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

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.

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. List of archaebacteria and bacteria from the National Park of Urmia Lake.

Domain	Phylum	Class	Order	Family	Genus	Species	Ref.
Archaea	Euryarchaeota	Halobacteria	Halobacteriales	Halobacteriaceae	Haloterrigena	sp. 1	[3]
					Halosiccatus	H. urmianus 2	[4]
					Halovarius	H. luteus 3	[5]
Bacteria	Firmicutes	Bacilli	Bacillales	Bacillaceae	Ornithinibacillus	sp. 4	[6]
				Planococcaceae	Planomicrobium	sp. 4	[6]
	Proteobacteria	Gamma proteobacteria	Pseudomonadales	Moraxellaceae	Psychrobacter	sp. 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%.

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. List of microfungi harvested from soils of the National Park of Urmia Lake (localities: Kaboudan Island, Espir Island, Golmankhaneh Port, Mahabad Road) [7].

Division	Class	Order	Family	Genus	Species
Ascomycota	Ascomycetes	Incertae sedis	Incertae sedis	Sarocladium	S. strictum
	Dothideomycetes	Capnodiales	Davidiellaceae	Cladosporium	C. cladosporioides
		Pleosporales	Pleosporaceae	Alternaria	A. chlamydospora
					A. rhizophorae
				Bipolaris	B. prieskaensis
	Dothideomycetes	Pleosporales	Pleosporaceae	Embellisia	E. chlamydospora
					E. tellustris
				Ulocladium	U. alternariae
	Eurotiomycetes	Eurotiales	Trichocomaceae	Penicillium	P. expansum
	Leotiomycetes	Helotiales	Sclerotiniaceae	Botrytis	B. cinerea
	Sordariomycetes	Hypocreales	Hypocreaceae	Acremonium	A. larvarum
					A. potronii
				Acrostalagmus	A. luteoalbus
				Trichoderma	T. atroviride
					T. harzianum
			Incertae sedis	Trichothecium	T. roseum
			Nectriaceae	Fusarium	F. tricinctum
			Stachybotryaceae	Stachybotrys	S. chartarum
		Incertae sedis	Apiosporaceae	Arthrinium	A. phaeospermum
		Sordariales	Chaetomiaceae	Chaetomium	C. truncatulum

).

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. List of lichen from the National Park of Urmia Lake (localities: Rahmanloo and Saraydeh) [8].

Phylum	Class	Order	Family	Genus	Species
Ascomycota	Lecanoromycetes	Teloschistales	Teloschistaceae	Caloplaca	C. ferrugineoides

).

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. 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].

Phylum	Class	Order	Family	Genus	Species
Chlorophyta	Chlorophyceae	Volvocales	Dunaliellaceae	Dunaliella	D. bardawil
					D. parva
					D. salina
					D. tertiolecta

.

7. Parasites

The knowledge of parasitic infections in wildlife is necessary for management of protected areas and national parks.

Table 5. List of reported parasites at pelicans and some mammalians from the National Park of Urmia Lake.

Phylum	Class	Order	Family	Genus	Species	Host	Locality	Ref.
Arthropoda	Insecta	Phthiraptera	Menoponidae	Piagetiella	P. titan	pelicans 1	Nine Islands	[10]
Apicomplexa	Conoidasida	Eucoccidiorida	Eimeriidae	Eimeria	E. ahsata	wild sheep 2	Kaboudan Island	[11]
					E. faurei	wild sheep	Kaboudan Island	[11]
					E. ovinoidalis	wild sheep	Kaboudan Island	[11]
					E. parva	wild sheep	Kaboudan Island	[11]
Nematoda	Adenophorea	Trichurida	Trichuridae	Trichuris	spp.	yellow deer 3	Ashk Island	[12]
					T. discolor	wild sheep	Kaboudan Island	[13]
					T. georgicus	wild sheep	Kaboudan Island	[13]
					T. infundibulus	wild sheep	Kaboudan Island	[13]
					T. ovis	wild sheep	Kaboudan Island	[13]
					T. skrjabini	wild sheep	Kaboudan Island	[13]
					T. vondwei	wild sheep	Kaboudan Island	[13]
Nematoda	Chromadorea	Rhabditida	Molineidae	Nematodirus	N. archari	wild sheep	Kaboudan Island	[13]
					spp.	yellow deer	Ashk Island	[12]
			Trichostrongylidae	Ostertagia	O. lyrata	wild sheep	Kaboudan Island	[13]
					O. ostertagi	wild sheep	Kaboudan Island	[13]
					O. trifurcata	wild sheep	Kaboudan Island	[13]
	Secernentea	Ascaridida	Toxocaridae	Toxocara	T. vitulorum	yellow deer	Ashk Island	[12]
		Strongylida	Dictyocaulidae	Dictyocaulus	D. filaria	wild sheep	Kaboudan Island	[14]
			Protostrongylidae	Muellerius	spp.	wild sheep	Kaboudan Island	[14]
				Protostrongylus	P. rufescens	wild sheep	Kaboudan Island	[14]
			Trichostrongylidae	Marshallagia	M. marshalli	wild sheep	Kaboudan Island	[13]
Platyhelminthes	Cestoda	Cyclophyllidea	Anoplocephalidae	Moniezia	M. benedeni	wild sheep	Kaboudan Island	[13]
			Taeniidae	Echinococcus	E. granulosus	wild sheep	Kaboudan Island	[14]
Platyhelminthes	Cestoda	Cyclophyllidea	Taeniidae	Taenia	T. hydatigena	wild sheep	Kaboudan Island	[14]

¹ Pelecanus onocrotalus; ² Ovis orientalis Gmilini; ³ Dama dama mesopotamica.

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. List of insects in the Western part of National Park of Urmia Lake.

Class	Order	Family	Genus	Species	Ref.
Insecta	Diptera	Tachinidae	Lespesia	L. frenchii 1	[15]
			Nilea	N. anatolica	[16]
			Bithia	B. glirina	[15]
	Hemiptera	Reduviidae	Rhynocoris	R. persicus	[17]
	Hymenoptera	Braconidae	Cotesia	C. ofella	[18]
				C. vanessae	[18]
		Ichneumonidae	Phaenolobus	P. saltans	[19]
	Lepidoptera	Sesiidae	Chamaesphecia	C. schizoceriformis	[15]
		Noctuidae	Simyra	S. dentinosa	[20]
		Sphingidae	Hyles	H. euphorbiae	[21]
	Orthoptera	Pamphagidae	Iranotmethis	I. persa	[22]

¹ Synonym with Masicera sphingivora.

.

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. List of crustaceans from the National Park of Urmia Lake.

Sub-Phylum	Class	Order	Family	Genus	Species	Ref.
Crustacea	Branchiopoda	Anostraca	Branchinectidae	Branchinecta	B. orientalis 1	[23]
			Thamnocephalidae	Phallocryptus	P. spinosaI 2	[23]
		Notostraca	Triopsidae	Triops	T. 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%.

.

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. List of reptiles from the National Park of Urmia Lake.

Class	Order	Family	Genus	Species *	Ref.
Reptilia	Squamata	Agamidae	Phrynocephalus	P. belioscopus	[25]
		Lacertidae	Darevskia	D. raddei	[26]
			Eremias	E. pleskei	[25]
				E. velox	[25]
			Lacerta	L. brandti	[25]
				L. strigata	[25]
				L. trilineata	[25]

* Note: There are no specific localities have been reported for those species.

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. List of mid-winter birds from the National Park of Urmia Lake [27].

Class	Order	Family	Genus	Species *
Aves	Anseriformes	Anatidae	Branta	B. ruficollis
			Mergus	M. serrator
	Charadriiformes	Scolopacidae	Limosa	L. lapponica
	Gruiformes	Gruidae	Grus	G. virgo
	Pelecaniformes	Ardeidae	Bubulcus	B. ibis

* Note: There are no specific localities have been reported for those species.

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. List of fossils from the National Park of Urmia Lake.

Phylum	Class	Order	Family	Genus	Species	Ref.
Bryozoa	Gymnolaemata	Cheilostomata	Membraniporidae	Membranipora	M. fenestrate 1	[28]
		Cheilostomatida	Celleporidae	Cellepora	C. gracilis 1	[28]
	Stenolaemata	Cyclostomata	Cavidae	Polytrema (Ripisoecia)	P. spongiosa 1	[28]
			Diastoporidae	Diastopora	D. gemmifera 1	[28]
			Cerioporidae	Ceriopora	C. anomala 1	[28]
					C. palmate 1	[28]
Cnidaria	Anthozoa	Scleractinia	Faviidae	Astrea	A. defrancei 1	[28]
					A. ellisiana 1	[28]
					A. guettardi 1	[28]
				Solenastrea	S. turonensis 2	[29]
			Microsolenidae	Thamnaraea (Dendraraea)	T. polymorpha 2	[29]
			Phyllocoeniidae	Phyllocoenia	P. archiaci 2	[28,29]
Cnidaria	Anthozoa	Scleractinia	Poritidae	Porites	P. dendroidea 1	[28]
					P. leiophylla 1	[29]
			Echinolampadidae	Echinolampas	E. complanatus 1	[28]
		Clypeasteroida	Clypeasteridae	Clypeaster	C. aff. Imperialis 3	[30]
					C. altus 1	[28]
					C. crassicostatus 1	[28]
					C. guentheri 3	[30]
					C. martini 3	[30]
Mollusca	Bivalvia	Carditoida	Carditidae	Cardita	sp.1	[28]
		Ostreoida	Ostreidae	Ostrea	O. virleti 1	[28]
					O. excavate 1	[28]
					O. lamellose 1	[28]
					O. pseudodigitalina 1	[28]
			Pectinidae	Chlamys	C. malvinae 1	[28]
				Pecten	P. 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]
			Spondylidae	Spondylus	S. bifrons 1	[28]
		Veneroida	Veneridae	Meretrix	M. incrassate 1	[28]
					M. persiensis 1	[28]
				Venus	V. aglaurae 1	[28]
	Cephalopoda	Ammonitida	Perisphinctidae	Perisphinctes	P. curvicosta 1	[31]
	Gastropoda	Archaeogastropoda	Haliotidae	Haliotis	H. philberti 1	[28]
		Mesogastropoda	Cassidae	Cassis	sp. 1	[28]
			Ficidae	Pyrula	P. cingulate 1	[28]
			Strombidae	Strombus	S. bonelli 1	[28]
			Turritellidae	Turritella	T. archimedis 1	[28]
					T. gradate 1	[28]
					T. rotifer 1	[28]
		Neogastropoda	Conidae	Conus	sp. 1	[28]
			Fasciolariidae	Latrius	L. 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.

.

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.