Research

A biometric and ecologic comparison between Artemia from Mexico and Chile

Thalía B Castro¹ , Gonzalo Gajardo^2* , Jorge M Castro^1* and Germán M Castro^1*

¹  Universidad Autónoma Metropolitana-Xochimilco. Departamento "El Hombre y su Ambiente Calzada del Hueso No.1100. Col. Villa Quietud 04960, D.F., Mexico

²  Laboratory of Genetics & Aquaculture, Department of Basic Sciences. Universidad de los Lagos, Osorno, Chile

author email corresponding author email* Contributed equally

Saline Systems 2006, 2:13doi:10.1186/1746-1448-2-13

The electronic version of this article is the complete one and can be found online at: http://www.salinesystems.org/content/2/1/13

Received:	27 September 2006
Accepted:	24 November 2006
Published:	24 November 2006

© 2006 Castro et al; licensee BioMed Central Ltd.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background

A preliminary biometric and ecologic database for the brine shrimp Artemia from Mexico and Chile is presented. The area abounds in small and seasonal ponds and large inland lakes, the latter mainly located in Mexico, although relatively large and isolated lakes are found in complex hydrological settings in pre-high plateau areas of Chile. This paper summarizes research efforts aimed at the localization, characterization, and evaluation of the aquaculture potential of Artemia populations in Mexico and Chile, which exhibit great habitat diversity (ponds, salterns, coastal lagoons, sea arms, coastal and inland lakes), contrasting weather conditions and different levels of isolation and human intervention.

Results

This study covered locations between 29° north latitude (Baja California, Mexico) to 50° south latitude (Puerto Natales, Chile). Biological characteristics considered are species name, reproductive mode, cyst diameter, chorion thickness, and nauplius length, whereas ecological data include pond size, pH, salinity, temperature, and water ionic composition. Artemia franciscana is the only species found in Mexico, it exists together with A. persimilis in Chile, though separated geographically. Ecological differences in habitat exist between both regions but also within countries, a pattern particularly clear with regard to water composition. Surprisingly, a Mexican (Cuatro Ciénegas, A. franciscana) and a Chilean location (Torres del Paine, A. persimilis) share habitat characteristics, at least for the period when data were collected. The discriminat analysis for cyst diameter and nauplius length shows that Artemia from only one location match in cyst diameter with those from San Francisco Bay (SFB) (Point Lobos), and one (Marquez) is far apart from SFB and all the others. The Chilean locations (Pampilla, Cejar, Cahuil, Llamara, Yape) share cyst diameter, but tend to differ from SFB. The remaining Mexican locations (Juchitan, Ohuira, Yavaros) are well separated from all the others. With regard to nauplii length, populations tend to distribute in a relatively random manner, being Marquez the location differing the most in cyst diameter from SFB.

Conclusion

This database will contribute to the knowledge of radiation centers and serves as a baseline for further biogeographic studies, population characterization, management, and monitoring of Artemia biodiversity. Likewise, the impact of colonization and translocations for aquaculture purposes can be better assessed with a baseline for reference. Mexico and Chile exemplify the need to increase and further integrate regional information to tackle fundamental problems underlying practical utilization of Artemia.

Background

The brine shrimp Artemia is widely distributed in salt lakes, coastal lagoons, and solar saltworks in all continents, except Antarctica [1]. Since the initial record of 80 Artemia sites (Abonyi, 1915; Artom, 1922; Stella, 1933; Mathias, 1937; all cited in Persoone & Sorgeloos [2], the number has steadily increased, for example, Vanhaecke et al. [3] and Triantaphyllidis et al. [4], reported a total of 350 and 500 Artemia locations, respectively. The search for new Artemia populations, or locally adapted populations, is relevant to solve fundamental questions on population differentiation in stressful habitats, but also to counterbalance the decline of Artemia cysts, which are highly demanded for aquaculture [5]. Hence, the search for alternative Artemia resources has intensified in recent years, especially in large and productive inland lakes that are amenable to commercial exploitation.

This study gathers and compares biometric and reproductive data of Artemia populations from ecologically diverse ecosystems (ponds, salterns, salt ponds, coastal lagoons, sea arms, coastal and inland lakes) from Mexico and Chile, two countries with potential Artemia sources for aquaculture. Important morphological and geological changes, such as the joining of North and South America during the Tertiary and the rising of the occidental and oriental slopes of the Andes Mountains, have influenced the area in the past, greatly affecting the current distribution pattern of many aquatic species.

Two Artemia species are currently found in the Americas, A. franciscana (Kellog, 1906) and A. persimilis (Piccinelli & Prosdocimi, 1968). The former is widely distributed over the Americas, whilst the latter was thought to be restricted to Argentina [6]. However, the finding of A. persimilis in a very unusual site in the Chilean Patagonia [7] and later of A. franciscana in Argentina [8], changed the distribution scenario. Most populations in Chile and adjacent areas are recognized as A. franciscana, but exhibit varying degrees of genetic differentiation in relation to the commonly used A. franciscana type (San Francisco Bay, Salt Lake) [9-11]. This distribution pattern requires more systematic and careful data analysis of populations in radiation centers, since A. persimilis could be in the process of colonizing new habitats in Chile and other countries in South America, while A. franciscana, a very successful colonizer [1], has been translocated by aquaculture activities and is currently expanding its range in Europe and Asia. This database will be useful for the spatial and temporal monitoring of Artemia biodiversity, particularly considering the ability of Artemia to invade other environments, either by translocation for aquaculture purposes or through natural dispersal, as has been demonstrated in the western Mediterranean for A. franciscana [12,13].

Results

Artemia sites in Mexico

Habitat information

Artemia ranges from 32° and 14° north latitude, and between 117° (Northeast of Baja California) and 86° West (Isla Mujeres). Seventeen Artemia populations have been recorded so far in this country, 14 of them in coastal areas (4 in the Gulf of Mexico, 10 in the Pacific Coast) whereas the rest corresponds to inland habitats [14]. Table 1 describes the geographic location, size, and altitude of the Artemia sites studied so far in Mexico. The largest site is Guerrero Negro, in the Baja California Peninsula, with 33,000 ha, whereas San Jose, in the same Peninsula, is the smallest (0.5 ha) and comparable in size to San Crisanto in the Yucatan Peninsula. Texcoco, in the State of Mexico, is located at the highest altitude (2,250 m above sea level).

The main water component of biotopes studied so far is sodium chloride, with the exception of Cuatro Cienegas, State of Coahuila, in which sulphate predominates (Table 2).

Biological data

Of all populations recorded in this area, 13 have been studied with respect to reproduction (crosses with A. franciscana) and morphology, whilst fragmentary genetic information (allozyme and chromosome) is available. These populations combine the two usual modes of reproduction (encystment and ovoviviparity), depending on the local conditions [6,15-28].

Table 3 provides cysts, chorion thickness, and nauplii measurements. The El Marquez population in Oaxaca depicts the biggest cyst diameter and the thickest chorion, whilst samples from Bahia de Lobos and Celestun showed the smallest cysts and nauplii.

Artemia sites in Chile

Habitat information

Table 4 displays geographical coordinates, size, and altitude of the Artemia sites arranged from north to south, with the Salar (saltflat) Surire (18° South latitude) and Laguna Amarga (50° South latitude) being at opposite ends. The former is at the highest altitude in the Americas (4,200 m above sea level) in the Atacama Desert, reputedly one of the most arid areas in the world [9]. The desert, located in the subtropical area of Chile and limited by the Pacific Ocean to the West and the Andes Mountains to the East, in the so-called pre-high plateau zone, has plenty of saltflats, which are complex hydrological units that very likely evolved from a lacustrine system through a combination of geological, morphological, hydrological, volcanic and climatic factors [19]. Such saltflats represent therefore interesting and unique Artemia sites due to their isolation, altitude, and extreme ecological conditions (5 to 40°C day-night variation in summer time) [9], that offer few chances for colonization and/or survival of foreign populations.

Laguna Amarga (50° south latitude) is closer to the sea and correspondingly exhibits relatively high concentrations of sodium chloride, whereas high-plateau inland lakes in northern Chile, such as Surire, are athalassohaline, with high content of sulphate (60.38 g L^-1) and potassium (7.48 g L^-1) (Table 5).

Biological data

The largest cysts diameter is found in Laguna Amarga (254.7 μm), whilst Poza Pampilla (220.5 μm) is the smallest. The longest and shortest nauplii are found in the Salar de Llamara (424 μm) and Poza Pampilla (395 μm), respectively (Table 6). Laboratory cross-breeding experiments show different degrees of reproductive output and varying ratios of offsprings in the form of cyst and nauplii, depending on whether crosses are within or between species [11,30-33].

Data integration

The discriminant analysis of figure 1 integrates water composition results from both areas. Although variation exists within Mexico and Chile, greater differentiation was observed between habitats at the regional level, i.e., between countries. Surprisingly, a Mexican (Cuatro Ciénegas, A. franciscana) and a Chilean location (Torres del Paine, A. persimilis) share habitat characteristics, at least for the period when data were collected. Figure 2 shows the discriminat analysis for cyst diameter (a) and nauplius length (b). One location matches cyst diameter with San Francisco Bay (SFB) (Point Lobos) and one (Marquez) is far apart from SFB and all the others. The Chilean locations (Pampilla, Cejar, Cahuil, Llamara, Yape) share cyst diameter, but tend to differ from SFB. The remaining Mexican locations separate well from all the others (Juchitan, Ohuira, Yavaros). Clear differences in cyst diameter are observed among Mexican populations. With regard to nauplii length, populations tend to distribute in a relatively random manner over the two axes, with Marquez, the location greatly differing in cyst diameter to SFB now coming closer to it.

Discussion

Too often management decisions are taken without the back-up of basic knowledge. Many reasons justify the need to document biometric and ecologic characteristics of Artemia sites, either worldwide or at regional level. Firstly, Artemia offers a good model to understand how natural populations evolve, considering the isolation and extreme ecological conditions of hypersaline habitats that promote the differentiation of local populations, or adaptations. Hence the speciation mode best describing the Artemia situation is adaptive divergence [6,34]. Secondly, local populations exhibit differences in specific phenotypic traits some of which are of practical interest (cyst diameter, nauplii length) for aquaculture. Thirdly, Artemia biodiversity is being threatened by the translocation of species and/or populations aimed at improving aquaculture operations or salt production, particularly in developing countries. Last but not least, A. franciscana often the best choice for aquaculture, is a successful invader that could threaten locally adapted or native populations or species, as reported in the Western Mediterranean for parthenogenetic types and A. salina [12,13]. For these reasons, a biometrical and ecological database should serve as a baseline for further spatial and temporal monitoring of A. franciscana and A. persimilis. For the former species, relatively pure gene pools would be those located in inland lakes of northern Chile. Additionally, Chile is the southern end for the distribution of A. franciscana and normally populations in the edge of distribution tend to differ from those in the center [35]. On the other hand, Mexico is located, relatively, at the central area of distribution for A. franciscana, as compared to Chile, and combines the occurrence of exploited and non-exploited salt lakes.

Although this work is aimed to document key biometric and ecological characteristics of Artemia sites in both countries, beyond to what has been reported so far [36], this incipient database allows for some initial conclusions. For example, water ionic composition of Artemia habitats from Mexico and Chile differ as expected (Fig 1). Some within-country variations exist but it is interesting to see two Chilean (Salar de Atacama; Torres del Paine) and one Mexican population (Cuatro Cienegas) segregated from the rest. This is somewhat correlated with the genetic composition. Salar de Atacama (SAT) is genetically distinct from the rest of the Chilean populations (ascribed to A. franciscana), and from San Francisco Bay, the reference sample often used for species verification [37]. Since Torres del Paine (TPA) corresponds to A. persimilis, this would be an indication that A. franciscana and A. persimilis share, to some extent, some habitat characteristics. However, this remains to be proved.

The observed divergence of Artemia locations from both areas offers the possibility of finding new populations for aquaculture. As summarized in this paper, only A. franciscana, the most widely distributed species in the Americas, is found in Mexico, whilst Chile has both, A. franciscana and A. persimilis, though separated geographically [30,1], offering an interesting opportunity to understand the ecological separation of these sibling species.

The average cyst diameter reported for Artemia franciscana is 237 ± 14 μm, while the average nauplii length is 431 ± 23 μm [3]. As expected, most populations considered in this study are highly heterogeneous, with cyst diameter deviating from the reference sample of A. franciscana, except for Lobos in Mexico (see Fig. 2). Although small-sized A. franciscana populations (SFB, GSL) are preferred for aquaculture, the heterogeneity in cyst diameter in the samples should be seen as an opportunity for aquaculture diversification, as different species have different larval sizes.

Differential environmental conditions in Mexico and Chile and the magnitude of Artemia exploitation in Mexico, which is contrasting to the situation in Chile, are likely to explain the observed north-south cyst differences (cyst tends to be smaller in Chile). Likewise, heterogeneity in cyst diameter in the Mexican samples is greater than in the Chilean ones, which tend to group relatively closer in Fig 2.

Some fundamental and practical conclusions emerge from this study. Habitat heterogeneity, particularly water ionic composition, correlates with heterogeneity observed in cyst diameter and nauplii length. At least for the period considered, Mexican samples showed greater cyst diameter variability, though it is possible that the higher level of human intervention in Mexico plays a role (Artemia and salt production often imply population translocation). This might be also a reflection of the higher variability expected at the center of distribution (Mexico) in comparison to populations in the periphery (Chile). Hence, it is clear that biological properties of populations need to be complemented with more careful and systematic description of Artemia environments, particularly considering their monitoring on a long-term basis. Updating the database, including other traits, is thus a need for understanding the evolution of Artemia populations in nature and the consequences this might have in opening opportunities for invasion or colonization of new populations or species.

Methods

As this work gathers published information, methodology is extensively described in each of the 21 and 10 papers cited from Mexico and Chile, respectively. Although information is still insufficient, papers from Mexico cover 10 States, whereas that from Chile deals with the two New World species that are found in amazingly contrasting settings: A. franciscana in lakes scattered in one of the driest deserts in the world and A. persimilis at one of the southernmost latitudes where Artemia is found.

Data in the Access file are classified according the following criteria: geographic coordinates, biotope information (pond size, pH, salinity, temperature, cations, e.g., sodium, potassium, calcium, magnesium), and anions (chloride, sulphate, carbonates, and bicarbonates), and biological data (species name, reproductive mode, cyst diameter, chorion thickness. and nauplius length).

Calculations and statistics

The main ecological characteristics of the different habitats in Mexico and Chile obtained in this paper were analyzed by a multivariate discriminant analysis using Statgraphics (Satistical Graphics Co., Rockville, USA), with the origin of sites taken as the separation factor.

Authors' contributions

TBC Co-designed the manuscript, participated in Mexican populations data collections and wrote the manuscript.

GG Co-designed the manuscript, participated in Chilean populations data collections and wrote the initial English version of the manuscript.

JMC and GMC participated in Mexican populations data collections, co-edited the manuscript and performed data analyses.

All authors have read and approved the final manuscript.

Acknowledgements

The need to set local and regional databases stems from discussions carried out within the framework of the project Artemia biodiversity (EU contract Nr.ICA4-2000-10067), coordinated by the Laboratory of aquaculture & Artemia Reference Center, University Gent, Belgium. The authors are indebted to Professor Jim Clegg for suggestions to an earlier version of the manuscript. Ingrid Brust polished the English version of the manuscript.

References

1. Gajardo G, Parraguez M, Colihueque N: Karyotype analysis and chromosome banding of the Chilean-Peruvian scallop Argopecten purpuratus (Lamarck, 1819).

   Journal of Shellfish Research 2002, 21(2):585-590.

2. Persoone G, Sorgeloos P: General aspects of the ecology and biogeography of Artemia. In The brine shrimp Artemia Ecology Culturing Use in Aquaculture. Volume 3. Edited by: Persoone G, Sorgeloos P, Roels O, Jaspers E. Universa press, Wetteren, Belgium; 1987:3-24.

3. Triantaphyllidis GV, Abatzopoulos TJ, Sorgeloos P: Review of the biogeography of the genus Artemia (Crustacea, Anostraca).

   Journal of Biogeography 1998, 25:213-226. Publisher Full Text

4. Torrentera L, Dodson SI: Morphological diversity of populations of Artemia (Branchiopoda) in Yucatan.

   Journal of Crustacean Biology 1995, 15(1):86-102. Publisher Full Text

5. Dhont J, Sorgeloos P: Applications of Artemia. In Artemia Basic and Applied Biology. Edited by: Abatzopoulos Th, Beardmore JA, Clegg JS, Sorgeloos P. Kluwer Academic Publishers, Dordrecht; 2002:251-277.

6. Abreu-Grobois FA: A review of the genetics of Artemia. In Artemia Research and its Applications Morphology Genetics Population Characteristics. Volume 1. Edited by: Sorgeloos P, Bengtson DA, Decleir W, Jaspers E. Universa press, Wetteren, Belgium; 1987:61-99.

7. Gajardo G, Colihueque N, Parraguez M, Sorgeloos P: International study on Artemia . LVIII. Morphological differentiation and reproductive isolation of Artemia populations from South America.

   International Journal of Salt Lake Research 1998, 7(2):133-151.

8. Cohen RG, Amat F, Hontoria F, Navarro JC: Preliminary characterization of some Argentinean Artemia populations from la Pampa and Buenos Aires provinces.

   International Journal of Salt Lake Research 1999, 8:329-340.

9. Gajardo G, Wilson R, Zuñiga O: Report on the occurence of Artemia in a saline deposit of the Chilean Andes.

   Crustaceana 1992, 63(2):169-174.

10. Gajardo G: Genetical and phenotypical characterization of Artemia populations from South America: relevance for aquaculture.

    Memorias II Congreso Ecuatoriano de Acuicultura 1993, 91-95.

    (ISBN-9978-82-400-6)

11. Gajardo MG, Beardmore AJ: Electrophoretic evidence suggests that the Artemia found in the Salar de Atacama, Chile, is A. franciscana Kellog.

    Hydrobiologia 1993, 257:65-71.

12. Amat F, Hontoria F, Ruiz O, Green AJ, Sánchez MI, Figuerola F, Hortas F: The American brine shrimp as an exotic invasive species in the western Mediterranean.

    Biological Invasions 2005, 7:37-47. Publisher Full Text

13. Green AJ, Sanchez MI, Amat F, Figuerola J, Hontoria F, Ruiz O, Hortas F: Dispersal of invasive and native brine shrimps Artemia (Anostraca) via waterbirds.

    Limnology and Oceanography 2005, 50(2):737-742.

14. Castro BT, Malpica SA, Castro MJ, Castro MG, De Lara AR: Environmental and biological characteristics of Artemia ecosystems in México: An updated review. In Aquatic ecosistems of Mexico Status and Scope. Edited by: Munawar M, Lawrence SG, Munawar IF, Malley DF. Ecovision World Monograph Series. Backhuys Publishers, Leiden, The Netherlands; 2000:121-201.

15. Castro BT: Biología y cultivo de Artemia franciscana en el ex lago de Texcoco, de Ecatepec, Estado de México.

    PhD Thesis Universidad Nacional Autónoma de México 1993.

16. Castro BT, Castro MJ, López CJ, Miramontes B, Malpica SA, Castro MG, De Lara AR: Primeros estudios del branquiopodo Artemia,. en las salinas "Real de las Salinas", Campeche.

    Oceanología 1998, 17:15-27.

17. Castro G, Castro J, De Lara R, Gallardo C, Salazar I, Sanchez B: Características biométricas generales, modo de reproducción y aislamiento reproductivo de la población silvestre de Artemia sp. de Las Salinas de Hidalgo, San Luis Potosí.

    Revista Latinoamericana de Acuicultura 1989, 39:18-25.

18. Castro MG, Castro MJ, Castro BT, De Lara AR, Malpica SA: Evaluación de la composición y la densidad de la población de Artemia franciscana en la salina Tres Hermanos en Yavaros, Sonora.

    Oceanología 1996, 1:127-136.

19. Castro BT, Castro MG, Castro MJ, Malpica SA, De Lara AR: Características morfométricas y calidad de los quistes de Artemia sp. (Crustacea: anostraca), habitante de aguas sulfatadas de Coahuila, México.

    Ciencias Marinas 1997, 491-503.

20. Castro MJ, Malpica SA, Bravo CG, De Lara AR, Castro BT: Morfometria de la población de Artemia franciscana de Bahia de Ceuta, Sinaloa.

    Oceanología 1997, 14:155-167.

21. Castro MJ, Malpica SA, López CJ, Castro MG, Castro BT, De Lara AR: Evaluación morfometrica de la población de Artemia franciscana de Yavaros, Sonora.

    Oceanología 1997, 1:143-153.

22. Castro MJ, Malpica SA, Rodríguez GSA, Castro BT, De Lara AR: Análisis morfométrico de la Artemia spp. en las salinas Las Coloradas Oaxaca, México.

    Oceanología 1995, 2:117-128.

23. Castro BT, Sanchez LR, De Lara AR: Natural Sources of Brine Shrimp (Artemia) in Mexico. In Artemia Research and its applications Ecology Culturing use in Aquaculture. Volume 3. Edited by: Sorgeloos P, Bengtson DA, Decleir W, Jaspers E. Universa Press. Wetteren, Belgium; 1987:153-159.

24. Correa SF: Caracterización biológica y bioquímica de algunas poblaciones de Artemia franciscana Kellog, 1906. In PhD Thesis. Centro de Investigación Científica y Educación Superior de Ensenada, Baja California Mexico; 1991.

25. Diaz AFMI: Caracterizacion morfometrica y reproductiva de la población mexicana de Artemia sp. presente en la salina "Sol de Fuego", Bahia de Ohuira, Sinaloa, México; e hibridación con Artemia franciscana. In Thesis. Universidad Autónoma Metropolitana – Xochimilco México; 2000.

26. Gallardo RC, Castro MJ: Reproduction and genetics of Mexican Artemia. In Artemia Research and its applications Morphology Genetics Population Characteristics. Volume 1. Edited by: Sorgeloos P, Bengtson DA, Decleir W, Jaspers E. Universa Press. Wetteren, Belgium; 1987:249-253.

27. Nuñez VIP: Caracterización morfometrica y reproductiva de la población de Artemia sp. presente en la Laguna de Celestun, Yucatán; e hibridación con Artemia franciscana. In Thesis. Universidad Autónoma Metropolitana – Xochimilco México; 1999.

28. Tena V Informe Técnico centro de acuacultura del Departamento de Pesca Tonala Chiapas México; 1977.

29. Chong DG: The Cenozoic saline deposits of the Chilean Andes between 18°00' and 27°00' south latitude.

    Lecture Notes in Earth Sciences 1988., 17:

30. Gajardo G, Mercado C, Beardmore JA, Sorgeloos P: International study on Artemia. LX.

    Allozyme data suggest that a new Artemia population in southern Chile (50°29'S; 73°45'W) is A. persimilis 1999, 405:117-123.

31. Gajardo G, Beardmore JA: Coadaptation: lessons from the brine shrimp Artemia, "the aquatic Drosophila (Crustacea, Anostraca).

    Revista Chilena de Historia Natural 2001, 74:65-72.

32. Gajardo G, Parraguez P, Beardmore JA, Sorgeloos P: Reproduction in the brine shrimp Artemia : evolutionary relevance of cross-fertility tests.

    Journal of Zoologie 2001, 253:25-32.

33. Van Stappen G: Zoogeography. In Artemia Basic and Applied Biology. Edited by: Abatzopoulos Th, Beardmore JA, Clegg JC, Sorgeloos P. Kluwer Academic Publishers Dordrecht; 2002:171-224.

34. Montaño G, Buckle F: Variations in some physicochemical parameters in a hypersaline coastal lagoon of Baja California, Mexico.

    International Journal of Salt Lake Research 1996, 4:265-280.

35. Avise JC: Molecular markers natural history and evolution. Chapman & Hall, New York. USA; 1994.

36. Torrentera L, Dodson SI: Ecology of the brine shrimp Artemia in the Yucatan, Mexico, salterns.

    Journal of Plankton Research 2004, 26(6):617-624. Publisher Full Text

37. Gajardo G, da Conceição M, Weber L, Beardmore JÁ: Genetic variability and interpopulational differentiation of Artemia populations from South America.

    Hydrobiologia 1995, 302:21-29. Publisher Full Text

38. Del Castillo E, Farfan C: Hydrobiology of a salt pan from the peninsula of Baja California, Mexico.

    International Journal of Salt Lake Research 1997, 6:233-2.

39. Contreras YJA: Estudio prospectivo del camarón salado (Artemia sp.) en las marismas del ejido Aquiles Serdan (El Barranco), Municipio de Altamira, Tamaulipas, México. In Thesis. Escuela de Ciencias Biológicas Tampico Tamaulipas; 1987.

40. Enciso PP: Comparación de algunas características morfometricas de dos poblaciones de Artemia sp. de San Francisco California U.S.A. y Ecatepec Edo de México. In Thesis. Universidad Autónoma Metropolitana Xochimilco Mexico; 1989.

41. Ortega-Salas AA, Martínez V: Hydrological and Population Studies on Artemia franciscana in Yavaros, Sonora, México.

    Revista Biologia Tropical 1987, 35(2):233-239.

42. Castro BT: Distribución geográfica e importancia de Artemia en México y evaluación de la población en el sur de la Bahía de Ceuta, Sinaloa, México. In Reporte de Investigación No. 6. Universidad Autónoma Metropolitana – Xochimilco; 1980.

43. Zuñiga O, Wilson R, Amat F, Ontoria F: Distribution and characterization of Chilean populations of the brine shrimp Artemia (Crustacea Branchiopoda Anostraca).

    International Journal of Salt Lake Research 1999, 8:23-40.

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