Diversity 2014, 6(1), 102-132; doi:10.3390/d6010102

Review
Biodiversity of the Hypersaline Urmia Lake National Park (NW Iran)
Alireza Asem 1,,*, Amin Eimanifar 2,,*, Morteza Djamali 3, Patricio De los Rios 4 and Michael Wink 2
1
Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao 266003, China
2
Institute of Pharmacy and Molecular Biotechnology (IPMB), Heidelberg University, Im Neuenheimer Feld 364, Heidelberg D-69120, Germany; E-Mail: wink@uni-hd.de
3
Institut Méditerranéen de Biodiversité et d'Ecologie (IMBE: UMR CNRS 7263/IRD 237/Aix-Marseille Université), Europôle Méditerranéen de l'Arbois, Pavillon Villemin BP 80, 13545, Aix-en Provence Cedex 04, France; E-Mail: morteza.djamali@imbe.fr
4
Environmental Sciences School, Natural Resources Faculty, Catholic University of Temuco, Casilla 15-D, Temuco 4780000, Chile; E-Mail: patorios@msn.com
These authors contributed equally to this work.
*
Authors to whom correspondence should be addressed; E-Mails: asema@ouc.edu.cn (A.A.); A.Eimanifar@uni-heidelberg.de (A.E.); Tel.: +86-150-6624-4312 (A.A.); Fax: +86-532-8203-2216 (A.A.); Tel.: +49-6221-544-880 (A.E.); Fax: +49-6221-544-884 (A.E.).
Received: 3 December 2013; in revised form: 13 January 2014 / Accepted: 27 January 2014 /
Published: 10 February 2014

Abstract

: Urmia Lake, with a surface area between 4000 to 6000 km2, is a hypersaline lake located in northwest Iran. It is the saltiest large lake in the world that supports life. Urmia Lake National Park is the home of an almost endemic crustacean species known as the brine shrimp, Artemia urmiana. Other forms of life include several species of algae, bacteria, microfungi, plants, birds, reptiles, amphibians and mammals. As a consequence of this unique biodiversity, this lake has been selected as one of the 59 biosphere reserves by UNESCO. This paper provides a comprehensive species checklist that needs to be updated by additional research in the future.
Keywords:
biodiversity; hypersalinity; Urmia Lake; National Park

1. Introduction

Urmia Lake is the 20th largest lake in the world. The surface area of this salt lake varies between 2300 to 6000 km2 (Figure 1) for two main reasons. First, its hydrology largely depends on precipitation in the catchment area. Secondly, extremely gentle slopes of its marginal plains lead to inundation of large areas even by small water level rises. The average altitude is 1274 m above sea level and the salinity ranges between 120 g/L and more than 300 g/L. 102 islands have been recorded in this lake. Today, only the Islami (Shahi) Peninsula is inhabited by humans, but the “Limit of the World from the East to the Westthe oldest Persian geography bookwritten by anonymous author(s) in 982 A.D., described Kaboudan Island as suitable for human settlement [1].

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Figure 1. Geographical localisation of Urmia Lake in the northwestern of Iran.

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Figure 1. Geographical localisation of Urmia Lake in the northwestern of Iran.
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Contrary to widespread opinion, Urmia Lake is a second hypersaline lake with an active food web compared to the Dead Sea (with a salinity of >340 g/L), which includes bacteria, archaea, algae, protozoa and ciliates [2,3,4]. Urmia Lake is saltier than the Aral Sea (>100 g/L) [5] and Karabogaz Gol (40−100 g/L in the deep zone, 170−250 g/L in the northwest and southwest parts of the bay) [6]. The lake hosts diverse bacterial communities, hyperhalophilous phytoplanktons, and notably the macrozooplankton crustacean, the brine shrimp Artemia urmiana. Thus, with regard to its ecological significance, unique biodiversity and the presence of indigenous communities, Urmia Lake has been recognized as a Protected Field since 1967 and was designated as a National Park in 1976 as one of 59 biosphere reserves by UNESCO [7]. In 1975, it was also registered in the Ramsar Convention on Wetlands as a wetland of international importance [7]. Although the lake is a UNESCO biosphere reserve, several development projects have had detrimental consequences for biodiversity.

The lake is divided into north and south parts, separated by a dike-type causeway, which has a small gap (1400 m) that allows a limited exchange of water between the two sides [7] (Figure 1). About 35 dams have been built on 21 permanent rivers flowing to the lake [8], which restrict the influx of fresh water. In the last decade, Urmia Lake has been affected by a transformation in the hydrological regime, due to climate instability and the construction of dams [9]. Water resource development projects are diverting enormous quantities of fresh water and preventing a replenishment of lake water, which is lost to evaporation [10]. The intensive development of agriculture during the last decades and the resultant over-exploitation of groundwater have also deprived the lake of one of its main water input resources.

A progressive drought has caused fundamental changes in the physio–chemical composition of the lake-the salinity exceeds >300 g/L, the surface area has decreased to less than 2366 km2, the lake level has decreased to 1271 m, the volume of water has decreased from 42 to 22 billion m3 between 1995 and 2010, and the water depth has decreased to 6 m, whereas reservoirs of dams have increased from 1.624 billion m3 to 3.568 billion m3 [9,11,12].

Climate and anthropogenic alterations are recognized as crucial factors in population declines and even the risk of extinctions in most ecosystems [13,14]. A decrease of population density would ultimately limit dispersal, as well as gene flow, among populations. This will eventually lead to the loss of genetic diversity [15]. On the other hand, an increased rate of dispersal can also disturb local genetic adaptation [16]. At present, the severe drought which happened in 2003–2004 is jeopardizing the biodiversity of the lake [17].

In this review, we have summarized the available information on the biodiversity of the lake ranging from bacteria and fungi to plants and animals. Apparently, the existing information is incomplete and more detailed future studies are required for a complete inventory of the biodiversity of Urmia Lake.

2. Archaebacteria and Bacteria

Urmia Lake harbours a diverse group of bacterial species (Table 1). Two pathogenic bacteria Clostridium perfringens and Enterococcus faecalis have been identified in the lake water and particularly in the estuary sediments. As these bacteria constitute the natural flora of the human digestive tract, their presence in the lake water and sediments suggests that they have originated from the inflow of urban waste water into Urmia Lake [18,19].

In Urmia Lake, the muds contain green sulphur-bacteria, purple sulphur-bacteria and ferro-bacteria [19,20]. Halophilic archaebacteria can usually synthesize red and pink pigments in response to environmental stress [21,22,23]. During the summer of 2008, the water of Urmia Lake around Kaboudan Island changed from blue, its normal colour, to red [24]. This was the first report of this event that may be attributed to the bloom of Archaebacteria or of Dunaliella or both (see [25]).

Table Table 1. List of Archaebacteria and Bacteria from Urmia Lake.

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Table 1. List of Archaebacteria and Bacteria from Urmia Lake.
DomainPhylumClassOrderFamilyGenusSpeciesReference
ArchaeaEuryarchaeotaHalobacteriaHalobacterialesHalobacteriaceaeHaloarculasp.[23,26]
Halobacteriumsp.[23]
Haloferaxsp.[22]
Halorubrumsp.[23]
BacteriaActinobacteriaActinobacteriaActinomycetalesMicrobacteriaceaeMicrobacteriumsp.[27]
MicrococcaceaeKocuriasp.[27]
Micrococcussp.[27]
SanguibacteraceaeSanguibactersp.[27]
BacteroidetesCytophagiaCytophagalesCytophagaceaeAdhaeribactersp.[27]
Pontibactersp.[27]
FlammeovirgaceaeCesiribactersp.[27]
Incertae sedisIncertae sedisRhodothermaceaeSalinibactersp.[27]
CyanobacteriaCyanophyceaeChroococcalesChroococcaceaeChroococcussp.[28]
MicrocystaceaeAnacystissp.[28]
Gloeocapsasp.[29,30]
SpirulinaceaeSpirulinaS. maxima[30]
NostocalesNostocaceaeAnabaenasp.[28,31]
Nostocsp.[29,30]
OscillatorialesOscillatoriaceaeLyngbyasp.[28]
Oscillatoriasp.[28,29,30,31,32]
SynechococcalesSynechococcaceaeSynechococcussp.[28]
BacteriaFirmicutesBacilliBacillalesBacillaceaeBacillusB. licheniformis[33]
sp.[27,34,35,36]
Gracilibacillussp.[27]
Halobacillussp.[27,34,36,37]
Oceanobacillussp.[27]
Piscibacillussp.[27]
Pontibacillussp.[27]
Thalassobacillussp.[27,34]
VirgibacillusV. halodenitrificans[38]
sp.[37]
PlanococcaceaePlanococcussp.[27]
StaphylococcaceaeStaphylococcussp.[27]
LactobacillalesCarnobacteriaceaeAlkalibacteriumsp.[27]
EnterococcaceaeEnterococcusE. faecalis *[18]
ClostridiaClostridialesClostridiaceaeClostridiumC. perfringens[18]
ProteobacteriaAlphaproteobacteriaCaulobacteralesCaulobacteraceaeBrevundimonassp.[27]
RhodobacteralesRhodobacteraceaeParacoccussp.[27]
GammaproteobacteriaAlteromonadalesAlteromonadaceaeMarinobactersp. H57B71[36]
Marinobactersp.[27,34,36,37]
IdiomarinaceaeIdiomarinasp. Y24[36]
EnterobacterialesEnterobacteriaceaePlesiomonasP. shigelloides[39]
Providenciasp.[27]
BacteriaProteobacteriaGammaproteobacteriaOceanospirillalesHahellaceaeHalospinaH. denitrificans[36]
HalomonadaceaeChromohalobacterC. salexigens[40]
HalomonasH. ventosae[36,41]
H. sediminis YIM C248[36]
sp.[37]
HalovibrioH. denitrificans[36]
Salicolasp.[27,36]
PseudomonadalesPseudomonadaceaePseudomonassp.[36]
VibrionalesVibrionaceaeVibrioV. mimicus[39,42]
V. alginolyticus[39,42]
V. fluvialis[39,42]
XanthomonadalesXanthomonadaceaeLysobactersp.[27]

Reference: [18] Saberi (1987): lake water and particularly in the estuary sediments; [22] Asgarani et al. (2006): lake water; [23] Bahari et al. (2009): salt crystals; [33] Rezazadeh-Bari (1992): coastal sediments; [28] Ryahi et al. (1994): lake water; [32] Shoa-Hasani et al. (1996): lake water; [39] Arash-Rad (2000): in fresh biomass of Artemia urmiana samples from Urmia Lake; [42] Yousefbeygi and Rahimlou (2001): in fresh biomass of Artemia urmiana samples from Urmia Lake; [31] Mohebbi et al. (2006): lake water; [37] Rohban et al, (2007): lake water; [34] Amoozegar and Zahraei, (2007): lake water; [41] Yousefi et al, (2007): coastal salty soils; [40] Yousefi et al, (2007): lake water; [38] Rafiee et al, (2007): soil specimens of lake; [35] Sadramehr et al, (2008): lake water; [26] Taran (2011): lake water; [29] Asadi (2011): lake water; [30] Asadi et al. (2011): lake water; [36] Zununi-Vahe et al. (2011): water and soil specimens of lake; [27] Mehrshad et al. (2012): water, sediments, salt crystals and residue of plants in in the western coastal line of lake; * Synonymous with Streptococcus faecalis.

3. Microfungi

Fungi are a large group of eukaryotic organisms with worldwide distribution, inhabiting a diverse range of extreme habitats from deserts to hypersaline environments [43]. Investigations of the distribution of fungi in extremely hypersaline environments are rare. Numerous fungi have been identified from Artemia cysts and hypersaline water. Fungal contamination of Artemia cysts is possibly one of the important reasons for their reduced hatchability, and therefore one of the main problems in cyst processing and culture [44]. Twelve fungi have been reported in some halophytes and glycophytes of islands and also from the western shores of Urmia Lake [45]. A list of fungi species from Urmia Lake is presented in Table 2.

Table Table 2. List of Microfungi from Urmia Lake.

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Table 2. List of Microfungi from Urmia Lake.
DivisionClassOrderFamilyGenusSpeciesReference
AscomycotaAscomycetesIncertae sedisIncertae sedisEpicoccumsp.[44]
DothideomycetesPleosporalesPleosporaceaeAlternariasp.[44]
EurotiomycetesEurotialesTrichocomaceaeAspergillusA. flavus[44]
A. fumigatus[44]
A. niger[44]
PenicilliumP. chrysogenum[46]
P. polonicum[46]
sp.[44]
SordariomycetesHypocrealesNectriaceaeFusariumF. incarnatum[44]
sp.[44]
MicroascalesMicroascaceaeScopulariopsissp.[44]
GlomeromycotaGlomeromycetesDiversisporalesAcaulosporaceaeAcaulosporasp.[45]
GlomeralesGlomeraceaeGlomusG. aggregatum[45]
G. clarum[45]
G. clavisporum[45]
G. constrictum[45]
G. coremioides[45]
G. etunicatum[45]
G. fasciculatum[45]
G. fecundisporum[45]
G. geosporum[45]
G. microaggregatum[45]
G. mosseae[45]
G. verruculosum[45]
ZygomycotaZygomycetesMucoralesMucoraceaeAbsidiasp.[44]
Rhizopussp.[44]

Reference: [44] Ownagh et al. (2008): freshly harvested cysts of Artemia urmiana; [45] Khara (2004): arbuscular mycorrhiza in some halophytes and glycophytes of islands and the western coasts of the Urmia Lake; [46] Niknejad et al. (2013): water of Urmia Lake.

4. Phytoplankton

The algal flora of Urmia Lake was studied by Plattner in 1960 [47], who reported Enteromorpha intestinalis as a macroscopic alga [18,20]. E. intestinalis produces considerable amounts of β-carotene, a red-coloured carotenoid with antioxidant properties [20]. Urmia Lake contains a diverse assemblage of phytoplankton species, with Dunaliella as the major species (more than 95% of the total phytoplankton in number) and an important fraction of diatoms such as Navicula and Nitzschia [31]. Dunaliella is a green halophilic alga which bears two flagellates and produces high amounts of β-carotene. This phytoplankton is the major food source for Artemia in the Urmia Lake. It seems that phytoplankton populations in the lake benefit from the increased salinity that has reduced the number of other species and favoured the dominance of Dunaliella. Usually, in the early spring, especially in Golmankhane Port, a bloom of Dunaliella occurs near the shore line which changes the water colour to yellow (see [48]). A current list of phytoplankton composition in Urmia Lake is given in Table 3.

Table Table 3. List of phytoplankton species from Urmia Lake.

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Table 3. List of phytoplankton species from Urmia Lake.
PhylumClassOrderFamilyGenusSpeciesReference
HeterokontophytaBacillariophyceaeBacillarialesBacillariaceaeNitzschiasp.[28,31]
CymbellalesCymbellaceaeCymbellasp.[31,32]
NaviculalesNaviculaceaeAmphiprorasp.[28,31]
Naviculasp.[28,29,31]
PleurosigmataceaeGyrosigmasp.[31]
PinnulariaceaePinnulariasp.[31]
SurirellalesSurirellaceaeCymatopleurasp.[31]
Surirellasp.[31]
ThalassiophysalesCatenulaceaeAmphorasp.[28]
CoscinodiscophyceaeThalassiosiralesStephanodiscaceaeCyclotellasp.[31,32]
FragilariophyceaeFragilarialesFragilariaceaeDiatomasp.[31]
Synedrasp.[31]
ChlorophytaChlorophyceaeSphaeroplealesSelenastraceaeAnkistrodesmussp.[28,31]
VolvocalesDunaliellaceaeDunaliellasp.[28,31,32]
VolvocaceaePandorinasp.[28]
UlvophyceaeUlotrichalesMonostromataceaeMonostromasp.[28]
UlvalesUlvaceaeEnteromorphaE. intestinalis[47]

Reference: [28] Ryahi et al. (1994); [32] Shoa-Hasani et al. (1996); [31] Mohebbi et al. (2006); [47] Plattner (1960).

5. Land Plants

Because of the diversity of soils and topography, Urmia Lake islands possess a diverse flora. Table 4 shows the checklist of plants in the Urmia Lake National Park. The halophilous vegetation around Urmia Lake displays an interesting gradient of salinity-tolerance, ranging from annual obligatory hygro-halophytic communities on lake marshes dominated by Salicornia spp. up to hydrophytic communities dominated by Alisma plantago-aquatica. The latter species grows on the margins of salty and brackish water marshes where the fresh groundwater dilutes the salt contents of the soil [49,50]. The constant occurrence of plant communities in this habitat may suggest that salt-water inundation plays the main role in plant distribution. Inundation seems to act mainly through increasing soil moisture and affecting soluble salt contents to levels suitable for life.

Several cryptic species in the area still need to be identified. This is the case for a rare liverwort Riella aff. cossoniana, whose spores have only recently been discovered in ancient and recent sediments of the lake [50].

Table Table 4. List of plants on islands and in salt marshes of Urmia Lake.

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Table 4. List of plants on islands and in salt marshes of Urmia Lake.
OrderFamilyGenusSpeciesReference
AlismatalesAlismataceaeAlismaA. plantago-aquatica[49]
AraceaeArumsp.[51]
ButomaceaeButomusB. umbellatus[49]
ApialesApiaceaeAlococarpumA. erianthum[51,52]
BupleurumB. falcatum[51,52]
B. gerardii[51,52]
EryngiumE. billardieri[51,52]
MalabailaM. secacul[51,52]
PimpinellaP. tragium[51,52]
ScandixS. stellata[51,52]
TorilisT. leptophylla[51,52]
ZosimaZ. absinthifolia[51,52]
AsparagalesAmaryllidaceaeAlliumA. akaka[51,52]
sp.[51]
AsparagaceaeBellevaliasp.[51,52]
LeopoldiaL. caucasica1[51,52]
IridaceaeCrocussp.[51,52]
IrisI. barnumae[51,52]
I. spuria[49]
sp.[51]
IxioliriaceaeIxiolirionI. tataricum[52]
OrchidaceaeDactylorhizaD. umbrosa[49]
XanthorrhoeaceaeEremurusE. spectabilis[51,52]
AsteralesAsteraceaeAmberboaA. nana[51,52]
ArtemisiaA. fragrans[45,49,53]
A. haussknechtii[51,52]
sp.[51]
AsterA. tripolium[49]
CentaureaC. aucheri[51,52]
C. ustulata[51,52]
C. virgata[51,52]
CirsiumC. alatum[49]
Cousiniasp.[51,52]
Crepissp.[51,52]
CrupinaC. vulgaris[51,52]
EchinopsE. orientalis[45]
sp.[51,52]
GarhadiolusG. angulosus[52]
HelichrysumH. rubicundum[51,52]
InulaI. aucheriana[49]
KoelpiniaK. linearis[49]
AsteralesAsteraceaeLactucaL. serriola[53]
L. undulata[51,52]
PicrisP. kotschyi[51,52]
SaussureaS. salsa[49]
ScorzoneraS. laciniata[49]
SenecioS. vernalis[45]
sp.[51,52]
SteptorhamphusS. tuberosus[52]
Taraxacumsp.[49]
TragopogonT. graminifolius[49]
T. marginatus[51,52]
XeranthemumX. squarrosum[51,52]
BoraginalesBoraginaceaeAnchusaA. arvensis[51,52]
BuglossoidesB. arvensis[52]
HeliotropiumH. samoliflorum[49,51,52]
HeterocaryumH. laevigatum[52]
MoltkiaM. longiflora[51,52]
NonneaN. caspica[51,52]
BrassicalesBrassicaceaeAethionemaA. carneum[51,52]
AlyssumA. linifolium[45]
A. murale[51,52]
A. szovitsianum[51,52]
sp.[51,52]
DescurainiaD. sophia[45]
ErysimumE. sisymbrioides[49]
HutchinsiaH. procumbens[53]
IsatisI. buschiana[51,52]
LepidiumL. aucheri[49]
L. cartilagineum[49,53]
Malcolmiasp.[51,52]
NesliaN. apiculata[51,52]
CapparaceaeCapparisC. spinosa[51,52]
CleomaceaeCleomeC. iberica[51,52]
CaryophyllalesAmaranthaceaeAtriplexA. aucheri[51,52]
A. hastata[49]
A. patula[51,52]
A. tatarica[49]
A.verrucifera[45,49,53]
sp.[51,52]
CamphorosmaC. monspeliaca[49,53]
ChenopodiumC. murale[51,52]
sp.[51]
ClimacopteraC. crassa[49]
CaryophyllalesAmaranthaceaeHalanthiumH. rarifolium[49,52,53]
HalocnemumH. strobilaceum[49,52,53]
HalopeplisH. pygmaea[49]
HalostachysH. caspica[49,51,52]
KalidiumK. caspicum[49]
NoaeaN. mucronata[51,52]
PetrosimoniaP. brachiata[49,53]
P. glauca[49]
SalicorniaS. maritime2[45,49,51,52,53]
SalsolaS. crassa[51,52,53]
S. dendroides[51,52]
S. kali[45]
S. laricina[51,52]
S. soda[49,53]
S. verrucosa[51,52]
SuaedaS. acuminata[52]
S. altissima[45,49,53]
S. crassifolia[53]
S. maritima[49,53]
S. microphylla[49,51,52]
sp.[51]
CaryophyllaceaeAcanthophyllumA. mucronatum[51,52]
CerastiumC. inflatum[51,52]
DianthusD. orientalis[51,52]
sp.[51,52]
Gypsophilasp.[51]
MinuartiaM. hamata[51,52]
ParonychiaP. kurdica[51,52]
SaponariaS. viscosa[51,52]
SileneS. conoidea[45,51,52]
S. marshallii[51,52]
S. spergulifolia[51,52]
sp.[51,52]
SpergulariaS. marina[49,53]
S. salina3[49,53]
VeleziaV. rigida[51,52]
FrankeniaceaeFrankeniaF. hirsuta[49,51,52,53]
F. pulverulenta[49,51,52,53]
PlumbaginaceaeAcantholimonsp.[51,52]
LimoniumL. bellidifolium[49]
L. carnosum[49]
L. caspium[51,52]
L. gmelinii[49]
L. meyeri[49,52,53]
PsylliostachysP. leptostachya[49,53]
CaryophyllalesPlumbaginaceaePsylliostachysP. spicata[49]
PolygonaceaeAtraphaxisA. spinosa[51,52]
PolygonumP. aviculare[51,52]
RumexR. conglomeratus[45,49]
R. crispus[49,51,52]
R. tuberosus[51,52]
TamaricaceaeReaumuriaR. cistoides[52]
TamarixT. kotschyi[49]
T. octandra[49]
T. octandra[49]
T. ramosissima[49,51,52]
DipsacalesDipsacaceaeDipsacussp.[45]
PterocephalusP. canus[52]
ScabiosaS. rotata[52]
sp.[52]
ValerianaceaeValerianellaV. amblyotis[52]
V. coronata[52]
V. oxyrrhyncha[52]
V. vesicaria[52]
EphedralesEphedraceaeEphedraE. procera[51,52]
EricalesPrimulaceaeAndrosaceA. maxima[52]
FabalesFabaceaeAlhagiA. pseudalhagi[49,53]
sp.[51]
AstragalusA. eriocarpus[51,52]
A. oxyglottis[51,52]
sp.[45,51,52]
Glycyrrhizasp.[51]
LotusL. tenuis[49]
MedicagoM. radiata[51,52]
M. rigidula[51,52]
M. sativa[51,52]
TrifoliumT. arvense[51,52]
T. fragiferum[49]
TrigonellaT. asteroides[51,52]
T. filipes[51,52]
T. monantha[51,52]
T. spruneriana[51,52]
ViciaV. michauxii[51,52]
GentianalesRubiaceaeCallipeltisC. cucullaris[51,52]
CrucianellaC. gilanica[51,52]
C. latifolia[51,52]
GaliumG. aparine[51,52]
G. verticillatum[51,52]
GentianalesRubiaceaeRubiasp.[51,52]
GeranialesGeraniaceaeErodiumE. ciconium[52]
E. cicutarium[51,52]
E. oxyrrhynchum[51,52]
GeraniumG. rotundifolium[51,52]
LamialesLamiaceaeEremostachysE. moluccelloides[52]
HymenocraterH. bituminosus[52]
LamiumL. amplexicaule[52]
MenthaM. longifolia[49]
SalviaS. ceratophylla[51,52]
S. hydrangea[51,52]
S. multicaulis[51,52]
S. reuteriana[51,52]
sp.[51,52]
ScutellariaS. theobromina[51,52]
SideritisS. montana[51,52]
TeucriumT. polium[51,52]
ThymusT. fedtschenkoi[51,52]
ZiziphoraZ. capitata[51,52]
Z. tenuior[51,52]
OrobanchaceaeOrobanchesp.[52]
PlantaginaceaeLinariaL. micrantha[51,52]
L. simplex[51,52]
PlantagoP. major[49]
P. maritima[49,53]
VeronicaV. anagallis-aquatica[49]
V. beccabunga[49]
ScrophulariaceaeScrophulariaS. variegata[51,52]
VerbascumV. nudicaule[52]
V. songaricum[51,52]
V. thapsus[51,52]
LilialesLiliaceaeGageaG. reticulata[52]
TulipaT. montana[51,52]
MalpighialesEuphorbiaceaeEuphorbiaE. heteradenia[51,52]
E. myrsinites[51,52]
E. phymatosperma[51,52]
E. szovitsii[52]
HypericaceaeHypericumH. hyssopifolium[52]
H. scabrum[52]
PhyllanthaceaeAndrachneA. aspera[52]
ViolaceaeViolaV. rupestris[51,52]
MalvalesCistaceaeHelianthemumH. ledifolium[51,52]
ThymelaeaceaeDaphneD. mucronata[52]
MalvalesThymelaeaceaeDiarthronD. vesiculosum[52]
MyrtalesOnagraceaeChamerionC. angustifolium[49]
PinalesCupressaceaeJuniperusJ. excelsa[51,52]
PoalesCyperaceaeBolboschoenusB. maritimus[49]
CarexC. distans[49]
C. divisa[49]
sp.[51,52]
CyperusC. fuscus[49]
C. laevigatus[49]
EleocharisE. palustris[49]
JuncaceaeJuncusJ. acutus[49]
J. gerardii[49]
J. heldreichianus[49]
J. inflexus[49]
J. maritimus[49]
PoaceaeAegilopsA. columnaris[51]
A. triuncialis[51,52]
AeluropusA. littoralis[45,49,52,53]
AgropyrumA. elongatum[49]
AgrostisA. stolonifera[49]
AlopecurusA. arundinaceus[49]
ArrhenatherumA. kotschyi[52]
AvenaA. fatua[51,52]
sp.[51]
BeckmanniaB. eruciformis[49]
BromusB. danthoniae[51,52]
B. scoparius[45]
B. tectorum[52]
CatabrosaC. aquatica[49]
CrypsisC. schoenoides[49]
C. vaginiflora[49]
CynodonC. dactylon[49]
EremopyrumE. triticeum[49]
F. arundinacea[49]
Festucasp.[51]
GaudinopsisG. macra[52]
HordeumH. geniculatum[49]
H. leporinum[52]
H. spontaneum[52]
sp.[51]
MelicaM. jacquemontii[52]
NardurusN. subulatus[52]
ParapholisP. incurva[49]
Phleumsp.[51]
PhragmitesP. australis[45,49,51,52]
PoaP. bulbosa[51,52]
P. persica4[52]
PoalesPoaceaePolypogonP. trivialis[49]
P. monspeliensis[49]
P. semiverticillata[49]
PuccinelliaP. bulbosa[49,53]
P. distans[49]
SclerochloaS. dura[49]
StipaS. barbata[45,51,52]
TaeniatherumT. crinitum[52]
ZingeriaZ. trichopoda[49]
RanunculalesBerberidaceaeBerberisB. integerrima[51,52]
LeonticeL. leontopetalum[52]
PapaveraceaeFumariaF. parviflora[51]
F. vaillantii[51,52]
Glaucium5sp.[51]
PapaverP. argemone[51,52]
P. glaucium[52]
sp.[51,52]
RanunculaceaeAdonisA. aestivalis[51,52]
BatrachiumB. trichophyllum[49]
Consolidasp.[51]
DelphiniumD. quercetorum[51,52]
Ranunculussp.[51,52]
ThalictrumT. isopyroides[51,52]
T. sultanabadense[51,52]
RosalesCannabaceaeCeltisC. glabrata[51,52]
MoraceaeFicusF. carica[51]
RhamnaceaeRhamnusR. pallasii[51]
RosaceaeAmygdalusA. trichamygdalus[51,52]
CerasusC. microcarpa[51,52]
Cotoneastersp.[51,52]
PotentillaP. recta[49]
Prunussp.[51]
UrticaceaeParietariaP. judaica[51,52]
SapindalesAnacardiaceaePistaciaP. atlantica[51,52]
NitrariaceaeNitrariaN. sibirica[51,52]
PeganumP. harmala[51,52]
TetradiclisT. tenella[52]
RutaceaeHaplophyllumH. perforatum[52]
SapindaceaeAcerA. monspessulanum[51,52]
SaxifragalesCrassulaceaeRosulariaR. persica[52]
SedumS. hispanicum[52]
SphaerocarpalesRiellaceaeRiellaaff. Cossoniana 6[50]
SolanalesConvolvulaceaeConvolvulusC. lineatus[51,53]
CressaC. cretica[49]
SolanalesConvolvulaceaeCuscutasp.[51]
SolanaceaeHyoscyamusH. pusillus[51,52]
LyciumL. ruthenicum[49,51,52]
Solanumsp.[51]
ZygophyllalesZygophyllaceaeZygophyllumZ. fabago[51,52]

Reference: [45] Khara (2004); [49] Asri and Ghorbanli (1997); [50] Djamali et al. (2008); [52] Zehzad (1989); [53] Asri (1993); [51] Nasiri et al. (1996); 1 synonym with Muscari caucasicum; 2 synonym with Salicornia herbacea and Salicornia herbacea; 3 synonym with Spergularia media; 4 synonym with Eremopoa persica; 5 synonym with Glacium; 6 see text.

6. Brine Shrimp Artemia

The brine shrimp Artemia (Crustacea: Anostraca) is a small crustacean adapted to hypersaline habitats, of Urmia Lake. It was first reported from the lake in 982, more than one thousand years ago [54]. In Curzon’s published work “Persia and the Persian Question” (1892, Volume i, p. 533), he described Artemia as a species of small “Jelly-Fish” [55,56]. In the first reports of A. Günther and R.T Günther, it was interpreted as a “Medusa”, “a species of Branchipus” [57] and “the Artemia group of varieties of the Branchipus type” [58]. Finally, Günther pointed out that this bisexual species belongs to the genus Artemia [59] (p. 509), and the species was nomenclatured as Artemia urmiana [60] (p. 395).

Barigozzi et al. (1987) [61] reported the existence of only parthenogenetic populations of Artemia based on a single sample from Urmia Lake. However, another study of Artemia cysts (which are encysted gastrula embryos) collected from the western shore-line of Urmia Lake in 1987 revealed that Urmia Lake has both bisexual and parthenogenetic populations in the surrounding lagoons, especially on the western shore of the lake [62]. Sediment cores suggest that parthenogenetic populations of Artemia have lived in Urmia Lake for at least 5000 years [11]; however, the oldest remains of Artemia that have been recovered from a sediment core from this lake are 200,000 years old [63]. The two parthenogenetic Artemia populations from the Urmia Lake basin (those in the coastal lagoons and interior of the lake) have been tentatively attributed to two morphotypes that are not yet completely separated [64]. Several studies have shown that biometrical, morphometrical and genetic variations exist in A. urmiana [65,66,67]. The results indicate that ecological speciation is an ongoing process in Urmia Lake [67].

7. Brine Fly Ephydra

The brine fly Ephydra urmiana (Diptera: Ephydridae) has been described by R.T. Günther near the margin of the Urmia Lake (the mouth of the Nazlu Chai (Nazlu River) at Superghan [Suporqun]) [68] (p. 415). Breeding and feeding of E. urmiana totally depends on the lake. Eggs of the genus Ephydra are attached to an algae mat [69]. The main food sources of adults and larvae are algae, some bacteria, and protozoa [70,71,72]. Nemenz [73] had observed adults of Ephydra cinerea feeding on masses of algae washed ashore at the Great Salt Lake in Utah, USA.

8. Land and Freshwater Molluscs

The biodiversity of molluscs is documented in Table 5.

Table Table 5. List of land and freshwater molluscs from the Island of Koyun Daghi (Kaboudan).

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Table 5. List of land and freshwater molluscs from the Island of Koyun Daghi (Kaboudan).
PhylumClassOrderFamilyGenusSpeciesReference
MolluscaGastropodaStylommatophoraChondrinidaeChondrinaP. granum1[74]
EnidaeGeminulaG. isseliana2[74]
G. continens3[74]
HygromiidaeHelicellaH. acutistria[74]
PupillidaeGibbulinopsisG. signata4[74]

1 synonymous with Pupa granum; 2 synonymous with Buliminus (Chondrulus) didymodus; 3 synonymous with Buliminus (Amphiscopus) continens; 4 synonymous with Pupa signata.

9. Birds

The islands, beaches, and lagoons of Urmia Lake are excellent habitats for resident breeding species and winter visitors. Several species which love saline lakes with a rich food source, such as flamingos, terns, gulls and waders, are typical residents or migrants to Urmia Lake. Table 6 lists the birds of Urmia Lake National Park basin and surrounding regions, a list which is apparently incomplete, especially for migrant species.

Table Table 6. List of birds from Urmia Lake National Park basin and surrounding regions. (B = breeder, SM = summer migrant, WM = winter migrant, PM = passage migrant).

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Table 6. List of birds from Urmia Lake National Park basin and surrounding regions. (B = breeder, SM = summer migrant, WM = winter migrant, PM = passage migrant).
OrderFamilyGenusSpeciesStatusReference
AccipitriformesAccipitridaeAccipiterA. nisusWM[75]
AegypiusA. monachusB[75]
AquilaA. chrysaetosB[51,75]
A. clangaPM[76]
ButeoB. buteoPM[76]
B. rufinusB[75]
CircaetusC. gallicusB[76]
CircusC. aeruginosusB, PM[69]
C. cyaneusPM, WM[76]
C. macrourusPM[76]
C. pygargusB[76]
GypaetusG. barbatusB[76]
GypsG. fulvusB[51,75]
HaliaetusH. albicillaWM[75]
NeophronN. percnopterusB, PM[51,75,76]
MilvusM. migransB, PM[76]
AnseriformesAnatidaeAnasA. acutaWM, SM[51,75,76]
A. clypeataWM, B, PM[51,75,76]
A. creccaB, PM[76]
A. platyrhynchosB, WM[51,75]
AnseriformesAnatidaeAnasA. penelopeWM, PM[76]
A. querquedulaB, PM[76]
A. streperaWM, PM[76]
AnserA. erythropusWM[76]
A. albifronsWM[76]
A. anserB, WM[51,75,76]
AythyaA. ferinaPM[76]
A. nyrocaB[76]
A. fuligulaPM, WM[76]
BucephalaB. clangulaPM[76]
CygnusC. bewickiiWM[76]
C. cygnusWM[51,75]
C. olorWM[76]
MarmaronettaM. angustirostrisB, WM[76]
MergusM. albellusWM[76]
M. merganserWM[76]
OxyuraO. leucocephalaB[51,75]
TadornaT. ferrugineaB, PM[51,75,76]
T. tadornaB, PM[51,75,76]
ApodiformesApodidaeApusA. apusB, PM[76]
A. melbaB, PM[76]
BucerotiformesUpupidaeUpupaU. epopsB, PM[76]
CaprimulgiformesCaprimulgidaeCaprimulgusC.europaeusB[76]
CharadriiformesBurhinidaeBurhinusB. oedicnemusB[51,75]
CharadriidaeCharadriusC. asiaticusPM[76]
C. alexandrinusB, PM[76]
C. dubiusB, PM[76]
C. hiaticulaPM[76]
C. leschenaultiiB[76]
C. morinellusPM[76]
PluvialisP. squatarolaPM[76]
VanellusV. indicusPM[76]
V. spinosusB[76]
V. vanellusB, WM[51,75,76]
GlareolidaeGlareolaG. pratincolaB[75]
HaematopodidaeHaematopusH. ostralegusB[76]
LaridaeChroicocephalusC. geneiB, PM[76]
C. ridibundusB, PM[75,76]
HydrocoloeusH. minutusWM[76]
LarusL. cachinnansWM[76]
L. ichthyaetusWM[76]
L. armenicusB[75]
L. canusWM[75]
RecurvirostridaeHimantopusH. himantopusB, PM[51,75,76]
CharadriiformesRecurvirostridaeRecurvirostraR. avosettaB, PM[76]
ScolopacidaeArenariaA. interpresPM[76]
CalidrisC. alpinaPM, WM[76]
C. minutaPM[76]
C. temminckiiPM[76]
C. ferrugineaPM[76]
ActitisA. hypoleucosB, PM[75,76]
GallinagoG. gallinagoWM, PM[75,76]
LimosaL. limosaWM, PM[76]
LymnocryptesL. minimusPM[76]
NumeniusN. arquataPM, WM[76]
N. phaeopusPM[76]
PhalaropusP. lobatusPM[76]
PhilomachusP. pugnaxPM[76]
TringaT. erythropusWM, PM[76]
T. glareolaPM[76]
T. ochropusPM[76]
T. nebulariaPM[76]
T. stagnatilisPM[76]
T. totanusB, PM[76]
XenusX. cinereusPM[76]
StercorariidaeStercorariusS. pomarinusPM[76]
SternidaeChlidoniasC. nigerPM[76]
C. hybridusB, PM[76]
C. leucopterusPM[51,75]
GelochelidonG. niloticaB, PM[76]
SternulaS. albifronsB[76]
SternaS. hirundoB, PM[76]
HydroprogneH. caspiaB, PM[76]
CiconiiformesCiconiidaeCiconiaC. ciconiaB, SM[51,75]
C. nigraPM[76]
ColumbiformesColumbidaeColumbaC. liviaB[51,75]
C. oenasB[75]
C. palumbusB, WM[51,76]
StreptopeliaS. decaoctoPM[76]
S. turturB, PM[76]
CoraciiformesCerylidaeCeryleC. rudisPM[76]
CoraciidaeCoraciasC. garrulusB, PM[76]
MeropidaeMeropsM. apiasterB, PM[76]
M. persicusB[76]
FalconiformesFalconidaeFalcoF. biarmicusB[75]
F. cherrugB, WM[75,76]
F. columbariusPM[75,76]
F. peregrinusB, PM[76]
FalconiformesFalconidaeFalcoF. naumanniB[77]
F. subbuteoB, PM[75,76]
F. tinnunculusB, WM[51,75,76]
GalliformesPhasianidaeAlectorisA. chukarB[51,75]
CoturnixC. coturnixB, PM[51,75]
PerdixP. perdixB[76]
TetraogallusT. caspiusB[76]
GruiformesGruidaeGrusG. grusPM[75]
RallidaeFulicaF. atraB[51,75]
GallinulaG. chloropusB, WM[51,75,76]
RallusR. aquaticusPM[76]
OtidiformesOtididaeOtisO. tardaB, WM, PM[76]
PasseriformesAcrocephalidaeAcrocephalusA. arundinaceusB[76]
A. dumetorumPM[76]
A. schoenobaenusPM[76]
A. scirpaceusB, PM[76]
A. melanopogonB[76]
AlaudidaeCalandrellaC. brachydactylaB[76]
C. rufescensB, WM, PM[76]
EremophilaE. alpestrisWM[76]
GaleridaG. cristataB[75]
MelanocoryphaM. calandraB, PM[76]
M. bimaculataB, PM[75,76]
CettiidaeCettiaC. cettiB[76]
CinclidaeCinclusC. cinclusB[76]
CorvidaeCorvusC. coraxB[51,75]
C. frugilegusB, WM[76]
C. cornixB[76]
C. monedulaB, WM[76]
GarrulusG. glandariusB[75]
PicaP. picaB[51,75]
PyrrhocoraxP. graculusB[75]
P. pyrrhocoraxB[51,75,76]
EmberizidaeEmberizaE. cineraceaPM[76]
E. citrinellaWM[76]
E. calandraB, WM[75,76]
E. melanocephalaB[76]
E. schoeniclusB, PM, WM[76]
FringillidaeCarduelisC. cannabinaPM, WM[76]
C. carduelisB, WM[76]
C. flavirostrisWM[76]
C. spinusWM[76]
FringillaF. coelebsB, PM[76]
PasseriformesFringillidaeRhodopechysR. sanguineaB, WP[75,76]
HirundinidaeDelichonD. urbicumB[76]
HirundoH. rusticaB[76]
RipariaR. ripariaB, PM[76]
LaniidaeLaniusL. collurioB, PM[76]
L. minorB[76]
L. senatorPM, WM[76]
MotacillidaeAnthusA. campestrisB, PM[76]
A. cervinusPM[76]
A. pratensisWM[76]
A. spinolettaB, PM, WM[76]
A. trivialisPM[76]
MotacillaM. albaB, WM[75]
M. citreolaPM[51]
M. flavaB, PM[51,75,76]
MuscicapidaeCercotrichasC. galactotesB, PM[76]
LusciniaL. svecicaPM[76]
OenantheO. desertiB, PM[76]
O. hispanicaB[76]
O. finschiiB, PM[76]
O. isabellinaB, PM[76]
O. oenantheB, PM[76]
ErithacusE. rubeculaWM[75]
LusciniaL. megarhynchosB[76]
PhoenicurusP. ochrurosB[76]
SaxicolaS. rubicolaB, PM[76]
MonticolaM. saxatilisB[77]
TurdusT. pilarisWM[76]
T. viscivorusWM[76]
OriolidaeOriolusO. oriolusB, PM[76]
ParidaeCyanistesC. caeruleusB, WM[76]
ParusP. majorB[76]
PasseridaeCarpospizaC. brachydactylaB[76]
PasserP. montanusB[76]
P. domesticusB[51,75]
PetroniaP. petroniaB[76]
PhylloscopidaePhylloscopusP. collybitaPM[76]
P. trochiloidesPM[76]
RemizidaeRemizR. pendulinusB[76]
SittidaeSittaS. tephronotaB[76]
SturnidaePastorP. roseusB, PM[76]
SturnusS. vulgarisB[51,75]
SylviaS. communisB, PM[76]
PasseriformesSturnidaeSylviaS. mystaceaB, PM[76]
S. nisoriaPM[76]
S. currucaPM[77]
TichodromadidaeTichodromaT. murariaB[76]
TroglodytidaeTroglodytesT. troglodytesWM[76]
PelecaniformesArdeidaeArdeaA. albaWM[76]
A. cinereaB, WM, PM[51,75,76]
A. purpureaB, PM[76]
ArdeolaA. ralloidesB, PM[76]
BotaurusB. stellarisPM[51,75]
EgrettaE. garzettaB, WM, PM[51,75,76]
IxobrychusI. minutusB[76]
NycticoraxN. nycticoraxB[76]
PelecanidaePelecanusP. onocrotalusB[76]
ThreskiornithidaePlataleaP. leucorodiaPM[76]
PlegadisP. falcinellusB, PM[76]
PhoenicopteriformesPhoenicopteridaePhoenicopterusP. ruberB, WM[51,75,76]
PiciformesPicidaeDendrocoposD. syriacusB[51,75]
PodicipediformesPodicipedidaePodicepsP. nigricollisB, WM, PM[76]
P. cristatusB, WP, WM[75,76]
TachybaptusT. ruficollisB, WP[51,75]
PteroclidiformesPteroclidaePteroclesP. orientalisB[76]
StrigiformesStrigidaeAtheneA. noctuaB[51,75]
BuboB. buboB[51,75]
StrixS. alucoB[51,75]
SuliformesPhalacrocoracidaePhalacrocoraxP. carboWM[76]
P. pygmeusWM[76]

Reference: [51] Nasiri et al. (1996); [75] Alipour (2009); [76] Aliabadian (2013) (personal communication); Taxonomical status has been checked with Wink (2013) [77].

10. Amphibians and Reptiles

The Urmia Lake area harbours several amphibian and reptile species (Table 7). Amphibian and reptile communities might be faced with a possible threat of extinction due to unsuitable ecological conditions in Urmia Lake. Special care should be taken to maintain these species in the lake.

Table Table 7. List of amphibia and reptiles from Urmia Lake.

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Table 7. List of amphibia and reptiles from Urmia Lake.
ClassOrderFamilyGenusSpeciesLocalityRef.
AmphibiaAnuraBufonidaePseudepidaleaP. viridis1some islands of Urmia Lake and the shores of Urmia Lake[51,75]
HylidaeHylaH. savignyithe shores of Urmia Lake[75]
RanidaeRanaR. ridibundathe shores of Urmia Lake[75]
CaudataSalamandridaeNeurergusN. crocatus2west mountains of Urmia Lake[78,79,80]
ReptiliaSquamataAgamidaeParalaudakiaP. Caucasia3some islands of Urmia Lake[75]
TrapelusT. lessonaehas been collected around the lake in 2012[81]
ColubridaeColuberC. Schmidti4some islands of Urmia Lake and the shores of Urmia Lake[51,75]
platycepsP. najadum5the shores of Urmia Lake[75]
EirenisE. punctatolineatusthe shores of Urmia Lake[75]
HemorrhoisH. ravergieri6the shores of Urmia Lake[75]
TelescopusT. fallaxthe shores of Urmia Lake[75]
GeckonidaeCyrtopodionC. scabrumhas been collected around the lake in 2012[81]
LacertidaeApathyaA. cappadocica7some islands of Urmia Lake[75]
LacertidaeEremiasE. argutathe shores of Urmia Lake[75]
OphisopsO. elegansIslands of Aruz and Shazalan (shah-saran)[82]
ScincidaeAblepharusA. bivittatusthe shores of Urmia Lake[75]
EumecesE. schneideriIsland of Koyun Daghi (Kaboudan) and Shazalan (shah-saran)[82]
TrachylepisT. aurata8Island of Koyun Daghi (Kaboudan)[82]
ViperidaeMacroviperaM. lebetina9some islands of Urmia Lake and the shores of Urmia Lake[51,75]
TestudinesTestudinidaeTestudoT. ibera10Island of Koyun Daghi (Kaboudan)[83]

Reference: [51] Nasiri et al. (1996); [75] Alipour (2009); [78] Cope (1862); [79] Stöhr et al. (2013); [80] Najafi-Majd and Kaya (2013); [81] Boulenger (1899); [82] Günther (1899); [83] Rastegar-Pouyani (2013) (personal communication); 1 synonymous with Bufo viridis; 2 Urmia Lake newt; 3 synonymous with Laudakia caucasia; 4 synonymous with Coluber jugularis; 5 synonymous with Coluber najadum; 6 synonymous with Coluber ravergieri; 7 subspecies: Apathya Cappadocica urmiana;synonym with Lacerta cappadocica urmiana; 8 subspecies: Treachylepis aurata transcaucasica; synonym with Trachylepis septemtaeniata; 9 subspecies: Macrovipera lebetina optusa; synonym with Vipera xanthina and Vipera lebetina; 10 synonymous with T. graeca, this species has been reported only from fragments of a carapace reported from islands of Urmia Lake [83].

11. Mammals

Some Armenian sheep, Ovis orientalis gmilini, were transferred to Kaboudan Island in 1895 and 1906 by one of the governors of Azerbaijan [84]. In 1970 and 1971, in order to control the population of Armenian sheep, two leopards, Panthera pardus, were introduced on Kaboudan Island; however, their corpses were found in 1982. During 1993, 49, and in 1995, 98 Armenian Sheep were transferred from Kaboudan Island to the Islami Peninsula [51,75,85].

Fifty-two Persian fallow deer, Dama dama mesopotamica, were transferred to Ashk Island between 1977 and 1989. Also in 1989, six of these deer (three males and three females) were introduced to Kaboudan Island in order to study their ecology [51,75,85]. Table 8 lists the Mammals of Urmia Lake National Park.

Table Table 8. List of mammals from Urmia Lake.

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Table 8. List of mammals from Urmia Lake.
OrderFamilyGenusSpeciesLocalityReference
ArtiodactylaBovidaeOvisO. orientalis1Kaboudan Island and Islami Peninsula[51,75,84,85]
CervidaeDamaD. dama2Kaboudan Island and Ashk Island[51,85]
CarnivoraCanidaeCanisC. aureusthe shores of Urmia Lake[75]
C. lupusthe shores of Urmia Lake[75]
VulpesV. vulpesthe shores of Urmia Lake[75]
FelidaePantheraP. pardus 3Kaboudan Island[51,75,85]
MustelidaeMartesM. foinathe shores of Urmia Lake[75]
MustelaM. nivalisthe shores of Urmia Lake[75]
ChiropteraEmballonuridaeTaphozousT. nudiventrissome islands of Urmia Lake and the shores of Urmia Lake[75]
RhinolophidaeRhinolophusR. ferrumequinumsome islands of Urmia Lake and the shores of Urmia Lake[75]
VespertilionidaeMyotisM. blythiisome islands of Urmia Lake and the shores of Urmia Lake[75]
M. mystacinussome islands of Urmia Lake and the shores of Urmia Lake[75]
PipistrellusP. kuhliisome islands of Urmia Lake and the shores of Urmia Lake[75]
P. pipistrellussome islands of Urmia Lake and the shores of Urmia Lake[75]
P. saviisome islands of Urmia Lake andthe shores of Urmia Lake[75]
InsectivoraErinaceidaeErinaceusE. europaeusthe shores of Urmia Lake[75]
SoricidaeCrociduraC. russulathe shores of Urmia Lake[75]
LagomorphaLeporidaeLepusL. capensisthe shores of Urmia Lake[75]
RodentiaCricetidaeArvicolaA. amphibious4the shores of Urmia Lake[75]
CricetulusC. migratoriusthe shores of Urmia Lake[75]
DipodidaeAllactagaA. elaterthe shores of Urmia Lake[75]
MuridaeApodemusA. sylvaticusthe shores of Urmia Lake[51,75]
MerionesM. persicusthe shores of Urmia Lake[75]
MusM. musculussome islands of Urmia Lake and the shores of Urmia Lake[51,75]

Reference: [51] Nasiri et al. (1996); [75] Alipour (2009); [84] Günther (1899); [85] Ziaie (1996); 1 subspecies: Ovis orientalis gmelini; 2 subspecies: Dama dama mesopotamica; 3 They do not presently exist on Kaboudan Island (see text); 4 synonymous with Arvicola terrestris.

12. Hidden Biodiversity

Our knowledge of the biodiversity of a given area or ecosystem is based on the species already discovered and described by biologists. However, the list of plants and animals is subject to change in that new species are discovered in the field, taxonomic revisions based on the application of molecular techniques are carried out, or both.

The case of Riella aff. cossoniana, whose spores have only recently been discovered in ancient and recent sediments of the lake, is worth mentioning [50]. Riella is a liverwort extremely rarely encountered in the field, owing to the very particular ecological conditions needed for the germination of its spores. In Urmia Lake, the spores of this liverwort have been documented in the sediment archives since about 200,000 years ago, and they are also found in recent sediments, showing that the plant is still thriving in brackish water ponds and springs around the lake. However, despite its presence in sediments of salt lakes in many salt and brackish water wetlands, this plant has never been documented in Iran by botanists [50]. Today, Riella is considered an endangered plant in many places in semi-arid regions of the world (e.g., [86]). The above example indicates that the conservation of aquatic ecosystems around the lake is of primordial importance for the conservation of such hidden components of the biodiversity.

13. Urmia Lake Hydrological Variations and their Impact on the Biodiversity

Palaeoecological and geochemical investigations of long sediment cores from Urmia Lake have revealed that lake levels underwent dramatic changes during the glacial-interglacial cycles of the Quaternary period [17,50,87]. Based on the total thickness of the fluvio-lacustrine infill of the Urmia Lake basin, as revealed by geophysical explorations and the dated 100-m long core samples taken from the central basin, the age of the lake can be grossly estimated at >600,000 years. Pollen evidence shows that the aquatic vegetation composition and density has greatly fluctuated in response to these hydrological changes during the last 200,000 years. The most important development of aquatic vegetation took place during glacial, rather than interglacial periods (see Figure 8 in [88] for details). During the Last Glacial (70 ka to 17 ka) and Penultimate Glacial (190 ka to 130 ka), numerous time intervals with extensive development of fresh- to brackish water macrophytic vegetation may be observed. These periods have been interpreted as high lake levels during which the lake chemistry became considerably less saline [50]. Although the glacial periods are known as periods with a significant loss of biodiversity, they were times of a more diversified plant and most probably animal life within the lake and in its associated ecosystems. The presence of several peaks of brackish to fresh water dinoflagellates and Pediastrum (green alga) indicate that the algal life also increased in response to the dilution of lake water [17,50,87,88].

14. Conclusions

The biodiversity of Urmia Lake is impressive, even if the species inventory is far from being complete. More and detailed studies, probably including the use of DNA barcoding, are needed to document the composition of this hypersaline lake, which faces the threat of vanishing. Saline lakes provide a fragile environment which needs careful protection to avoid the extinction of highly adapted species. Palaeoecological evidence clearly shows that dramatic lake level fluctuations have always been part of the lake’s history and have modulated the diversity and dynamics of microbial plant and animal life in the lake. The recent environmental crisis of Urmia Lake is not an excuse to intervene in such a fragile ecosystem. Wiser restoration strategies should be selected in such a way as to minimize the artificial interventions in the lake and associated ecosystems.

Acknowledgments

Our thanks are due to R. Hershler, J. Harasewych, N. Rastegar-Pouyani, E. Rastegar-Pouyani, M.A. Amoozegar, S. Saadat, A. Asgarani, Y. Asri, M. Garshasbi, M. Tafrihi, A Mahmoodi, H. Jabbari, R. Siahsarvie, M. Aliabadian, F. Mohebi, H. Bahadorani, and F. Khatmi for a painstaking job of preparing references and checking species lists. The help of Jim Clegg (University of California, USA) for improving the English is greatly acknowledged.

Conflicts of Interest

The authors declare no conflict of interest. MW is Editor-in-Chief of DIVERSITY.

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