Comparing the potential for dispersal via waterbirds of a native and an invasive brine shrimp

1. Migratory waterbirds are likely to have a major role in the spread of many exotic aquatic invertebrates by passive dispersal. However, in the field, this has so far only been confirmed in the case of the American brine shrimp Artemia franciscana, which is spreading quickly around the Mediterranean region. 2. We compared experimentally the capacity of A. franciscana and the native brine shrimp Artemia parthenogenetica to disperse via migratory shorebirds. After Artemia resting eggs (cysts) were fed to Redshank Tringa totanus and Dunlin Calidris alpina, we compared the proportion that survived gut passage, their hatchability and their retention time within the gut. We also tested the ability of cysts to stick to the feathers of Black‐tailed Godwit Limosa limosa. 3. The proportion of ingested cysts retrieved from faeces was the same for each Artemia species (8%), and there were no significant differences in retention time (mean 1.2 h and maximum 10 h for A. parthenogenetica, 1.4 and 12 h for A. franciscana) or hatchability (11% versus 14%). The two shorebird species showed similar retention times and retrieval rates, but cysts recovered from Dunlin had a significantly higher hatchability. Only one of the 1000 A. parthenogenetica cysts and three of the 1000 A. franciscana cysts stuck to feathers. 4. These results indicate that both non‐native and native brine shrimps have a similar high capacity for endozoochory via birds, and that the invasiveness of A. franciscana is probably explained by its competitive superiority owing to high fecundity and release from cestode parasitism. Owing to their different migratory behaviour, Redshank and Dunlin are likely to have different roles as brine shrimp vectors. Brine shrimps provide a suitable model for understanding the role of birds in the dispersal of exotic aquatic invertebrates.     

Effects of diet on development and reproduction of the predatory pentatomids Picromerus bidens and Podisus maculiventris

The effects of five diets (larvae of Galleria mellonella L., larvae of Spodoptera littoralis (Boisduval), eggs of Ephestia kuehniella Zeller, cysts of Artemia franciscana Kellogg and an artificial diet based on bovine meat) on development, survival and reproduction of two predatory stinkbugs, Picromerus bidens L. and Podisus maculiventris (Say), were studied in the laboratory. Both species successfully completed immature development on the foods offered, except for P. bidens on cysts of A. franciscana. Significant effects of diet on developmental duration were found in both species. Total developmental time from second instar to adult ranged from 25.0 to 41.5 days and from 18.7 to 46.0 days in P. bidens and P. maculiventris, respectively. Nymphal survival of P. maculiventris was superior to that of P. bidens on all diets tested. Nymphal survival of P. maculiventris was greater than 92% on all diets except on A. franciscana cysts, yielding only 50% survival to adulthood. Survival of P. bidens fed on eggs of E. kuehniella was higher than that of conspecifics fed on caterpillar prey or artificial diet (89% on flour moth eggs vs. 68 and 80% on G. mellonella and S. littoralis and only 50% on meat diet). Fresh weight of newly emerged females of both pentatomids was affected by the diet offered to the predators during their nymphal stage. Females of P. maculiventris produced viable eggs on all diets except on cysts of A. franciscana and had mean fecundities of 691, 436, 608 and 344 eggs per female on S. littoralis, G. mellonella, E. kuehniella eggs and the meat diet, respectively. Females of P. bidens laid eggs only on live prey with mean fecundities of 94 and 38 eggs per female on S. littoralis and G. mellonella, respectively. The results indicate a lower nutritional plasticity of P. bidens as compared with P. maculiventris. An erratum to this article can be found at     

International study on Artemia XLIX. Salinity effects on survival,maturity, growth,biometrics, reproductive and lifespan characteristics of a bisexual and a parthenogenetic population of Artemia

Two Artemia populations, a bisexual from San Francisco Bay (California, USA) and a parthenogenetic from Tanggu area (Tianjin province, People's Republic of China) are assayed for their tolerance and fitness in various salinity levels. This study was carried out under laboratory conditions where salinity effects upon special characteristics of the two Artemia populations, such as survival, growth rate, maturation, morphology, fecundity and life duration, were recorded. This evaluation revealed that the two populations examined exhibits significant differences in their response against elevated salinity levels. Furthermore, specific biometric parameters can be a useful tool for the discrimination and/or determination of their distribution in a mixed population, which, in fact, is the case in Tanggu salt works. Artemia franciscana seems to be a more effective colonizer at higher salinities. The data presented in this study may generate useful suggestions for proper management of the solar saltworks at Tanggu although further experimentation is needed.International interdisciplinary study on Artemia populations coordinated by the Laboratory of Aquaculture & Artemia Reference Center, University of Ghent, Belgium.     

Further evidence and characterization of Artemia franciscana (Kellogg, 1906) populations in Argentina

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.     

Segmentation in the crustacean Artemia: engrailed staining studied with an antibody raised against the Artemia protein

We have studied the process of post-embryonic segmentation in the anostracan crustacean Artemia franciscana using a specific antibody raised against the engrailed protein of this organism. Three cephalic segments are specified during embryonic development, before larval hatching, whilst trunk (thoracic) segmentation begins after the first stage free-swimming nauplius larva has emerged from the dormant cyst. Thus, cephalic and trunk segmentation seem to be at least in part independent and superimposed processes. Trunk stripes of engrailed expression are added one at a time as segments are generated from the posterior growth zone. The first detectable decision in engrailed expression is the establishment of a line of engrailed-expressing cells, interpretable as delineating the parasegmental boundary. The subsequent widening of engrailed stripes is not correlated with cell lineage events but is probably mediated by the combination of inheritance of the active state and recruitment of new cells into the engrailed-expressing stripe.     

Changes in a hydropsychid guild downstream from a eutrophic impoundment

The production of unicellular algae is laborious and is a major constraint for the culturing of aquatic filter-feeders. Because of their small particle size and their high protein content yeasts are considered as a promising substitute for micro-algae. Furthermore, recent work has shown that baker's yeast can be converted into a digestible diet for Artemia by chemical treatment. The present study documents the use at laboratory scale of this manipulated yeast as an algal substitute for the culture of two anostracan species. The experiments were conducted with the brine shrimp artemia franciscana and the fairy shrimp Streptocephalus proboscideus. A similar experimental set-up was used for both species. The algal diet, consisting of Dunaliella tertiolecta for A. franciscana and Selenastrum capricornutum for S. proboscideus, was substituted at various levels by two types of treated baker's yeast: a fresh form and a dried product which was rich in highly unsaturated fatty acids (HUFA). The chemically-treated yeast offers promising possibilities as an algal substitute for Artemia; i.e. replacing 75% of the algae by the dried yeast resulted in similar survival and even higher growth rates in comparison with the reference algal diet; for the treated fresh yeast similar results could be achieved by up to 95% substitution. For S. proboscideus, a substitution of 75% by either of the yeast products resulted in good survival, though growth did not exceed 80% of the observed growth in the algal control. A diet consisting solely of yeast resulted in poor survival for larvae of both species. Experiments were run to investigate whether this was due to a sub-optimal feeding regime, nutritional deficiencies, or deterioration of the water quality.     

Group 1 LEA proteins contribute to the desiccation and freeze tolerance of Artemia franciscana embryos during diapause

Water loss either by desiccation or freezing causes multiple forms of cellular damage. The encysted embryos (cysts) of the crustacean Artemia franciscana have several molecular mechanisms to enable anhydrobiosis—life without water—during diapause. To better understand how cysts survive reduced hydration, group 1 late embryogenesis abundant (LEA) proteins, hydrophilic unstructured proteins that accumulate in the stress-tolerant cysts of A. franciscana, were knocked down using RNA interference (RNAi). Embryos lacking group 1 LEA proteins showed significantly lower survival than control embryos after desiccation and freezing, or freezing alone, demonstrating a role for group 1 LEA proteins in A. franciscana tolerance of low water conditions. In contrast, regardless of group 1 LEA protein presence, cysts responded similarly to hydrogen peroxide (H₂O₂) exposure, indicating little to no function for these proteins in diapause termination. This is the first in vivo study of group 1 LEA proteins in an animal and it contributes to the fundamental understanding of these proteins. Knowing how LEA proteins protect A. franciscana cysts from desiccation and freezing may have applied significance in aquaculture, where Artemia is an important feed source, and in the cryopreservation of cells for therapeutic applications.     

Anostracan cysts found in California salt lakes

The salt lakes of California are home to four genera and eight species of Anostraca. The cysts of most of these species are readily distinguished using a combination of cyst and geographic characters. Cyst identification is a valuable tool that can allow a look at fairy shrimp ecology when adults are not available. For example, fossil anostracan cysts from 500-year-old Mono Lake sediments show more character variation than currently exists in extant Artemia monica, indicating a greater diversity of Anostraca at that time. Continuing desertification, both natural and man-made, in the Mono Lake area over the last 500 years is associated with decreased diversity in the Mono Lake anostracan fauna.     

Observations on future sea level changes in the Venice lagoon

The identification of the environmental conditions inducing different ecophysiological responses in the different strains and populations of the brine shrimp Artemia should improve the understanding of their biogeographic distribution. Nauplii from two Argentinean brine shrimp populations, Artemia persimilis from Salinas Grandes de Hidalgo (province of La Pampa) and Artemia franciscana from Laguna Mar Chiquita (province of Cordoba), were grown up until adulthood at different salinities (30, 60, 90, 120 gL⁻¹) and temperatures (12, 21, 28°C). The aim was to assess the effects of these different conditions on prereproductive life span and reproductive traits. Results evidenced that at 21 and 28°C, at any salinity, A. franciscana from Laguna Mar Chiquita attained higher survival and fecundity, after a shorter prereproductive period, than A. persimilis from Salinas Grandes de Hidalgo. These data support that A. franciscana, considered a superspecies, exhibits higher phenotypic plasticity than A. persimilis, and that A. persimilis is better adapted to lower temperatures than A. franciscana. These differences in temperature and salinity tolerance could explain the present distribution of these two species in the South Cone in South America. Handling Editor: J. Melack     

Life history,resting egg formation,and hatching may explain the temporal-geographical distribution ofArtemia strains in the Mediterranean basin

Life history traits are presented for the sexual species (Artemia tunisiana) and for parthenogenetic diploid and tetraploid strainsA. parthenogenetica reared at 15 °, 24 ° and 29.5 °C.In laboratory cultures, we present evidence that the seasonal appearance of the sexualArtemia tunisiana (the dominant winter-spring population), and of two parthenogenetic populations ofArtemia (the dominant spring-summer populations) in certain Spanish saltworks is controlled by temperature through its effect on reproductive and survival traits. Minimum and maximum reproductive output and survival for the sexual and parthenogenetic populations, respectively, occurred at a typical temperature (24 °C) of the late-spring season when the sexual population is replaced by parthenogenetic forms. Furthermore, the high production and hatchability of cysts from the sexual population at low temperatures (15 °C), and of the parthenogenetic populations at middle temperature (24 °C), indicate the role of dormancy as an adaptation regulating seasonal occurrence.     

Aspects of the population dynamics of Neosarmatium meinerti at Mgazana, a warm temperate mangrove swamp in the East Cape, South Africa, investigated using an indirect method

Encysted embryos (cysts) of the brine shrimp, Artemia provide an excellent model system for the study of biochemical adaptation to environmental extremes. Here, we describe an experiment in which cysts of A. franciscana from the San Francisco Bay (SFB), California, U.S.A., were inoculated into experimental ponds in the Mekong Delta region of Vietnam where water temperatures are much higher than the SFB. Cysts produced in each of three successive growing seasons (1996–1998) were collected and examined in the laboratory for resistance to high temperature and relative contents of three stress proteins (Hsp-70, artemin and p26). Thermal adaptation took place rapidly, during the first growing season. The increase in thermal tolerance was reflected in an overall increase in stress protein content, compared to SFB cysts used for the initial inoculation. Also examined were cysts of A. tibetiana collected from a lake on the high plateau of Tibet, PR China, almost 4.5 km above sea level. These cysts were very sensitive to high temperatures, and contained much lower levels of all stress proteins examined, compared to A. franciscana cysts from SFB and Vietnam. Cysts of A. sinica, collected from a hypersaline lake in Inner Mongolia, PR China, were examined in the same fashion and found to be similar to SFB cysts in terms of thermal resistance and stress protein content. The harsh environments in which Artemia are found, and the great diversity of its habitats, world-wide, provide excellent opportunities to relate the ecological setting of an organism to the underlying physiological and biochemical processes enabling its survival.     

Biomonitoring of trace metal contamination in mangrove-lined Brazilian coastal systems using the oyster Crassostrea rhizophorae: comparative study of regions affected by oil, salt pond and shrimp farming activities

The oyster Crassostrea rhizophorae has been used as a biomonitor of trace metal contamination in two Brazilian coastal systems. C. rhizophorae were collected in January 1998 from 15 stations (from 4 coastal inlets (including 1 estuary) and 1 coastal beach) near Macau, Rio Grande do Norte (RN), Brazil, a region affected by the activities of the oil industry and salt manufacture in coastal salt ponds; oysters were also collected in September 1999 from 8 stations in the Curimatau estuary (RN), an estuary becoming increasingly affected by shrimp farming activities. C. rhizophorae is a net accumulator of trace metals and can be used as a biomonitor, the accumulated soft tissue concentrations representing integrated records of bioavailable metal over the life of the oyster. At Macau, significant differences in oyster accumulated concentrations (and hence bioavailabilities to the oyster) of Fe, Zn, Cu, and Mn were found between stations; raised zinc availabilities at the coastal site are in close proximity to oil industry activities but the very high availabilities of Fe, Cu and Mn in the Rio dos Cavalos estuary originate from an unknown source. In the Curimatau estuary, bioavailabilities of Mn, Pb and Cd, but particularly of Cu and Zn, to the oysters are raised at the two most downstream sites, the only sites below the effluent of a large shrimp farming enterprise. The oysters also act as a local food source, and concentrations of Zn, Cu and Pb of some of the oysters are above typical public health recommended limits.     

Historical frequency of wind dispersal events and role of topography in the dispersal of anostracan cysts in a semi-arid environment

Propagules of several freshwater invertebrates are passively dispersed by wind, but the importance of wind as a dispersal vector remains poorly understood. We examined the historical frequency of wind dispersal events in cysts of Artemia franciscana. A threshold wind speed of ~5 km/h was required to begin dispersing surface-resting cysts, beyond which cyst dispersal increased rapidly with increasing wind speed. The analysis of wind speed and cyst dispersal data from our field experiment and wind data for the last 45 years from a nearby airport revealed that wind events strong enough to disperse most cysts at a wind-exposed site are common, occurring on ~16 snow-free days per year and occurring consistently over long time periods. In a topographically uneven landscape, however, wind speeds vary substantially from one location to another; wind speeds at our exposed site were 69% higher than in a nearby wind-sheltered depression. Accordingly, winds strong enough to disperse most cysts from this sheltered site occurred on only 5 days of the 45 year period. Cysts are thus less likely to disperse from, and more likely to settle in, sheltered depressions than wind-exposed areas. Sheltered areas could thus function as traps for wind-dispersing propagules.     

Two highly diverged New World Artemia species, A. franciscana and A. persimilis, from contrasting hypersaline habitats express a conserved stress protein complement

The brine shrimp Artemia is a well known animal extremophile adapted to survive in very harsh hypersaline environments. We compared the small stress proteins artemin and p26, and the chaperone hsc70 in encysted embryos (cysts) of the New World species, A. franciscana and A. persimilis. Cysts of the former, from San Francisco Bay, USA (SFB), were used essentially as a reference for these proteins, while both species were from locations in Chile where they occur in habitats at latitudinal extremes, the Atacama desert and Patagonia. These two species are phylogenetically distant, A. persimilis being closer to the Old World species, whilst A. franciscana is considered younger and undergoing evolutionary expansion. Using western blotting we found all three stress proteins in cysts from these five populations in substantial although variable amounts. The protein profiles revealed by Coomassie staining after electrophoresis (SDS-PAGE) were similar qualitatively, in spite of marked differences in the habitats from which these populations originated, and the long time since they diverged. We interpret these findings as further evidence for the adaptive importance of these three conserved proteins in coping with the variable, but severe stresses these encysted embryos endure.     

Speciation in the Artemia genus: Mitochondrial DNA analysis of bisexual and parthenogenetic brine shrimps

From the cloned mitochondrial DNAs (mtDNAs) isolated from two bisexual species, one Mediterranean, Artemia salina, and one American, Artemia franciscana, and two parthenogenetic (diploid and tetraploid) strains of Artemia parthenogenetica collected in Spain, physical maps have been constructed and compared. They are extremely different among themselves, much more than the differences between Drosophila melanogaster and D. yakuba and in the same range of different mammalian species such as mouse/rat or man/cow. The nucleotide sequences of two regions of mtDNA encoding parts of the cytochrome c oxidase subunit I (COI) and cytochrome b (Cytb) genes have been determined in the two bisexual species and the two parthenogenetic strains. Comparisons of these sequences have revealed a high degree of divergence at the nucleotide level, averaging more than 15%, in agreement with the differences found in the physical maps. The majority of the nucleotide changes are silent and there is a strong bias toward transitions, with the CT substitutions being highly predominant. The evolutionary distance between the two Artemia parthenogenetica is high and there is no clear relationship with any of the bisexual species, including the one present nowadays in Spain. Using a combination of molecular (mtDNA) and morphological markers it is possible to conclude that all of these Artemia isolates should be actually considered as belonging to different species, even the two Artemia parthenogenetica diploidica and tetraploidica.On sabbatical leave from Departamento de Bioquímica, Facultad de Veterinaria, Universidad Complutense de Madridearly Italian artemiologists to designate the Medi-Beatriz Batuecas died in an accident during the Christmas holy days of 1988 after she had initiated this workCorrespondence to: R. Garesse     

Colonization and dispersal patterns of the invasive American brine shrimp Artemia franciscana (Branchiopoda: Anostraca) in the Mediterranean region

Cysts of the brine shrimp Artemia franciscana are harvested from the Great Salt Lake (GSL) and San Francisco Bay (SFB) saltworks in the USA, and marketed worldwide to provide live food for aquaculture. This species has become invasive across several countries. We investigated (1) if the introduced populations in the Mediterranean region could have originated from these USA populations, (2) how the genetic diversity of Mediterranean compares to that at GSL and SFB, and (3) if genetic patterns in the Mediterranean can shed light on colonization routes. We sequenced a fragment of the cytochrome c oxidase subunit I and screened microsatellites loci from Mediterranean populations and the two putative USA sources. Haplotypes from Mediterranean populations were identical or closely related to those from SFB and GSL, and not related to other available American populations. Microsatellite analyses showed a reduced population diversity for most Mediterranean populations suggesting bottleneck effects, but few populations were showing similar or higher genetic diversity than native ones, which are likely to be admixed from both GSL and SFB because of multiple introductions. Results suggest natural dispersal, potentially via flamingos, between two Spanish populations. Our analyses show that all invaded populations could have originated from those commercialized USA populations.     

Heterochromatin in the genus Artemia

A bisexual species of the genus Artemia (Crustacea, Phyllopoda), Artemia franciscana Barigozzi of San Francisco Bay and a parthenogenetic population of Artemia sp. of Tsing-Tao (China), both with 42 chromosomes, were compared with respect to the microscopic structure of the interphase larval nucleus, the microscopical structure of the prophase chromosomes and the DNA structure. — Artemia franciscana exhibits several chromocenters in the resting nucleus, heterochromatic blocks located at the end of the prophase chromosomes, and a large amount of repetitive DNA (Alu I 110-bp fragments). The other Artemia sp. lacks chromocenters, heterochromatic blocks in the chromosomes, and the Alu I DNA. The two populations thus differ by a remarkable amount of repetitive DNA.The authors dedicate this paper to Professor Hans Bauer, on the occasion of his 80th birthday     

Preliminary genetic data on some Caribbean Artemia franciscana strains based on RAPD's

A total of fourteen Artemia samples from Colombia, Venezuela, Curaçao (Netherlands Antilles), Puerto Rico, and reference samples from U.S.A. (San Francisco Bay, SFB) belonging to the superspecies Artemia franciscana, and Argentina (A. persimilis), were analysed with the RAPD technique in order to demonstrate genetic dissimilarities. Pearson's correlation coefficients between the DNA banding patterns were calculated. They served as input values for the construction of UPGMA dendrograms. The results indicate that, within the collection of Colombian, Venezuelan and the two Netherlands Antilles Artemiacyst samples examined, two different groups seem to exist. Geographically, the mountainous area of Sierra Nevada de Santa Marta separates these two groups (lower Caribbean to the South and middle Caribbean to the North). Although the Caribbean, North and South American populations belong to A. franciscana, genetic discontinuities are to be expected due to habitat differences and geographic isolation. The Sierra Nevada (with an altitude of about 5800 m) emerges as the barrier very likely to explain the observed RAPD differences. Little genetic variability was present in the Colombian samples from Manaure that were collected almost every ten years, nor in the samples from Galerazamba collected almost two decades apart, although these samples were more likely subjected to different prevailing environmental conditions. The SFB population did not show a very close relation with all Caribbean populations analyzed, including the Puerto Rican. All A. franciscana populations analyzed were divergent from A. persimilis(Argentina).     

Development and reproduction of Adalia bipunctata on factitious and artificial foods

The native coccinellid Adalia bipunctata (L.) (Coleoptera: Coccinellidae) may be an alternative to exotic species like Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) for the biological control of aphid pests in Europe. The availability of adequate factitious or artificial foods may help optimize its mass production. This study examines the nutritional value of Ephestia kuehniella Zeller (Lepidoptera: Phycitidae) eggs plus bee pollen, pea aphids Acyrthosiphum pisum (Harris) (Hemiptera: Aphididae) and mixtures of bee pollen and cysts of Artemia franciscana Kellogg (Branchiopoda: Artemiidae) and/or a lyophilized artificial diet based on bovine meat and liver. Reproducing adults of A. bipunctata were obtained on all diets tested, but immature survival, adult weights, development times and reproductive rates differed among diets. Over 84% of first instars fed on E. kuehniella eggs plus pollen or aphids survived to adulthood. Feeding predator larvae on pollen combined only with A. franciscana cysts or artificial diet yielded 40–55% immature survival, but survival increased to 74% when all of these components were mixed. Adult weights of A. bipunctata on the mixtures of pollen, A. franciscana cysts and/or artificial diet were 55–75% of those on aphids or on E. kuehniella eggs plus pollen. Lifetime fecundity was superior on E. kuehniella eggs plus pollen (1,864 eggs) to that on the other diets (264–889 eggs). The use of mixtures of plant and animal foods for A. bipunctata and other predators may contribute to increasing the cost-effectiveness of commercial mass production by reducing inputs of natural prey like aphids, or of nutritious but expensive factitious foods like lepidopteran eggs.