Francisco Amat

Spanish National Research Council, Madrid, Madrid, Spain

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Publications (23)23.71 Total impact

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    Article: A revision of Artemia biodiversity in Macaronesia.
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    ABSTRACT: In a biogeographical context, the term Macaronesia broadly embraces the North Atlantic archipelagos of the Azores, Madeira, Selvagens, the Canary Islands, and Cape Verde. The peculiar arid climatic conditions in some of these places have led to the development of marine salt exploitations, which can be counted among the hypersaline habitats of the brine shrimp Artemia (Branchiopoda, Anostraca). Parthenogenetic populations of this anostracan were described in the Canary Islands during the last decades of the 20th century, while the American Artemia franciscana species was recently found in the Cape Verde archipelago. Following an invasive pattern, this exotic species has recently reached the Canary Islands, too. This paper reports information dealing with biotope loss (solar saltworks) in this biogeographical region, together with possible consequences concerning the arrival of invasive species, two factors that frequently promote dramatic biodiversity losses. The discussion of this threat focuses mainly on the Canary Islands archipelago where native species of Artemia still exist.
    Aquatic biosystems. 10/2012; 8(1):25.
  • Article: Genetic characterization of Argentinean Artemia species with different fatty acid profiles
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    ABSTRACT: The Anostracan genus Artemia is composed by several sibling species reproductively isolated, but identical or very similar in outward appearance. The genus shows also an underlying striking variability from the biochemical point of view, regarding especially the fatty acid profile of the cysts and nauplii. In Argentina, Artemia is represented by two bisexual species: A. franciscana and A. persimilis. Former studies have shown that A. franciscana is present in northern of 36º and that A. persimilis is constrained southwards of 37° S. In general, there is good agreement between morphological and cytogenetic comparisons of Argentinean populations with respect to species discrimination. However, new Argentinean Artemia populations are being analyzed morphologically and it becomes necessary to further investigate if the genetic adscription of these populations is congruent with the results obtained from the current morphological analyses. Restriction fragment length polymorphism (RFLP) analysis of a fragment of the 16S rRNA mitochondrial gene was used to investigate the genetic diversity and population structure of 10 new Artemia populations from Argentina. The mitochondrial DNA (mtDNA) results showed a similar pattern to that of previous cytogenetic and morphological analyses with the two Argentinean species appearing as highly divergent. The presence of A. persimilis in southern Argentina and the southernmost Chilean population was confirmed unveiling a novel picture of species distribution in the country. A. franciscana showed a unique haplotype. Populations of A. persimilis appeared highly structured, although their clustering did not follow a clear geographic pattern. The different Argentinean Artemia populations analyzed were characterized by high variability in their fatty acids, showing both marine- and freshwater-type profiles. For the first time, the investigation of the relatedness between the fatty acid composition in Artemia and genetic markers was attempted. The study aimed at the putative association of molecular markers with marine versus freshwater-type populations. A lack of correlation between RFLP patterns at mtDNA and the fatty acid (FA) profiles was found in the A. persimilis populations which was discussed from the point of view of two main genetic hypotheses and/or phenotypic plasticity.
    Hydrobiologia 04/2012; 610(1):223-234. · 1.78 Impact Factor
  • Article: Records of cysticercoids of Fimbriarioides tadornae Maksimova, 1976 and Branchiopodataenia gvozdevi (Maksimova, 1988) (Cyclophyllidea, Hymenolepididae) from brine shrimps at the Mediterranean coasts of Spain and France, with a key to cestodes from Artemia spp. from the Western Mediterranean
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    ABSTRACT: Cysticercoids of two cestode species isolated from brine shrimps from the Mediterranean coasts of Spain and France are described. Fimbriarioides tadornae Maksimova, 1976 (adults known as parasites of Tadorna tadorna) was recorded from Artemia parthenogenetica and A. franciscana from Spain (Bras del Port and River Ebro Delta, respectively), and from A. franciscana from Aigues-Mortes, France (new geographical record). Branchiopodataenia gvozdevi (Maksimova, 1988) (adults known as parasites of Larus genei) was recorded from A. parthenogenetica (Bras del Port, Spain), A. salina (San Pedro del Pinatar, Spain) and A. franciscana (River Ebro Delta, Spain); this is the first record of the species in Europe. An illustrated key to cysticercoids of 12 cestode species from Artemia spp. from the Western Mediterranean is proposed.
    Acta Parasitologica 04/2012; 54(2):143-150. · 0.79 Impact Factor
  • Article: Transport of brine shrimps via the digestive system of migratory waders: dispersal probabilities depend on diet and season
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    ABSTRACT: Waterbirds are known to disperse invertebrate propagules that survive gut passage, but there is very little information about how the probability of dispersal changes at different times of the annual cycle when birds move in different directions, or how it is affected by changes in diet. We studied internal transport of brine shrimp Artemia cysts by migratory waders in the Odiel saltworks in south-west Spain. Viable cysts of parthenogenetic Artemia were abundant in the faeces and regurgitated pellets of redshank Tringa totanus, pellets of spotted redshank T. erythropus, and faeces of black-tailed godwit Limosa limosa during spring and/or autumn migrations in 2001–2002, but were not recorded during winter. Godwits did not produce pellets, and spotted redshank faeces were not sampled. Significant correlations between the number of cysts in a pellet or faecal sample and the proportion of that sample constituted by Artemia adults suggested that most cysts were ingested while in the ovisacs of gravid females. The proportion of cysts destroyed during digestion increased when accompanied by harder food items or grit, and when fewer cysts were ingested. The median number of intact cysts was higher in redshank faeces than in their pellets, but cysts extracted from pellets were more likely to hatch. A higher proportion of redshank pellets contained Artemia cysts in spring than in autumn, but more redshank migrated through the area in autumn. Significantly fewer cysts were recorded in redshank pellets in winter than in spring or autumn. Our results confirm that there is potential for long-distance dispersal of Artemia cysts via waders during both northwards (spring) and southwards (autumn) migrations.
    Marine Biology 04/2012; 151(4):1407-1415. · 2.28 Impact Factor
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    Article: Artisanal salt production in Aveiro/Portugal - an ecofriendly process.
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    ABSTRACT: Solar salinas are man-made systems exploited for the extraction of salt, by solar and wind evaporation of seawater. Salt production achieved by traditional methods is associated with landscapes and environmental and patrimonial values generated throughout history. Since the mid-twentieth century, this activity has been facing a marked decline in Portugal, with most salinas either abandoned or subjected to destruction, making it necessary to find a strategy to reverse this trend.It is, however, possible to generate revenue from salinas at several levels, not merely in terms of good quality salt production, but also by obtaining other products that can be commercialized, or by exploring their potential for tourism, and as research facilities, among others. Furthermore, with an adequate management, biodiversity can be restored to abandoned salinas, which constitute important feeding and breeding grounds for resident and migratory aquatic birds, many of which are protected by European Community Directives.The aims of this manuscript are to present a brief overview on the current state of sea salt exploitation in Portugal and to stress the importance of recovering these salinas for the conservation of this particular environment, for the regional economy, the scientific community and the general public. The Aveiro salina complex is presented in detail, to exemplify salina structure and functioning, as well as current problems and potential solutions for artisanal salinas.
    Saline Systems 11/2011; 7(1):3. · 1.18 Impact Factor
  • Article: Artemia Biodiversity in Algerian Sebkhas
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    ABSTRACT: This paper summarizes the results of a study that comprised a survey along with a morphological characterization of Artemia populations from seven sebkhas, one chott, and an inland salt lake in Algeria. Sebkhas and chotts are two different types of closed inland basins. Morphological characters together with a multivariate discriminant analysis applied to morphometric data obtained from adult specimens cultured under standard conditions, were used to differentiate the species and strains. The bisexual species A. salina (L., 1758) is present in seven of these saltmarshes, but frequently cooccurs with diploid and tetraploid parthenogenetic strains. The biodiversity pattern of the populations of Artemia in Algeria appears to be similar to that found in the rest of the western Mediterranean region.
    Crustaceana 08/2011; 84(9):1025-1039. · 0.46 Impact Factor
  • Article: Participation of metanauplii and juvenile individuals of Artemia parthenogenetica (Branchiopoda) in the circulation of avian cestodes.
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    ABSTRACT: Adult crustaceans of the genus Artemia (brine shrimps) are intermediate hosts in the life cycle of cestode species parasitic in aquatic birds as their definitive hosts. However, there are no data on the role of larval and juvenile brine shrimps in the transmission of avian helminth parasites. In order to examine the possible role of early developmental stages (nauplii, metanauplii and juveniles) of Artemia for the circulation of avian cestodes, the natural cestode infection in the population of Artemia parthenogenetica from La Mata Lagoon, Mediterranean coast of Spain, was studied. Metacestodes (cysticercoids) of four cestode species were recorded in adult brine shrimps: Flamingolepis liguloides and Flamingolepis flamingo (hymenolepidids parasitic in flamingos), Confluaria podicipina (a hymenolepidid species parasitic in grebes) and Eurycestus avoceti (a dilepidid species parasitic in avocets, stilts, plovers and, to a lesser extent, in flamingos). No cysticercoids were found in nauplii. Two species, F. liguloides and F. flamingo, were found in metanauplii and juvenile brine shrimps. Only 36.3% of the cysticercoids of F. liguloides occurred in adult brine shrimps; the remaining 63.7% were parasitic in metanauplii (39.6%) and juveniles (24.1%). Similarly, the metacestodes of F. flamingo were also distributed among various age groups: in adults (44.4% of cysticercoids), juveniles (27.8%) and metanauplii (27.8%). These results indicate that the early developmental stages of Artemia have an important role for the circulation of certain parasite species. No cysticercoids of C. podicipina and E. avoceti were recorded in larval and juvenile brine shrimps. The selective infestation of larval brine shrimps with flamingo parasites is probably associated with the feeding behaviour of definitive hosts, which are filtering predators; in contrast, grebes and waders pick brine shrimps individually one by one. The possible underlying mechanism for selective infestation of metanauplii and adults by certain cestode species is associated with the size of parasite eggs, allowing only cestode species with small eggs to be ingested by larval brine shrimps.
    Parasitology Research 10/2010; 108(4):905-12. · 2.15 Impact Factor
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    Article: Evolutionary origin and phylogeography of the diploid obligate parthenogen Artemia parthenogenetica (Branchiopoda: Anostraca).
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    ABSTRACT: Understanding the evolutionary origin and the phylogeographic patterns of asexual taxa can shed light on the origin and maintenance of sexual reproduction. We assessed the geographic origin, genetic diversity, and phylogeographic history of obligate parthenogen diploid Artemia parthenogenetica populations, a widespread halophilic crustacean. We analysed a partial sequence of the Cytochrome c Oxidase Subunit I mitochondrial gene from an extensive set of localities (including Eurasia, Africa, and Australia), and examined their phylogeographic patterns and the phylogenetic relationships of diploid A. parthenogenetica and its closest sexual relatives. Populations displayed an extremely low level of mitochondrial genetic diversity, with one widespread haplotype shared by over 79% of individuals analysed. Phylogenetic and phylogeographic analyses indicated a multiple and recent evolutionary origin of diploid A. parthenogenetica, and strongly suggested that the geographic origin of parthenogenesis in Artemia was in Central Asia. Our results indicate that the maternal sexual ancestors of diploid A. parthenogenetica were an undescribed species from Kazakhstan and A. urmiana. We found evidence for multiple origin of parthenogenesis in Central Asia. Our results indicated that, shortly after its origin, diploid A. parthenogenetica populations underwent a rapid range expansion from Central Asia towards the Mediterranean region, and probably to the rest of its current geographic distribution. This contrasts with the restricted geographic distribution, strong genetic structure, and regional endemism of sexual Artemia lineages and other passively dispersed sexual continental aquatic invertebrates. We hypothesize that diploid parthenogens might have reached their current distribution in historical times, with a range expansion possibly facilitated by an increased availability of suitable habitat provided by anthropogenic activities, such as the spread of solar saltworks, aided by their natural dispersal vectors (i.e., waterbirds).
    PLoS ONE 01/2010; 5(8):e11932. · 4.09 Impact Factor
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    Article: Phylogeography and local endemism of the native Mediterranean brine shrimp Artemia salina (Branchiopoda: Anostraca).
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    ABSTRACT: There has been a recent appreciation of the ecological impacts of zooplanktonic species invasions. The North American brine shrimp Artemia franciscana is one such alien invader in hyper-saline water ecosystems at a global scale. It has been shown to outcompete native Artemia species, leading to their local extinction. We used partial sequences of the mitochondrial Cytochrome c Oxidase Subunit 1 (COI or cox1) gene to investigate the genetic diversity and phylogeography of A. salina, an extreme halophilic sexual brine shrimp, over its known distribution range (Mediterranean Basin and South Africa) and to assess the extent of local endemism, the degree of population structure and the potential impact of traditional human saltpan management on this species. We also examined the phylogenetic relationships in the genus Artemia using COI sequences. Our results show extensive regional endemism and indicate an early Pleistocene expansion of A. salina in the Mediterranean Basin. Subsequent population isolation in a mosaic of Pleistocene refugia is suggested, with two or three refugia located in the Iberian Peninsula. Two instances of long-distance colonization were also observed. Surprisingly, given its strong phylogeographical structure, A. salina showed a signature of correlation between geographical and genetic distance. Owing to strong 'priority effects', extensive population differentiation is retained, despite dispersal via migrant birds and human management of saltpans. The foreseeable expansion of A. franciscana is likely to be followed by substantial loss of genetic diversity in Mediterranean A. salina. Large genetic divergences between Mediterranean and South African A. salina suggest that the latter deserves species status.
    Molecular Ecology 07/2008; 17(13):3160-77. · 5.52 Impact Factor
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    Chapter: The American brine shrimp as an exotic invasive species in the western Mediterranean
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    ABSTRACT: The hypersaline environments and salterns present in the western Mediterranean region (including Italy, southern France, the Iberian Peninsula and Morocco) contain autochthonous forms of the brine shrimp Artemia, with parthenogenetic diploid and tetraploid strains coexisting with the bisexual species A. salina. Introduced populations of the American brine shrimp A. franciscana have also been recorded in these Mediterranean environments since the 1980s. Based on brine shrimp cyst samples collected in these countries from 1980 until 2002, we were able to establish the present distribution of autochthonous brine shrimps and of A. franciscana, which is shown to be an expanding invasive species. The results obtained show that A. franciscana is now the dominant Artemia species in Portuguese salterns, along the French Mediterranean coast and in Cadiz bay (Spain). Co-occurrence of autochthonous (parthenogenetic) and American brine shrimp populations was observed in Morocco (Mar Chica) and France (Aigues Mortes), whereas A. franciscana was not found in Italian cyst samples. The results suggest these exotic A. franciscana populations originate as intentional or non-intentional inoculations through aquacultural (hatchery effluents) or pet market activities, and suggest that the native species can be rapidly replaced by the exotic species.
    12/2005: pages 37-47;
  • Article: Further evidence and characterization of Artemia franciscana (Kellogg, 1906) populations in Argentina
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    ABSTRACT: Aim  This paper reports the presence of Artemia franciscana (Kellogg, 1906) in Mar Chiquita (CHI) salt lake and in Las Tunas (TUN) lagoon, as well as at a shallow lake in Salinas Grandes (Province of Córdoba) in Argentina. To date, this species has been considered absent from Argentina. This study also provides further data on the characterization of the A. franciscana populations from this area.Location  Province of Córdoba (Argentina).Methods  The cyst samples collected at the three hypersaline environments were measured to assess its mean diameter with a dissecting microscope. The length of the nauplii hatched from the cysts was also determined with the microscope. The adults raised from these nauplii under strictly controlled conditions were analysed for 12 morphological parameters and compared through multivariate discriminant analysis with other American populations. Fatty acids from the total lipids were analysed by gas chromatography. Reproductive compatibility was evaluated from single-pair intraspecific and interspecific crosses of adult specimens.Results  The results endorse the morphometric assimilation of the Artemia populations of this area to other American populations of the A. franciscana‘super-species’, together with its morphometric differentiation from the species A. persimilis (Piccinelli & Prosdocimi, 1968). The more conspicuous population from CHI shows cross-fertility with A. franciscana original from San Francisco Bay (California, USA). Both populations from CHI and TUN show cross-fertility between them and reproductive isolation with A. persimilis from Hidalgo (Province of La Pampa), which to date is considered to be endemic or exclusive of hypersaline ecosystems in Argentina. The reproductive characteristics displayed by the population from TUN lagoon suggest the existence of an occasional hybridization between A. franciscana and A. persimilis (Papeschi et al., 2000). Artemia cysts from CHI and TUN show a fatty acid profile rich in eicosapentaenoic acid differing markedly from the fatty acid profiles found in A. persimilis cysts.Main conclusions: Artemia franciscana is present in Argentina at 36° S and north of this latitude. Artemia persimilis is confined to the south of latitude 37°10′ S. There are different pieces of evidence that point to a certain level of hybridization of the two species taking place in the land belt between these parallels.
    Journal of Biogeography 10/2004; 31(11):1735 - 1749. · 4.54 Impact Factor
  • Article: Enrichment of Artemia nauplii in PUFA, phospholipids, and water-soluble nutrients using liposomes
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    ABSTRACT: Different liposome formulations, includingseveral combinations of membrane composition,type of vesicle (multilamellar and largeunilamellar vesicles), preparation method, andvehiculated nutrient, have been assayed asbioencapsulation products to enrich Artemia nauplii with nutrients for feeding fish larvae.The stability of the liposome preparationsunder conditions of use as enrichment producthas been tested using water soluble fluorescentmarkers as leakage indicators. The content ofthe fatty acids and lipid classesbioencapsulated in Artemia nauplii withliposomes has been analyzed by gas and thinlayer chromatography, respectively, andcompared with other enrichment products. Theeffect of the liposome enriched Artemianauplii used as food for fish larvae has beenevaluated in sea bass cultures. Liposomes withhigh content in polyunsaturated fatty acidsleak out more than 50% of their aqueous phasein less than 2 hours, unless they arestabilized with cholesterol and formed as largeunilamellar vesicles. Such vesicles hold70% of the encapsulated material for 8 hours.Liposome enriched nauplii in this study reflectthe influence of the enrichment products,however, they are far from the commercialemulsion (Super Selco) in terms ofdocosahexaenoic acid content, except for thenauplii enriched with liposomes made of purekrill phospholipid extract by the method ofdetergent solubilization. The liposome enrichednauplii show a higher amount of polar lipids incontrast to the feed enriched with emulsions.The larvae fed liposome enriched nauplii haveonly a slightly lower docosahexaenoic acidcontent than those fed emulsion enrichednauplii. The results obtained confirm thesuitable potential use of liposomes as foodsupplement in larviculture. Problems andadvantages are discussed.
    Aquaculture International 12/2002; 11(1):151-161. · 0.91 Impact Factor
  • Article: Preliminary characterization of some Argentinean Artemia populations from La Pampa and Buenos Aires provinces
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    ABSTRACT: Artemia populations were sampledin four hypersaline ecosystems in continentalevaporitic basins from the Argentinean provinces of LaPampa and Buenos Aires. Biometrics of cysts andnauplii were performed. The morphometrics of adultfemales under standard culture conditions, studied bymultivariate discriminant analysis, provided evidencethat these populations belonged to the species A.persimilis; this was further supported bycross-breeding tests established between one of thesepopulations (Salinas Grandes de Hidalgo, province ofLa Pampa) and a population of A. franciscanafrom San Francisco Bay (California, USA), which showedreproductive isolation and barriers to gene flowbetween both populations.
    International Journal of Salt Lake Research 11/1999; 8(4):329-340.
  • Article: Distribution and characterization of Chilean populations of the brine shrimp Artemia (Crustacea, Branchiopoda, Anostraca)
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    ABSTRACT: Hypersaline habitats in Chile, from marine solar salt pans to saline lagoons and pools in Andean salars, were prospected in search of Artemia populations. These saline ecosystems were characterized through physico-chemical parameters and ionic composition of their brines. Biometrics of cysts and nauplii, as well as morphometrics by using multivariate discriminant analysis for adult specimens evidenced that the Chilean populations of brine shrimp belong to A. franciscana. Cross-breeding results supported the former hypothesis of conspecific Chilean populations, and their differences with A. persimilis, also endemic to the New World, but restricted to Argentinean sites.
    International Journal of Salt Lake Research 01/1999; 8(1):23-40.
  • Article: Effects of nauplial density, product concentration and product dosage on the survival of the nauplii and EFA incorporation during Artemia enrichment with liposomes
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    ABSTRACT: In order to determine an optimal enrichment protocol with krill phospholipid liposomes, three different experiments were carried out to evaluate the effects of nauplial density, the concentration of liposome, and the number of doses delivered to the nauplii on the survival and the essential fatty acid (EFA) bioencapsulation in Artemia nauplii. No survival differences were found between the different liposome treatments and the control nauplii enriched with a commercial emulsion. This result confirms that previously described mortalities during Artemia enrichment with liposomes can be minimized and controlled. On the other hand, the EFA incorporation obtained from the three experiments indicates that maximal bioencapsulation is achieved when incubations are carried out under nauplial densities of 300 nauplii ml− 1, where liposomes are dispensed in a single dose at the beginning of the incubation yielding a concentration of 0.5 g l− 1. These findings complete those obtained in two preliminary studies, and propose a well defined enrichment protocol with krill liposomes as an alternative complementary method to improve the nutritional value of the Artemia nauplii used as food for marine fish larvae.
    Aquaculture.
  • Article: Role of parasites in the successful invasion of Mediterranean salterns by the exotic invasive Artemia franciscana
    Natural Resources and Environmental Issues.
  • Article: The use of a multidisciplinary approach for the characterization of a diploid parthenogenetic Artemia population from Torre Colimena (Apulia, Italy)
  • Article: Updating Geographic Distribution of Artemia urmiana Günther, 1890 (Branchiopoda: Anostraca) in Europe: An Integrated and Interdisciplinary Approach
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    ABSTRACT: Artemia urmiana (a species previously considered endemic of Lake Urmia, NW Iran) has been found in Lake Koyashskoe, a hypersaline lake on the Black Sea coast of the Crimean peninsula (Ukraine). Therefore, this is the first record of A. urmiana in Europe which updates its distribution. The species identification was based on an integrated and interdisciplinary approach using discriminant analysis of the morphometric characters, scanning electron microscopy, and molecular profile analysis. The data derived from the above mentioned approaches converge to significant similarity of the population under investigation with A. urmiana. The updated geographic distribution of the species, deriving from the present report, asks for additional contribution of other disciplines (e.g., avian dispersal of cysts, history of salt trade) to be finally clarified. At present we suggest that the punctuated geographic distribution of A. urmiana is probably linked to its low dispersal capability, and we suppose that its presence in two distant sites could be explained by historical human salt trade between Lake Urmia and the ancient port of Kimmerik, whose remains have been found in the present Lake Koyashskoe.
  • Article: Lipid conversions during enrichment of Artemia
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    ABSTRACT: Artemia nauplii were enriched for 24 h with radiolabelled fatty acid ethyl esters and then starved for a subsequent period of 24 h. Analyses of the distribution of radioactivity in lipids from samples taken at the end of the enrichment period and after the subsequent starvation showed that the ethyl esters were readily converted into other lipid classes, mainly triacylglycerols, during assimilation by the nauplii. The proportions of radioactivity recovered in free fatty acids and phospholipids increased during the starvation period indicating the mobilisation of fatty acids from triacylglycerols for use in catabolism and in the formation of biomembrane lipids. The distribution pattern of radioactivity from [U–]22:6n−3 in the fatty acids of the nauplii demonstrates that Artemia are capable of retroconverting 22:6n−3 to 20:5n−3.
    Aquaculture.
  • Article: Effect of aeration on the efficiency of Artemia enrichment with EFA-rich emulsion and liposomes
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    ABSTRACT: A commercial emulsion and EFA-rich liposomes have been used as Artemia nauplii enrichment products in a study designed to determine the effect of the aeration on the enrichment efficiency and its importance as a source of variability in the final naupliar fatty acid content. With this purpose, fatty acid profiles of nauplii enriched under uncontrolled aeration conditions were compared to nauplii enriched under different controlled aeration modes. Concretely, both emulsions and liposomes were tested in six enrichment series resulting from the combination of three different airflows and two air diffusion systems. Moreover, the naupliar survival after the enrichment process was estimated since some mortality was previously recorded in liposome enrichments. The results revealed a small effect of aeration on both the EFA incorporation and naupliar survival in the emulsion treatment. However, liposome treated nauplii underwent the influence of the different aeration modes both in terms of EFA incorporation and naupliar survival. In general, the liposome enrichments showed the highest EFA incorporation when the enrichment procedures were carried out at low airflows. Besides, the use of airstones improved the enrichment efficiency at the lowest airflow, whereas this diffusion system produced a decrease of the EFA content in liposome enriched nauplii at the highest airflow. In spite of the unquestionable effect of aeration on the EFA enrichment in liposome enrichments, other concomitant factors must be acting in the process since variability still occurred even with the control of aeration.
    Aquaculture. 257:382-392.