Iran. J. Ichthyol. (September 2015), 2(3): 177–193 Received: June 7, 2015 © 2015 Iranian Society of Ichthyology Accepted: August 27, 2015 P-ISSN: 2383-1561; E-ISSN: 2383-0964 doi: http://www.ijichthyol.org
Ichthyofauna of Urmia basin: Taxonomic diversity, distribution and conservation
Hamid GHASEMI1, Arash JOULADEH ROUDBAR2, Soheil EAGDERI*3, Keivan ABBASI4, Saber VATANDOUST5, Hamid Reza ESMAEILI6
1Eastern Azerbaijan Agriculture and Natural Resources Research Center, P.O. Box: 53555-141 Tabriz, Iran. 2Department of Fisheries, Faculty of Natural Resources, Sari University of Agricultural Sciences and Natural Resources, Sari, Iran. 3Department of Fisheries, Faculty of Natural Resources, University of Tehran, Karaj, Iran. 4Iranian Fisheries Sciences research, Inland Waters Aquaculture Research Center, Agricultural Research Education and Extension Organization (AREEO), Bandar Anzali, Iran. 5Department of Fisheries, Babol Branch, Islamic Azad University, Babol, Iran. 6Department of Biology, College of Sciences, Shiraz University, Shiraz, 71454–Iran. * Email: [email protected]
Abstract: Fish biodiversity investigation in Urmia basin which is a part of Irano- Anatolian hot spot aimed to determine the state of fish in this endorheic basin. Based on the obtained results, freshwater fish species of the Urmia basin comprise 29 species in 25 genera, 7 families, 5 orders and one class. The most diverse order is the Cypriniformes with 23 species (79.31%) followed by Salmoniformes and Perciformes each with two species (2 species, 6.9%), Siluriformes and Cyprinodontiformes each with one species (1 species, 3.45%). The most diverse family is the Cyprinidae with 20 species (69%), Nemacheilidae (3 species, 10.3%), Salmonidae (2 species, 6.9%) followed by, Siluridae, Poeciliidae, Percidae and Gobiidae each with only one species (3.45 %). This basin comprises five endemic species to the basin itself (only found in Urmia basin, 17.24%) and 11 exotic species (37.93%). Zarrineh River had high species diversity and Sufi and Shahri Rivers had low species diversity. The fish composition and community structure of Urmia basin have been changed during the last few years due to (i) human-induced disturbance or anthropogenic activities including hydrological alteration, introduction of exotic species, over-fishing, unusual methods of fishing, rapid sedimentation, and land erosion and (ii) natural disturbance such as climate change which causes drought in this basin. Most of the native (including endemic) fishes of the Urmia basin have not been assessed for the IUCN Red List and some others have been considered as Least Concern or Data Deficient which is suggested to be re-assessed.
Keywords: Iran, Urmia basin, Permanent river, Biodiversity, Fishes.
Introduction drainage basins (Fig. 1) including both exorheic Iran is one of the most complex geographical areas of where the rivers and lakes drain to the sea and Palearctic realm and due to its considerable extent in endorheic, where rivers drain to an internal basin Southwest Asia has tremendous biodiversity. It is such as a lake, or are lost in the desert, and have no bordering the Oriental and African zones (Coad & connection with the sea (Coad 2015; Esmaeili et al. Vilenkin 2004) and its north-west, west and south- 2015; Jouladeh Roudbar et al. 2015). Paying west, are parts of Irano-Anatolian hot spot with high attention to biodiversity conservation of these basins biodiversity especially freshwater fish (Esmaeili et from different aspects is crucial and needs more al. 2010, 2014a). Iran is divided into nineteen investigation. Diversity is a key issue in
177
Iranian Journal of Ichthyology (September 2015), 2(3): 177-193
Fig.1. Map of Iran showing 19 basins including Urmia basin (L.M: Lake Maharlu basin). environmental protection and it aims to protect the be known as Lake Kabuda (Kabodan), from the word environment to maintain the maximum possible for "azure" in Persian, or 'կապույտ' number of native species in an area. ("Kapuyt/Gabuyd") in Armenian. Its Latin name was Today, growing agricultural, industrial activities Lacus Matianus so it is referred to in some texts as and fish breeding operations at inland waters on one Lake Matianus or Lake Matiene. hand and construction activities, such as building Lake Urmia, one of the largest saltwater lakes on hydraulic structures, on the other hand caused a need earth and a highly endangered ecosystem, is on the for further studies in these basins or ecoregions brink of a major environmental disaster similar to the including Urmia basin. catastrophic death of the Aral Sea (AghaKouchak et Urmia basin and its center international wetland al. 2015) which will affect the whole basin. Urmia of Urmia Lake are considered as important and Lake is an important natural asset with considerable valuable ecosystems in northwestern Iran. The lake is cultural, economic, aesthetic, recreational, scientific, named after the provincial capital city of Urmia, conservation and ecological value (Kelts & Shahrabi originally an Assyrian name meaning Puddle of 1986; Karbassi et al. 2010). It is a closed-basin water. Its ancient Old Persian name was Chichast wetland for which the only outlet is evaporation and (meaning, "glittering"–a reference to the glittering the inlet is precipitation, rivers, runoff flow and mineral particles suspended in the lake water and negligible groundwater inflow. With a new found along its shores). In medieval times it came to composite of multi-spectral high resolution satellite 178 Ghasemian et al.-Ichthyofauna of Urmia basin
Fig.2. Urmia basin and its main rivers. observations, AghaKouchak et al. (2015) and Jaafari major elements of biodiversity. et al. (2013) showed that the area of this Iranian lake This paper attempts to provide (i) an updated has decreased by around 88% in the past decades, far taxonomic fish diversity including natives, endemics, more than previously reported (~25% to 50%). exotics and transplanted species, (ii) information on Drastic changes to lake health are suggested to be the distribution and (iii) data on conservation status primarily consequences of aggressive regional water of fish species, from the Urmia basin of Iran. resources development plans, intensive agricultural activities, anthropogenic changes to the system, and Materials and Methods upstream competition over water (AghaKouchak et Study area: The Urmia basin is located in northwest al. 2015). In this basin, flowing rivers that were the of Iran with a total area of 51800km2. The Urmia major ecosystems and provided the large amount of Lake is the largest lake in the country and a Ramsar water for lake are also under severe pressures due to Site and is also one of the world's saltiest bodies of the above mentioned factors and lack of perspective water with about 128-149km long and 40-60km in environmental management along with notable wide. This lake is salty with a salinity up to 340.0gl- changes in ecological conditions. All of these 1 (mostly 217-235gl-1) and fishless (Kelts & Shahrabi parameters reduce habitat values and thus threaten its 1986; Ghaheri et al. 1999; Coad 2015). It is on the biodiversity. For this reason, one of the most brink of a major environmental disaster now effective ways to achieve biodiversity conservation (AghaKouchak et al. 2015). and restoration is to monitor its diversity in the The Urmia Lake is the terminal basin for a species, ecosystem and genetic levels which are three number of streams and rivers (Ghaheri et al. 1999). 179 Iranian Journal of Ichthyology (September 2015), 2(3): 177-193
Cornwallis (1976) notes both the draining of these marshes and the cessation of freshwater discharge from the Mahabad River. Lake Gory is a fresh to brackish lake near Tabriz occupying 120ha. It is fed by precipitation, springs and small streams, with overflow through a small stream (Coad 2015). Qanats are also found in this basin where surface water is saline. Dams are found on the Zarrineh River and on the river which flows through Mahabad paralleling the Zarrineh. The Nowruzlu Dam on the Zarrineh is occupying 1000ha and it is water storage reservoir with heavy input from surrounding farming activities. The Alavian Dam near Maragheh is a Fig.3. Type localities of enedmic species in the Urmia reservoir of 145 million cu m. The Nahand Reservoir Lake basin; = Acanthobrama urmianus; = Dam northeast of Tabriz has a capacity of 30 million Alburnoides petrubanarescui; = Alburnus atropatenae and = Petroleuciscus ulanus. cu m. Other dams include those at Ahar, Tabriz, Hashtrud, Hasanlu, Mianeh and Heris. The Prominent perennial streams include the Zarrineh Hassanlou Reservoir Dam at Naqadeh has a capacity River entering from the south and draining part of the of 107 million cu m (Coad 2015). Among the rivers northern Zagros with the Tata'u or Simineh River as of this basin, ten crucial and permanent rivers (Aji a major tributary. The saline Aji Chay or Talkheh Chay, Sufi Chay, Qaleh Chay, Mordugh Chay, (with hardness of 820mg/l; Surber 1969) from the Simineh Rud, Zarrineh Rud, Mahabad Chay, Shahri east draining the flanks of the Sabalan mountains and Chay and Nazlo Chay) were selected to study their Kuh-e Sahand, and the smaller streams from the west fish diversity (Fig. 2). This basin is type locality of such as the Zowla Chay, Nazlu Chay, Shahr Chay several fish species (Fig. 3). and Baranduz Chay (Coad 2015). In addition, there This paper has been resulted from the works are several lakes and marshes in this basin. Lake Kobi listed in the references (mainly from Saadati 1977; is a Ramsar Site in this basin at the south of Lake Armantrout 1980; Coad 2006,2015; Abbasi et al. Urmia and northeast of Mahabad. It comprises the 2005; Bogutskaya & Coad 2009; Esmaeili et al. fresh to brackish lake and associated but 2010; Moradi & Eagderi 2014) and also by discontinuous marshes of about 1200ha. The Shur examination or accessing available data in Gol, Yadegarlu and Dorgeh Sangi are endorheic ichthyological collections in Iran (e.g., ZM-CBSU, lakes at the south of Lake Urmia and northwest of Zoological Museum of Shiraz University, Collection Mahabad comprising 2500ha of lakes and associated of Biology Department, Shiraz; CMNFI, Canadian marshes. They are fed by precipitation, springs and Museum of Nature, Ottawa, Canada (see Coad 2015), small streams. (Khan et al. 1992; Coad 2015). Gerde recent fish collection of authors and extensive field Gheet and Mamiyand are freshwater marshes south expeditions till June 2015 from different river of Lake Urmia and north of Mahabad. The Ghara systems of the Urmia basin of Iran (Fig. 2). Gheshlaq freshwater marshes is located at south of Lake Urmia and north of Mahabad. Large parts of Results these marshes were drained by the "Mahabad Based on the obtained results, freshwater fish species Multipurpose Drainage and Irrigation Project" in the of the Urmia basin comprise 29 species in 25 genera, 1970s despite environmental concerns (Coad 2015). 7 families, 5 orders and one class. The most diverse 180 Ghasemian et al.-Ichthyofauna of Urmia basin
order is the Cypriniformes with 23 species (79.31%) followed by Salmoniformes and Perciformes each with two species (2 species, 6.9%), Siluriformes and Cyprinodontiformes each with one species (1 species, 3.45%). The most diverse family is the Cyprinidae with 20 species (69%), Nemacheilidae (3 Fig.5. Alburnus atropatenae from Chalechai, Urmia species, 10.3%), Salmonidae (2 species, 6.9%) basin, Iran. followed by, Siluridae, Poeciliidae, Percidae and Gobiidae each with only one species (3.45 %). This basin comprises five endemic species to the basin itself (only found in Urmia basin, 17.24%) including (Acanthobrama urmianus, Alburnus atropatenae, Alburnoides petrubanarescui Petroleuciscus ulanus and Romanogobio persus), and 11 exotic species Fig.6. Alburnus hohenackeri from Urmia basin, Iran. (37.93%) (See Table 1). Genus Barbus Cuvier, 1816 Checklist 6. Barbus cf. cyri De Filippi, 1865 (Figs. 7, 8) * = endemic to Iranian basins, ** = exotic (Figs. 4- 19). Class Actinopterygii Order Cypriniformes (2 families, 19 genera and 23 species) Family Cyprinidae (17 genera and 20 species) Genus Abramis Cuvier, 1816 1. Abramis brama (Linnaeus, 1758) Genus Acanthobrama Berg, 1916 2. Acanthobrama urmianus (Günther, 1899) * (Fig. 4).
Fig.7. Aji Chai River, Urmia basin, natural habitat of Barbus cf. cyri. (in 1995).
Fig.4. Acanthobrama urmianus from Mahabad Chai, Urmia basin, Iran. Genus Alburnoides Jeitteles, 1861 3. Alburnoides petrubanarescui Bogutskaya & Coad, 2009 * Genus Alburnus Rafinesque, 1820 4. Alburnus atropatenae Berg, 1925 * (Fig. 5). Fig.8. Sofi Chai River, Urmia basin, natural habitat of 5. Alburnus hohenackeri Kessler, 1877 (Fig. 6). Barbus cf. cyri and Alburnus atropatenae (in 1995).
181 Iranian Journal of Ichthyology (September 2015), 2(3): 177-193
Genus Capoeta Valenciennes, 1842 7. Capoeta capoeta (Güldenstaedt, 1773) (Figs. 9, 10). Comment: Capoeta capoeta gracilis (Keyserling, 1861) and C. capoeta heratensis (Keyserling, 1861) are Iranian subspecies but this wide-ranging species needs revision. Both subspecies has been recognised as a full species by authors. Scaphiodon asmussii Keyserling, 1861 and Capoeta gibbosa Nikol'skii, Fig.11. Carrasius auratus from Ghaleh Khani 1897 are Iranian synonyms. reservoir, Urmia basin.
Fig.9. Capoeta capoeta, Simineh River, Iran.
Fig.12. Carrasius gibelio from Ghaleh Khani reservoir, Urmia basin. Genus Cyprinus Linnaeus, 1758 11. Cyprinus carpio Linnaeus, 1758 ** Comment: Native populations in the Caspian Sea basin; also introduced there and elsewhere in Iran. Genus Hemiculter Bleeker, 1859 12. Hemiculter leucisculus (Basilewsky, 1855) ** Genus Hypophthalmichthys Bleeker, 1859 13. Hypophthalmichthys molitrix (Valenciennes, Fig.10. Ghale Chai River, Urmia basin, natural habitat 1844) ** of Capoeta capoeta and Alburnus atropatenae (in 1995). 14. Hypophthalmichthys nobilis (Richardson, 1844) ** Genus Carassius Jarocki, 1822 Genus Luciobarbus Heckel, 1843 Comment: The author of the genus follows 15. Luciobarbus mursa (Güldenstaedt, 1773) (Fig. Bogutskaya and Naseka (2004). 13). 8. Carassius auratus (Linnaeus, 1758) ** (Fig. 11). 9. Carassius gibelio (Bloch, 1782) ** (Fig. 12). Comment: Kottelat & Freyhof (2007); Bogutskaya et al. (2008, with question); Esmaeili et al. (2010) and Kalous et al. (2012) considered it as distinct species.
Genus Ctenopharyngodon Steindachner, 1866 Fig.13. Luciobarbus mursa, Zarrineh River, Iran. 10. Ctenopharyngodon idella (Valenciennes, 1844) **
182 Ghasemian et al.-Ichthyofauna of Urmia basin
Genus Petroleuciscus Bogutskaya, 2002 Genus Romanogobio Bănărescu, 1961 16. Petroleuciscus ulanus (Günther, 1899) * (Figs. 19. Romanogobio persus (Günther, 1899)* (Fig. 17). 14, 15).
Fig.17. Romanogobio persus, Zarrineh River, Iran. Genus Squalius Bonaparte, 1837 20. Squalius orientalis (Nordmann, 1840) Fig.14. Petroleuciscus ulanus Mahabad Chai River, Family Nemacheilidae (2 genera and 3 species) Iran. Comment: Formerly included in the family Cobitidae or the family was named Balitoridae (see Tang et al. 2006; Kottelat & Freyhof 2007; Freyhof et al. 2011; Esmaeili et al. 2014a). Genus Oxynoemacheilus Bănăraescu & Nalbant, 1967 21. Oxynoemacheilus bergianus (Derzhavin, 1934) (Fig. 18).
Fig.15. Mahabad Chai, habitat of Petroleuciscus Fig.18. Oxynoemacheilus bergianus, Zarrineh River, ulanus. Iran. Genus Pseudorasbora Bleeker, 1859 22. Oxynoemacheilus brandtii (Kessler, 1877) (Fig. 17. Pseudorasbora parva (Temminck & Schlegel, 19). 1846) ** Genus Rhodeus Agassiz, 1832 18. Rhodeus amarus (Bloch, 1782) (Fig. 16).
Fig.19. Oxynoemacheilus brandtii, Zarrineh River, Iran. Comment: Oxynoemacheilus angorae (Steindachner, 1897) - Frequently reported from Caspian Sea and Lake Urmia basins. Nemacheilus angorae was originally described from Angora (=Ankara, Turkey). However this taxon may be a catchall Fig.16. Female Rhodeus amarus, Zarrineh River, Iran. species in Iran, e.g. Nemacheilus angorae
183 Iranian Journal of Ichthyology (September 2015), 2(3): 177-193
Table 1. Fish species of Urmia basin, * endemic to Urmia basin only.
Family Species Status Red List status Reference Abramis brama Native Least Concern Freyhof & Kottelat, 2008 Acanthobrama urmianus Endemic* Data Deficient Devi & Boguskaya 2009 Alburnoides petrubanarescui Endemic* Not assessed Alburnus atropatenae Endemic* Not assessed Alburnus hohenackeri Native Not assessed Barbus cf. cyri Native Not assessed Capoeta capoeta Native Least Concern Freyhof, 2014 Carassius auratus Exotic Carassius gibelio Exotic Ctenopharyngodon idella Exotic Cyprinidae Cyprinus carpio Exotic Hemiculter leucisculus Exotic Hypophthalmichthys molitrix Exotic Hypophthalmichthys nobilis Exotic Luciobarbus mursa Native Least Concern Freyhof, 2014 Petroleuciscus ulanus Endemic* Not assessed Pseudorasbora parva Exotic Not assessed Rhodeus amarus Native Least Concern Freyhof & Kottelat, 2008 Romanogobio persus Endemic* Not assessed Squalius orientalis Native Not assessed Paracobitis malapterura Native Not assessed Nemacheilidae Oxynoemacheilus bergianus Native Least Concern Freyhof, 2014 Oxynoemacheilus brandtii Native Least Concern Freyhof, 2014 Siluridae Silurus glanis Native Least Concern Freyhof & Kottelat, 2008 Oncorhynchus mykiss Exotic Salmonidae Salmo trutta Native Least Concern Freyhof, 2013 Poeciliidae Gambusia holbrooki Exotic Percidae Sander lucioperca Native Least Concern Freyhof & Kottelat, 2008 Gobiidae Rhinogobius smilis Exotic lenkoranensis Abdurakhamanov, 1962 may be a species) distinct taxon and the species in the Caspian Sea Family Salmonidae (2 genera and 2 species) basin in Iran. Freyhof et al. (2011) doubt that Genus Oncorhynchus Suckley, 1861 O. angorae s.s. occurs in the Caspian Sea basin and it 25. Oncorhynchus mykiss (Walbaum, 1792) ** may not be present in Iran at all. Genus Salmo Linnaeus, 1758 Genus Paracobitis Bleeker, 1863 26. Salmo trutta Linnaeus, 1758 23. Paracobitis malapterura (Valenciennes, in Cuvier Comment: Its taxonomic status is under revision. & Valenciennes, 1846) Salmo trutta Linnaeus, 1758 was recognised in the Comment: See Freyhof et al. (2014) for its presence Caspian Sea but its subspecies is now regarded as a at Soufi-Chai River at Maraaghe, Urmia basin based full species (Naseka & Bogutskaya 2009). Based on on one specimen provided by Dr. R. Patimar Coad (2015), the Liqvan Chai in the Lake Orumiyeh (Gonbad University, Iran). basin contains a distinctive trout and Liqvan Chay Order Siluriformes (1 family, 1 genus and 1 species) trout were stocked in the Ab-e Bazuft of the upper Family Siluridae (1 genus and 1 species) Karun River (Tigris River) basin in the autumn of Genus Silurus Linnaeus, 1758 1975 but this failed (Prosek 2003). Jolodar and 24. Silurus glanis Linnaeus, 1758 Abdoli (2004) give its distribution in the Caspian Order Salmoniformes (1 family, 2 genera and 2 basin as in upstream waters from the Aras to the 184 Ghasemian et al.-Ichthyofauna of Urmia basin
Table 2. Fish species of Urmia lake basin and their distribution in ten rivers.
Chay
No Scientefic name -
Aji Aji Ghale Sofi Mardogh Zarrineh Simineh Mahabad Shahar Godar Nazlo 1 Abramis brama + + 2 Acanthobrama urmianus + + + + + + + 3 Alburnoides petrubanarescui + + + + 4 Alburnus atropatenae + + + + + + + + + + 5 Alburnus hohenackeri + + 6 Barbus cf. cyri + + + + + + + + + 7 Capoeta capoeta + + + + + + + + 8 Carassius gibelio + + + + + + + 9 Carassius auratus + + + + + + 10 Ctenopharyngodon idella + + + 11 Cyprinus carpio + + + + + 12 Hemiculter leucisculus + + + 13 Hypophthalmichthys molitrix + + + + 14 Hypophthalmichthys nobilis + + + + 15 Luciobarbus mursa + + 16 Petroleuciscus ulanus + + + 17 Pseudorasbora parva + + + + + 18 Rhodeus amarus + + + 19 Romanogobio persus + + + + + + 20 Squalius orientalis + + + + + + 21 Oxynoemacheilus bergianus + + + 22 Oxynoemacheilus brandti + + + + + + + + + 23 Paracobitis malapterurus + + 24 Silurus glanis + + 25 Oncorhynchus mykiss + + + + 26 Salmo trutta + + 27 Gambusia holbrooki + + + 28 Sander lucioperca + 29 Rhinogobius smilis + Total species 20 9 4 12 23 17 20 4 13 4
Tajan, absent in the Atrak and Gorgan rivers. Also analysed from complete mtDNA control region found in the Jajrud (Ouseley 1819-1823), in the Karaj sequences, 12 microsatellite loci and morphological River (Fortescue 1924; Derzhavin 1929; Berg 1949), characters by Hashemzadeh et al. (2012). Based on and from the vicinity of Damavand (? Damavand their mtDNA haplotype data, the Urmia (Orumieh) River) (Fraser 1825), and numerous other localities and southern Caspian populations did not differ in the Namak Lake basin (see Armantrout (1980) for significantly, but the Namak basin-Karaj population localities from the 1970s and Esmaeili et al. (2010) presented a unique haplotype closely related to the for more recent general distributions). However, haplotypes of the other populations. Nümann (1969) seems to indicate that fish in the Order Cyprinodontiformes (1 family, 1 genera and 1 Karaj River were stocked about 100 years previously species) from Caspian Sea Rivers. Interrelationships, origin Comment: The fossil of a cyprinodontid fish and phylogenetic affinities of brown trout, Salmo (Cyprinodontidae), Aphanius persicus (Priem, 1908) trutta populations from the southern Caspian Sea has been reported from Urmia basin (Teimori et al. basin, Urmia and Namak Lake basins in Iran were 2011; Esmaeili et al. 2012, 2014b)
185 Iranian Journal of Ichthyology (September 2015), 2(3): 177-193
Family Poeciliidae (1 genera and 1 species) Introduction and translocation of fish species, Genus Gambusia Poey, 1854 subspecies re-assessment and new records are the 27. Gambusia holbrooki Girard, 1859 ** main reasons of higher number of Urmia fishes in Order Perciformes (2 families, 2 genera and 2 2015. Ichthyological diversity of Urmia basin can be species) categorized into native, endemic and exotic fishes: Family Percidae (1 genera and 1 species) I) Natives: Native species is a species occurring Genus Sander Oken, 1817 within the range it occupies (or could occupy) 28. Sander lucioperca (Linnaeus, 1758) ** naturally, independent of human activity. There are Comment: Perca lucioperca was originally described 18 native fish species in Urmia basin of which 5 are from European lakes. endemics. Family Gobiidae (1 family, 1 genus and 1 species) II) Endemics: A taxon is endemic to an area if it Comment: It has been considered in the order occurs there and nowhere else (Gaston & Spicer Gobiiformes by some authors (Tacker and Roje 1998). The area can be defined by political 2011). boundaries, such as country or department endemics, Genus Rhinogobius Gill, 1859 or by ecological boundaries, such as a species 29. Rhinogobius similis Gill, 1859** endemic to a distinct drainage basin (Gaston & Comment: Rhinogobius similis was described from Spicer 1998). Endemic species are an important part Shimoda, Japan. Reported from Anzali wetland by of the natural heritage of a country and of global Keyvan Abbasi (see, Esmaeili et al. 2014a, c) and significance. Therefore, areas with significant Moradi & Eagderi (2014) from the Urmia basin. The populations of endemics and/or genetically identity of introduced Rhinogobius in Iran needs to significant endemics are prime candidates for species be confirmed. conservation and the protection of habitats of special conservation or scientific value (Coad 2006). This Discussion basin comprises five confirmed endemic species to Ichthyological diversity: The inland ichthyofauna of the basin itself (only found in Urmia basin, 17.24%), Iran is comprised of i.e. approximately 222 species or including Acanthobrama urmianus, Alburnus more (Esmaeili et al. 2014 a, c; Freyhof et al. 2015; atropatenae, Alburnoides petrubanarescui, Mousavi-Sabet et al. 2015) in different physiographic Petroleuciscus ulanus and Romanogobio persus. basins. Historically, the Iranian Plateau had III) Exotics: Alien (exotic, non-indigenous) species numerous freshwater resources, including wetlands, is a species that has been transported by human rivers, lakes, and streams that provided suitable activity into an area outside its natural range. Similar habitats for many aquatic species especially for some to trends observed in other world regions, the number native and endemic species. Based on the obtained of non-native fish species introduced and established results, freshwater fish species of the Urmia basin in Iran has increased considerably over recent comprise 29 species in 25 genera, 7 families, 5 orders decades attaining to 25 confirmed species comprising and one class which shows less species diversity about 11.5% of the total confirmed freshwater fishes compared to the Caspian Sea (with 119 species), in this country (Esmaeili et al. 2014c). Aquaculture, Tigris (more than 70 species) and Persis (more than sport fishing, control of malaria, ornamental 40 species) basins (see Esmaeili et al. 2010, 2014a) purposes, research activities, demonstration in which might be due to absence of a marine national fairs and accidental introduction are the connection. Esmaeili et al. (2010) reported 19 species main reasons for these introductions (Coad & Abdoli in 5 families and 18 genera from Urmia basin 1993; Esmaeili et al. 2010). Some of them (e.g., showing 10 more recorded species within 5 years. Cyprinus carpio, Carassius auratus, Pseudorasbora 186 Ghasemian et al.-Ichthyofauna of Urmia basin
parva, Xiphophorus hellerii and Gambusia Urmia basin. holbrooki) have been established in natural water Based on the fish origin, Urmia fishes can be bodies acting as invasion species (Esmaeili et al. grouped to: 2014c). All of these species except Xiphophorus I) Native Ponto-Caspian fishes: Salmonidae hellerii are found in Urmia basin and have the same (S. trutta) and Percidae (S. lucioperca). situation. II) Non-native Ponto-Caspian fishes (Palaearctic): Eleven exotic fishes in 4 families are reported Siluridae (Silurus glanis) and Cyprinidae (e.g. from the Urmia basin. Cyprinidae with 8 species Capoeta capoeta, Barbus cf. cyri). (72.73% of exotic species) is ranked first followed by III) Exotic fishes: Eleven fishes in 4 families Salmonidae, Poeciliidae and Gobiidae each with 1 including Cyprinidae, Salmonidae, Poeciliidae and species (9.09% each). Aquaculture, sport fishing, Gobiidae. control of malaria, ornamental purposes, research IV) Endemic fishes: Endemic taxa include those activities, demonstration in national fairs and fishes which are restricted to the Urmia basin accidental introduction are the main reasons for these southern and there is no record of them in other introductions (Esmaeili et al. 2010; 2014). neighboring basins and countries. These include the Ctenopharyngodon idella, Cyprinus carpio, cyprinid fishes, A. urmianus, A. atropatenae, Hypophthalmichthys molitrix, H. nobilis and A. petrubanarescui, P. ulanus and R. persus. Oncorynchus mykiss are commercially valuable Threats to fish diversity: Fresh water is a resource exotic species recorded from this basin and probably that may be extracted, diverted, contained or introduced to the natural aquatic ecosystems by fish contaminated by humans in ways that compromise its farmers. In addition, Alburnus hohenackeri, value as a habitat for organisms. Freshwater Carassius auratus, C. gibelio, Hemiculter leucisculus, ecosystems globally are among the most threatened Pseudorasbora parva, Rhodeus amarus and ecosystems (Strayer & Dudgeon 2010). In Iran, they Rhinogobius similis have been probably introduced face significant reductions in biodiversity, which can or translocated to this basin along with commercially be linked to overexploitation through human important cyprinds from the Caspian Sea basin as population growth, water pollution, flow accidental introduction. Furthermore, G. holbrooki modification, drought, destruction or degradation of has been released as a control agent for Anopheles habitat, and invasion by exotic or regionally controlling (i.e. control of malaria) (Tabibzadeh et al. translocated species (Coad 1980; Esmaeili et al. 1970). Sander lucioperca has been stocked in the 2010, 2014c). Zarreinerud, 70km upstream of Miandoab in 1971 These freshwater species, and especially those (Griffiths et al. 1972) as a control species for with limited distribution, are threatened by increasing undesirable fishes. Introductions always carry risks droughts over recent decades and increased for the native biota. The introduction of a non-native utilization of water resources for agricultural and species in an ecosystem is always likely to present an industrial purposes. In addition, the increased ecological risk if the species is able to integrate itself construction of dams has destroyed habitat and successfully into the ecosystem (Gozlan & Newton isolated the remaining populations. Some of these 2009), resulting in possible detrimental interactions species are also subject to illegal harvest, and unless with native species or even on ecosystem functioning mitigated, the combination of these threatening (Gozaln et al. 2010). Competition, habitat change, factors will eventually lead to the extinction of most, genetic changes and introduction of parasites and if not all, of the populations of these species. disease suggest being the most important impacts of Fragmentation of habitats and microhabitats the invasive species on native and endemic fishes of through factors, including agriculture, burning 187 Iranian Journal of Ichthyology (September 2015), 2(3): 177-193
Fig.20. Dam construction on Aji Chai River in Urmia Fig.22. Habitat alteration in Aji (Talkehrud) River, basin (1995). Urmia basin, habitat of Capoeta capoeta and Alburnus atropatenae (2012).
Fig.21. Bridge construction on Aji Chai River in Urmia basin (in 1995). Fig.23. Habitat alteration in Godar Chai River, Urmia vegetation, forestry, mining, and highways (Figs. 20- basin, habitat of Alburnus atropatenae. 23) can isolate populations and result in reduced world (Rahel 2007; Leprieur et al. 2008). genetic diversity, increased mortality, increased Ichthyogeography: Palynological evidence from predation pressure, increased edge habitat, reduced Lake Urmia indicates a late Pleistocene to early habitat quality, and invasive species colonization Holocene history (Jamali et al. 2008). (Al-Sheikhly et al. 2013; Mifsud 2014). Therefore, Ichthyogeography of Urmia basin has been habitat connectivity is essential for the long-term summarized in Coad (2015). The Urmia Lake was variability of aquatic animals. A growing demand for formed during the late Pliocene-Pleistocene and lies some ornamental fishes in the aquarium trade and at 1275-1300 meter above sea level and may had a aquaculture is also another threat to fish diversity in connection to the Caspian Sea basin during Urmia basin which has to be considered. The Pleistocene although this is in dispute (Schweizer globalization of trade and communication has made 1975). Pleistocene shorelines from 30 to 115m above preventing and controlling new introductions the present level have been confirmed, and the lake extremely difficult because human activities can covered twice its present area, but this would not easily transfer species to different places around the permit an external discharge (Coad 2015). Berg
188 Ghasemian et al.-Ichthyofauna of Urmia basin
(1940) reports benches at levels of about 1800m, effective conservation measures should be done on 1650-1550m and 1500-1360m, which may represent fish fauna in this basin. In some vital fish ecosystems shorelines, and a level of about 1570m would have such as Zarrineh River, Mahabad Chay, Mordugh had an outlet to the Aras River basin through the Chay, Aji Chay and Simineh River, that are crucial in Kara-tepe Pass in the northwest and across the plain terms of species diversity and spawning areas, near Khvoy. Saadati (1977) suggests two connections restoration and protection are of great importance. It with the Caspian Sea, an early one in the Pliocene to is also suggested that more comprehensive studies early Pleistocene resulting in endemic species such should be conducted on environmental impact of as A. urmianus, A. petrubanarescui, A. atropatenae introducing exotic species on native and endemic fish and P. ulanus and a later one in the late Pleistocene fauna in this basin. resulting in species which are the same as the Caspian As most of the threats especially introduction of or only subspecifically distinct. Stream capture may fish species are due to anthropologic activities, is have allowed the entry of some species in recent seems that the most promising approach is changing times as evidenced by S. trutta population (Coad human behavior as suggested by Azevedo-Santos et 2015). al. (2015). According to Fischer et al. (2012) and Species in common with the Caspian Sea basin Azevedo-Santos et al. (2015) changing the human include O. bergianus, O. brandtii, S. orientalis, behavior and basic values is a tremendous challenge, B. cyri, L. mursa, C. capoeta, S. glanis, and A. brama. but it is the most effective way to create awareness Groombridge (1992) notes that the ichthyofauna of and lead to better practices. These goals can be this region needs to be re-exanimated. Naseka (2010) achieved via education (in any of its forms) and via recognised the Urmia basin as a district within a west the dissemination of high quality information to Asian transitional region related zoogeographically society, specifically to stake-holders that are related to the East Transcaucasia district (southern Caspian to aquaculture, fishkeeping and sport fishing Sea area from the Kura to Atrek River). Both these (Azevedo-Santos et al. 2015) which are applicable in districts are linked to Iranian endorheic basins, Iran too. including those listed as ecoregions in Abell et al. For conservation strategies, species with a (2008), namely Namak Lake, Dasht-e Kavir, Lut, limited distribution such as narrow distribution range Esfahan and Sistan, plus Kor, Sirjan, Maharlu (narrow-range endemics), including A. urmianus, Kerman-Na'in and Hamoun-e Jazmurian basins in A. atropatenae, A. petrubanarescui, P. ulanus and this work. This basin has been considered as on the R. persus are of greater importance than species with freshwater ecoregions comprises the drainage basin a wide distribution range. Habitat monitoring is of Lake Orumiyeh (= Reza’iyeh, Urmia, Urmi, urgent for investigating the population status of the Urumiyeh), which lies in northwest Iran. It is native, endemic, and nonnative fishes. Moreover, bounded by the Caspian Highlands ecoregion to the gaining basic information about their natural history, east and the Upper Tigris-Euphrates basin to the community structure, and the biodiversity of regional west. systems is highly recommended. It is also Conservation: Based on the Red list data base (IUCN recommend that estimation of genetic diversity is 2015), most of the native (including endemic) fishes necessary at the population level, particularly for of the Urmia basin have not been assessed for the those populations that have been segmented by IUCN Red List and some others have been human activities such as habitat alterations by considered as Least Concern or Data Deficient (Table constructing of dams. Integrated watershed 1) which is suggested to be re-assessed. management plan, new approaches for water usage According to the results it seems that more (higher efficiency irrigation systems), and 189 Iranian Journal of Ichthyology (September 2015), 2(3): 177-193
anticipation of experts in different fields to predict in Iraq. Amphibian and Reptile Conservation 6(4): losses should be considered. Finally it is suggested 42-49. that maps of conservation hot spots be drawn based Armantrout, N.B. 1980. The freshwater fishes of Iran. on a combination of several factors (e.g., human PhD thesis. Department of Fisheries, Oregon State population density, aquaculture activity, habitat University, Corvallis, Oregon, USA. Berg, L.S. 1949. Presnovodnye ryby Irana i sopredel'nykh modifications, exotic introductions) and risk level of stran [Freshwater fishes of Iran and adjacent incurring losses to local–global biodiversity (e.g., countries]. Trudy Zoologicheskogo Instituta number of critically endangered species). Akademii Nauk SSSR 8: 783-858. Bogutskaya, N.G. & Coad, B.W. 2009. A review of Acknowledgments vertebral and fin-ray counts in the genus We are thankful to Shiraz and Tehran Universities Alburnoides (Teleostei: Cyprinidae) with a and Environment Department of West and East description of six new species. Zoosystematica Azarbaijan provinces for financial supports. We are Rossica 18(1): 126-173. pleased to thank R. Zamanian Nejhad, R. Khaefi, Bogutskaya, N.G. & Naseka, A.M. 2004. Katalog S. Babai, Gh. Kamran, Y. Shams and M. Nasri for beschelyustnykh i ryb presnykh i solonovatykh vod helping with fish collections in Iran. Rossii c nomenklaturnymi i taksonomicheskimi kommentariyami [Catalogue of Agnathans and
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