniatsi
Affiliation:
Department of Genetics, Development and Molecular Biology, School of Biology, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
Dimitrios Kouroupis
Affiliation:
Department of Genetics, Development and Molecular Biology, School of Biology, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
Konstantinos Marathiotis
Affiliation:
Department of Genetics, Development and Molecular Biology, School of Biology, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
Ilias Kappas
Affiliation:
Department of Genetics, Development and Molecular Biology, School of Biology, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
Horst Kaiser
Affiliation:
Department of Ichthyology and Fisheries Science, PO Box 94, Rhodes University, 6140, South Africa
Theodore J. Abatzopoulos*
Affiliation:
Department of Genetics, Development and Molecular Biology, School of Biology, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
*
Correspondence should be addressed to: T.J. Abatzopoulos, Department of Genetics Development and Molecular Biology, School of Biology, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece email: abatzop@bio.auth.gr
Get access Rights & Permissions [Opens in a new window]

Abstract

Detailed molecular data of Artemia (Crustacea, Anostraca) from South Africa are scarce. Here, we provide for the first time genetic data on the species status and phylogeography of Artemia from this region after an extensive sampling expedition. Our 16S rRNA RFLP analysis of 27 Artemia populations, including seven from South African sites, provides evidence for the presence of a mixed bisexual and parthenogenetic component in this area. Phylogenetic and network analyses reveal that three (out of seven) Artemia populations from South Africa belong to the invasive A. franciscana, two of them belong to A. salina while the last two contain both parthenogenetic and bisexual (A. salina) individuals. From a total of 18 haplotypes identified, seven were recorded from South Africa. To our knowledge, this is the first confirmed report of A. franciscana in this region. Its invasiveness is reaffirmed by evidence for the complete replacement of the native A. salina population from Velddrif Saltworks. However, in other cases, parthenogens seem to modify the capacity of A. franciscana to replace natives. Results on the genetic identification of South African Artemia provide insights into the dynamics of invasion and co-occurrence and highlight effects on species interactions and on biodiversity in inland aquatic invertebrates.

Keywords

brine shrimpendemicitybiogeographyAfricaspecies interactionsArtemia
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 94 , Issue 4 , June 2014 , pp. 775 - 785
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abatzopoulos, T.J., Kastritsis, C.D. and Triantaphyllidis, C.D. (1986) A study of karyotypes and heterochromatic associations in Artemia, with special reference to two N. Greek populations. Genetica 71, 3–10.CrossRefGoogle Scholar
Abatzopoulos, T.J., Zhang, B. and 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.CrossRefGoogle Scholar
Abatzopoulos, T.J., Beardmore, J.A., Clegg, J.S. and Sorgeloos, P. (2002a) Artemia: basic and applied biology. Dordrecht: Kluwer Academic Press.CrossRefGoogle Scholar
Abatzopoulos, T.J., Kappas, I., Bossier, P., Sorgeloos, P. and Beardmore, J.A. (2002b) Genetic characterization of Artemia tibetiana (Crustacea: Anostraca). Biological Journal of the Linnean Society 75, 333–344.CrossRefGoogle Scholar
Abatzopoulos, T.J., Agh, N., Van Stappen, G., Rouhani, S.M. and Sorgeloos, P. (2006) Artemia sites in Iran. Journal of the Marine Biological Association of the United Kingdom 86, 299–307.CrossRefGoogle Scholar
Abatzopoulos, T.J., Amat, F., Baxevanis, A.D., Belmonte, G., Hontoria, F., Maniatsi, S., Moscatello, S., Mura, G. and Shadrin, N.V. (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.CrossRefGoogle Scholar
Amarouayache, M., Derbal, F. and Kara, M.H. (2009) Biological data on Artemia salina (Branchiopoda, Anostraca) from Chott Marouane (northeast Algeria). Crustaceana 82, 997–1005.CrossRefGoogle Scholar
Amat, F., Barata, C. and Hontoria, F. (1995) A Mediterranean origin for the Veldrif (South Africa) Artemia Leach population. Journal of Biogeography 22, 49–59.CrossRefGoogle Scholar
Amat, F., Hontoria, F., Ruiz, O., Green, A.J., Sánchez, M.I., Figuerola, J. and Hortas, F. (2005) The American brine shrimp as an exotic invasive species in the western Mediterranean. Biological Invasions 7, 37–47.CrossRefGoogle Scholar
Bandelt, H.J., Forster, P. and Röhl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.CrossRefGoogle ScholarPubMed
Baxevanis, A.D. (2006) Morphological and genetic differentiation of Old World Artemia strains. PhD thesis. Aristotle University of Thessaloniki, Thessaloniki, Greece.Google Scholar
Baxevanis, A.D. and Abatzopoulos, T.J. (2004) The phenotypic response of ME2 (M. Embolon, Greece) Artemia clone to salinity and temperature. Journal of Biological Research—Thessaloniki 1, 107–114.Google Scholar
Baxevanis, A.D., El-Bermawi, N., Abatzopoulos, T.J. and Sorgeloos, P. (2004) Salinity effects on maturation, reproductive and life span characteristics of four Egyptian Artemia populations (International Study on Artemia. LXVIII). Hydrobiologia 513, 87–100.CrossRefGoogle Scholar
Baxevanis, A.D., Triantaphyllidis, G.V., Kappas, I., Triantafyllidis, A., Triantaphyllidis, C.D. and 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.CrossRefGoogle Scholar
Baxevanis, A.D., Kappas, I. and Abatzopoulos, T.J. (2006) Molecular phylogenetics and asexuality in the brine shrimp Artemia. Molecular Phylogenetics and Evolution 40, 724–738.CrossRefGoogle ScholarPubMed
Ben Naceur, H., Ben Rejeb Jenhani, A. and Romdhane, M.S. (2010) Biological characterization of the new invasive brine shrimp Artemia franciscana in Tunisia: Sabkhet Halk El-Menzel. International Journal of Biological and Life Sciences 6, 131–137.Google Scholar
Ben Naceur, H., Ben Rejeb Jenhani, A. and Romdhane, M.S. (2012) Quality characterization of cysts of the brine shrimp Artemia salina from Tunisia focusing on their potential use in aquaculture. Journal of Biological Research—Thessaloniki 17, 16–25.Google Scholar
Bilton, D.T., Freeland, J.R. and Okamura, B. (2001) Dispersal in freshwater invertebrates. Annual Review of Ecology and Systematics 32, 159–181.CrossRefGoogle Scholar
Bossier, P., Xiaomei, W., Catania, F., Dooms, S., Van Stappen, G., Naessens, E. and Sorgeloos, P. (2004) An RFLP database for authentication of commercial cyst samples of the brine shrimp Artemia spp.. International Study on Artemia LXX. Aquaculture 231, 93–112.CrossRefGoogle Scholar
Dhont, J. and Sorgeloos, P. (2002) Applications of Artemia. In Abatzopoulos, T.J., Beardmore, J.A., Clegg, J.S. and Sorgeloos, P. (eds) Artemia: basic and applied biology. Dordrecht: Kluwer Academic Press, pp. 251–277.CrossRefGoogle Scholar
El-Bermawi, N., Baxevanis, A.D., Abatzopoulos, T.J., Van Stappen, G. and Sorgeloos, P. (2004) Salinity effects on survival, growth and morphometry of four Egyptian Artemia populations (International Study on Artemia. LXVII). Hydrobiologia 523, 175–188.CrossRefGoogle Scholar
El-Gamal, M. (2010) Morphometric and molecular variability of three Artemia strains (El–Max and Wadi El-Natrun, Egypt and San Francisco Bay, U.S.A). Journal of American Science 6, 98–107.Google Scholar
El-Magsodi, M.O., El-Ghebli, H.M., Hamza, M., Van Stappen, G. and Sorgeloss, P. (2005) Characterization of Libyan Artemia from Abu Kammash Sabkha. Libyan Journal of Marine Science 10, 19–30.Google Scholar
Excoffier, L., Smouse, P. and Quattro, J. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.CrossRefGoogle ScholarPubMed
Figuerola, J. and Green, A.J. (2002) Dispersal of aquatic organisms by waterbirds: a review of past research and priorities for future studies. Freshwater Biology 47, 483–494.CrossRefGoogle Scholar
Gajardo, G., Abatzopoulos, T., Kappas, I. and Beardmore, J. (2002) Evolution and speciation. In Abatzopoulos, T.J., Beardmore, J.A., Clegg, J.S. and Sorgeloos, P. (eds) Artemia: basic and applied biology. Dordrecht: Kluwer Academic Press, pp. 225–250.CrossRefGoogle Scholar
Gajardo, G., Crespo, J., Triantafyllidis, A., Tzika, A., Baxevanis, A.D., Kappas, I. and Abatzopoulos, T.J. (2004) Species identification of Chilean Artemia populations based on mitochondrial DNA RFLP analysis. Journal of Biogeography 31, 547–555.CrossRefGoogle Scholar
Gertzen, E.L. and Leung, B. (2011) Predicting the spread of invasive species in an uncertain world: accommodating multiple vectors and gaps in temporal and spatial data for Bythotrephes longimanus. Biological Invasions 13, 2433.CrossRefGoogle Scholar
Green, A.J. and Figuerola, J. (2005) Recent advances in the study of long-distance dispersal of aquatic invertebrates via birds. Diversity and Distributions 11, 149–156.CrossRefGoogle Scholar
Green, A.J., Sánchez, M.I., Amat, F., Figuerola, J., Hontoria, F., Ruiz, O. and Hortas, F. (2005) Dispersal of invasive and native brine shrimps Artemia (Anostraca) via waterbirds. Limnology and Oceanography 50, 737–742.CrossRefGoogle Scholar
Griffiths, C.L. (1999) Crustacean systematic in South Africa—status and historical overview. Transactions of the Royal Society of South Africa 54, 43–52.CrossRefGoogle Scholar
Hajirostamloo, M. and Pourrabbi, R. (2011) Genetic differentiation of Artemia franciscana in a new environment (Iran). World Journal of Zoology 6, 16–21.Google Scholar
Hamer, M. (2010) African invertebrates in the international year of biodiversity. African Invertebrates 51, 223–230.CrossRefGoogle Scholar
Hickman, C.P. -Jr., Roberts, L.S. and Larson, A. (2001) Integrated principles of zoology. New York: McGraw-Hill.Google Scholar
Hontoria, F. and Amat, F. (1992) Morphological characterization of adult Artemia (Crustacea, Branchiopoda) from different geographical origins. Mediterranean populations. Journal of Plankton Research 14, 949–959.CrossRefGoogle Scholar
Kaiser, H., Gordon, A.K. and Paulet, T.G. (2006) Review of the African distribution of the brine shrimp genus Artemia. Water SA 32, 597–603.Google Scholar
Kappas, I., Abatzopoulos, T.J., Van Hoa, N., Sorgeloos, P. and Beardmore, J.A. (2004) Genetic and reproductive differentiation of Artemia franciscana in a new environment. Marine Biology 146, 103–117.CrossRefGoogle Scholar
Kappas, I., Baxevanis, A.D., Maniatsi, S. and Abatzopoulos, T.J. (2009) Porous genomes and species integrity in the branchiopod Artemia. Molecular Phylogenetics and Evolution 52, 192–204.CrossRefGoogle ScholarPubMed
Maniatsi, S., Kappas, I., Baxevanis, A.D., Farmaki, T. and Abatzopoulos, T.J. (2009a) Sharp phylogeographic breaks and patterns of genealogical concordance in the brine shrimp Artemia franciscana. International Journal of Molecular Sciences 10, 5455–5470.CrossRefGoogle ScholarPubMed
Maniatsi, S., Baxevanis, A.D. and Abatzopoulos, T.J. (2009b) The intron 2 of p26 gene: a novel genetic marker for discriminating the two most commercially important Artemia franciscana subspecies. Journal of Biological Research—Thessaloniki 11, 73–82.Google Scholar
Maniatsi, S., Baxevanis, A.D., Kappas, I., Deligiannidis, P., Triantafyllidis, A., Papakostas, S., Bougiouklis, D. and Abatzopoulos, T.J. (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.CrossRefGoogle ScholarPubMed
McElroy, D., Moran, P., Birmingham, E. and Kornfield, J. (1991) REAP: the restriction enzyme analysis package, version 4.0. Orono, ME: University of Maine.Google Scholar
Micklin, P. (2007) The Aral Sea disaster. Annual Review of Earth and Planetary Sciences 35, 47–72.CrossRefGoogle Scholar
Mito, T. and Uesugi, T. (2004) Invasive alien species in Japan: the status quo and the new regulation for prevention of their adverse effects. Global Environmental Research 8, 171–191.Google Scholar
Mooney, H.A. and Gleland, E.E. (2001) The evolutionary impact of invasive species. Proceedings of the National Academy of Sciences of the United States of America 98, 5446–5451.CrossRefGoogle ScholarPubMed
Muñoz, J., Gómez, A., Green, A.J., Figuerola, J., Amat, F. and Rico, C. (2010) Evolutionary origin and phylogeography of the diploid obligate parthenogens Artemia parthenogenetica (Branchiopoda: Anostraca). PLoS ONE 5, e11932. doi:10.1371/journal.pone.0011932.CrossRefGoogle Scholar
Mura, G. and Nagorskaya, L.L. (2005) Notes on the distribution of the genus Artemia in the former USSR countries (Russia and adjacent regions). Journal of Biological Research—Thessaloniki 4, 139–150.Google Scholar
Mura, G., Baxevanis, A.D., Lopez, G.M., Hontoria, F., Kappas, I., Moscatello, S., Fancello, G., Amat, F. and Abatzopoulos, T.J. (2005) The use of a multidisciplinary approach for the characterization of a diploid parthenogenetic Artemia population from Torre Colimena (Apulia, Italy). Journal of Plankton Research 27, 895–907.CrossRefGoogle Scholar
Mura, G., Kappas, I., Baxevanis, A.D., Moscatello, S., D'Amico, Q., Lopez, G.M., Hontoria, F., Amat, F. and Abatzopoulos, T.J. (2006) Morphological and molecular data reveal the presence of the invasive Artemia franciscana in Margherita di Savoia salterns (Italy). International Review of Hydrobiology 91, 539–554.CrossRefGoogle Scholar
Mura, G., Özkütük, S.R., Aygen, C. and Cottarelli, V. (2011) New data on the taxonomy and distribution of anostracan fauna from Turkey. Journal of Biological Research—Thessaloniki 15, 17–23.Google Scholar
Palumbi, S.R. (1996) Nucleic acids II: the polymerase chain reaction. In Hillis, D.M., Moritz, C. and Mable, B.K. (eds) Molecular systematics. Sunderland, MA: Sinauer Associates, pp. 205–247.Google Scholar
Pinto, P.M., Bio, A., Hontoria, F., Almeida, V. and Vieira, N. (2013) Portuguese native Artemia parthenogenetica and Artemia franciscana survival under different abiotic conditions. Journal of Experimental Marine Biology and Ecology 440, 81–89.CrossRefGoogle Scholar
Ricciardi, A. (2007) Are modern biological invasions an unprecedented form of global change? Conservation Biology 21, 329–336.CrossRefGoogle ScholarPubMed
Ruebhart, D.R., Cock, I.E. and Shaw, G.R. (2008) Invasive character of the brine shrimp Artemia franciscana Kellogg 1906 (Branchiopoda: Anostraca) and its potential impact on Australian inland hypersaline waters. Marine Freshwater Research 59, 587–595.CrossRefGoogle Scholar
Schneider, S., Roessli, D. and Excoffier, L. (2000) Arlequin ver. 2.000: a software for population genetics data analysis. Geneva: Genetics and Biometry Laboratory, University of Geneva.Google Scholar
Shadrin, N. and Anufriieva, E. (2012) Review of the biogeography of Artemia Leach, 1819 (Crustacea: Anostraca) in Russia. International Journal of Artemia Biology 2, 51–61.Google Scholar
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.CrossRefGoogle ScholarPubMed
Thiéry, A. and Robert, F. (1992) Bisexual populations of the brine shrimp Artemia in Sète-Villeroy and Villeneuve saltworks (Languedoc, France). International Journal of Salt Lake Research 1, 47–63.CrossRefGoogle Scholar
Triantaphyllidis, G.V., Abatzopoulos, T.J., Miasa, E. and Sorgeloos, P. (1996) International study on Artemia. LVI. Characterization of two Artemia populations from Namibia and Madagascar: cytogenetics, biometry, hatching characteristics and fatty acid profiles. Hydrobiologia 355, 97–106.CrossRefGoogle Scholar
Triantaphyllidis, G.V., Criel, G.R.J., Abatzopoulos, T.J., Thomas, K.M., Peleman, J., Beardmore, J.A. and Sorgeloos, P. (1997) Morphological and molecular characters suggest conspecificity of all bisexual European and North African Artemia populations. International Study on Artemia LVII. Marine Biology 129, 477–487.CrossRefGoogle Scholar
Triantaphyllidis, G., Abatzopoulos, T. and Sorgeloos, P. (1998) Review of the biogeography of the genus Artemia (Crustacea, Anostraca). Journal of Biogeography 25, 213–226.CrossRefGoogle Scholar
Valverde, J.R., Batuecas, B., Moratilla, C., Marco, R. and Garesse, R. (1994) The complete mitochondrial DNA sequence of the crustacean Artemia franciscana. Journal of Molecular Evolution 39, 400–408.CrossRefGoogle Scholar
Vanhaecke, P., Tackaert, W. and Sorgeloos, P. (1987) The biogeography of Artemia: an updated review. In Sorgeloos, P., Bengston, D.A., Decleir, W. and Jaspers, E. (eds) Artemia research and its applications. Morphology, genetics, strain characterization, toxicology. Volume 1. Wetteren: Universa Press, pp. 129–155.Google Scholar
Vanschoenwinkel, B., Gielen, S., Seaman, M. and Brendonck, L. (2008a) Any way the wind blows—frequent wind dispersal drives species sorting in ephemeral aquatic communities. Oikos 117, 125–134.CrossRefGoogle Scholar
Vanschoenwinkel, B., Gielen, S., Vandewaerde, H., Seaman, M. and Brendonck, L. (2008b) Relative importance of different dispersal vectors for small aquatic invertebrates in a rock pool metacommunity. Ecography 31, 567–577.CrossRefGoogle Scholar
Van Stappen, G. (2002) Zoogeography. In Abatzopoulos, T.J., Beardmore, J.A., Clegg, J.S. and Sorgeloos, P. (eds) Artemia: basic and applied biology. Dordrecht: Kluwer Academic Press, pp. 171–224.CrossRefGoogle Scholar
Van Stappen, G., Yu, H., Wang, X., Hoffman, S., Cooreman, K., Bossier, P. and 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/Archiv für Hydrobiologie 170, 21–28.CrossRefGoogle Scholar
Van Stappen, G., Litvinenko, L.I., Litvinenko, A.I., Boyko, E.G., Marden, B. and Sorgeloos, P. (2009) A survey of Artemia resources of Southwest Siberia (Russian Federation). Reviews in Fisheries Science 17, 116–148.CrossRefGoogle Scholar
Vikas, P.A., Sajeshkumar, N.K., Thomas, P.C., Kajal, Chakraborty and Vijayan, K.K. (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.CrossRefGoogle Scholar