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Phylogenetic analysis of exotic invasive species of Brine Shrimp Artemia Leach, 1819 (Branchiopoda, Anostraca) in Al Wathba Wetland Reserve (UAE; Abu Dhabi)

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The taxonomic identity of an unknown Artemia population inhabiting the Al Wathba Wetland Reserve in Abu Dhabi, U.A.E., was determined using phylogenetic analysis of the mitochondrial marker Cytochrome Oxidase Subunit 1 ( COI ). The results showed that the examined population belongs to an exotic invasive species, Artemia franciscana . Based on the distribution pattern of haplotypes, the studied population could possibly have originated from that inhabiting the Great Salt Lake (Utah, U.S.A.).
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Crustaceana 92 (4) 495-503
PHYLOGENETIC ANALYSIS OF EXOTIC INVASIVE SPECIES OF THE
BRINE SHRIMP ARTEMIA LEACH, 1819 (BRANCHIOPODA, ANOSTRACA)
IN AL WATHBA WETLAND RESERVE (U.A.E.; ABU DHABI)
BY
ANITHA SAJI1), AMIN EIMANIFAR2), PRITPAL S. SOORAE1), SHAIKHA AL DHAHERI1),
WEIDONG LI3), PEI-ZHENG WANG3)and ALIREZA ASEM3,4)
1)Terrestrial and Marine Biodiversity Sector, Assessment and Conservation, Environment
Agency — Abu Dhabi, P.O. Box 45553, Abu Dhabi, United Arab Emirates
2)Independent Research Scientist, Industrial District, 21601 Easton, Maryland, U.S.A.
3)College of Life Sciences and Ecology, Hainan Tropical Ocean University, Yucai Rd, Sanya
572000, P.R. China
ABSTRACT
The taxonomic identity of an unknown Artemia population inhabiting the Al Wathba Wetland
Reserve in Abu Dhabi, U.A.E., was determined using phylogenetic analysis of the mitochondrial
marker Cytochrome Oxidase Subunit 1 (COI). The results showed that the examined population
belongs to an exotic invasive species, Artemia franciscana. Based on the distribution pattern of
haplotypes, the studied population could possibly have originated from that inhabiting the Great
Salt Lake (Utah, U.S.A.).
Key words. — Artemia, invasive species, COI, Abu Dhabi, U.A.E., Great Salt Lake
RÉSUMÉ
L’identité taxonomique d’une population inconnue d’Artemia, habitant la réserve d’Al Wathba
Wetland à Abu Dhabi, U.A.E., a été déterminée en utilisant l’analyse phylogénétique du marqueur
mitochondrial Cytochrome Oxidase Subunit 1 (COI). Les résultats montrent que la population
examinée appartient à une espèce invasive exotique, Artemia franciscana. Sur la base du modèle de
distribution des haplotypes, la population étudiée pourrait être originaire du Grand Lac Salé (Utah,
U.S.A.).
Mots clés. — Artemia, espèce invasive, COI, Abu Dhabi, U.A.E., Grand Lac Salé
4)Corresponding author; e-mail: asem.alireza@gmail.com
©Koninklijke Brill NV, Leiden, 2019 DOI 10.1163/15685403-00003884
496 ANITHA SAJI ET AL.
INTRODUCTION
The brine shrimp Artemia Leach, 1819 is widely distributed in more than 600
geographical sites on all continents except Antarctica (Van Stappen, 2002), and
includes seven described bisexual species and in addition a number of partheno-
genetic populations (Asem et al., 2010). Four bisexual species are native to the Old
World, namely Artemia salina (Linnaeus, 1758) (Mediterranean basin), Artemia
urmiana Gunther, 1899 (Lake Urmia, Iran and the Crimean salt lakes, Russia),
Artemia sinica Cai, 1989 (China and Mongolia) and Artemia tibetiana Abatzopou-
los, Zhang & Sorgeloos, 1998 (Qinghai — Tibetan Plateau, China). The other three
bisexual species live in the New World, Artemia monica Verrill, 1869 (Mono Lake,
U.S.A.), Artemia franciscana Kellogg, 1906 (North America, Central America and
South America) and Artemia persimilis Piccinelli & Prosdocimi, 1968 (Argentina
and Chile) (Asem et al., 2010; Rogers, 2013). Parthenogenetic populations are
found in the Old World and in Oceania (Van Stappen, 2004). Furthermore, there
is a large number of Artemia populations reported with unknown taxonomic status
across the world (Van Stappen, 2004), which should be conserved for their contri-
bution to natural biodiversity.
Just four Artemia sites have been reported from the Arabian Peninsula, including
Saudi Arabia (2 sites), Kuwait (1 site) and the United Arab Emirates (1 site), which
were all reported as “unknown populations” (Vanhaecke et al., 1987; Aspinall
& Hellyer, 1999; Van Stappen, 2002). The first report of Artemia in the Al
Wathba Wetland Reserve dates back to that of Aspinall & Hellyer in 1999 (Van
Stappen, 2002). The primary studies done so far documented the population as
belonging to a bisexual species (Al Dhaheri & Saji, 2013; Saji et al., 2016; Saji
et al., unpublished data). The aim of the present study thus was to determine
the taxonomic status of an existing Artemia population found in the Al Wathba
Wetland Reserve.
MATERIAL AND METHODS
Study area and sampling
The Al Wathba Wetland Reserve (AWWR) (24°1515.59N 54°3638.57E) is
located at 40 km east of Abu Dhabi, has a 4.9 km2average surface area, with
approximately 1.5 km in length and 0.5 km in width, and has a maximum depth of
2 m (Brook et al., 2004; Al Dhaheri & Saji, 2013) (fig. 1).
Adult specimens of Artemia were collected from 6 stations using a Sampling
Two Conical Nets, (40 cm long by 30 cm diameter with 100 μm diameter mesh),
by pulling for 10 meters at the surface in November and December 2010.
EXOTIC INVASIVE ARTEMIA IN U.A.E., ABU DHABI 497
Fig. 1. Map of the study area: the Al Wathba Wetland Reserve in Abu Dhabi, United Arab Emirates
(U.A.E.).
DNA extraction, PCR amplification and sequencing
Total DNA was separately extracted from part of the antenna of 22 adult
males and females (1 : 1) following the Chelex®100 Resin method (Bio-Rad
Laboratories, Hercules, CA, U.S.A.). A fragment of mitochondrial Cytochrome C
Oxidase Subunit I (COI) was amplified using the invertebrate universal primers
LCO1490/HC02198 (Folmer et al., 1994). The thermal cycler PCR conditions
wereasfollows:acycleof3minat94°C,followedby35cyclesof45sat94°C,
60 s at 45°C, and 60 s at 72°C, with a final step of 5 min at 72°C (Asem et al.,
2016).
Sequence alignment and phylogenetic analyses
Sequences were aligned using MEGA ver. 6.00 with the default parameters
(Tamura et al., 2013). Our own DNA dataset was composed of 22 sequences
with 740 bp, after the alignment. The absence of pseudogenes was confirmed
using the sequence of protein coding for each one and the fact that there were no
multiple mutations or deletion(s) and duplication(s) in the analysed sequences. To
find the phylogenetic relationship among the collected samples from the AWWR
and with other bisexual species, we included five COI sequences (four sequences
for A. persimilis) for each species from GenBank (table I). The Online NCBI
498 ANITHA SAJI ET AL.
TABLE I
Information on and COI GenBank accession numbers of Artemia species used in this study
Species Abbreviation Number of
individuals
Accession
numbers
References
A. urmiana
Gunther, 1899
URM 4 JX512748-751 Eimanifar & Wink (2013)
A. sinica Cai,
1989
SIN 4 KF691298-301 Eimanifar et al. (2014)
A. tibetiana
Abatzopoulos,
Zhang &
Sorgeloos,
1998
TIB 4 KF691215-218 Eimanifar et al. (2014)
A. salina
(Linnaeus,
1758)
SAL 4 KF691512-515 Eimanifar et al. (2014)
A. persimilis
Piccinelli &
Prosdocimi,
1968
PER 4 DQ119647 Hou et al. (2006)
HM998992 Maniatsi et al. (2011)
EF615594 Wang et al. (2008)
EF615593 Wang et al. (2008)
A. franciscana
Kellogg, 1906
FRA 4 KJ863440-443 Eimanifar et al. (2014)
Unidentified AWWR 22 MH221175-196 This study
Genomic BLAST software (https://blast.ncbi.nlm.nih.gov/Blast.cgi) was utilized
to confirm the taxonomic status of the different species sequences that were used
for the phylogenetic analyses. The phylogenetic tree was reconstructed using
Bayesian inference (BI) as implemented in MrBayes 3.2.2 on XSEDE (Miller
et al., 2010). To estimate the genealogical relationships among haplotypes of
the examined individuals and A. franciscana, a median network was generated
using the median-joining algorithm as implemented in the Network program ver.
5.0.0.3 (Bandelt et al., 1999). The sequences of A. franciscana were chosen
from two natural habitats in the U.S.A., including the Great Salt Lake (GSL),
Utah (29 individuals: KF662960, KF662968, KF662970, KF662971, KF662976,
KF662977) and San Francisco Bay (SFB), California (37 individuals: KF662960,
KF662968, KF662970, KF662975) (Muñoz et al., 2013).
RESULTS AND DISCUSSION
During sampling, the average salinity, temperature and pH were recorded as
81 ppt, 25°C and 7.8, respectively.
According to the BI phylogenetic tree based on the COI dataset, all examined
Artemia individuals from the AWWR were grouped in the clade of A. franciscana
EXOTIC INVASIVE ARTEMIA IN U.A.E., ABU DHABI 499
(fig. 2). The results thus confirmed that the AWWR has been invaded by the
American native species A. franciscana, and no evidence was found that could
possibly document the existence of an endemic population of Artemia in the
AWWR.
The 88 COI sequences of A. franciscana revealed six distinct haplotypes, of
which H1 and H2 were the major types, grouped with 48 and 27 sequences,
respectively (fig. 3 and table II). H1 appeared composed of 47.92% GSL, 43.75%
AWWR and 8.33% SFB sequences, while H2 contained 96.29% and 3.71% of
the sequences from SFB and GSL, respectively. There was one more sequence
of the AWWR material that was shared with two others from GSL, i.e., in H4.
With regard to the distribution of sequences in the haplotype network, the genetic
structure of the COI marker in AWWR presented a high sequence similarity with
the GSL source.
Artemia is a crustacean with commercial importance in the aquaculture industry
(Sorgeloos et al., 2001). Various products of Artemia, especially enriched nauplii,
are widely used as live food in fishery and aquaculture (Lavens & Sorgeloos, 1996;
Touraki et al., 2012; Yin et al., 2012). Since the 1970s, A. franciscana has been
introduced intentionally into many salt habitats in Asia, Australia and the Western
Mediterranean (Amat et al., 2005, 2007; Ben Naceur et al., 2010; Muñoz & Pacios,
2010; Scalone & Rabet, 2013; Muñoz et al., 2014; Eimanifar et al., 2014).
A. franciscana, the inhabitant of the Great Salt Lake (GSL), has been generally
used in the aquaculture industry for cysts and biomass production (Sorgeloos et
al., 2001). According to our results, the distribution of sequences in the haplotype
network verified a hypothesis that the Great Salt Lake can be the origin of an exotic,
invasive Artemia in the AWWR. Although there is no evidence to confirm that A.
franciscana had been introduced intentionally into Al Wathba Wetland Reserve for
commercial purposes, it supports a suitable habitat for migratory birds, especially
the greater flamingo (Phoenicopterus roseus Pallas, 1811). The first population of
greater flamingos resided in the AWWR in 1993 (Al Dhaheri, 2004). Green et al.
(2005) suggested migrating of shorebirds is one of the major tools for dispersal
of invasive and native brine shrimps of the genus Artemia. It seems that migratory
birds, particularly the greater flamingo, may play a key role in the dispersal of non-
native A. franciscana into Al Wathba Wetland Reserve from neighbouring sites in
the Middle East. There are a few confirmed sites in the Middle East that are invaded
by exotic invasive A. franciscana, including Iran (Nough, Maharlu Lake, Mahshahr
port, Nough catchment) and Iraq (Garmat Ali) (Eimanifar et al., 2014).
Therefore, in conclusion we can state, that comprehensive studies need to be
carefully performed considering the biodiversity of American A. franciscana in
Middle East, in order to get a clear picture of the dispersal and distribution of the
species in this part of the world.
500 ANITHA SAJI ET AL.
Fig. 2. The COI phylogeny of the Artemia specimens analysed, based on the Bayesian Inference
approach. The numbers behind major nodes denote posterior probabilities. Daphnia tenebrosa G. O.
Sars, 1898 (GenBank accession no. HQ972028) was used as an outgroup.
EXOTIC INVASIVE ARTEMIA IN U.A.E., ABU DHABI 501
Fig. 3. The relationship of COI haplotypes distribution among Artemia individuals from the Great
Salt Lake (GSL), San Francisco Bay (SFB) and the Al Wathba Wetland Reserve.
TABLE II
Haplotype information for the network of Artemia haplotypes designed in this study (see fig. 3)
Haplotype No. Total number
of individuals
GSL (No. —
Percentage)
SFB (No. —
Percentage)
AWWR (No. —
Percentage)
H1 48 23 — 47.99% 4 — 8.33% 21 — 43.75%
H2 27 1 — 3.71% 26 — 96.29% 0 — 0%
H3 8 2 — 25% 6 — 75% 0 — 0%
H4 3 2 — 66.66% 0 — 0% 1 — 3.34%
H5 1 1 — 100% 0 — 0% 0 — 0%
H6 1 0 — 0% 1 — 100% 0 — 0%
ACKNOWLEDGEMENTS
Our thanks are due to Prof. Shi-Chun Sun (Ocean University of China, China)
for his permission to use his laboratory facilities for this study. The help of Dr.
Richard John Obrien Perry (EAD Research Committee) with the English text is
highly appreciated. The study was supported by the Environment Agency — Abu
Dhabi (EAD).
502 ANITHA SAJI ET AL.
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First received 5 December 2018.
Final version accepted 18 December 2018.
... Unintentional escapes caused by normal use in hatcheries and/or transmission by migratory waterfowl should be considered as a secondary factor in the distribution of A. franciscana in new habitats. At present, A. franciscana has been colonized in numerous regions across Eurasia, especially in the Mediterranean (Amat et al., 2005;Mura et al., 2006;Van Stappen, 2008;Muñoz, 2009;Ben Naceur et al., 2010, Eimanifar et al., 2014Scalone and Rabet, 2013;Horvath et al., 2018;Saji et al., 2019;Eimanifar et al., 2020) and Australia (Asem et al., 2018). ...
... Two Artemia sites have been reported in the United Arab Emirates (UAE) (Aspinall and Hellyer, 1999;Sivakumar et al., 2018). Saji et al. (2019) have documented the invasive A. franciscana in Al Wathba Wetland Reserve (AWWR). Evidence that Artemia has been introduced intentionally into these localities for commercial activity is lacking (Saji et al., 2019). ...
... Saji et al. (2019) have documented the invasive A. franciscana in Al Wathba Wetland Reserve (AWWR). Evidence that Artemia has been introduced intentionally into these localities for commercial activity is lacking (Saji et al., 2019). In 1998, before the introduction of the greater flamingos in Godolphin Lakes (GL), cysts of Artemia were distributed in those water bodies (Sivakumar et al., 2018). ...
Article
Full-text available
Artemia franciscana, native to America, has recently colonized as non-indigenous population in Asia, Europe, North Africa, and Australia. We evaluated the effects of the colonization of A. franciscana on genetic differentiation in new environments in the United Arab Emirates (UAE). We used the COI marker to determine the genetic structure and origins of exotic populations in the UAE. Results confirmed the colonization of A. franciscana in two localities. Invasive populations of A. franciscana had significantly lower genetic variation than native populations in the Great Salt Lake and San Francisco Bay. Results showed that the studied populations could not have colonized directly from natural American habitats, and they possibly were from secondary introduction events of other non-indigenous populations. Genetic analysis yielded different demographic patterns for the studied invasive populations. The population in Al Wathba Wetland Reserve (AWWR) demonstrated demographic expansion, whereas in Godolphin Lakes (GL), it reached a demographic equilibrium. Neutrality tests showed an excess of recent and historical mutations in the COI gene pool of invasive AWWR Artemia in the new environment. The results suggest that different ecological conditions in new environments can exert selective pressures during the introduction of an exotic population, which can affect genetic variation.
... Unintentional escapes caused by normal use in hatcheries and/or transmission by migratory waterfowl should be considered as a secondary factor in the distribution of A. franciscana in new habitats. At present, A. franciscana has been colonized in numerous regions across Eurasia, especially in the Mediterranean (Amat et al., 2005;Mura et al., 2006;Van Stappen, 2008;Muñoz, 2009;Ben Naceur et al., 2010, Eimanifar et al., 2014Scalone and Rabet, 2013;Horvath et al., 2018;Saji et al., 2019;Eimanifar et al., 2020) and Australia (Asem et al., 2018). ...
... Two Artemia sites have been reported in the United Arab Emirates (UAE) (Aspinall and Hellyer, 1999;Sivakumar et al., 2018). Saji et al. (2019) have documented the invasive A. franciscana in Al Wathba Wetland Reserve (AWWR). Evidence that Artemia has been introduced intentionally into these localities for commercial activity is lacking (Saji et al., 2019). ...
... Saji et al. (2019) have documented the invasive A. franciscana in Al Wathba Wetland Reserve (AWWR). Evidence that Artemia has been introduced intentionally into these localities for commercial activity is lacking (Saji et al., 2019). In 1998, before the introduction of the greater flamingos in Godolphin Lakes (GL), cysts of Artemia were distributed in those water bodies (Sivakumar et al., 2018). ...
Article
Full-text available
Artemia franciscana, native to America, has recently colonized as non-indigenous population in Asia, Europe, North Africa, and Australia. We evaluated the effects of the colonization of A. franciscana on genetic differentiation in new environments in the United Arab Emirates (UAE). We used the COI marker to determine the genetic structure and origins of exotic populations in the UAE. Results confirmed the colonization of A. franciscana in two localities. Invasive populations of A. franciscana had significantly lower genetic variation than native populations in the Great Salt Lake and San Francisco Bay. Results showed that the studied populations could not have colonized directly from natural American habitats, and they possibly were from secondary introduction events of other non-indigenous populations. Genetic analysis yielded different demographic patterns for the studied invasive populations. The population in Al Wathba Wetland Reserve (AWWR) demonstrated demographic expansion, whereas in Godolphin Lakes (GL), it reached a demographic equilibrium. Neutrality tests showed an excess of recent and historical mutations in the COI gene pool of invasive AWWR Artemia in the new environment. The results suggest that different ecological conditions in new environments can exert selective pressures during the introduction of an exotic population, which can affect genetic variation.
... Two Artemia sites have been reported from the United Arab Emirates 22,23 . Saji et al. 20 have documented invasive A. franciscana in Al Wathba Wetland Reserve. There is no evidence that Artemia had been introduced intentionally into these localities for commercial activity, but it has prepared a suitable habitat for the greater flamingos and other native shore birds 20 . ...
... Saji et al. 20 have documented invasive A. franciscana in Al Wathba Wetland Reserve. There is no evidence that Artemia had been introduced intentionally into these localities for commercial activity, but it has prepared a suitable habitat for the greater flamingos and other native shore birds 20 . In 1998, before introduction of the greater flamingos in Godolphin Lakes, cysts of Artemia were distributed in the water body 23 . ...
... Our results have also documented the colonization of same species in Godolphin Lakes locality.The San Francisco Bay (SFB) and Great Salt Lake (GSL) are the two main sources of Artemia that have usually been used to culture in other saline ecosystems for industrial aquaculture and fishery activates to produce Artemia cysts and biomass13,20,21,34 , for this reason these populations were considered in this analysis to find out the genetic alterations of the colonized populations in new non-native environments.Mitochondrial DNA represented some exceptional characteristics consisting rapid evolutionary rates, maternal origin, and lack of recombination35,36 . Then mitochondrial markers are important for apprehension the tracing and explanation the source of non-indigenous species in new habitats 20,21,37-40 . ...
Preprint
Artemia franciscana, native to America, has recently colonized non-indigenous populations in Eurasia, Mediterranean regions and Australia. In present we sought to evaluate the potential effects of colonization of A. franciscana on genetic differentiation in the new environments in UAE. We used the COI marker to determine population genetic structure and identify the origins of exotic populations in UAE. Our findings have confirmed the colonization of both localities by A. franciscana. Genetic variation of invasive A. franciscana were exclusively lower than native population in Great Salt Lake and San Francisco Bay. Results have showed the studied population could not possibly have colonized directly from natural American localities, perhaps resulting from secondary introduction events from other non-indigenous populations. Genetic analysis have yielded different demographic patterns for invasive studied populations. Al Wathba Wetland Reserve (AWWR) population have represented demographic expansion. In contrast, Godolphin Lakes (GL) population was at demographic equilibrium. Neutrality tests have documented the excess of both recent and historical mutations in the COI gene pool of invasive AWWR Artemia throughout establishment in the new environment.
... Generally, the long-distance translocations of the American species Artemia franciscana to other non-indigenous regions have occurred as a result of commercial activities, which have been fully documented previously [2,[15][16][17][18]. Artemia franciscana is a successful invader in saltwater ecosystems due to its faster filter-feeding rate, a high potential of reproduction [15,19], and a better physiological immune system, which is associated with nutritional behavior against cestode parasites [15] than the native species. ...
... Previous studies on A. franciscana have documented that invasive populations demonstrated genetic variations relative to the native American source populations [2,17,18,[22][23][24]. The low genetic diversity in the non-indigenous populations has been attributed to the founder effect [22] or population bottleneck due to the decreasing of population size in introduced populations during the process of establishment [17]. ...
... A partial sequence of the mitochondrial marker cytochrome c oxidase subunit I (COI) was utilized to identify the taxonomical status of the studied populations using phylogenetic analyses as implemented in the MEGA X program (Temple University, Philadelphia, USA) [2,17,18]. To identify the taxonomical status of the studied populations, the COI reference sequences from the recognized bisexual species and parthenogenetic populations were downloaded from GenBank (Table 2). ...
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Due to the rapid developments in the aquaculture industry, Artemia franciscana, originally an American species, has been introduced to Eurasia, Africa and Australia. In the present study, we used a partial sequence of the mitochondrial DNA Cytochrome Oxidase subunit I (mt-DNA COI) gene and genomic fingerprinting by Inter-Simple Sequence Repeats (ISSRs) to determine the genetic variability and population structure of Artemia populations (indigenous and introduced) from 14 different geographical locations in Western Asia. Based on the haplotype spanning network, Artemia urmiana has exhibited higher genetic variation than native parthenogenetic populations. Although A. urmiana represented a completely private haplotype distribution, no apparent genetic structure was recognized among the native parthenogenetic and invasive A. franciscana populations. Our ISSR findings have documented that despite that invasive populations have lower variation than the source population in Great Salt Lake (Utah, USA), they have significantly revealed higher genetic variability compared to the native populations in Western Asia. According to the ISSR results, the native populations were not fully differentiated by the PCoA analysis, but the exotic A. franciscana populations were geographically divided into four genetic groups. We believe that during the colonization, invasive populations have experienced substantial genetic divergences, under new ecological conditions in the non-indigenous regions.
... However, human commercial interests have also come along with disturbances in brine shrimp species distribution, even compromising the survival of some. The large demand of Artemia for fish farming triggered the introduction and invasion of the North American cultivated species Artemia monica Verrill, 1869 (= A. franciscana Kellogg, 1906) into coastal salterns all over the world (Triantaphyllidis et al. 1994;Amat et al. 2007;Mura et al. 2006;Ruebhart et al. 2008;Scalone and Rabet 2013;Saji et al. 2019). This species is displacing the Mediterranean native species Artemia salina (Linnaeus, 1758) (Oscoz et al. 2010;Horváth et al. 2018) possibly due to its high adaptive potential and physiological plasticity that enhance its invasion range capacity (Dlugosch and Parker 2008). ...
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Brine shrimps ( Artemia ) have undergone geographic range and demographic expansions as a result of their interaction with humans since the beginning of salt harvesting. This interaction has favoured the expansion of some species but compromising the survival of others. Mediterranean native populations of Artemia salina from coastal salterns and lagoons are facing the presence and expansion of the introduced and invasive American species Artemia monica (= A . franciscana ). However, this species could not be the only threat. Parthenogenetic populations of the Asian species A . urmiana and A . sinica are widespread along the Mediterranean and other areas of the world. In this work, with the use of large cox1 and mitogenomic datasets, phylogenetic and phylogeographic inferences, and a time calibrated tree, we confirmed the Asian origin and recent arrival of the current Western Mediterranean parthenogenetic populations of Artemia . In addition, the replacement of Iberian populations of A . salina by Asiatic parthenogenetic populations lead us to recognize parthenogens as invasive. Current salterns development and commercial importance of Artemia make human-mediated introduction probable. These results demonstrate again the impact that changing human interests have on population expansion or decline of species adapted to anthropogenic habitats. Artemia salina decline makes urgent the implementation of conservation measures such as its use in fish farming and salt production or its inoculation in inland salterns.
... Artemia franciscana Kellogg, 1906 is native to the Americas, but was widely introduced across Eurasia and threatens and/or outcompetes native Artemia populations (Amat et al., 2007;Mura et al., 2006;Muñoz et al., 2008). Records from the Arabian Peninsula include unidentified Artemia populations from Kuwait and Saudi Arabia (Triantaphyllidis et al., 1998;Thiéry, 1996) and A. franciscana was recorded from the United Arab Emirates (Saji et al., 2019). Native or invasive forms could easily show up in appropriate saline habitat in Qatar. ...
... The mitochondrial markers, COX1 and 16S, have been successfully used in phylogeny of branchiopods [60][61][62][63][64][65]. To date only COX1 has been utilized for phylogenetic studies on Artemia, nevertheless mitogenomic results demonstrated significant difference in the nucleotide composition of ATP8, ATP6, ND3, ND6, ND1 and COX3. ...
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In the previously published mitochondrial genome sequence of Artemia urmiana (NC_021382 [JQ975176]), the taxonomic status of the examined Artemia had not been determined, due to partheno�genetic populations coexisting with A. urmiana in Urmia Lake. Additionally, NC_021382 [JQ975176] has been obtained with pooled cysts of Artemia (0.25 g cysts consists of 20,000–25,000 cysts), not a single specimen. With regard to coexisting populations in Urmia Lake, and intra- and inter-specific variations in the pooled samples, NC_021382 [JQ975176] cannot be recommended as a valid se�quence and any attempt to attribute it to A. urmiana or a parthenogenetic population is unreasonable. With the aid of next-generation sequencing methods, we characterized and assembled a complete mitochondrial genome of A. urmiana with defined taxonomic status. Our results reveal that in the previously published mitogenome (NC_021382 [JQ975176]), tRNA-Phe has been erroneously attributed to the heavy strand but it is encoded in the light strand. There was a major problem in the position of the ND5. It was extended over the tRNA-Phe, which is biologically incorrect. We have also identified a partial nucleotide sequence of 311 bp that was probably erroneously duplicated in the assembly of the control region of NC_021382 [JQ975176], which enlarges the control region length by 16%. This partial sequence could not be recognized in our assembled mitogenome as well as in 48 further examined specimens of A. urmiana. Although, only COX1 and 16S genes have been widely used for phylogenetic studies in Artemia, our findings reveal substantial differences in the nucleotide composition of some other genes (including ATP8, ATP6, ND3, ND6, ND1 and COX3) among Artemia species. It is suggested that these markers should be included in future phylogenetic studies.
... The mitochondrial markers, COX1 and 16S, have been successfully used in phylogeny of branchiopods [60][61][62][63][64][65]. To date only COX1 has been utilized for phylogenetic studies on Artemia, nevertheless mitogenomic results demonstrated significant difference in the nucleotide composition of ATP8, ATP6, ND3, ND6, ND1 and COX3. ...
Article
Full-text available
In the previously published mitochondrial genome sequence of Artemia urmiana (NC_021382 [JQ975176]), the taxonomic status of the examined Artemia had not been determined, due to parthenogenetic populations coexisting with A. urmiana in Urmia Lake. Additionally, NC_021382 [JQ975176] has been obtained with pooled cysts of Artemia (0.25 g cysts consists of 20,000–25,000 cysts), not a single specimen. With regard to coexisting populations in Urmia Lake, and intra- and inter-specific variations in the pooled samples, NC_021382 [JQ975176] cannot be recommended as a valid sequence and any attempt to attribute it to A. urmiana or a parthenogenetic population is unreasonable. With the aid of next-generation sequencing methods, we characterized and assembled a complete mitochondrial genome of A. urmiana with defined taxonomic status. Our results reveal that in the previously published mitogenome (NC_021382 [JQ975176]), tRNA-Phe has been erroneously attributed to the heavy strand but it is encoded in the light strand. There was a major problem in the position of the ND5. It was extended over the tRNA-Phe, which is biologically incorrect. We have also identified a partial nucleotide sequence of 311 bp that was probably erroneously duplicated in the assembly of the control region of NC_021382 [JQ975176], which enlarges the control region length by 16%. This partial sequence could not be recognized in our assembled mitogenome as well as in 48 further examined specimens of A. urmiana. Although, only COX1 and 16S genes have been widely used for phylogenetic studies in Artemia, our findings reveal substantial differences in the nucleotide composition of some other genes (including ATP8, ATP6, ND3, ND6, ND1 and COX3) among Artemia species. It is suggested that these markers should be included in future phylogenetic studies.
... In Europe, A. franciscana was first detected in Portugal in the 1980s (Hontoria et al., 1987) and a decade later in France (Thiéry and Robert, 1992). Since then, it has progressively invaded most hypersaline ecosystems of the Mediterranean basin, including those of Spain and Italy (Amat et al., 2005(Amat et al., , 2007Horváth et al., 2018), North Africa (Morocco, Tunisia) (Amat et al., 2005(Amat et al., , 2007Naceur et al., 2010), and has reached the Middle East (Iran, Egypt, Arab Emirates) (Hajirostamloo and Pourrabbi, 2011;Sheir et al., 2018;Saji et al., 2019). It is also present in Australia, Brazil, India, China and Kenya (Ruebhart et al., 2008;Camara, 2001;Zheng et al., 2004;Krishnakumar and Munuswamy, 2014;Ogello et al., 2014). ...
Article
In recent decades, brine shrimps of the genus Artemia has suffered a major biodiversity loss in the Mediterranean region due to the introduction of the highly invasive A. franciscana. Pollution has been proposed as an important factor limiting this global invasion. Contrary to the general acceptation that pollution tends to favour invasive species, it has been postulated that local adaptation of native Artemia to pollution may prevent or delay colonization by the exotic species. To provide insight into this “pollution resistance hypothesis”, we investigated the individual effect of acute toxicity of mercury (Hg) and zinc (Zn) on the survival of six different native and invasive Artemia populations from the Iberian Peninsula collected from areas with different levels of Hg- and Zn-pollution. The Hg and Zn 24 h-LC50 values for Artemia nauplii of the different populations varied between 20 and 70 mg Hg L⁻¹, and between 350 and 450 mg Zn L⁻¹, respectively. Native Artemia from Cabo de Gata (SW Spain) showed significantly higher survival at high Hg concentrations than other populations, which may be explained by the longer history of Hg-pollution in that area from mining activities, compared to the other sites. In contrast, differences between populations in response to high Zn levels were weak, and inconsistent with the environmental differences in Zn concentrations. Discussion of the results of this work was done in relation to the “pollution resistance hypothesis” and conclude that Hg pollution may limit the invasion by A. franciscana in some study sites for an uncertain length of time.
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Piper methysticum G. Forst., commonly known as Kava, is a dioecious perennial herb which is traditionally an important medicinal plant. The plant is used to treat fever, respiratory diseases, seizures, and urogenital problems. The present study was designed to evaluate the antioxidant, cytotoxic, membrane stabilizing and analgesic potential of methanol extract of Piper methysticum leaf. Phytochemical screenings of the crude extract revealed the occurrence of acidic compounds, alkaloids, glycosides, reducing sugars, gums, flavonoids, and combined reducing sugars. During antioxidant activity test, the total phenolic content of methanol extract was 42.66 mg gallic acid equivalent/100 g extract and it displayed the IC 50 value of 6.59 µg/ml to remove DPPH free radicals as compared to the standard butylated hydroxyl toluene (IC 50 = 6.38 µg/ml). The extract showed cytotoxicity against brine shrimp nauplii with an LC 50 of 60.94 μg/ml. Moreover, the test extract was found to be effective for stabilizing erythrocyte membrane against hypotonic solution induced hemolysis. The extract exhibited dose-dependent pain-relieving activity in mice. At doses of 250-and 500-mg/kg body weight, the plant sample revealed 26.9 2% and 37.95 % of reduction in pain sensation induced by acetic acid, respectively when compared to the standard diclofenac-Na (54.81%). The above results suggest that the selected plant extract possesses antioxidant, cytotoxic, membrane stabilizing and analgesic activities.
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Long term monitoring programme on Brine shrimp (Artemia sp.) is being carried out by the Environment Agency, Abu Dhabi, United Arab Emirates (EAD) with the prime purpose of understanding the population dynamics, ecology and habitat requirements of Artemia at Al Wathba Lake, situated within Al Wathba Wetland Reserve, which is an artificial wetland near Abu Dhabi City. The present study, being a component of this programme, intends to understand the influence of chemical parameters such as dissolved oxygen, nitrate, nitrite, phosphate, ammonia and total organic carbon on Artemia biomass and cyst production at different sites of the Al Wathba Lake. The study was carried out by sampling lake water quarterly for a period of 5 years from 2010 to 2014. The Artemia population was found to have direct impact of the above mentioned parameters on its abundance. The abundance was highest during the year 2010. Further, temperature, dissolved oxygen, and nitrate were found to be the most crucial parameters for production of Artemia. Furthermore, this study aimed to determine the significant relationship between physico-chemical parameters and Artemia sp. population dynamics and cyst production.
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Using two nuclear (ITS1 and Na+/K+ ATPase) and three mitochondrial (COI, 16S and 12S) markers, we determined the genetic variation and evolutionary relationship of parthenogenetic and bisexual Artemia. Our analyses revealed that mitochondrial genes had higher genetic variation than nuclear genes and that the 16S showed more variety than the other mitochondrial genes in parthenogenetic populations. Triploid parthenogens showed lower genetic variation than diploid ones, whereas the tetra- and pentaploids had greater genetic distance than diploid parthenogens. No shared haplotype was found between individuals of parthenogenetic populations and Asian bisexual species with the exception of Na+/K+ ATPase (Artemia tibetiana). Only mitochondrial markers can demonstrate phylogenetic relationships, and showed that the parthenogenetic Artemia is a polyphyletic group in which the diploid lineages share a common ancestor with Artemia urmiana while tetraploids are closely related to Artemia sinica. The triploid and pentaploid linages are likely to be directly derived from diploid and tetraploid parthenogens, respectively. Subsequently, west Asia is origin for di-/triploids, and tetra-/pentaploids rose from East Asia.
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A checklist of the Anostraca (fairy shrimp) is presented with synonyms. More than 700 anostracan taxa are presented, of which 407 are considered valid families, genera and species. Chresonyms are provided for taxa redescribed according to modern standards. Nomenclatural problems are examined and resolved concerning the genus Chirocephalus and its junior synonym Galaziella. The presentation of the suborders and families follows recent molecular phylogenetic analyses presented elsewhere.
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Asia harbors a diverse group of sexual and asexual Artemia species, including the invasive Artemia franciscana, which is native to the Americas. The phylogeny of Asian Artemia species and the phylogeography of the introduced A. franciscana from 81 sampling localities in Eurasia, Africa and America were elucidated using mitochondrial (COI) and nuclear DNA (ITS1) sequences. According to a COI phylogeny, 6 distinctive genetic groups were recognized, with a complex phylogeographic structure among Asian Artemia. A haplotype complex which includes parthenogenetic lineages is distributed in 39 inland geographical localities in Asia, illustrating a wide distribution with a narrow genetic structure on this continent. The invasive A. franciscana was discovered in 31 geographical localities along the southern and eastern coastal regions of Asia. Three sexual species (A. sinica, A. tibetiana and A. urmiana) have a restricted distribution in certain geographical localities in Asia. In contrast to COI phylogeny reconstruction, ITS1 sequences showed inconsistency with the COI tree, indicating incomplete lineage sorting which provided the low genetic divergence in the Asian clade. Asian A. franciscana showed higher haplotype diversity as compared to the source population from the Great Salt Lake (USA), which could be attributed to multiple introductions by mass dispersal in Asia via human activities. The invasive success of A. franciscana in Asia could lead to a long-term biodiversity disturbance of the autochthonous Artemia species on the continent.
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Since Darwin's time, waterbirds have been considered an important vector for the dispersal of continental aquatic invertebrates. Bird movements have facilitated the worldwide invasion of the American brine shrimp Artemia franciscana, transporting cysts (diapausing eggs), and favouring rapid range expansions from introduction sites. Here we address the impact of bird migratory flyways on the population genetic structure and phylogeography of A. franciscana in its native range in the Americas. We examined sequence variation for two mitochondrial gene fragments (COI and 16S for a subset of the data) in a large set of population samples representing the entire native range of A. franciscana. Furthermore, we performed Mantel tests and redundancy analyses (RDA) to test the role of flyways, geography and human introductions on the phylogeography and population genetic structure at a continental scale. A. franciscana mitochondrial DNA was very diverse, with two main clades, largely corresponding to Pacific and Atlantic populations, mirroring American bird flyways. There was a high degree of regional endemism, with populations subdivided into at least 12 divergent, geographically restricted and largely allopatric mitochondrial lineages, and high levels of population structure (Φ ST of 0.92), indicating low ongoing gene flow. We found evidence of human-mediated introductions in nine out of 39 populations analysed. Once these populations were removed, Mantel tests revealed a strong association between genetic variation and geographic distance (i.e., isolation-by-distance pattern). RDA showed that shared bird flyways explained around 20% of the variance in genetic distance between populations and this was highly significant, once geographic distance was controlled for. The variance explained increased to 30% when the factor human introduction was included in the model. Our findings suggest that bird-mediated transport of brine shrimp propagules does not result in substantial ongoing gene flow; instead, it had a significant historical role on the current species phylogeography, facilitating the colonisation of new aquatic environments as they become available along their main migratory flyways.
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Cysts of the brine shrimp Artemia franciscana are harvested from the Great Salt Lake (GSL) and San Francisco Bay saltworks (SFB) in the U.S.A, 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 U.S.A. populations, (2) how the genetic diversity of the Mediterranean compares with that at GSL and SFB, and (3) if genetic patterns in 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 U.S.A. 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 showing similar or higher genetic diversity than native ones, which are likely to be admixed from both GSL and SFB due to 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 commercialised U.S.A. populations.
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We announce the release of an advanced version of the Molecular Evolutionary Genetics Analysis (MEGA) software, which currently contains facilities for building sequence alignments, inferring phylogenetic histories, and conducting molecular evolutionary analysis. In version 6.0, MEGA now enables the inference of timetrees, as it implements our RelTime method for estimating divergence times for all branching points in a phylogeny. A new Timetree Wizard in MEGA6 facilitates this timetree inference by providing a graphical user interface (GUI) to specify the phylogeny and calibration constraints step-by-step. This version also contains enhanced algorithms to search for the optimal trees under evolutionary criteria and implements a more advanced memory management that can double the size of sequence data sets to which MEGA can be applied. Both GUI and command-line versions of MEGA6 can be downloaded from www.megasoftware.net free of charge.
Chapter
‘Artemia is widely distributed on the five continents in many salt lakes, coastal lagoons, and solar saltworks’ — this, or a variation on the same theme, is the standard opening phrase in most scientific contributions related to brine shrimp zoogeography. This chapter is no exception to this rule.
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Endemic Artemia franciscana populations can be found throughout the American continent and also as an introduced specie in several country all over the world, such as in the Mediterranean region where Artemia franciscana was identified as an invasive specie replacing native Artemia parthenogenetica and Artemia salina. In the present study, the characterization of the new invasive Artemia franciscana reported from Sabkhet Halk El-Menzel (Tunisia) was done based on the cysts biometry, nauplii instar-I length, Adult sexual dimorphism and fatty acid profile. The mean value of the diameter of non-decapsulated and decapsulated cysts, chorion thickness and naupliar length is 235.8, 226.3, 4.75 and 426.8 µm, respectively. Sexual dimorphism for adults specimen showed that maximal distance between compound eyes, diameter for compound eyes, length of first antenna and the abdomen length compared to the total body length ratio, are the most important variables for males and females discrimination with a total contribution of 62.39 %. The analysis of fatty acid methyl esters profile of decapsulated cysts resulted in low levels of linolenic acid (LLA, C18:3n-3) and high levels of eicosapentaenoic acid (EPA, C20:5n-3) with 3.11 and 11.10 %, respectively. Low quantity of docosahexaenoic acid (DHA, 22:6n-3) was also observed with 0.17 mg.g-1 dry weight.
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The aim of this study was to evaluate the effects of Artemia nauplii enriched with different concentrations of highly unsaturated fatty acids (HUFAs) on the lipid metabolic response, peroxidation, and antioxidant defence status of the lined seahorse (Hippocampus erectus) juveniles. Twenty‐day‐old juveniles were fed Artemia nauplii enriched with four different concentrations (0.0 µL/L [control, A], 13.5 µL/L [B], 27.0 µL/L [C], and 54.0 µL/L [D]) of HUFAs (two thirds DHA and one third EPA) for 30 d. The activities of lipase and lipoproteinlipase of the juveniles significantly increased with increasing HUFA concentration; however, the activities of malate dehydrogenase and lactate content decreased with increasing HUFA concentration. Alkaline phosphatase activity and pyruvic acid content were not significantly different among the three treatments and the control. Malonaldehyde content was significantly negatively related to the enrichment concentrations (in Treatments A, B, and C); however, it increased significantly in Treatment D. The activities of superoxide dismutase in Treatments A and B were significantly higher than that in Treatments C and D. Catalase activity increased significantly from the control to Treatment C, then decreased significantly in Treatment D. Glutathione peroxidase activities increased significantly with increasing concentration of HUFAs, and peaked in Treatment D. The results indicate that dietary HUFAs are able to modify some enzymatic activities, and moderate dietary HUFA supplementation significantly promotes lipid metabolism and reduces lipid peroxidation products by enhancing antioxidant defence in the juveniles. However, excess HUFAs may result in adverse effects on the enzymatic activities in the juveniles, which might be related to oxidative stress.