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Open AccessReview

Update of “Biodiversity of the Hypersaline Urmia Lake National Park (NW Iran)”

by Alireza Asem 1,*,†, Amin Eimanifar 2,*,† and Michael Wink 3
1
Institute of Evolution & Marine Biodiversity, Ocean University of China, 5 Yushan Road, Qingdao 266003, China
2
Honey Bee Research and Extension Laboratory (HBREL), Department of Entomology and Nematology, University of Florida, Steinmetz Hall, Natural Area Dr., P.O. Box 110620, Gainesville, FL 32611, USA
3
Institute of Pharmacy and Molecular Biotechnology (IPMB), Heidelberg University, Im Neuenheimer Feld 364, 69120 Heidelberg, Germany
*
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
Academic Editor: Ipek Kurtboke
Diversity 2016, 8(1), 6; https://doi.org/10.3390/d8010006
Received: 9 January 2016 / Revised: 22 February 2016 / Accepted: 1 March 2016 / Published: 8 March 2016

Abstract

Urmia Lake, an endorheic salt lake in northwestern Iran, was registered in the Ramsar Convention on Wetlands as a wetland of international importance, also a UNESCO biosphere reserve. In this review, we have updated our last checklist in 2014 with available information on the biodiversity of the lake.
Keywords: biodiversity; hypersalinity; Urmia Lake; national park biodiversity; hypersalinity; Urmia Lake; national park

1. Background

Lake Urmia (37°42′ N, 45°19′ E) is one of the largest hypersaline lakes in the world and the habitat of a unique bisexual Artemia urmiana and some rare species (Figure 1). Our 2014 article in diversity entitle Biodiversity of the hypersaline Urmia Lake National Park (NW Iran) covered most of the reported species from this national park [1]. This paper updates and extends previous checklist for foraminifers, archaebacteria and bacteria, microfungi, lichen, phytoplankton, nematodes, apicomplexa, flatworms, arthropods, birds, reptiles and several fossils. In the present update, we have included additional new information on the biodiversity of Urmia Lake which were not included in the previous article due to newly published articles and unavailability of old articles in the web. Urmia Lake has been subject to the drastic ecological and hydrological events which caused a rapid decline of population density of some of the valuable organisms such as brine shrimp Artemia. We believe that the current check list would enable us to deeply understand the rich biodiversity of Urmia Lake and subsequently design an integrated environmental guideline to protect living animals against environmental tensions.

2. Fossils from Paleozoic Limestone

Microscopical studies of limestone rocks from the island of Shazalan (Shah-saran) revealed remains of foraminifers, including Endothyra bowmanni (Endothyridae), Valvulina bulloides (Valvulinidae) and Nodosaria radicula (Nodosariidae) [2].

3. Archaebacteria and Bacteria

Urmia Lake harbours a rich collection of archaebacteria and bacteria. They play a major role in the food chain of Urmia Lake ecosystem. Table 1 includes the updated list of archaebacterial and bacterial species in the water, soil and mud of Urmia Lake.

4. Microfungi

Fungi are cosmopolitan eukaryotic organisms which have worldwide distribution, inhabiting diverse extreme ecotypes from deserts to hypersaline environments. The present update lists 20 species of hyphomycetes fungi explored in soils of the National Park of Urmia Lake (Table 2).

5. Lichen

Lichens are composite, symbiotic organisms made up from members of algae or cyanobacteria (or both) living among filaments of a fungus. Caloplaca ferrugineoides is a single lichen identified from Urmia Lake National Park (Table 3).

6. Phytoplankton

The main algal flora of Urmia Lake has been listed in our previse checklist in 2014 [1]. Urmia Lake contains a diverse assemblage of phytoplankton, with Dunaliella as the dominant alga. It is a green halophilic alga which produces high amounts of β-carotene. This phytoplankton is the major food source for Artemia in the Urmia Lake [1]. Recently, four species of Dunaliella have been identified using 18S rDNA gene [9]. A current list of Dunaliella species in Urmia Lake is given in Table 4.

7. Parasites

The knowledge of parasitic infections in wildlife is necessary for management of protected areas and national parks. Table 5 documents the checklist of parasites of pelicans, wild sheep and yellow deer in the Urmia Lake National Park.

8. Insects

A list of uncommon species of insects from surrounding areas of Urmia Lake is presented in Table 6.

9. Crustacea

Temporary aquatic micro-ecosystems i.e. ponds and lagoons, around Urmia Lake provide special habitats for crustaceans. The biodiversity of crustacean is documented in Table 7.

10. Reptiles

The surrounding regions of Urmia Lake harbour several species of reptiles. Their 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 at the lake [1]. Table 8 shows the updated list of reptiles in surrounding regions of Urmia Lake National Park.

11. Mid-winter Birds

Our comprehensive bird checklist of Urmia Lake consists of resident breeding species and winter visitors [1]. Table 9 shows new members of mid-winter birds from the National Park of Urmia Lake

12. Fossils

The first and only scientific study of fossils of Urmia Lake goes back to collected samples by Robert T. Gunther (1869–1940) in the late nineteenth century. The list of fossils species from Urmia Lake is presented in Table 10.
The extended and updated list further highlights the high biodiversity of Urmia Lake and surrounding areas. Unfortunately, the desertification and loss of water in Urmia Lake has continued [32] which will further endanger the unique ecosystem and its biodiversity. Urgent measures are required to stop this development.

Author Contributions

Alireza Asem and Amin Eimanifar conceived the study and equally contributed of the manuscript. Michael Wink reviewed drafts.

Conflicts of Interest

The authors declare no conflict of interest. M.W. is Editor-in-Chief of Diversity.

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Figure 1. Geographical localization of Urmia Lake in the northwestern of Iran.
Figure 1. Geographical localization of Urmia Lake in the northwestern of Iran.
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Table 1. List of archaebacteria and bacteria from the National Park of Urmia Lake.
Table 1. List of archaebacteria and bacteria from the National Park of Urmia Lake.
DomainPhylumClassOrderFamilyGenusSpeciesRef.
ArchaeaEuryarchaeotaHalobacteriaHalobacterialesHalobacteriaceaeHaloterrigenasp. 1[3]
HalosiccatusH. urmianus 2[4]
HalovariusH. luteus 3[5]
BacteriaFirmicutesBacilliBacillalesBacillaceaeOrnithinibacillussp. 4[6]
PlanococcaceaePlanomicrobiumsp. 4[6]
ProteobacteriaGamma proteobacteriaPseudomonadalesMoraxellaceaePsychrobactersp. 4[6]
1 Locality: Shores of Bari, Golmankhaneh Port, Chichest, Rashakan, Kazem Dashi, Gholmankhaneh, Gamichi, Shahi peninsula, Western and Eastern coastlines of Urmia Lake Bridge; Salinity: 24.15%–28.4%; 2 Locality: Has not been reported, Salinity: 32%; 3 Locality: Has not been reported, Salinity: Saturated; 4 Locality: Seven stations in the Eastern shores of Lake (localities had not been clearly explained); Salinity: 23%–32%.
Table 2. List of microfungi harvested from soils of the National Park of Urmia Lake (localities: Kaboudan Island, Espir Island, Golmankhaneh Port, Mahabad Road) [7].
Table 2. List of microfungi harvested from soils of the National Park of Urmia Lake (localities: Kaboudan Island, Espir Island, Golmankhaneh Port, Mahabad Road) [7].
DivisionClassOrderFamilyGenusSpecies
AscomycotaAscomycetesIncertae sedisIncertae sedisSarocladiumS. strictum
DothideomycetesCapnodialesDavidiellaceaeCladosporiumC. cladosporioides
PleosporalesPleosporaceaeAlternariaA. chlamydospora
A. rhizophorae
BipolarisB. prieskaensis
DothideomycetesPleosporalesPleosporaceaeEmbellisiaE. chlamydospora
E. tellustris
UlocladiumU. alternariae
EurotiomycetesEurotialesTrichocomaceaePenicilliumP. expansum
LeotiomycetesHelotialesSclerotiniaceaeBotrytisB. cinerea
SordariomycetesHypocrealesHypocreaceaeAcremoniumA. larvarum
A. potronii
AcrostalagmusA. luteoalbus
TrichodermaT. atroviride
T. harzianum
Incertae sedisTrichotheciumT. roseum
NectriaceaeFusariumF. tricinctum
StachybotryaceaeStachybotrysS. chartarum
Incertae sedisApiosporaceaeArthriniumA. phaeospermum
SordarialesChaetomiaceaeChaetomiumC. truncatulum
Table 3. List of lichen from the National Park of Urmia Lake (localities: Rahmanloo and Saraydeh) [8].
Table 3. List of lichen from the National Park of Urmia Lake (localities: Rahmanloo and Saraydeh) [8].
PhylumClassOrderFamilyGenusSpecies
AscomycotaLecanoromycetesTeloschistalesTeloschistaceaeCaloplacaC. ferrugineoides
Table 4. List of phytoplankton from the National Park of Urmia Lake (localities: Western and Eastern coastlines of Urmia Lake Bridge and Gamichi; Salinity: 32.2%–38%) [9].
Table 4. List of phytoplankton from the National Park of Urmia Lake (localities: Western and Eastern coastlines of Urmia Lake Bridge and Gamichi; Salinity: 32.2%–38%) [9].
PhylumClassOrderFamilyGenusSpecies
ChlorophytaChlorophyceaeVolvocalesDunaliellaceaeDunaliellaD. bardawil
D. parva
D. salina
D. tertiolecta
Table 5. List of reported parasites at pelicans and some mammalians from the National Park of Urmia Lake.
Table 5. List of reported parasites at pelicans and some mammalians from the National Park of Urmia Lake.
PhylumClassOrderFamilyGenusSpeciesHostLocalityRef.
ArthropodaInsectaPhthirapteraMenoponidaePiagetiellaP. titanpelicans 1Nine Islands[10]
ApicomplexaConoidasidaEucoccidioridaEimeriidaeEimeriaE. ahsatawild sheep 2Kaboudan Island[11]
E. faureiwild sheepKaboudan Island[11]
E. ovinoidaliswild sheepKaboudan Island[11]
E. parvawild sheepKaboudan Island[11]
NematodaAdenophoreaTrichuridaTrichuridaeTrichurisspp.yellow deer 3Ashk Island[12]
T. discolorwild sheepKaboudan Island[13]
T. georgicuswild sheepKaboudan Island[13]
T. infundibuluswild sheepKaboudan Island[13]
T. oviswild sheepKaboudan Island[13]
T. skrjabiniwild sheepKaboudan Island[13]
T. vondweiwild sheepKaboudan Island[13]
NematodaChromadoreaRhabditidaMolineidaeNematodirusN. archariwild sheepKaboudan Island[13]
spp.yellow deerAshk Island[12]
TrichostrongylidaeOstertagiaO. lyratawild sheepKaboudan Island[13]
O. ostertagiwild sheepKaboudan Island[13]
O. trifurcatawild sheepKaboudan Island[13]
SecernenteaAscarididaToxocaridaeToxocaraT. vitulorumyellow deerAshk Island[12]
StrongylidaDictyocaulidaeDictyocaulusD. filariawild sheepKaboudan Island[14]
ProtostrongylidaeMuelleriusspp.wild sheepKaboudan Island[14]
ProtostrongylusP. rufescenswild sheepKaboudan Island[14]
TrichostrongylidaeMarshallagiaM. marshalliwild sheepKaboudan Island[13]
PlatyhelminthesCestodaCyclophyllideaAnoplocephalidaeMonieziaM. benedeniwild sheepKaboudan Island[13]
TaeniidaeEchinococcusE. granulosuswild sheepKaboudan Island[14]
PlatyhelminthesCestodaCyclophyllideaTaeniidaeTaeniaT. hydatigenawild sheepKaboudan Island[14]
1 Pelecanus onocrotalus; 2 Ovis orientalis Gmilini; 3 Dama dama mesopotamica.
Table 6. List of insects in the Western part of National Park of Urmia Lake.
Table 6. List of insects in the Western part of National Park of Urmia Lake.
ClassOrderFamilyGenusSpeciesRef.
InsectaDipteraTachinidaeLespesiaL. frenchii 1[15]
NileaN. anatolica[16]
BithiaB. glirina[15]
HemipteraReduviidaeRhynocorisR. persicus[17]
HymenopteraBraconidaeCotesiaC. ofella[18]
C. vanessae[18]
IchneumonidaePhaenolobusP. saltans[19]
LepidopteraSesiidaeChamaespheciaC. schizoceriformis[15]
NoctuidaeSimyraS. dentinosa[20]
SphingidaeHylesH. euphorbiae[21]
OrthopteraPamphagidaeIranotmethisI. persa[22]
1 Synonym with Masicera sphingivora.
Table 7. List of crustaceans from the National Park of Urmia Lake.
Table 7. List of crustaceans from the National Park of Urmia Lake.
Sub-PhylumClassOrderFamilyGenusSpeciesRef.
CrustaceaBranchiopodaAnostracaBranchinectidaeBranchinectaB. orientalis 1[23]
ThamnocephalidaePhallocryptusP. spinosaI 2[23]
NotostracaTriopsidaeTriopsT. cancriformis 3[23,24]
1 Locality: Rashakan region; Salinity: 0.1%; 2 Locality: Zanbil and Chichest regions; Salinity: 1.7%–2%; 3 Locality: The lagoon near the Southern part of Urmia Lake/Rashakan region; Salinity: 0.1%.
Table 8. List of reptiles from the National Park of Urmia Lake.
Table 8. List of reptiles from the National Park of Urmia Lake.
ClassOrderFamilyGenusSpecies *Ref.
ReptiliaSquamataAgamidaePhrynocephalusP. belioscopus[25]
LacertidaeDarevskiaD. raddei[26]
EremiasE. pleskei[25]
E. velox[25]
LacertaL. brandti[25]
L. strigata[25]
L. trilineata[25]
* Note: There are no specific localities have been reported for those species.
Table 9. List of mid-winter birds from the National Park of Urmia Lake [27].
Table 9. List of mid-winter birds from the National Park of Urmia Lake [27].
ClassOrderFamilyGenusSpecies *
AvesAnseriformesAnatidaeBrantaB. ruficollis
MergusM. serrator
CharadriiformesScolopacidaeLimosaL. lapponica
GruiformesGruidaeGrusG. virgo
PelecaniformesArdeidaeBubulcusB. ibis
* Note: There are no specific localities have been reported for those species.
Table 10. List of fossils from the National Park of Urmia Lake.
Table 10. List of fossils from the National Park of Urmia Lake.
PhylumClassOrderFamilyGenusSpeciesRef.
BryozoaGymnolaemataCheilostomataMembraniporidaeMembraniporaM. fenestrate 1[28]
CheilostomatidaCelleporidaeCelleporaC. gracilis 1[28]
StenolaemataCyclostomataCavidaePolytrema (Ripisoecia)P. spongiosa 1[28]
DiastoporidaeDiastoporaD. gemmifera 1[28]
CerioporidaeCerioporaC. anomala 1[28]
C. palmate 1[28]
CnidariaAnthozoaScleractiniaFaviidaeAstreaA. defrancei 1[28]
A. ellisiana 1[28]
A. guettardi 1[28]
SolenastreaS. turonensis 2[29]
MicrosolenidaeThamnaraea (Dendraraea)T. polymorpha 2[29]
PhyllocoeniidaePhyllocoeniaP. archiaci 2[28,29]
CnidariaAnthozoaScleractiniaPoritidaePoritesP. dendroidea 1[28]
P. leiophylla 1[29]
EchinolampadidaeEchinolampasE. complanatus 1[28]
ClypeasteroidaClypeasteridaeClypeasterC. aff. Imperialis 3[30]
C. altus 1[28]
C. crassicostatus 1[28]
C. guentheri 3[30]
C. martini 3[30]
MolluscaBivalviaCarditoidaCarditidaeCarditasp.1[28]
OstreoidaOstreidaeOstreaO. virleti 1[28]
O. excavate 1[28]
O. lamellose 1[28]
O. pseudodigitalina 1[28]
PectinidaeChlamysC. malvinae 1[28]
PectenP. benedictus 1[28]
P. burdigalensis 1[28]
P. convexo-costatus 1[28]
P. flabelliformis 1[28]
P. simplex 1[28]
P. suburmiensis 1[28]
sp. 1[28]
SpondylidaeSpondylusS. bifrons 1[28]
VeneroidaVeneridaeMeretrixM. incrassate 1[28]
M. persiensis 1[28]
VenusV. aglaurae 1[28]
CephalopodaAmmonitidaPerisphinctidaePerisphinctesP. curvicosta 1[31]
GastropodaArchaeogastropodaHaliotidaeHaliotisH. philberti 1[28]
MesogastropodaCassidaeCassissp. 1[28]
FicidaePyrulaP. cingulate 1[28]
StrombidaeStrombusS. bonelli 1[28]
TurritellidaeTurritellaT. archimedis 1[28]
T. gradate 1[28]
T. rotifer 1[28]
NeogastropodaConidaeConussp. 1[28]
FasciolariidaeLatriusL. crispus 1[28]
1 There are no specific localities had been reported for those species; 2 Island of Koyun Daghi (Kaboudan); 3 Guvarchin Kala, at the extreme Northern end of Urmia Lake.
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