Research Article

Waterbirds as Bio-indicators in Lake Uromia Ecosystem Changes  

Behrouz Behrouzi-Rad
Dep. of Environment, Ahvaz branch, Islamic Azad University, Ahvaz, Iran
Author    Correspondence author
International Journal of Marine Science, 2016, Vol. 6, No. 43   doi: 10.5376/ijms.2016.06.0043
Received: 19 Aug., 2016    Accepted: 27 Oct., 2016    Published: 31 Oct., 2016
© 2016 BioPublisher Publishing Platform
This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Preferred citation for this article:

Behrouzi-Rad B., 2016, Waterbirds as Bio-indicators in Lake Uromia Ecosystem Changes, International Journal of Marine Science, 6(43): 1-13 (doi: 10.5376/ijms.2016.06.0043)


The main factor for stability of Lake Uromia ecosystem is amount of its water, which provides suitable habitat for terrestrial and waterbirds. In normal condition, average depth of water and area of the lake were five meter and 483000 hectare in 1980 (wet year of lake Uromia), but the depth reduced to less than one meter and area less than 100000 hectare in 2015. Reduction of area and water depth of lake caused variation of breeding population and species number of birds in Lake Uromia. In this paper, reduction of breeding bird's population and species number of birds in 1980, compared with 2015, that lake was dried and the area of the lake reduced to less than twenty percent of normal condition. forty tow species of waterbirds, thirty eight species of waders and wading birds and 109 species of terrestrial birds were reported in Lake Uromia in 1980(at wet years), but in 2015, the species of birds reduced to sixteen species of waterbirds, sixty three species of terrestrial, twenty one species of waders and wading birds. Fifty tow breeding bird's species in 1980 reduced to seventeen species in Lake Uromia in 2015. Breeding indicator species were Phoenicopterus ruber 100000 pairs, Pelecanus onocratelus 3500 pairs, Tadorna tadorna 5000 pairs, Larus genei 5000 pairs and Larus armenicuss 8000 pairs, but in 2015, only seventeen species of birds have been bred, and breeding population of Larus armenicuss and Phoenicotrus ruber reduced to less than 100 pairs, Tadorna tadorna 50 pairs and other breeding indicator species near to zero. Reduction of breeding population and species number of birds are signs of the disintegration of Lake Uromia ecosystem.

Waterbirds population; Species number; Lake Uromia

The Lake Uromia was established as a protected area in 1960s, changed to National Park in 1974, and designated as a UNESKO (MAB) biosphere reserve in June 1976 (Dep. of Environment of West Azarbaijan, 1976; Cornwallis, 1976; Evans, 1994; Scott, 1995), also designated as a Ramsar sites on 23 June 1975 (Ramsar convention bureau 2015), and has been identified as an "Important Bird Area" by Birdlife International since 1994 (Evans 1994). It is more than 60 years that managed by Department of Environment of Iran (Dep. of Environment of West Azarbaijan 2015, Scott 1995 and 2001, Evans 1994). Uromia Lake bed sludge was used to treat skin diseases and it was one of the best places for ecotourism attraction. Lake Uromia had the important role in ecosystem balance in northwest of Iran (Scott 2001). Several species and thousands of pairs of aquatic and terrestrial birds were breeding in Lake Uromia. Ringing of the Juvenile of the breeding species of waterbirds carried of more than 40 years in the lake by the ornithology unit of Dep. of the Environment of Iran, and lots of juvenile of Phoenicoterus ruber, Pelecanus onocrotalus, Larus genei and Larus armenicuss have been ringed during 40 years (Argyle 1975, Behrouzi-Rad 1980, 1981 and 1995, Dep. of Environment of West Azarbaijan, 2015). Because of drying, ecological function of the lake Uromia disturbed and the breeding habitats of the birds disturbed and the breeding colony of the birds decomposed. There were 102 small and large islands in the lake Uromia in 1980; six islands (Islami, Kabodan, Espir, Arezo, Ashk and Dugouzlar) were important habitats for breeding birds, Fig (1).    
In 1980, 189 species of terrestrial and water birds reported(Scott et al., 1971; Behrouzi-Rad, 2001) which 109 species (42%) were terrestrial, belonged to 34 family, 42 species (22.22%) waterfowl belonged 6 families, 38 species (20%) waders and wading, belonged 8 families (Behrouzi- Rad 1990 and 1995). Most of these species were not seen in 2015 (tables 1, 2, 3 and 4). The aim of this study was to demonstrate, the effect of drying of lake on waterfowl breeding population and bird's species number variation in Lake Uromia.


Fig 1 Lake Uromia in 1980s and 2015 (Google earth, 2015)


Methods and Materials

Study Area

The Lake Uromia lies at 1280 m and located at 37o30'N45o30'E in a large internal drainage basin in western Azarbaijan Province, 60 km southwest of Tabriz (Dep. of Environment of West Azarbaijan, 2015, Evans 1994, scott. 1995). Area of the lake was 483000 hectare in normal condition (Dep. of Environment of West Azarbaijan, 2015). There are 102 small and large islands, the smallest island is Angoushte Osman with area less than 5 m2 and the largest one is Kabodan with area 3125 ha in a large, shallow, hyper saline lake. Also there is extensive fringing brackish to saline marshes, in a large internal drainage basin in the uplands of northwestern Iran (Scott 1995). The lake was of great importance as a breeding area for many species of waterbirds, notably Phoenicopterus ruber, Pelecanus onocrotalus, Larus genei, Larus armenicuss and Tadorna tadorna, and staging area for migratory species in spring and autumn, (Scott 1995 and 2001, Evans 1994). The lake is protected as a National park, Ramsar Site, Biospher Reservior and Important Bird Area (Evans 1994 Scott 1995, Behrouzi-Rad 2001, Dep. of Environment West Azarbayjan 2015). The average depth of lake was about 5 meter in 1980 (Dep. of Environment of West Azarbaijan, 2015), but in 2015, south part of the lake was dried complete and north part was less than one meter(Jaica 2015). Salinities range from 80 to 280 in 1980, but in 2015 it was 540 p.p.t. (Dep. of West Azarbaijan, 2015, Jaica 2015). There was a buildup brine shrimp Artemia uromiana, during the wet years, but in 2015 the lake was devoid of Artemia uromiana. The lake is too saline to support any plants or animals. The shoreline vegetation was dominated by species of Atriplex sp, Frankenia sp and Suaeda sp. The marshes at the south of lake have typical saltmarsh plant communities with Juncus sp, some Phragmites australis at river mouths, and occasional stand of Tamarix sp. remnant stands of Pistashia atlantica woodland survive on the larger islands, notably Kabodan, and Ashk (Scott 1995, Evans 1994). Other conspicuous plants on the larger islands include Ramnus pallasii, Artemisia sp, Dianthus sp, Cerasseus sp, Ephedra sp, Hordeum sp, and Bromus sp.


Birds Count Method

Breeding population of waterbirds and species number of all birds was counted by total count method on January and August in 1980 and 2015. The juvenile of the Pheonicoterus ruber have been counted by total count method in the water and were multiplied by 2 (because one chick belonged to both parents). Breeding population of Larus genei, Larus armenicus, and Pelecanus onocrotalus, estimated by nests count on the islands and multiplied by 2. The breeding population of Tadorna tadorna estimated by total count of birds that their chicks could not fly and they were swimming in the water with their chicks. Population of other breeding species estimated by total nests counts. We couldn't estimate the breeding population of terrestrial birds, only reported the nest or chicks of them on the islands on ground, trees or crack of rocks. Wintering population of waterbirds counted by total count in January in 1980 and 2015.    



189 species of birds were observed in Lake Uromia in January and August1980 (at that time the lake Uromia was full of water), that included 38.18% birds of Iran (at that time the species number of Iranian birds were 495 species (Scott et al., 1971) and 100 species in 2015 that included 19% of Iranian birds (species number of Iranian birds reported 548 species in 2015, (Iranian birds Record Committee, 2015) table (1). Changes in bird's population of Lake Uromia are shown in table (1).



Table 1 Number of species of birds in Lake Uromia in 1980 and 2015


Terrestrial Birds in Lake Uromia

109 (57.67%) species of birds in Lake Uromia were terrestrial and observed on Kabodan, Espir, Ashk, Islami, Arezo islands and coasts of Lake Uromia in 1980, reduced to 63 species in 2015. The terrestrial breeding and non-breeding specie in 1980 and 2015 are shown in table (2).


Waterbirds in Lake Uromia

Observed and reported species of waterbirds in 1980 and 2015 are shown in table3. Population of waterbirds was 80891 individuals belonged to 80 species in 1980, reduced to 5675 individuals and 37 species in 2015. Reduction of waterbirds population was 93% and species number was 46.25%. Breeding population of the waterbirds were 129893 pairs belonged to 29 species, reduced to 297 pairs and 11 species. Reduction was 99.77% and 62% respectively in 2015 table (3).


Statuses of the indicator breeding species in Lake Uromia were as below:


1-Greater Flamingo Phoenicopterus ruber

Greater Flamingo is protected species in Iran and was breeding in Lake Uromia since 1957(Dep. of Environment of West Azerbaijan, 1976). Breeding habitats of this species in Lake Uromia were Ashk, Espir, and Dugouzlar Island since 1957 until the lake dried. Breeding population of the species was counted 20000 pairs in 1957, increased to 100000 pairs in 1980, and reduced to less than 100 pairs in 2015 (Dep. of Environment of West Azarbaijan 1976, Scott 2001, Behrouzi-Rad, 1980, 1990, and 2015). Non-breeding birds population of the species were 20000 in 1980, but there was not non-breeding population in Lake Uromia in 2015, table (3) (Behrouzi-Rad 2015).



Table 2 Terrestrial birds in Lake Uromia in 1980 and 2015 (Behrouzi-Rad 1980 and 2015)


2-White Pelican Pelecanus onocrotalus

The White Pelican Pelecanus onocratalus is protected species in Iran and the Lake Uromia was only main breeding habitat of the species in Iran since 1957 until the lake dried. Breeding population of White Pelican varied between 50 to 3500 pairs since 1957-1980 (Scott 1995, Behrouzi-Rad, 2001) that bred only on Dugouzlar islands in Lake Uromia. It is more than five years that this species not breed in the lake; also it did not breed in 2015.


3-Slender Billed Gull Larus genei

First Breeding of the Slender Billed Gull Larus genei reported in lake Uromia in 1957 (Dep of the Environment of Uromia, 1976). This species was bred on Kabodan, Espir, and Ashk islands until 1980. Breeding population of the species varied 3000-5000 pairs during breeding years ( Scott 1995, Behrouzi-Rad 2001), but was zero in 2015 table(3).



Table 3 Waterbirds species counted in Lake Uromia in1980 and 2015


4-Armenian Gull Larus armenicus

The Armenian Gull Larus armenicus was breeding on most of 102 islands in Lake Uromia since 1957 until 2001(Dep.of Environment of West Azarbaijan, 2015), but the main and important breeding habitats of the species were Kabodan, Ashk, Espir, Dugouzlar, Chairly, Ardashe and Shahsanamlar islands. Breeding population varied between 5000-8000 pairs during the breeding years. Breeding population were 8000 and less than 100 pairs in 1980 and 2015 respectively.



Table 4 Key species birds of Lake Uromia


5- Shelduck Tadorna tadorna

The Shelduck Tadorna tadorna is swimmer bird, but breed on Ask, Espir, Kabodan and Arezo Island during wet year. Breeding population varied between 1000-5000 pairs during 1957-2001.In the recent years especially in 2015, the breeding population were less than 50 pairs.


6-White Headed Duck Oxyura leucocephala

The White Headed Duck is a globally threatened (Vulnerable) species and protected in Iran. The main breeding habitats of the species were Gopi-baba-Ali and Kaniborazan wetlands at south of Lake Uromia. Breeding population of White Headed duck varied between 3to 5 pairs until 2001, but there were not breeding population in the wetlands in 2015.


Sensitive Habitats for Breeding Species

The sensitive habitats for six breeding species in Lake Uromia were, Kabodan, Ashk, Espir, Arezo and Dugouzlar Islands. All breeding population of White Pelican and main breeding population of Greater Flamingo were bred on Dugouzlar island, Shellduck and main breeding population two gulls species were bred on Ask, Espir, Kabodan and Arezo islands. In 2015 the south of lake Uromia dried complete and the depth of north of part of the lake reduced less than one meter (Jaica 2015). All of the islands located in south part of lake in the dried part, and, all the islands connected to the dry ecosystem on around of lake. They were not islands and not suitable habitats for waterbirds breeding population in 2015. For this reason, the breeding population of breeding species destroyed completely in 2015.


Key Species of Birds of Lake Uromia

The Lake Uromia ecosystem is extremely important for globally and regionally threatened species or those that 1% or more population of species wintering or breeding in lake Uromia (Table 4).



Before drying Lake Uromia, 102 small and large islands, coasts and wetlands at south part of Lake Uromia were suitable habitats for wintering, passage and breeding population of waterbirds and terrestrial birds. The Dughouzlar islands were extremely important for breeding Pelecanus onocrotalus (50-3500 pairs). The Ashk, Dugouzlar , Espir, Arezo islands were important for breeding Phoenicopterus ruber (15000-100000 pairs), Egretta garzetta (40-90 pairs), Plegadis falcinellus (40-100+pairs), Tadorna tadorna (3000-5000 pairs), Tadorna ferruginea (100-500 pairs), Larus armenicus (5000-8000pairs), Larus genei (3000-5000 pairs. The wetlands and coasts of southern part of Lake Uromia were extremely important for breeding Anser anser (3-5pairs), Marmaroneta angustristris (10-25pairs), Aythya nyroca (3-11pairs), Himantopus himantopus (200-500 pairs, table (2). The Pelicans, Gulls, Spoonbills, Little Egret, and many of the flamingos breed on a group of small islands near the south end of the lake, and flight to the extensive brackish and freshwater wetlands on the plain to the south of the lake to feed (Argyle 1975, Scott 1995). Compound of birds community in Lake Uromia were waterbirds 24%, Terresterial birds 54% and wading and wader 22%. The birds of Lake Uromia include, 9% Filter feeder (Plankton eaters), Benthos eaters 20%, Omnivorous 5% Carnivorous 19%, Herbivorous 22%, fish eating birds 6% and insectivorous 19% (Table 1and2). Savege (1964) surveyed the lake in 1960 and found only about 100 non-breeding flamingos; he located some old nest-mounds, and speculated that flamingos had bred in the past. However, some 10000 to12000 birds were found breeding in 1965 and 1966, and in 1970, there were an estimated 40000 birds at the colony (Scott 1995 and 2001). Aerial censuses of the breeding colonies in 1971 and 1972 indicated 15000-20000 pairs in both years, with an additional 5000-10000, non-breeding present (Scott 1995 and 2001). Flamingos are known to have bred in large number at Lake Uromia every year since then, and number appear to be increasing slightly, with perhaps as many as 100000 breeding pairs before drying the lake. After hatching, the chicks gather together in large crèches and swim to the south end of the lake to feed in the extensive shallows. Most other species of waterfowl breed on the mudflats surrounding the lake or in the extensive fresh to brackish marshes at the main river mouths. The vast mudflats surrounding the lake were the most important autumn staging area for migratory shorebirds and Anas querquedula in Iran, while the open water of the lake occasionally huge number of ducks. Over 425000 waterbirds of at least 53 species were recorded in the Uromyieh lake basin during an aerial survey on 29-31 August 1973(Scott 1995). The islands in Lake Uromia were the only known breeding locality for Falco biarmicus in Iran (at least five pairs) and also provide nesting sites for at least 10 pairs of Neophron percnopterus, Falco cherrug and Falco peregrinus have been recorded during the summer month and may breed; Gyps fulvus and Aegypius monachus were regular visitors from the surrounding hills and Haliaeetus albicila and Falco columbarius occur in winter (Argyle 1975, Scott 1995 and 2001). The great bustard Otis tarda was a regular visitor to the plain around the south part of the lake. In the 1980, with up to 25 being recorded in August, but the bird were not known to breed in the area (Behrouzi-Rad 2001). At least 187 species of birds have been recorded in the National Park (Scott 1995). Three Globally Threatened species Marmaronetta angustirostris, Aythya nyroca and Oxyura leucocephala were regularly breeder in southern wetlands (Kaniborazan and Gopibaba-Ali) of Lake Uromia. It was particularly important for it large breeding colonies of Pelecanus onocrotalus, Phoenicopterus ruber, Larus armenicus and Larus geneai, but also supports over 1% of the regional breeding population of seven other species of waterfowl (Argyle 1975, Evans 1994). During the migration season and in winter, it regularly supports over 1% of the regional population of an additional 29 species of waterfowl, table (4) (Scott 1995 and 2001, Evans 1994). Wild Sheep Ovis gemelini were introduced on to Kabodan Island in the 19th century while Persian Fallow Deer Dama mesopotamica were introduced onto Ashak Islandin late 1970s. The sheep population Peaked at over 4000 in 1970-1980, but then declined to only about less than 800 in 2015. The Persian Fallow Deer population peaked up over 300 in 1980s, but reduced to only about less than 20 in 2015. Several of the islands notably Ashk, Kabodan, Espir and Arezo, supports almost pristine stands of Azerbayjan Pistachio Pistacia atlantica forest. The Ashk, Espir, Arezo, Dughouzlar and Kabodan islands were sensitive habitats for breeding species of waterbirds, some terrestrial birds, Wild Sheep and Persian Fallow Deer. In 2015 the all mentioned islands connected to the main ground at around of the lake and there were not any islands. However, all bird communities, Wild Sheep and Persian Fallow Deer population crack up. The lake supports an abundant growth of the alga Enteromorpha intestinallis (Ulvaceae) and there was a buildup of brine shrimp Artemia Uromiana during the summer month in wet years also in 1980s, but in 2015 reduced to zero. Variation of breeding and wintering population of birds are bio-indicators for ecological water need of Lake Uromia ecosystem, because each group of Waterbirds preform special depth of water, food and habitats, that these factors can be used to protect and manage the Lake Uromia. The crack up of the Lake Uromia ecosystem unfolds at agricultural grounds and effect on the local people life in near future. 



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