. J. Ichthyol. (June 2015), 2(2): 71–78 Received: March 01, 2015 © 2015 Iranian Society of Ichthyology Accepted: May 29, 2015 P-ISSN: 2383-1561; E-ISSN: 2383-0964 doi: http://www.ijichthyol.org

Geographic distribution of the genus Agassiz, 1832 in Iran (Teleostei: )

Arash JOULADEH ROUDBAR1, Hamid Reza ESMAEILI2*, Ali GHOLAMIFARD2, Rasoul ZAMANIAN2, Saber VATANDOUST3

1Department of Fisheries, Faculty of Natural Resources, Sari University of Agricultural Sciences and Natural Resources, Sari, Iran. 2Department of Biology, College of Sciences, Shiraz University, Shiraz, 71454–Iran. 3Department of Fisheries, Babol Branch, Islamic Azad University, Babol, Iran. * Email: [email protected]

Abstract: Distribution of the genus Chondrostoma in Iran, which is mostly known from the , , Kor River and Esfahan basins was mapped. The Kura nase, Chondrostoma cyri is reported from Armenia, Georgia and Iran and it is found in the streams and draining to the western coast of the Caspian Sea from the Kuma River in the north southward to the Kura and River basins in the south. The king or Mesopotamian nase, C. regium is widely distributed in Turkey, Iran, and Syria. It is found in the Qweik and Orontes River basins (Mediterranean Sea basin), the endorheic Esfahan basin and exorheic Tigris- and Zohreh River basins ( basin). The Kor nase, C. orientale is distributed only in the endorheic Kor River basin of Iran and prefers medium to large streams and also large rivers.

Keywords: Distribution pattern, Fish diversity, Middle East, Iran.

Introduction muzzle well arched, with very hard oral lips and a The nases, genus Chondrostoma Agassiz, 1832 sharp border” (Durand et al. 2003; Gante et al. 2007) (Etymology: Chondrostoma: Greek, chondros = (for detailed characters of the genus see Elvira cartilage + Greek, stoma = mouth, referring to the (1997); Robalo et al. (2007) and Coad (2015)). characteristic horny layer on the lower lip) belong to According to the nature of data used to diagnose the family Cyprinidae, subfamily species (i.e., morphological and osteological features distributed from the Iberian Peninsula and France to or molecular characters) the number of species the Caspian Sea, Esfahan and Tigris-Euphrates included in the genus differs. Twenty-six species are basins (Zardoya & Doadrio 1999; Durand et al. 2003; recognized for Chondrostoma by Elvira (1997) based Nelson 2006; Robalo et al. 2007; Esmaeili et al. on mainly osteological characters, as well as one new 2014; Mahboobi Soofiani et al. 2014; Coad 2015; described species from Turkey (C. beysehirense) by Keivany et al. 2015). The genus is particularly Bogutskaya (1997) on pure morphological grounds. diversified in the Iberian Peninsula, where over one- The variation of criteria among authors and the third of the known species is found including eleven discrepancies between molecular and morphological endemic species and more taxa are await formal data generated a troublesome situation concerning description (Robalo et al. 2005; Gante et al. 2007). the delimitation of the genus Chondrostoma, which The genus Chondrostoma composed of small to remains as yet unresolved. The recent findings of medium-sized fishes is characterized by “a mouth new Chondrostoma species (e.g. C. almacai) in the clearly subterminal, with transverse or arched slit, Iberian Peninsula which lack the horny layer on the without barbel, and with the upper jaw forming a lower lip, considered by some authors (Elvira 1987, 71

Iranian Journal of Ichthyology (June 2015), 2(2): 71-78

Fig.1. Global distribution map of Chondrostoma species of Iran (modified from Froese & Pauly (2014)).

1997) to be an important diagnostic feature of the distribution of the genus and construct an updated genus illustrate well that data obtained from map for these fishes in Iran using DIVA-GIS (7.5.0) morphology and from cytochrome b gene sequences software. are decoupled in this genus, as some authors consider that the mouth-related characters lack phylogenetic Materials and methods utility (Durand et al. 2003; Doadrio & Carmona In this study, distribution pattern of Chondrostoma 2004; Robalo et al. 2007). Overall, 35 species are from entire drainage basins of Iran was mapped. included in the Chondrostoma genus based on Materials for this study are resulted from (I) morphological and molecular grounds (Robalo et al. Available published data (Saadati 1977; Armantrout 2007). Iran hosts three species: the Kura nase, C. cyri 1980; Abdoli 2000; Ghorbani Chafi 2000; Abbasi Kessler 1877; the King nase, C. regium (Heckel 2009; Esmaeili et al. 2010a, 2011a; Mahboobi 1843); and the Oriental (Kor) nase, C. orientale Soofiani et al. 2014; Coad 2015; Keivany et al. Bianco & Bănărescu 1982. Basic information on the 2015); (II) Extensive fieldworks that provided the general biology, , karyology and geographic coordinate datasets for Chondrostoma morphology of these species is readily available from distribution till 2015 (from authors especially from the pertinent literature (e.g. Abdoli 2000; Esmaeili et the Zoological Museum of Shiraz University, al. 2010a; Mahboobi Soofiani et al. 2014; Coad Collection of Biology Department, Shiraz 2015). Here we provide updated information on the (ZM_CBSU) data bank provided by H.R. Esmaeili).

72 Jouladeh Roudbar et al.-Chondrostoma distribution in Iran

Fig.2. Global distribution map of Chondrostoma species of Iran (modified from Froese & Pauly (2014)).

Distribution map of the genus Chondrostoma was constructed with DIVA-GIS (7.5.0) software (Hijmans et al. 2012). Global distribution map of the three Chondrostoma species is illustrated based on available data in Froese & Pauly (2014).

Results The global distribution map of three species of Chondrostoma and their distributions in the Iranian Fig.3. Chondrostoma cyri from Aras River, Caspian Sea basin, March 2012, courtesy of K. Abbasi. boundary are illustrated in Figs. 1-2 and can be summaries as below: Chondrostoma regium: The King nase or Chondrostoma cyri: Chondrostoma cyri (Fig. 3) has Mesopotamian nase, C. regium (Fig. 5) is distributed been reported from Armenia, Georgia and Iran and it wider than the other two species (Figs. 1-2) and has is found in the rivers draining to the western coast of been reported from southern Anatolia, Turkey, Iran, the Caspian Sea from the Kuma River in the north Iraq and Syria. It is found in Kueik (Qweik), southward to the Kura and Aras river basins in the endorheic Esfahan basin and exorheic Tigris- south (Figs.1-2). It is found principally in streams Euphrates and Zohreh basins (). and rivers (Fig. 4). The reports from Tigris River basin of Iran include: 73 Iranian Journal of Ichthyology (June 2015), 2(2): 71-78

Fig.6. Gandoman wetland, Tigris River basin, natural Fig.4. Aras River, natural habitat of Chondrostoma habitat of Chondrostoma regium. cyri.

Fig.5. Chondrostoma regium from Gandoman wetland, the Tigris River basin of Iran. a stream in Ab-e Shalamzar drainage, Sharestan-e Bakhtiari va Chahar Mahall (previous political Fig.7. Upper reaches of the Zayandeh River, Esfahan divisions), a stream 3 km east of Boldaji, Kashkan basin, natural habitat of Chondrostoma regium. River drainage, River at Nokhor, Khorramabad , Bashar River at Mokhtar village (Yasuj), River, Kashkan River, Gamasiab River near Khersan River at Kota village (), Marbor River, Kermanshah, Javari spring near Ravansar, Diyala Gandoman Wetland, Fahlian River at Berim bridge River drainage, , River at (Noorabad), Abol Fares River (between , Zard River, a stream in the Khersan River and ), Fahlian bridge (Noorabad), drainage, Kalwi Chay near Piranshar, Alvand River Zayandehrud River (between Azadegan and Ghaleh near Sar-e Pol-e Zahab, Razavar River, Qareh Su Shahrokh villages), Zayandeh River Dam Lake, tributary, north of Kermanshah, Gamasiab River at Bazoft and Kuhrang Rivers in the upper Karun River Ghale Ghobad village (Nahavand), Gamasiab River basin and the Hawr al Azim marsh. It prefers a wide at Dehnow village (Nahavand), Gamasiab River at range of habitats from medium sized streams to large Cheshmeh Mahi village, Firoozan (Nahavand), lowland rivers (Figs. 6-7) with low or high water Sarab-e- Maran at Firoozan road to Kangavar, Do Ab current and also marshes and reservoirs from which stream near Do Ab village (Kangavar), Garous it migrates to rivers and streams to spawn. stream at Garous village (Kangavar), Dinavar River Chondrostoma orientale: Chondrostoma cyri (between Bistoon and Songhor), Razavar River at orientalis Bianco and Banarescu, 1982 was originally Kermanshah- Kamyaran road), Saymareh River at described from the "Pulwar River near ", Saymareh bridge, Talkhab River below Saymareh Kor River basin, , Iran. It is now valid 74 Jouladeh Roudbar et al.-Chondrostoma distribution in Iran

According to the distribution of three studied primary freshwater fishes of the genus Chondrostoma (C. cyri, C. regium and C. orientale), they are restricted almost to the north west and western parts of Iran not reaching to eastern and south eastern basins (e.g. the Kavir, Makran, Persis, Hormuz, Mashkid and Jazmurian basins). Evolution and dispersion of freshwater fishes are closely related Fig.8. Chondrostoma orientale from the Kor River to paleogeography and especially to the history of basin of Iran. basin connections, as a consequence of the geological development of landscapes. Chondrostoma is a northern genus of the subfamily Leuciscinae and its colonization should have come from the through river connections through the . Based on several lines of evidences (see Durand et al. 2002), it has been suggested that all Leuciscinae lineages sampled in the Middle East also occur in the Euro-Mediterranean region which are in agreement with authors such as Berg (1949) and Coad (1996) who considered that Fig.9. Kor River, natural habitat of Chondrostoma the Middle Eastern ichthyofauna is descended from orientale. the Euro-Mediterranean (Palaearctic). Perea et al. as Chondrostoma orientale Bianco and Banarescu, (2010) also proposed an initial colonization of 1982. The Oriental or Kor nase (Fig. 8) is distributed Europe from Southwestern Asia via the only in the Kor River basin of Iran (Esmaeili et al. Balkanian/Anatolian/Iranian landmass at the 2010b; Coad 2015; Eschmeyer 2015). It has been beginning of the Early Oligocene, which precisely reported from the Kor River at , Kor River matches the initial splitting of the most basal at Bande Amir, Pulvar (Sivand) River, Pulvar River leuciscins. at Naqsh-e Rostam and irrigation ditch 32 km from Durand et al. (2003) reconstructed the the Kor River bridge, all parts of the endorheic Kor phylogenetic relationships of the genus River basin. It prefers medium to large streams and Chondrostoma using the whole cytochrome b gene also large rivers (Fig. 9). sequence and compared the two freshwater fish dispersion hypotheses: (I) Dispersion around the Discussion Mediterranean Sea during the Lago Mare phase of It has been shown that having the knowledge of the Messinian salinity crisis (Bianco’s hypothesis) natural distribution and zoogeographic features of and (II) An older and more gradual colonization of freshwater fishes helps to identify hotspots of the Mediterranean rivers (Banarescu’s hypothesis). biodiversity, endemism, possible population Based on their phylogenetic analyses, Durand et al. connectivity and phylogeography which are useful (2003) identified two levels of divergences, implying for conservation priority planning. Moreover, two radiation events in the Chondrostoma genus. The historical biogeographical analyses of freshwater first radiation mainly concerned Mediterranean fishes provide a natural link between the geological species, whereas the second one includes Danubian and biotic evolution of a region. and Mesopotamian species. According to them, the 75 Iranian Journal of Ichthyology (June 2015), 2(2): 71-78

first radiation appears consistent with a Messinian basin of Tigris River (Esmaeili et al. 2010b; Coad dispersion during the Lago Mare, 5.3 million years 2015). The Zayandeh River is the principal feature of ago, whereas the second one may correspond to a the Esfahan basin and rises in the Zagros Mountains Mesopotamian dispersion through the Black Sea to east of the Zardkuh (meaning "Yellow Mountain") the Danube system. According to their results, the and flows east for about 300 km to its terminal basin, Lago Mare theory is strengthened, and a more recent the Batlaq-e Gavkhuni (Coad 2015). The Zayandeh and pre-Pleistocene colonization of the Danube from basin is connected to the upper Karun River basin Mesopotamian freshwater fishes was suggested. (which drains to the Persian Gulf) by the first Present available data reveals that the genus Kuhrang Tunnel constructed in 1953. A third tunnel Chondrostoma could be categorized in three major is under construction. There are two possible groups based on their natural distribution range. (I) mechanisms for distribution of C. regium in the Narrow distribution range (C. orientale), (II) Medium Esfahan basin: (I) It could have been translocated to distribution range (C. cyri) and (III) Wide the Esfahan basin incidentally via human or by the distribution range (C. regium). destruction and reduction of geographical barriers Chondrostoma orientale is restricted to the Kor (construction of the Kuhrang Tunnel). (II) Since the River basin and a rare and vulnerable species as Esfahan basin is adjacent to the Tigris River, it might comprehensive effort to collect it was failed during have been dispersed through the headwater capture the past 10 years collected only 3 specimens from which is common in the Zagros Mountains Kor River basin in 2005 (Sayyadzadeh and Joladeh (Oberlander 1965) and in Anatolia and pluvial Roudbar 2014). Severe drought, habitat conditions in the past would have facilitated fish modifications, dam construction, pollution and dispersal (Coad 1987, 1996). Probably this species is parasite infection (Sayyadzadeh and Joladeh colonized in the Tigris River basin and expanded its Roudbar 2014) are the main threats to this fish. distributional range from the different directions to Conducting monitoring and conservation programs the Esfahan basin. in the whole Kor River basin to locate any existence Chondrostoma cyri shows medium distribution populations are recommended. range in comparison to C. regium and is found in the Chondrostoma regium is a widespread species Kura and Aras drainages in the Caspian Sea basin, found in the Qweik, Euphrates and Tigris drainages inhabits piedmont and Mountain Rivers with strong from the northern tributaries in Anatolia to the current and rock to gravel bottom (Freyhof 2014). It southern marshes in Iraq (Freyhof 2014). This is also is expected that the populations are very slowly found in the Esfahan basin and Karun sub-drainage declining due to the threats in the area (Freyhof in Iran, but is often quite rare. It is suspected not to 2014). Extensive efforts to collect this fish from the decline fast enough to qualify for a threat category, Aras River yielded capturing only a few specimens or Near Threatened (NT) and is therefore assesses as showing declining population trend. a Least Concern (LC) species (Freyhof 2014). There are many threats in the area but none serious enough Acknowledgements to threaten this species. There is no conservation We wish to thank G. Sayyadzadeh, B. Parsi, action in place and none seems to be actually needed S. Mirghiasi and S. Ghasemian for their valuable help (Freyhof 2014). with the fish collections and Shiraz University for the Presence of C. regium in the Esfahan basin needs financial support. special attention. The Esfahan basin is an endorheic basin surrounded by the endorheic basins of Namak, Reference Kerman-Na'in, Sirjan, Kor River and the exorheic Abdoli, A. 2000. The Inland Water Fishes of Iran. Iranian 76 Jouladeh Roudbar et al.-Chondrostoma distribution in Iran

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