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) 91011. 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 1213.
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).
<p>Table 1</p>
Geographical location, altitude and size of Artemia sites in Mexico.
Site
State
Geographical coordinate
Altitude (m)
Size (ha)
References
La Salina
Baja California Norte
32°05'N 118°40'W
0
33
Del Castillo & Farfán (1997) [38]
San José
Baja California Norte
29°15'N 114°53'W
0
Correa (1991) [24]
Cuatro Ciénegas de Carranza
Coahuila
29°36'N 99°20'W
740
0.05
Castro et al. (1997) [19]
Guerrero Negro
Baja California Sur
27°30' – 28°N 113°45' – 114°25'W
0
33000
Data from Exportadora de Sal S.A. de C.V.
Isla del Carmen
Baja California Sur
26°0' N 111°40'W
Castro et al (1987) [23]
Salina tres Hermanos (Yavaros)
Sonora
26°40'N 109°35'W
0
40
Gallardo astro (1987) [26]. Abreu-Grobois (1987) [6]. Castro et al.(1996) [18] (1997) [21]. Correa (1991) [24].
Bahía de Ohuira (Ahome)
Sinaloa
25°36'N 109°02'W
10
Díaz (2000) [25]
Pichilingue
Baja California Sur
24°16'N 110°20'W
Castro et al. (1987) [23].
Bahía de Ceuta
Sinaloa
23°50'N 106°30'W
0
7140
Castro et al. (1997) [20]
El Barranco (Altamira)
Tamaulipas
22°36' N 97°52'W 22°35'N 97°54'W
0
Contreras (1987) [39]
Salinas de Hidalgo
San Luís Potosí
22°39'N 101°43'W
1777
Castro et al.(1989) [17] (2000) [14]
San Crisanto
Yucatán
21°15'N 89°10'W
0
0.05
Castro et al. (1987) [23]
Real de las Salinas
Campeche
20°02'N 90°14'W
10
63.16
Castro et al. (1998) [16]
Celestún
Yucatán
20°48' 90°15' 20°58'N 90°25'W
0
3000
Torrentera & Dodson (1995) [4]. Núñez(1999) [27]
Texcoco
Estado de México
19°32'N 99°00'W
2250
0.17
Castro(1993) [15], Gallardo astro (1987) [26], Enciso (1989) [40]
Las Coloradas
Oaxaca
15°33'N 95°33'W
0
aprox.50
Castro et al.(1995) [22]
Sistema lagunar de: Laguna del mar Muerto
Chiapas
15°58' – 16°30'N 93° – 94°30'W
0
Tena (1977) [28]
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).
<p>Table 2</p>
Main water parameters of Mexican Artemia sites.
Sites
Salinity (g/L)
Temperature (°C)
pH
Cl- (Mg/l)
SO4-2 (mg/l)
HC03- (mg/l)
CO3- (mg/l)
Na+ (mg/l)
K+ (mg/l)
Ca+2 (mg/l)
Mg+2 (mg/l)
Date
Reference
La Salina
290
22
7
April-84
Del Castillo y Farfán (1997) [38]
San José
184
25
7.2
February-89
Correa(1991) [24]. Montaño & Buckle (1996) [34]
Cuatro Ciénegas de Carranza
100–300
27
7.7
28 930
61 440
9 150
24 790
3 130
0
13 280
01/04/1994
Castro et al. (2000) [14]
Guerrero Negro
120
18–22
22/02/1999
Isla del Carmen
Salina tres Hermanos
183
24
8.10
April-70
Ortega & Martínez(1987) [41]
Bahía de Ohuira
20–25
8.6
Pichilingue
100–300
22
8.10
Bahía de Ceuta
100–300
22
8.2
77 790
14 164
5 760
October-89
Castro (1980) [42].
El Barranco (Altamira)
165
21
8
01/02/1986
Contreras(1987) [39]
Salinas de Hidalgo
80
17
9.84
2 240
228
52
84
2 696
230
01/11/1985
San Crisanto
26
Castro et al. (1987) [23]
Real de las Salinas
100–300
23.2
8.9
15 120
100
700
0
13 500
1 350
0
100
01/02/1998
Castro et al. (1998) [16]
Celestún
185
29.1
8.1
485
1348
1991–1992
Torrentera & Dodson (2004) [36]
Texcoco
40
15–16
7.6
1 438
26
610
48
15 590
20
322
June-90
Castro (1993) [15]
Las Coloradas
125
28
8.0
02/12/1992
Castro (1995) [22]
Sistema lagunar de: Laguna del mar Muerto
35
30
June-80
Tena (1977) [28]
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 61516171819202122232425262728.
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.
<p>Table 3</p>
Cyst diameter, chorion thickness and nauplius characteristics of Artemia franciscana populations in Mexico.
State
Sites
Full cyst Diameter (± SD)
Chorion thickness
Nauplius size (± SD)
Sonora
Tres Hermanos, Yavaros
229.1 ± 8.9
8.76
389.5 ± 15.3
Sinaloa
Sol de Fuego, Ohuira
266.3 ± 8.6
7.96
379.6 ± 19.4
Oaxaca
Juchitán
275.5 ± 13.0
8.26
450.3 ± 30.6
Campeche
Real de las Salinas
249.2 ± 8.1
9.98
465.3 ± 29.3
Coahuila
Cuatro Ciénegas
231.1 ± 4.3
9.11
472.4 ± 26.9
San Luís Potosí
Las Salinas de Hidalgo
292.3 ± 16.1
6.94
417.9 ± 23.3
Estado de Mexico
Texcoco
230.2 ± 4.5
8.93
422.6 ± 29.0
Yucatán
Celestún
211.9 ± 13.6
3.87
461.8 ± 13.5
Zacatecas
Zacatecas
230.2 ± 4.1
2.11
432.7 ± 15.7
Sonora
Bahía de Lobos
200.4 ± 5.5
3.07
391.9 ± 16.3
Quintana Roo
Puerto Morelos
238.3 ± 8.8
9.95
398.0 ± 8.2
Oaxaca
El Marquez
386.3 ± 6.6
10.78
419.0 ± 8.7
Yucatán
San Crisanto
247.4 ± 16.1
3.72
446.0 ± 12.4
The data are in micrometers (μm).
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.
<p>Table 4</p>
Geographical location, altitude and size of the Artemia sites in Chile.
Sites
Federal entity
Locality
Geographical coordinates
Altitude (m)
Size (ha)
References
Salar de Surire
I Región
Salar de Surire
18°48'S
69°04'W
4200
144 km2
Zuñiga et. al. (1999)* [43]
Salar de Llamara
I Región
Llamara
21°18'S
69°37'W
850
10.000ha
*
Pozas de Playa Yape
I Región
Iquique
20°40'S
70°15'W
0
4–28 m2
*
Laguna Cejas (Salar de Atacama)
II Región
San Pedro de Atacama
23°02'S
68°13'W
2400
Gajardo & Beardmore (1993) [11]; Zúñiga et al. (1999) [43]
Poza Pampilla
IV Región
Coquimbo
29°58'S
71°22'W
0
9 m2
*
Poza Palo Colorado
IV Región
Los Vilos
31°58'S
71°25'W
0
10 m2
*
Salinas de Cahuil
VI Región
Pichilemu
34°48'S
72°10'W
100 mt
4.5
*
Laguna Amarga
XII Región
Puerto Natales
50°29'S
72°45'W
80
227,6 ha
Zúñiga et al. (1999) [43]
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).
<p>Table 5</p>
Main water parameters of Chile Artemia sites.
Sites
Salinity (g/l)
Temperature (°C)
pH
Cl- (Mg/L)
SO4 -2 (mg/L)
HC03 - (mg/L)
CO3 - (mg/L)
Na+ (mg/L)
K+ (mg/L)
Ca+2 (mg/L)
Mg+2 (mg/L)
Date
Reference
Salar de Surire
102
4,5
8,5
46 370
11 030
150
40
31 860
7 480
1 360
1 270
July-1994
Gajardo y Beardmore (1993) [11]
Salar de Llamara
167
28
7,5
43 600
17 440
35 810
2 130
450
560
March-1994
Zuñiga et al.(1999) [43]
Pozas de Playa Yape
56
30
8,5
54 920
8 490
40
0
30 470
1 230
1 190
3 650
July-1994
Laguna Cejas (Salar de Atacama).
292
23
7,3
41 900
28 250
370
0,3
26 780
1 230
120
1 330
March-1994
Poza Pampilla
45
17
10,1
55 460
7 800
360
50
29 770
1 180
1 090
4 460
August-1994
Poza Palo Colorado
75
21,1
8,1
53 300
7 580
220
30
32 480
1 320
1 260
3 810
August-1994
Salinas de Cahuil
115
37
7,8
54 780
7 690
380
20
31 380
1 100
1 210
3 520
February-1995
Laguna Amarga
120
8,5
12
17 020
60 380
4 420
1 320
34 160
2 250
330
2 089
April-1995
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 1130313233.
<p>Table 6</p>
Cyst, chorion thickness and nauplius characteristics of Artemia franciscana and Artemia persimilis in Chile.
Sites
Artemia species
Full cyst Diameter (± SD)
Chorion thickness
Nauplius size
Laguna Cejar (Salar de Atacama)
Artemia franciscana
226.7 ± 9.1
6.15
451.7 ± 23.3
Salinas de Cahuil
Artemia franciscana
230.6 ± 8.9
6.7
399.3 ± 18.8
Pozas de Playa Yape
Artemia franciscana
241.0 ± 8.8
6.36
415.0 ± 26.1
Salar de Llamara
Artemia franciscana
232.0 ± 7.6
7.9
424.0 ± 19.7
Poza Pampilla
Artemia franciscana
220.5 ± 12.5
5.4
395.5 ± 22.4
Laguna Amarga
Artemia persimilis
254.7
-
413.3
Poza Palo Colorado
Artemia franciscana
236.8
-
417.5
The data are in micrometers (μm).
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.
<p>Figure 1</p>
Principal components analyses of water composition in different Artemia sites in Mexico-Chile
Principal components analyses of water composition in different Artemia sites in Mexico-Chile. Locations: 1 = Cuatro Cienegas, 2 = Bahía de Ceuta, 3 = Real de las Salinas, 4 = Texcoco, 5 = San Luis Potosí, 6 = Torre del Paine, 7 = Salar de Atacama, 8 = Salar de Llamara, 9 = Poza Pampilla, 10 = Salar de Surire, 11 = Poza Palo Colorado, 12 = Pozas de Playa Yape, 13 = Salinas de Cahuil.
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<p>Figure 2</p>
Discriminant anlyses of Artemia cysts (a) and nauplii (b), from México-Chile
Discriminant anlyses of Artemia cysts (a) and nauplii (b), from México-Chile. Locations:1 = San Luis Potosí, 2 = Juchitan, 3 = Ohuira, 4 = Yavaros, 5 = Real de las Salinas, 6 = Cuatro Cienegas, 7 = Texcoco, 8 = Zacatecas, 9 = Lobos Bay, 10 = Quintana Roo, 11 = Celestun, 12 = San Crisanto, 13 = El Marquez, 14 = Laguna Cejas, 15 = Poza Pampilla, 16 = Salinas de Cahuil, 17 = salar de Llamara, 18 = Pozas de PlayaYape, 19 = San Francisco Bay.
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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 634. 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 1213. 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 301, 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.