Research Article Hormuz River System As a Micro Hotspot Of

Iran. J. Ichthyol. (June 2020), 7(2): 181-196 Received: February 20, 2020 © 2020 Iranian Society of Ichthyology Accepted: June 24, 2020 P-ISSN: 2383-1561; E-ISSN: 2383-0964 http://www.ijichthyol.org Research Article

Hormuz River System as a micro hotspot of diversification for the aphaniid fishes in Iran

Azad TEIMORI*1, Hamid Reza ESMAEILI2

1Department of Biology, Faculty of Sciences, Shahid Bahonar University of Kerman, Kerman, Iran. 2Ichthyology and Molecular Systematics Research Laboratory, Zoology Section, Department of Biology, College of Sciences, Shiraz University, Shiraz, Iran. *Email: [email protected] Abstract: The Hormuz River System (HRS) is located in the southern coastal plain of the Zagros Mountains. Two main river drainages i.e., Mehran and Kol are known from this region, which are directly discharged to the Persian Gulf. The HRS has surprising diversity for tooth-carp fishes (family Aphaniidae). The present study aims to accentuate this notable diversity and discuss the possible cause of diversification of the tooth-carps in the HRS. To date, 15 Aphaniid species have been discovered from the Iranian drainage basins. Among them, 10 species belong to the genus Aphanius, four species belong to the genus Aphaniops, and a single species belonging to the genus Paraphanius. The HRS by having four species (22% of the Iranian tooth-carps) demonstrated the highest diversity among the other Iranian basins. Of these, one belongs to the genus Aphanius (A. darabensis) and three species belong to the genus Aphaniops (A. furcatus, A. ginaonis, and A. hormuzensis). By considering the degree of endemicity of the tooth-carps fauna relative to the territorial boundaries of drainages, the HRS has the highest endemicity, in which 31% of the Iranian endemic tooth- carp species present only in the HRS. The last connection of the Makran Basin with the HRS dates back to the late Pliocene and lower Pleistocene about 1.8 million years ago. Also, the other vicariance-based events like those events related to the last glacial maximum (21000- 18000 BP), population migration during the Early Holocene sea-level rise, and the Holocene to present-day have promoted the intra- and interspecific differentiation of tooth-carps in the HRS. Also, the geological situation of the HRS provided various extreme environmental conditions, which caused a particular increase in the diversification of the tooth-carp species.

Keywords: Aphanius, Aphaniops, Paraphanius, Extreme ecological condition, Geological history.

Citation: Teimori, A.& Esmaeili H.R. 2020. Hormuz River System as a micro hotspot of diversification for the aphaniid fishes in Iran. Iranian Journal of Ichthyology 7(2): 181-196.

Introduction 2012a). Based on the geological estimation, it has The Hormuz River System (HRS) includes several been separated from the other neighboring river river drainages locating in the southern coastal plain drainage (i.e., Helleh and Mond in the west and of the Zagros Mountains, southern Iran. The HRE Minab/Makran in the east) since the late Pliocene and drains into the Persian Gulf, near or at the Strait of Pleistocene (Hatzfeld et al. 2010). The last Hormuz (Fig. 1). It is separated in the west from the connection of the Makran Basin with the HRS Helleh and Mond River drainages (Persis) by the probably dates back to the late Pliocene and lower Kazerun Fault System (KFS), which separates the Pleistocene (i.e., 1.8 million years before the present) North Zagros from the Central Zagros, and in the (Regard et al. 2004). east, it is separated from the Minab River drainage In addition to the geological events, which have (Makran) by the Zendan Falt System (ZFS) (Regard been considered to be responsible for the isolation of et al. 2004; Hatzfeld et al. 2010; Teimori et al. the HRS from the other basins (Regard et al. 2004; 181

Iran. J. Ichthyol. (June 2020), 7(2): 181-196

Fig.1. The geographic location of the Hormuz River System (HRS) in the southern coastal plain of the Zagros Mountains, southern Iran. The HRE drains into the Persian Gulf, near or at the Strait of Hormuz. Hatzfeld et al. 2010), the local geologic events within the HRS have also been caused the isolation of hydrological networks and created various habitats (e.g., hot sulfuric springs, and river subsystems). This environment diversity and also habitat fragmentation caused a particular increase in fish species diversity of the HRS (e.g., Esmaeili et al. 2010, 2016; Teimori et al. 2012a, 2014, 2018). Regarding of hydrological networks, none of the rivers in the HRS has permanent water. The principal rivers in this region are Kol and Mehran Rivers. Both of these river drainages belong to the big Persian Gulf basin and drains directly into the Persian Gulf near Fig.2. Distribution of warm springs in Hormozgan the Strait of Hormuz (Fig. 1). Rainfall in HRS is low Province (Based on Hormozgan Regional Water Company data). and irregular and streams are not always perennial, while Qanats and spring-stream systems are the Hormozgan region, which are located totally in important refuges for the fish species and also other the central and western parts of the Hormuzgan organisms (Coad 1996). Besides, the warm springs Province (Fig. 2). In general, the water temperature are one of the most common surface indicators of in these springs varies from 24 to 50°C. Moreover, geothermal resources in the HRS, and also surface the flow rate of these springs is largely different so water is often rich with salt and sulfur (Porkhial et al. that it differs from a minimum low value of about 2013). 0.2l/s to a maximum amount of warm water for According to the Hormozgan Regional Water Genow spring, which is more than 170l/s (Porkhial et Company data, there are at least 26 warm springs in al. 2013). Most of the springs have neutral pH, and 182 Teimori and Esmaeili - Hormuz River System as a micro hotspot of diversification for the aphaniid fishes in Iran

The tooth-carp fishes of the family Aphaniidae. The tooth-carp fishes (family Aphaniidae) belong to the fin-rayed fish, Order Cyprinodontiformes. Unlike the members of family Cyprinodontidae, which are distributed in the New World (North and South America), the family Aphaniidae is native to the Old World and widely distributed in the West Palearctic regions (Wildekamp 1993; Freyhof et al. 2017). To date, 44 tooth-carp species are discovered as valid in the Old World (Wildekamp et al. 1999; Coad 2000, 2009; Hrbek & Meyer 2003; Hrbek et al. 2006; Esmaeili et al. 2014b; Teimori et al. 2012a, 2014, Fig.3. Location of geothermal regions in Hormozgan Province (Based on Hormozgan Regional Water 2018). The high species diversity seems to be found Company data). in Southwestern Asia (Near East), particularly in the inland waters of the Anatolia and the Iranian Plateau. the others are slightly acidic. Also, Chloride (Cl) Therefore, these two regions are known as the hot content of the warm springs varies quite spot for the tooth-carp fishes in the world. considerably, ranging from 20 to 11180mg/l Generally, the members of the family Aphaniidae (Porkhial et al. 2013). are characterized by relatively a thick oval body, The previous study on the location of warm large to moderate cycloid scales, and superior mouth springs in the Hormozgan Province revealed that with tricuspid teeth. Some morphological almost all of them are related to salt domes especially characteristics of the genus are as follows; dorsal fin in its western parts (Porkhial et al. 2013). In many positioned somewhat posteriorly 8-14 branched rays, cases, each salt dome has a distinct warm spring (Fig. lateral line system present only on the head, and anal 3). It means that some of the salt domes have suitable fin with 8-15 branched rays. An important distinctive conditions to create a geothermal resource and for all of the aphaniid species is clear sexual geothermal fluids can reach the surface in every dimorphism. corner of salt dome. Also, there are several hot Ecologically, most species of these fishes are sulfuric springs such as; Genow at the north of small up to eight cm and tolerate a wide range of Bandar-e-Abbas (29°24'07.9˝N, 51°16'35.4˝W), temperature and salinity regimes (Wildekamp 1993; Khurgu (27°31'34.1˝N, 56°28'08.2˝W), Faryab our field observations). These ecological abilities (27°25'16.2˝N, 54°16'28.0˝W), Khamir (26°58' allow them to translocate via drainage shifting and 25.9"N, 55°32'26.8˝W). These springs provided promote survival of relict populations in restricted special extreme ecological conditions (i.e., high habitats (Echelle & Echelle 1992; Teimori et al. water temperature, more than 37°C, sulfuric water 2018). The most common mechanism of and high salinity) for the living of aquatic organisms diversification for the tooth-carp fishes is proposed to including fishes. Most of these habitats are inhabited be the allopatric isolation by which many species by the tooth-carp fishes (family Aphaniidae) have been evolved in the near east and the (Reichenbacher et al. 2009; Esmaeili et al. 2014a,b; neighboring regions (Hrbek & Meyer 2003; Hrbek et Teimori et al. 2012a, 2014, 2018) and two endemic al. 2006; Teimori et al. 2012b, c; Nasrolah cichlid fish, Iranocichla hormuzensis and I. persa Pourmoghadam et al. 2014; Ariyaee et al. 2018). The (Esmaeili et al. 2010, 2016, 2018; Schwarzer et al. particular examples are the evolution of the tooth- 2017). carp species inhabited the inland drainages restricted 183 Iran. J. Ichthyol. (June 2020), 7(2): 181-196

to the Zagros Mountains in Iran (Hrbek et al. 2006; Material examined: Aphanius darabensis: ZM-CBSU Esmaeili et al. 2014a, b; Teimori et al. 2012a, b, 9713, holotype, 1, 24mm SL. – ZM-CBSU 9601, 2018) and also those species in the central mountains paratypes, 68, 19–35mm SL; Iran, Fars prov.: Kol of the Anatolia (Hrbek & Meyer 2003; Hrbek et al. River drainage, Korsiah Banaki spring, 2002). 28°46'24.96''N, 54°23'35.48''W. – ZM-CBSU 8683, Moreover, some tooth-carp species are known to 19, 15–28mm SL; – ZM-CBSU 10871, 11, 13–23mm be evolved as a result of regressive phenomena. For SL; Iran, Fars prov.: Kol River drainage, Dasht-e- example, the various degrees of reduction or Konar wetland, 28°09'23.1''N, 55°18'17.5"W. complete absence of scales in the Anatolian Aphaniops dispar: ZM-SBUK 101, 14, 26.2– Aphanius asquamatus (Grimm 1980; Villwock 37.9mm SL; Djibouti, Lake Assal, 11°40'36.6″N 1964), the absence of pelvic fins in Aphaniops 42°27'17.2″ W. apodus from Algeria (Parenti 1981; Sienknecht Aphaniops furcatus: ZM-CBSU 225, holotype, 1, 1999), and the complete absence of scales in 21mm SL; ZM-CBSU 211, paratypes, 14, 18–25mm Aphaniops furcatus from the southern Iran (Teimori SL; Iran, Hormuzgan prov.: Shur River about 20km et al. 2014). The regressive evolution has also been East of Bandar Abbas, 27°19''37.6'N, 56°28''10.2' W. reported for fossil tooth-carps (Gaudant 1993). Thus, Aphaniops ginaonis: ZM-SBUK 221, 10, 23.4– in addition to the primarily vicariance-based 34.2 mm SL; Iran, Hormuzgan Prov.: Genow hot speciation, ecological factors have also promoted the spring, 27°26'77.2″N E56°17'97.0″W. speciation processes in the tooth-carp fishes (Hrbek Aphaniops hormuzensis: ZM-FISBUK 157, & Meyer 2003; Teimori et al. 2014). holotype 1, 35.8mm SL. – ZM-FISBUK 164, As all, among vertebrates, the members of the paratypes, 11, 22–34mm SL; Iran, Hormuzgan Prov.: family Aphaniidae represent an interesting model for Mehran River at Gotab village, 27°80'39.8''N the study of biodiversity, the evolutionary and even 54°150'46.1''W. evolutionary-development (evo-devo) processes Aphaniops stoliczkanus: ZM-FISBUK 130, 10, (e.g., Tigano et al. 2006; Rocco et al. 2007; Teimori 26.4–38.9mm SL; Iran, Fars prov.: Howba spring, et al. 2014, 2018; Zeinali & Motamed 2017; 27°57'30.5″N E53°53'58.4″W. – ZM-FISBUK 170, Iranmanesh & Motamedi 2018; Motamedi et al. 10, Iran, Bushehr Prov.: Dalaki hot spring, 2019a, b). 29°24'07.9″N 51°16'35.4″W. – ZM-FISBUK 173, A decade of our experience in the study of tooth- 10, 27.5–40.6mm SL; Khuzestan Prov.: Sartang carp fishes in Iran has shown that the HRS in spring, 29°24'07.9″N 51°16'35.4″W. – ZM-FISBUK southern Iran has surprising diversity for these fishes. 200, 16, 27.3–39.5mm SL; Oman, Muscat prov.: The present study aims to summarize this remarkable coastal lagoon, Seeb city, 23°40'19.6″N diversification and discuss the possible cause of 58°12'21.3″W. – ZM-FISBUK 220, 30, 26.6– diversification for the aphaniids in the HRS. It should 38.3mm SL; Iraq, Anbar prov.: Fallujah, be noted that here we only focused on two main river 33°45'28.8″N 33°21'14.4″W. drainages in the Hormuzgan region i.e., Mehran and Kol rivers. Results To date, 15 aphaniid species have been discovered Materials and Methods and reported from the Iranian drainage basins, which This study has been compiled mainly from the could be divided into two groups (Esmaeili et al. extensive field expeditions and a decade of works of 2014b). The first group belongs to the genus the authors on the diversification of tooth-carp fishes Aphanius (the inland- and inland related species in various drainage basins of Iran from 2004-2019. group) comprising 10 species i.e., A. arakensis 184 Teimori and Esmaeili - Hormuz River System as a micro hotspot of diversification for the aphaniid fishes in Iran

Fig.4. The distribution pattern of the five tooth-carp species in southern Iran. Aphanius darabensis, Aphaniops ginaonis, A. furcatus, and A. hormuzensis are distributed only in the Hormuz River System (HRS), while Aphaniops stoliczkanus shows a wide distribution in the southwest and southeast drainages of Iran. Teimori, Esmaeili, Gholami, Zarei, Reichenbacher, Paraphanius (Esmaeili et al. 2010). They are 2012; A. darabensis Esmaeili, Teimori, Gholami, prominently distributed along the coastal line of the Reichenbcaher, 2014; A. farsicus Teimori, Esmaeili, Persian Gulf in southern Iran. These four Aphaniops Reichenbacher, 2011; A. isfahanensis Hrbek, species are A. furcatus Teimori, Esmaeili, Erpenbek, Keyvani, Coad, 2006; A. kavirensis Esmaeili, Reichenbacher, 2014, A. ginaonis (Holly, 1929), Teimori, Gholami, Reichenbcaher, 2014; A. hormuzensis Teimori, Esmaeili, Hamidan, A. mesopotamicus Coad, 2009; A. pluristriatus Reichenbacher, 2018, and A. stoliczkanus (Day, (Jenkins, 1910); A. shirini Gholami, Esmaeili, 1872), and single species of the genus Paraphanius is Erpenbeck, Reichenbacher, 2014; A. vladykovi P. mento (Heckel, 1843). It should be noted that Coad, 1988 and A. sophiae (Heckel, 1849). The P. mento has been recorded from southwestern Iran, IIRAS group consists of one native border of Iran-Iraq (Wildekamp, 1993), but its (A. mesopotamicus) and nine endemic species. occurrence in this region has not yet been confirmed These species are distributed in nine River drainages/ by the current studies of authors. These five species or basins, including the Tigris (A. vladykovi) in the are distributed in six river drainages/basins i.e., the west; Karun (A. mesopotamicus) in the S-west; Hormuz River System (A. furcatus, A. ginaonis, and Namak Lake (A. arakensis) in the center towards the A. hormuzensis) in the south; Jaz Murian north; Esfahan (A. isfahanensis) in the central; Kavir (A. stoliczkanus) in the S-east; Karun (A. kavirensis) in the northeast; Kor River (A. shirini (A. stoliczkanus and P. mento) in the S-west; Makran and A. sophiae) and Maharlu Lake (A. farsicus) in the (A. stoliczkanus) and Mashkid (A. stoliczkanus) in S-west; Hormuzgan A. darabensis) and Mond River the S-east, and Persis (A. stoliczkanus) in the south (A. pluristriatus) in the south of Iran. (Fig. 4). The second group is the brackish water tooth- By considering the pattern of the geographic carps, consisting of two genera Aphaniops and distribution of Aphanius species among the Iranian 185 Iran. J. Ichthyol. (June 2020), 7(2): 181-196

Fig.5. The percentage of the tooth-carp species (A), and the endemic species (B) in each river drainage or basin of Iran. drainage basins, it was found that the HRS by having River (Fig. 4). It is morphologically characterized by four species demonstrated the highest diversity of the the following features; the total number of dorsal fin tooth-carp fishes among the other basins in Iran rays 11–15, the total number of anal fin rays 10–13, (22%, see also Fig. 5A). Among these four species, the total number of pectoral fin rays 13–18, the total one belongs to the genus Aphanius (i.e., number of pelvic fin rays 5–8, the number of gill A. darabensis), while three belong to the genus rakers 10–13, and the lateral line scale series 23–28. Aphaniops (i.e., A. furcatus, A. ginaonis and Among the IIRAS species, A. darabensis is closely A. hormuzensis). By considering the degree of related to A. shirini in terms of phylogeny (Esmaeili endemicity of the tooth-carps fauna relative to the et al. 2014). However, it is distinguished by a higher territorial boundaries of drainages, the HRS again has number of flank bars in males (9–18 in A. darabensis the highest endemicity among the other river vs. 7–10 in A. shirini). drainages/basins in Iran, in which 31% of the Iranian Like other tooth-carp species, A. darabensis endemic tooth-carps present only in this basin (Fig. shows external sexual dimorphism. Males with 5B). Below each species is explained briefly: vertical flank bars (Fig. 6A), females without bars but with one small oval to lozenge-shaped black spot at Aphanius darabensis Esmaeili, Teimori, Gholami, the central base of the caudal fin and irregularly Reichenbacher, 2014 (Fig. 6) arranged thin brown vertical patches on the flank Type locality: Korsiah Banaki Spring-stream system (absent in males) (Fig. 6B). (28°46'24.96''N, 54°23'35.48''W, altitude 1027 m), To date, this species has been collected in the Iran, Kol River (Hormuz River System). Hormuzgan Basin only from three sites restricted to Distribution status: Endemic to HRS. the Kol River drainage (Fig. 4). The first locality, Korsiah Banaki (near Darab city) has dried out due to کپورماهی ,(Common name: Kol tooth-carp (English the recent droughts since 2005, and attempts in 2012 .(Farsi) دنداندار کل، کپورماهی دنداندار داراب Remarks: Aphanius darabensis is the only member of and 2013 by the authors to find the species again have the IIRAS group in the Hormuzgan Basin, which has failed. At the other localities, i.e. Dasht–e–Konar been discovered from the most upper part of the Kol wetland southeast of Darab city) and Golabi spring 186 Teimori and Esmaeili - Hormuz River System as a micro hotspot of diversification for the aphaniid fishes in Iran

Fig.6. Fresh male, 42mm TL (A) and preserved female, 40.3mm TL (B) specimens of Aphanius darabensis.

Fig.8. Fresh specimens of Aphaniops furcatus, (A) male, 27.5mm TL and (B) female, 25.3mm TL. Type locality: Shur River (27°19'37.6"N, 56°28'10.2"W, altitude 2m), Iran, Hormuz River System. Distribution status: Endemic to HRS. Common name: Iranian scaleless tooth-carp .(Farsi) کپورماهی دنداندار بدون فلس ایرانی ,(English) Remarks: Aphaniops furcatus is the only scaleless tooth-carp species in Iran, which is mainly Fig.7. Cheshmeh Golabi in the most upper stream of recognized from all congeners by the complete the Kol River drainage, the habitat of Aphanius absence of scales and slightly forked caudal fin with darabensis. the upper lobe slightly longer than the lower lobe. near Darab city (Fig. 7), A. darabensis occurs in the Additionally, it is distinguished from its relatives by low number of individuals. Thus, care should be the considering the following combination of taken to conserve this population. Drought and characters: the total number of dorsal fin rays 9–12, introductions of alien fishes, particularly Gambusia the total number of anal fin rays 9–11, the total holbrooki and Neotropical convict cichlid, number of pectoral fin rays 12–15, the total number Amatitlania nigrofasciata, are major threats to this of pelvic fin rays 5–6, the number of gill rakers 12– endemic fish species. 16; males with dark pigmentation at the base of the four anterior dorsal rays; single row of tricuspid teeth Aphaniops furcatus Teimori, Esmaeili, Erpenbeck, with the two lateral cusps shorter than the middle Reichenbacher, 2014 (Fig. 8) one; reduction in biomineralization of caudal

187 Iran. J. Ichthyol. (June 2020), 7(2): 181-196

shallow water and white salty layers around and within the river (Fig. 9B). It has not yet been assessed in the list of IUCN’s Red Data Book, but it should be included due to the low individual abundance, and habitat alteration and pollution owing to the anthropogenic activities (Teimori et al. 2014, 2020).

Aphaniops ginaonis (Holly, 1929) (Fig. 10) The main data are based on Coad (1980, 2000); Reichenbacher et al. (2009); Teimori et al. (2014, 2018) (آب گرم گنو) Type locality: Genow hot sulfuric spring )27°26'28''N, 56°18'20''W, altitude 212m) north of Bandar Abbas, Iran, Hormuz River System. Distribution status: Endemic to HRS. Common names: Genow tooth-carp (English), .(Farsi) کپورماهی دنداندار گنو Remarks: Aphaniops ginaonis is the only known Aphanius species in Iran with only a single extant population. It is restricted to Genow hot sulfuric Fig.9. Khurgu hot sulfuric spring (A), and Shur River (B) in the Hormuz River System (HRS). Both are the spring on the north of Bandar Abbas (Fig. 11). The habitats of Aphaniops furcatus and Aphaniops general morphology is somehow similar to hormuzensis. The arrows indicate white salty layers A. hormuzensis but shows some differences. It is around and within the spring and river. distinguished by considering the following characters: the total number of dorsal fin rays 4–7, skeleton such as thin epural bone (Teimori et al. the total number of pelvic fin rays 5–7, the total 2014). Like other tooth-carp species, A. furcatus number of pectoral fin rays 13–17, the total number shows external sexual dimorphism. Males (Fig. 8A) of anal fin rays 6–10, the numbers of gill rakers 13– usually have 7–11 vertical flank-bars, their dorsal, 21, the numbers of lateral line series scales 25–32, anal, caudal, pelvic and pectoral fins are white but and the numbers of vertebrate 26-30. The most with dark pigmentation on the base of the 1st–4th diagnosable character in A. ginaonis is having the dorsal rays. Females (Fig. 8B) display 7–9 dark fewer total number of dorsal fin rays, 5–7 as opposed circular blotches on their flanks, starting behind the to 8–11in A. hormuzensis. operculum and extending until the base of the caudal Like other tooth-carp species, A. ginaonis shows fin. external sexual dimorphism. Females have a higher Aphaniops furcatus occurs ecologically in habitats mean number of anal fin rays, total vertebrae and with extreme environmental conditions such as flank bars, and longer pelvic fins (Coad, 1980). Khurgu hot spring (Fig. 9A) with low oxygen Esmaeili & Gholami (2007) found that female scales concentration, mineral warm and salty sulfuric water. were larger than those in males. The male dorsal fin Generally, the spring-system habitats are has 4-5 horizontal rows of spots, fading dorsally, characterized by hot sulfuric water, low dissolved while the dorsal fin pigmentation in females is weak. oxygen, and muddy bed with algae (Fig. 9A), while The pectoral fins of males carry pigment the seasonal riverine habitats are characterized by 188 Teimori and Esmaeili - Hormuz River System as a micro hotspot of diversification for the aphaniid fishes in Iran

Fig.10. Fresh specimens of Aphaniops ginaonis, (A) male, 43.4mm TL and (B) female, 39.2mm TL. concentrated on the rays, weakly speckled in females (Fig. 10). Fig.11. Genow hot sulfuric spring in the Hormuz This species was described by Holly (1929) from River System (HRS), the only natural habitat of Aphaniops ginaonis. the Genow spring (Fig. 11). The spring does lie in the Genow Protected area. The individuals are rare. Coad Distribution status: Endemic to HRS. (1980) listed this species as rare. However, it is Common names: Genow tooth-carp (English), .(Farsi) کپورماهی دنداندار هرمز considered as vulnerable under the revised IUCN Red List Categories according to Coad (1998). Remarks: This species was previously known as Reichenbacher et al. (2009) regarded this species as A. dispar, however, a recent study showed that a valid but endangered species. Since this location is A. dispar is not distributed in Iran anymore, and under reconstruction almost every year and is species is A. hormuzensis (Teimori et al. 2018). Its available to the local people for the medical prepuce, morphological characters are as follows; the total therefore, the population is under risk and more number of dorsal fin rays 9-10, the total number of attention should be paid for its conservation. anal fin rays 9-10, the total number of pectoral fin rays 15-16, the total number of pelvic fin rays 7-8 Aphaniops hormuzensis Teimori, Esmaeili, rays, The numbers of gill rakers 14-16, the numbers Hamidan, Reichenbacher, 2018 (Fig. 12) of lateral line series scales 17, Scales along the flank Type locality: Mehran River, Gotab village, 15 km 26-29. o o south of Bastak (27 08'39.8"N, 54 15'46.1"W, Aphaniops hormuzensis is also distinguished from altitude 330 m), Iran, Hormuz River System. its relative (i.e., A. dispar species group) by the 189 Iran. J. Ichthyol. (June 2020), 7(2): 181-196

around eyes, small and denser than opercular pigments; all fins hyaline. In the male, body coloration dark brown, dorsal surface of the head and upper flank dark brown; belly and ventral part of head whitish-cream; 13 light vertical flank bars from the insertion of the pectoral fin to base of the caudal fin, no spots between bars. The histomicroscopy and normal anatomy of the major body organ systems in the adult of A. hormuzensis was studied by Motamedi et al. (2019a). The recent studies also revealed high regeneration ability in the A. hormuzensis for repairing the injured or missing organs such as fin rays and kidney (Zeinali & Motamed 2017; Iranmanesh & Motamedi 2018). In the Hormuz River System, A. hormuzensis occurs mainly in two types of habitats, i.e. brackish Fig.12. Fresh specimens of Aphaniops hormuzensis. rivers of exorheic drainages and hot sulfur springs. In (A) male, 36.8mm TL and (B) female, 32.4mm TL. both habitat types, A. hormuzensis can be found sympatrically with A. furcatus and also two endemic combination of the fish coloration (in males) and a cichlids, Iranocichla hormuzensis and I. persa unique combination of otolith characters. The males (Esmaeili et al. 2016; Schwarzer et al. 2017) (see also have 13–17 vertical light flank bars and two crescent- Fig. 9). shaped dark brown stripes on the caudal fin. Otoliths Two main river drainages are known in the HRS are rounded-trapezoid to rounded-triangular with a i.e., the Mehran River drainage, and the Kol River rounded or relatively straight dorsal rim and no drainage (Fig. 13). Aphaniops hormuzensis is found dorsal tip; the rostrum and antirostrum are relatively in both river drainages. However, the populations short and terminally rounded, the rostrum is slightly from these two river drainages show genetically a bit longer than the antirostrum. Also, it has a slightly variation. This is also true in the case of Iranocichla higher overall number of vertebrae (27–28) and more population distributed in this region (Esmaeili et al. caudal vertebrae (16) than A. dispar (24–25 and 13, 2016; Schwarzer et al. 2017). respectively) and A. richardsoni (26 and 15, respectively). Aphaniops hormuzensis is Discussion distinguished from A. kruppi by having 5–6 scale The HRS is a particular example of a region with rows on caudal-fin base (vs. 2–3 in A. kruppi), and diverse environmental variability. It is from A. ginaonis by having higher numbers of dorsal geographically situated along the coastal line of the fin rays (8–11 vs. 5–7). Persian Gulf and the Strait of Hormuz in southern Like other tooth-carp species, A. hormuzensis Iran. Almost all of the hot (and warm) springs in this shows external sexual dimorphism (Fig. 12). In the region are related to salt domes. The strong females, the ccoloration of the dorsal surface of the evaporation during the summertime seems to be head and upper flank dark brown; belly and lower another reason for the high concentration of salts (Ca, head whitish-cream; flank with 15-17 narrow dark Mg and Na) in this region. Also, almost all of the brown bars; dark brown pigments on the snout and mineral sub-ground springs in Hormuzgan are 190 Teimori and Esmaeili - Hormuz River System as a micro hotspot of diversification for the aphaniid fishes in Iran

Fig.13. Two main river drainages in the HRS. (A) Kol River drainage and (B) Mehran River drainage. surrounded by the mountains and salt hills and, species when populations become isolated (Teimori therefore, provided a high number of mineral et al. 2018). elements in the riverine system and particularly in the Several tooth-carp species have been evolved in hot springs. this basin owing to genetic drift, founder effects and Occurring of different extreme aquatic local adaptation to specific extreme environmental environments such as the hot sulfuric springs, conditions (Coad, 1980, 1998; Barton & brackish water (or high-salinity) rivers, coastal Charlesworth 1984; Teimori et al. 2014, 2018). lagoons and rivers, and also freshwater river and Aphaniops hormuzensis has underlined to be evolved spring-stream system in Hormuzgan have provided a as a result of ecological alternation and local habitat suitable condition for the ecological divergence of isolation in the river drainages of the HRS (Teimori the fish populations particularly the tooth-carps et al. 2018). The populations of A. hormuzensis in the (Esmaeili et al. 2010, 2016; Teimori et al. 2012a, HRS inhabit various environments consisting of 2014, 2018). Also, the active geologic history of the urban systems, salt marshes and estuaries along the land since the late Pliocene and Pleistocene (Hatzfeld coast of the Strait of Hormuz and also the inland et al. 2010) has created many unusual and isolated systems such as brackish water rivers and hot sulfuric habitats in this region. The habitat isolation and springs. Also, A. furcatus is another endemic species, ecological condition in Hormuzgan increased the which is living sympatrically with A. hormuzensis in species diversity (Esmaeili et al. 2010) and promote the water bodies of the Hormuzgan (Teimori et al. the population divergence (Teimori et al. 2012a, c, 2014, 2018). It is suggested to be evolved owing to 2018). the long colonizing of the ancestral population to Typically, the tooth-carp species are characterized extreme ecological conditions (high salt and sulfur by the high degree of adaptability to diverse habitats, concentration in water, low dissolved oxygen high morphological variability as well as high concentration, high water temperature) in the studied population divergence rates (e.g., Ferrito et al. 2007; region (Teimori et al. 2014). In addition to Khurgu Buj et al. 2015; Cavraro et al. 2017). Also, they have and Faryab sulfuric springs, which are home to the a remarkable capacity to adapt to adverse A. furcatus and A. hormuzensis (Teimori et al. 2014, environmental conditions and evolve into new 2018), Genow hot sulfuric spring is additional 191 Iran. J. Ichthyol. (June 2020), 7(2): 181-196

extreme habitat, which is located geographically Paraschistura naumanni (endemic Nemacheilidae). close to Khurgu (about 30 km), and home to another According to the report of the Department of endemic tooth-carp, A. ginaonis (Coad, 1980, 1998; Environment in Hormuzgan (2015), the other Reichenbacher et al. 2009). Water parameters biodiversity in this basin consisting of the aquatic and measured by Reichenbacher et al. (2009) for this terrestrial mammals (40 species), the native and habitat in February and August 2008 were close to migratory birds (308 species), reptiles (40 species), Khurgu spring (water temperature 35°C, pH 7.78, and marine fish (more than 423 species). This and conductivity 8,000μS cm−1). The water in Genow considerable diversity in a semi-desert region such as Spring is greenish and often has a strong sulfur odour, Hormuzgan shows that this small geographic region and the stream bed is mostly covered by stones, had a successful history of speciation in the past. The pebbles, and cyanobacteria (see also Reichenbacher most important evolutionary forces in this basin may et al. 2009). include the active geological history such as As a conclusion, the active geological history, the vicariance events during the last glacial maximum local allopatric divergence of the populations, and (21000-18000 BP), the Early Holocene sea-level rise, extreme environmental conditions could be and the local geological activities within the considered as the main factors responsible for the Hormuzgan. All these events have provided the diversification of the tooth-carp fishes in the HRS. current diversification in the HRS. Since the members of the tooth-carp fishes display a high capacity to shift between the various ecological Acknowledgements conditions, therefore, they could be particularly The authors would like to thank all the volunteers, attractive for biologists to study various biological especially past and current students from Shahid aspects such as phenotypic variation and plasticity, Bahonar University (Ichthyological Lab) of Kerman species diversity, zoogeography, evolutionary and Shiraz University (Ichthyology and Molecular processes. Besides, they have demonstrated a Systematics Research Laboratory). desirable potential for tissue regeneration (Zeinali & Motamedi 2017; Iranmanesh & Motamedi 2018; Funding Motamedi et al. 2019). This work was supported financially by Shahid Bahonar University of Kerman (SUBK) and Shiraz Conclusion University. The Hormuz River System (HRS) in southern Iran is the only region in Iran that is home to four species of References tooth-carps genera Aphanius and Aphaniops. In Ariyaee, M.; Hamidian, A.H.; Eagderi, S.; Ashrafi, S. & addition to the tooth-carp fishes, which show a high Poorbagher, H. 2018. Cadmium and arsenic endemicity in the HRS, the other fish groups also bioaccumulation and bio-concentration in the show well-known diversity. More than 28 fish endemic toothed carp Aphanius arakensis in salt species have been recorded from the HRS, in which water. International Journal of Aquatic Biology 6(1): 25-30. eight species are endemic to this basin. Examples are Barton, N.H. & Charlesworth, B. 1984. Genetic I. hormuzensis and I. persa (Cichlidae); revolutions, founder effects, and speciation. Annual Acanthobrama persidis and Garra persica (endemic Review of Ecology and Systematics 15: 133-164. Cyprinidae); Arabibarbus grypus, Carassobarbs Buj, I.; Miočić-Stošić, J.; Marčić, Z.; Mustafić, P.; luteus, Luciobarbus barbulus, Cyprinion watsoni, Zanella, D.; Mrakovčić, M. &. Ćaleta, M. 2015. Capoeta saadii (all native cyprinids); Population genetic structure and demographic history Mastacembemus mastacembelus (native eel fish) and of Aphanius fasciatus (Cyprinodontidae: 192 Teimori and Esmaeili - Hormuz River System as a micro hotspot of diversification for the aphaniid fishes in Iran

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195 Iran. J. Ichthyol. (June 2020), 7(2): 181–196 Received: February 20, 2020 © 2020 Iranian Society of Ichthyology Accepted: June 24, 2020 P-ISSN: 2383-1561; E-ISSN: 2383-0964 http://www.ijichthyol.org

مقاله پژوهشی سیستم رودخانه هرمز به عنوان یک نقطه داغ تنوع زیستی برای کپورماهیان دنداندار ایران

* آزاد تیموری 1، حمیدرضا اسماعیلی2 1بخش زیستشناسی، دانشکده علوم، دانشگاه شهید باهنر کرمان، کرمان، ایران 2آزمایشگاه تحقیقات ماهیشناسی و سیستماتیک مولکولی، بخش جانورشناسی، گروه زیستشناسی، دانشکده علوم، دانشگاه شیراز، شیراز، ایران.

چکیده: سیستم رودخانه هرمز )HRS( در دشت ساحلی جنوبی کوههای زاگرس واقع شده است. دو حوضه آبریز اصلی رودخانهای یعنی مهران و کل از این منطقه شناخته شده است که مستقیماً به خلیج فارس تخلیه میشوند. سیستم رودخانه هرمز از نظر کپورماهیان دنداندار )خانواده Aphaniidae( تنوع شگفت انگیزی دارد. پژوهش حاضر با هدف برجسته سازی این تنوع قابل توجه و بحث در مورد علت احتمالی تنوع کپورماهیان دنداندار در این سیستم رودخانهای انجام شده است. تاکنون 15 گونه از کپورماهیان دنداندار از حوضههای آبریز ایران کشف شده است. از بین آنها، 10 گونه متعلق به جنس Aphanius، چهار گونه متعلق به جنس Aphaniops و یک گونه واحد متعلق به جنس Paraphanius است و از این لحاظ، سیستم رودخانه هرمز با داشتن چهار گونه )٪22( بیشترین تنوع را نسبت به سایر حوضههای ایران نشان میدهد. از این میان، یک گونه متعلق به جنس A. darabensis) Aphanius) و سه گونه متعلق به جنس A. ginaonis ،A. furcatus) Aphaniops و .A hormuzensis( میباشد. سیستم رودخانه هرمز با در نظر گرفتن میزان بومزاد بودن فون کپورماهیان دنداندار نسبت به حوضه های آبریز نواحی مجاور، باالترین میزان

بومزادی را داراست، به طوری که 31٪ از گونه های بومزاد کپورماهیان دندان دار ایرانی فقط در HRS وجود دارد. آخرین اتصال حوضه مکران با HRS مربوط به اواخر

پلیوسن و پلیستوسن در حدود 8/1 میلیون سال پیش است. همچنین، سایر وقایع مبتنی بر ویکارینس مانند حوادث مربوط به آخرین یخچالهای طبیعی )18000-21000

BP(، مهاجرت جمعیت ماهیان در اوایل افزایش سطح دریا مربوط به هولوسن و نیز از هولوسن تا به امروز باعث افزایش تمایزهای درون و بین گونه ای کپورماهیان دنداندار شده است. همچنین، وضعیت زمینشناسی HRS شرایط محیطی متنوعی را فراهم کرده است که باعث افزایش قابل توجه تنوع گونههای کپورماهیان دنداندار شده است. کلماتکلیدی: آفانیوس، آفانیوپس، پارآفانیوس، شرایط اکولوژیکی سخت، تاریخ زمین شناسی.

196