. J. Ichthyol. (September 2015), 2(3): 133-147 Received: February 26, 2015 © 2015 Iranian Society of Ichthyology Accepted: July 30, 2015 P-ISSN: 2383-1561; E-ISSN: 2383-0964 doi: http://www.ijichthyol.org

Review Article

Review of the and pipefishes of Iran (Families Gasterosteidae and Syngnathidae)

Brian W. COAD

Canadian Museum of Nature, Ottawa, Ontario, K1P 6P4 Canada. Email: [email protected]

Abstract: The systematics, morphology, distribution, biology, economic importance and conservation of the sticklebacks and pipefishes of Iran are described, the are illustrated, and a bibliography on these is provided. There are two sticklebacks (Gasterosteus aculeatus, an exotic, and platygaster, a native) and one native pipefish (Syngnathus caspius), the natives found in the basin and the exotic in that basin and adjacent basins. The family Gasterosteidae is characterised by a compressed, fusiform body, teeth in bands in each jaw but none on the tongue or palate, a protractile mouth, 3 branchiostegal rays, no postcleithrum, no scales but a series of plates along the flank variably developed, sometimes absent, 2 or more (usually 3-16) isolated spines in front of a soft dorsal fin (usually 6-14 rays), and a pelvic fin with a strong spine and only 0-2 soft rays. The body of pipefishes of the family Syngnathidae is characteristic, being very thin and very elongated, and enclosed in bony rings as a form of armour. The body is divided into a trunk and a tail, the tail being prehensile in seahorses. The first trunk ring has the pectoral fin base and the last has the anus in it. The snout is elongated with a small toothless mouth at the tip. Gills are tufted and the gill opening is small. There are 1-3 branchiostegal rays. There is a single dorsal fin without spines, the pelvic fins are absent and the pectoral, anal and caudal fins may be absent too. The caudal is always small when present. The anal fin is always small with only 2-6 rays. Those without a caudal fin may have the tail prehensile, able to grasp and hold onto objects.

Keywords: Biology, Morphology, Gasterosteus, Pungitius, Syngnathus.

Introduction spiny eels and milkfishes (Coad 2015a, b). The freshwater ichthyofauna of Iran comprises a diverse set of families and species. These form Family Gasterosteidae important elements of the aquatic ecosystem and a Sticklebacks are found in marine and fresh waters of number of species are of commercial or other the cooler parts of the Northern Hemisphere. There significance. The literature on these fishes is widely are about 5 genera with about 18 species (Eschmeyer scattered, both in time and place. Summaries of the & Fong 2011) of which one is native to Iran and morphology and biology of these species were given another has been introduced. in a website (www.briancoad.com) which is updated This family of small fishes is characterised by a here, while the relevant section of that website is now compressed, fusiform body, teeth in bands in each closed down. Other families will also be addressed in jaw but none on the tongue or palate, a protractile a similar fashion as done for catfishes (Coad 2014), mouth, 3 branchiostegal rays, no postcleithrum, no 133

Iranian Journal of Ichthyology (September 2015), 2(3): 133-147

Fig.1. Line drawing of Gasterosteus aculeatus by S. Laurie-Bourque. scales but a series of plates along the flank variably of three isolated strong spines in front of the soft developed, sometimes absent, 2 or more (usually 3- dorsal fin, the body usually has strong bony scutes 16) isolated spines in front of a soft dorsal fin (usually along the flank developed as a keel on each side of 6-14 rays), and a pelvic fin with a strong spine and the caudal peduncle, a strong spine in the pelvic fin, only 0-2 soft rays. and a complex reproductive behaviour. The species in this family have been studied The threespine , and related extensively (Coad 1981; Paepke 1983; Wootton populations which act as good species but have not 1976; 1984; Paepke in Bănărescu & Paepke 2002). been formally named, have been studied extensively Coad (1987, 1998) and Coad & Abdoli (1996) place for their reproductive and other behaviours and for the species in context with the Iranian ichthyofauna. the insights that morphological variation and genetics There is variation in colour, body form, spine throw on evolution. numbers and development, and plate numbers. These variations in anatomy are matched by variations in Gasterosteus aculeatus Linnaeus, 1758 biology such as habitat, feeding and reproduction. (Figs. 1-2) Variation in behaviour, biology and in speciation Common names: Seh khar (= threespine), seh khareh makes these small fishes, which have little or sehkhareh, mahi seh khareh. [trekhiglaya commercial value, particularly important. Some of kolyushka or threespine stickleback in Russian; the variation is owing to environmental factors while threespine stickleback]. some has a genetic basis. Several books have been Systematics: Gasterosteus aculeatus was originally devoted to them and thousands of scientific studies. described from Europe. The complex systematics of Sticklebacks make excellent aquarium fishes. Their sticklebacks is not reviewed here. The Iranian reproductive behaviour is complex, involving specimens appear to be of a "marine" form with well- courtship and nest building. Some populations are developed scutes on the flanks but their origin is not wholly marine, freshwater resident, or are known. Krupp & Coad (1985) describe a Syrian anadromous and enter fresh water to breed. population with a low number of lateral plates. Key characters: The 3 strong dorsal spines, strong Genus Gasterosteus Linnaeus, 1758 pelvic fin spine with a single cusp at the base and the This genus is characterised by having a modal count row of plates along the flank are distinctive.

134 Coad-Review of the Sticklebacks and Pipefishes of Iran

Fig.2. Gasterosteus aculeatus, Astara Shore, October 2009, courtesy of K. Abbasi.

Morphology: First dorsal fin is comprised of usually flanks than freshwater ones which are more olive. 3 spines (2-4), second dorsal fin with 1 spine and 7- Generally the back is green-brown, olive or grey to 14 soft rays, anal fin with 1 spine and 6-13 soft rays, blue-black, flanks olive to silvery and the belly pectoral fin with 8-11, usually 10, branched rays and silvery-white. Fins are generally clear. The pelvic fin with 1 spine and 1 soft ray. Gill rakers peritoneum is silvery with large, widely spaced number14-27, are elongate and reach as far as the melanophores. Stream-dwellers have an irregular fourth adjacent raker when appressed. Vertebrae 27- pattern of dark spots on the flanks and the back is an 36. Plates along the flank 30-37; the Iranian iridescent dark green. specimens having a complete row of flank plates and Size: Reaches 11.0cm. a well-developed caudal peduncle keel, other Distribution: Found around the Northern Hemisphere populations may have an incomplete row or no plates in fresh and marine waters including Syria and at all. This species is very widespread and extremely Turkey in Southwest Asia. Reported as an variable over this range in the characters listed above introduction to Iran by Abdoli (1993a, b), Coad & and may well exceed the limits cited, e.g., dorsal fin Abdoli (1993) and Coad (1994, 1996) and widely spines are absent in some but the Iranian fish are recorded since, this species is found at the Neka of the typical marine form. The chromosome number Power Plant in Mazandaran near Behshahr, the Tajan is 2n=42 (Klinkhardt et al. 1995). The gut is short and River, the lower Gorgan River and Gorgan Bay, S-shaped. Qareh Su, Bandar-e Torkeman, Gomishan Lagoon, Two Iranian specimens had 3 dorsal fin spines the lower Babol, Haraz, Chalus, Tonekabon, and 10 or 11 soft rays, 1 anal fin spine and 7 soft rays, Langarud, Talar, Shirud, Shafa, Polarud and Safid 10 pectoral fin rays and 1 spine and 1 soft ray in the rivers, the Anzali Lagoon and the southeast Caspian pelvic fin. Scutes, including those forming the caudal Sea, the Astara Shore (K. Abbasi - see photograph peduncle keel, numbered 30 or 32. Total gill rakers above), the middle to upper Kashaf River in numbered 19 or 26. Khorasan in the Hari (= Tedzhen) River basin, and Sexual dimorphism: Breeding males develop a red the upper Kal Shur and upper Jomein rivers in the belly and throat, blue sides, light blue back and have Dasht-e Kavir basin (Abbasi et al. 1999; Kiabi et al. bright blue or turquoise eyes. 1999; Abdoli 2000; K. Abbasi, pers. comm. 2001; Colour: Marine populations are more silvery on the Esmaeili et al. 2003, 2010, 2014; Mostafavi & Abdoli

135 Iranian Journal of Ichthyology (September 2015), 2(3): 133-147

2003; Jolodar & Abdoli 2004; Naderi & Abdoli & Paepke (2002) is a recent review of literature. 2004; Niksirat et al. 2006; Mostafavi 2007; Banagar Niksirat et al. (2010) found stomach contents in the et al. 2008, 2009; Abdoli & Naderi 2009). southeast Caspian Sea comprised gammarids, Nereis Zoogeography: The exotic origin of the Iranian sp., chironomids, fishes, oligochaetes, fish eggs and population is not known but the complete row of hirudineans. Gammarids dominated in December and plates suggests a marine population. Sal'nikov (1995) January and were replaced by Nereis in February. reports this species from the southeastern Caspian The preference shifted to chironomids in July and to Sea and moving into the River in Turkmenistan fishes in October. in large numbers. He refers to it as the Black Sea- Reproduction: Spawning occurs from April to Azov three-spined stickleback but it is unclear October, varying with locality over the wide range of whether by this is meant its origin, its dispersal route this species. The male parental cycle at one site in or simply the nearest natural habitat for the species. Canada lasts 9-15 days with female interspawning Habitat: These sticklebacks inhabit inshore coastal intervals of 19 days. Males and females only waters, lakes, ponds, rivers and streams, and may be complete one spawning here, though laboratory anadromous. Marine and lake fish can be pelagic. studies show males capable of 5 reproductive cycles They are often found among algae. In Iran, this and females of producing a clutch of eggs every 3-4 species is caught at 30-100m by herring fishery ships days. Harsh physical conditions are probably the (K. Abbasi, pers. comm. 2001). cause. The male builds a barrel-shaped nest in Age and growth: Maximum life span is a little over 3 shallow, sandy areas from plant fragments glued years although some fish probably live only 1 year together on the bottom with kidney secretions. The and a few months, dying after they spawn. Paepke in nest is in an open area but near vegetation. The nest Bănărescu & Paepke (2002) is a recent review of has an opening at each end. The male has a complex literature. courtship dance with zig-zag motions and a leading Esmaeili & Ebrahimi (2006) give a significant motion to the nest. A responsive female adopts a length-weight relationship based on 500 Iranian fish submissive head up position, which also reveals the measuring 3.6-7.2cm standard length. The α-value egg-swollen belly. The male pokes his snout at the was 0.0090 and the b-value 3.428 (a b-value < 3 nest to indicate its position to the female, tipping his indicating a fish that becomes less rotund as length head sideways to display the bright red throat. The increases and a b-value >3 indicating a fish that male jabs the female with his snout through the nest becomes more rotund as length increases). Patimar et wall after she enters to stimulate egg release. He then al. (2010) studied this exotic in the Gomishan follows the female through the nest to fertilize the Wetland of the southeast Caspian Sea. Maximum eggs and drives the female away. Several females ages were 2+ years for males and 3+ years for females, may spawn in one nest which can contain up to 1026, and the length-weight relationship was yellowish 1.8mm diameter eggs. The male guards W=0.0042TL3.711 for immature fish, 0.0095TL3.1328 and fans the eggs and guards the fry. for males and 0.0075TL3.4678 for females. The sex Patimar et al. (2010) in their study on the ratio was 1:2.63 in favour of females. Gomishan Wetland found reproduction to occur in Food: Food is various crustaceans, aquatic and March-June, peaking in April. Large yolk-filled eggs terrestrial insects, snails, worms, fish eggs and fry with a mean diameter of 1.317mm (maximum (including their own species), and a wide variety of 1.96mm) numbered 128-885. Small white opaque other available organisms taken both on the bottom eggs were also found in the ovaries with a mean or pelagically. Copepods and chironomids tend to diameter of 0.549mm and numbered 311-4709. The dominate as food items. Again Paepke in Bănărescu mean absolute fecundity was 1241.69 eggs and mean 136 Coad-Review of the Sticklebacks and Pipefishes of Iran

Fig.3. Line drawing of Pungitius pungitius by S. Laurie-Bourque. relative fecundity was 535.24 eggs/g body weight. recently recorded exotic species in Iran, it is still Niksirat et al. (2010) found the breeding season in the comparatively rare but should not be accorded any southeast Caspian Sea began in March and lasted 5 status. The spread of this exotic species should be months. Condition factor, somatic condition factor monitored and its effects on native fishes observed. and hepatosomatic index increased at the beginning Sources: Further details on collections examined can of the spawning season and decreased as it be found in the museum catalogues. progressed. Iranian material: CMNFI 1993-0144, 1, 57.3mm Parasites and predators: Niksirat et al. (2006) record standard length, Mazandaran, Neka Power Plant Corynosoma strumosum in this species from the (36º51'48"N, 53º23'24"E); CMNFI 2008-0226, Iran, Gomishan Lagoon and Hosseinifard et al. (2010) the 1, 40.2mm standard length (no other locality data). acanthocephalan Bolbosoma caenoforme from fish in Comparative material: CMNFI 1981-0611, 124, the Shazdeh River, Babolsar. Many fishes and birds, 44.4-63.1mm standard length, Turkey Iznik Gölü and even snakes, seals and small mammals, feed on (40º26’N, 29º30’E); CMNFI 1983-0202, 5, 27.1- sticklebacks despite their protective spines which are 45.0mm standard length, Syria, headwaters of Nahr locked erect when they are disturbed. Sūrit (35º15’N, 35º58’E). Economic importance: The threespine stickleback has received much attention for its evolutionary Genus Pungitius Coste, 1848 interest, behaviour and utility as an experimental fish. This genus of sticklebacks is found in North America They may be predators on fish eggs and larvae, and and Eurasia with about 3-5 species (opinions vary) competitors for food, of more commercially but only one in Iran (Paepke in Bănărescu & Paepke important species. The Baltic Sea area has had 2002). It is distinguished by a series of 7-12 small sufficient numbers to support an oil extraction spines (much smaller than in the genus Gasterosteus) industry (Paepke in Bănărescu & Paepke 2002). In in front of the dorsal fin, arranged alternately to the the Iranian parts of the Caspian Sea this exotic may left and right, the pelvic fin has 1 spine and 0-1 soft compete with juvenile sturgeons for food and its rays, and the skin is naked or has small bony plates spread may account for the disappearance of the in a row along mid-flank. native Pungitius platygaster (Niksirat et al. 2010). Conservation: Lelek (1987) classifies this species as Pungitius platygaster (Kessler, 1859) intermediate to rare, locally vulnerable in Europe. (Figs. 3-4) The IUCN (2014) lists it as of Least Concern. As a Common names: Nohkhar or nokhareh (= ninespine), 137 Iranian Journal of Ichthyology (September 2015), 2(3): 133-147

Fig.4. Pungitius pungitius, Anzali Shore, May 2012, courtesy of K. Abbasi. mahi seh khareh nama (= threespine-like fish), mahi and Keivany et al. (1997) recognise P. platygaster as khardar (= spiny fish). [tikan balig in Azerbaijan; a distinct species since it is 100% distinguishable malaya yuzhnaya kolyushka or southern ninespine from other species in the genus. However, Keivany stickleback in Russian; Ukrainian stickleback]. & Nelson (2004) found that P. platygaster lay within Systematics: Gasterosteus platygaster was originally a polychotomy with subspecies of P. pungitius. described from Odessa and Aleshki on the Dnieper in Pungitius platygaster is retained as a full species until the Ukraine. Gasterosteus pungitius var. Kessleri the two taxa come into contact naturally, which will Yakovlev, 1870 and Gasterosteus pungitius var. test the hypothesis of Ziuganov & Gomeluk (1985). niger Yakovlev, 1870 both from lakes near Key characters: The small spines usually alternating Astrakhan, Volga River delta, Russia, Gasterosteus left and right in front of the dorsal fin are distinctive. platygaster var. caucasicus Kessler, 1877 from Morphology: This species is characterised by 22-34 Transcaucasia, and Pygosteus platygaster nuda Berg, bony plates along the flank, perhaps a response to 1905 from Lake Charkhal in the Ural River valley, predators (Ziuganov & Gomeluk 1985). The first 4- are synonyms. Syntypes of the latter are in the 12 plates are large (Keivany & Nelson 1998). There Zoological Institute, St. Petersburg (ZISP 10613) is no caudal peduncle keel. The plates in young fish (Eschmeyer et al. 1996; Kottelat 1997). are minute fragments of bone and difficult to see, Münzing (1969) retains this taxon as a distinct especially posteriorly. The body form is less elongate species but suggests that it may only be a subspecies than the related Pungitius pungitius. Dorsal fin spines of Pungitius pungitius (Linnaeus, 1758). Ziuganov & slightly curved, 7-11 (in Iranian specimens 8(7), Gomeluk (1985) studied hybridisation of this species 9(11)) and branched rays 6-11, anal branched rays 6- and P. pungitius under experimental conditions and 10, pectoral fin rays 9-11 (usually 10), and pelvic fin consider that they are at most subspecifically distinct. with 1 serrate spine and 0-2 soft rays, usually 1. They found 9 out of 19 morphological characters Rarely up to 4 dorsal fin spines may follow the distinguish this species from P. pungitius as well as a midline and not alternate markedly in Iranian fish. differing ecology. However there were no The last spine in the series is usually slightly longer ethological, nor presumably genetical, isolating than the others. Vertebrae number 29-31 (in Iranian mechanisms since F3 hybrids were fertile. Ziuganov specimens 29(9), 30(9)) and gill rakers 7-13, (1991), Keivany (1996), Keivany & Nelson (2004) reaching the base of the second raker below when

138 Coad-Review of the Sticklebacks and Pipefishes of Iran

appressed. The gut is short and S-shaped. The (Fortunatova 1961) although a few fish may reach 3 chromosome number is 2n=42 (Klinkhardt et al. years and maturity may be attained shortly before 1995). reaching 1 year (Paepke in Bănărescu & Paepke Sexual dimorphism: Colour at breeding is the most 2002). evident sexual dimorphism. Food: Diet is small invertebrates including Colour: Females are olive with greenish-brown chironomids. Eggs of commercially important fishes stripes, patches and mottling even during spawning. may be eaten. Males are jet black and develop a blue-white colour Reproduction: Reproduction can occur at high on the posterior side of the ventral spines as a temperatures, e.g., 28°C, at which eggs of stimulus for leading the females. The specimens P. pungitius die. Spawning begins at 17°C. In the described as var. kessleri were light grey and var. Volga delta spawning begins in late April and niger were black, perhaps non-spawners and continues to the middle of June but is most intensive spawners. The peritoneum is silvery. in the middle of May. Dense schools are formed Size: Attains 7.0cm standard length. which disperse after spawning with the fish Distribution: Found in the Black, Caspian and Aral becoming secluded in the heavy vegetation which seas and their basins. Reported from the southeast develops at this time (Fortunatova 1961). Fecundity Caspian Sea, southwest Caspian Sea and south- is up to 90 eggs. Males build nests out of the remains central Caspian Sea, the Anzali Mordab and Pir of the previous year's vegetation glued together with Bazar Roga, Ameerkalaye Lagoon near Lahijan, kidney secretions (Fortunatova 1961). A female Boojagh Wetland, and lower reaches of rivers such indicates readiness to spawn by a head-up posture as the Safid, Shakhzaderud (lower Babol), lower near the nest. The male performs a zig-zag dance and Karasu, Sheikan and Gorgan (Derzhavin 1934; leads the female to the nest entrance by angling his Holčik & Oláh 1992; Nejatsanatee 1994; Abbasi et head down at 60°, flashing his blue-white pelvic al. 1999; Kiabi et al. 1999; Khara et al. 2004, 2005; spines and moving by short jerks. The female enters Naderi & Abdoli 2004; Nezami & Khara 2004; the nest, the male taps her caudal peduncle to Abdoli & Naderi 2009). Keivany (1996) considers it stimulate egg deposition, she leaves and the male to be rare on the southern Caspian Sea coast. Jolodar enters the nest to fertilize the eggs. The leading part & Abdoli (2004) report it from brackish portions of takes only 10 seconds. Males guard the young for the Caspian Sea and rivers falling into it, being more several weeks after spawning. numerous in the Gomishan Lagoon. Parasites and predators: The Caspian seal, Pusa Zoogeography: Pungitius platygaster aralensis caspica, is a predator on this species (Krylov 1984) (Kessler, 1877) is reported from the western Uzboi as are such fishes as Perca fluviatilis, Esox lucius, lakes in Turkmenistan (Shakirova & Sukhanova Silurus glanis, Aspius aspius and Sander lucioperca 1994) and with canal construction projects may (Fortunatova 1961) and Neogobius melanostomus, ultimately reach the Caspian Sea basin. water snakes, pond turtles, frogs and fish-eating birds Habitat: Described as a benthivore living a cryptic (Ziuganov 1991). life in weed beds (Ziuganov & Gomeluk 1985). It can Economic importance: None; although Paepke in be found in fresh, brackish and marine waters. Bănărescu & Paepke (2002) consider it important as Age and growth: In the Volga delta, mature adults are a predator on mosquito larvae (and hence a biological 3.2-5.8cm long (mean 4.0cm) from April to July and control for malaria) in smaller water bodies. young-of-the-year are 1.2-2.8cm long (mean 2.3cm). Conservation: Holčík & Oláh (1992) report the loss Life span appears not to exceed 2 years as only of this species from the Anzali Mordab, where it was sexually mature adults are caught in spring once abundant, through a change in the environment 139 Iranian Journal of Ichthyology (September 2015), 2(3): 133-147

Fig.5. Line drawing of Syngnathus caspius by S. Laurie-Bourque.

Fig.6. Syngnathus caspius, Anzali Shore, December 2009, courtesy of K. Abbasi. to fresh water from brackish, siltation, oxygen 162.0mm standard length, Gilan, Anzali Lagoon depletion and loss of spawning grounds. Keivany (37º28’40”N, 49º27’42”E). (1966) considers it to be rare on the southern Caspian Comparative material: CMNFI 1981-0813, 3, 29.5- Sea coast while Kiabi et al. (1999) consider this 31.6mm standard length, Rumania, Lake Caraorman, species to be of least concern in the south Caspian Danube River delta (no other locality data). Sea basin according to IUCN criteria. Criteria include medium numbers, widespread range (75% of Family Syngnathidae water bodies), absent in other water bodies in Iran, The pipefishes and seahorses are found world-wide, and present outside the Caspian Sea basin. The IUCN mostly in tropical and warm-temperate waters, with (2014) lists it as of Least Concern. some brackish and freshwater species. There are 56 Sources: Descriptions of breeding and some meristic genera and about 341 species (Nelson 2006; characters are taken from Münzing (1969) and Eschmeyer & Fong 2015) but only one species of Ziuganov & Gomeluk (1985). Further details on pipefish is reported for Iranian fresh waters. collections examined can be found in the museum Maximum length is about 65cm. catalogues. The body of pipefishes is characteristic, being Iranian material: CMNFI 1970-0552, 1, 16.0mm very thin and very elongate, and enclosed in bony standard length, Gilan, Sowsar Roga (37º27'N, rings as a form of armour. The body is divided into a 49º30'E); CMNFI 1970-0554, 12, 17.5-22.0mm trunk and a tail, the tail being prehensile in seahorses. standard length, Gilan, Pir Bazar Roga (37º21'N, The first trunk ring has the pectoral fin base and the 49º33'E); CMNFI 1970-0567, 2, 17.7-21.4mm last has the anus in it. The snout is elongate with a standard length, Gilan, Pir Bazar Roga (37º21'N, small toothless mouth at the tip. Gills are tufted and 49º33'E); CMNFI 1970-0591, 2, 15.8-17.4mm the gill opening is small. There are 1-3 branchiostegal standard length, Gilan, Pir Bazar Roga (37º21'N, rays. There is a single dorsal fin without spines, the 49º33'E); CMNFI 1979-1215B, 1, 22.3mm standard pelvic fins are absent and the pectoral, anal and length, Gilan, Sowsar Roga (37º27'N, 49º30'E); caudal fins may be absent too. The caudal is always CMNFI 1993-0144, 1, 161.6mm standard length, small when present. The anal fin is always small with Mazandaran, Neka Power Plant (36º51’48”N, only 2-6 rays. Those without a caudal fin may have 53º23’24”E); CMNFI 2008-0112, 1, 93.6mm the tail prehensile, able to grasp and hold onto standard length, Gilan, swamp near Hendeh Khaleh objects. Pipefishes and seahorses have only one (37º23’N, 49º28’E); CMNFI 2008-0276, 3, 132.4- kidney, on the right side. Males usually have a pouch

140 Coad-Review of the Sticklebacks and Pipefishes of Iran

on the belly formed from two skin folds which meet reed fish from the Caspian Sea), suzan mahi (= at the mid-line. The female attaches eggs to the male needle fish). [xazar iynabaligi in Azerbaijan; belly or places them in a pouch (or marsupium). Here Kaspiiskaya igla-ryba or Caspian pipefish in the eggs develop and eventually leave after about 4- Russian; short-snouted pipefish, blackstripe 6 weeks through a slit or pore so the male "gives pipefish]. birth". Systematics: The Caspian pipefish has appeared Pipefishes and seahorses are found mostly in under several scientific names. Lueken (1967) shallow coastal areas and in estuaries but also occur demonstrated that Syngnathus nigrolineatus caspius down to about 400m and in the open ocean often Eichwald, 1831, the taxon generally referred to in the associated with floating seaweed. They are slow- literature as occurring in the Caspian Sea, is a moving because of their armour and easily picked up synonym of Syngnathus abaster Risso, 1827. by hand. Propulsion is by undulating the dorsal and Syngnathus abaster was originally described from pectoral fins. Since they cannot outswim most Nice, France. Other taxa of relevance are Syngnathus predators, they are often very well-camouflaged by ponticus Pallas, 1814 described in part from mouths colour, body form and by appendages which disrupt of rivers falling into the Caspian Sea, Syngnathus the body outline. Their food is small crustaceans nigrolineatus Eichwald, 1831 described from "Hab. sucked into the tube-like snout by a sudden in sinu Bacuensi, Murdofiensi Caspii maris", i.e., expansion of the buccal cavity. Many species have a Baku Bay, and also at Odessa on the Black Sea, life span of only about 2 years. Syngnathus caspius Eichwald, 1831 described from Dried seahorses and pipefishes are commonly "Hab. in sinu balchanensi Caspii maris" (Balkhan sold as curios and some family members have been Bay in the Caspian Sea), and Syngnathus bucculentus used as medicines or aphrodisiacs in the East. They Rathke, 1837 described from Sevastopol and are popular aquarium fishes. Certain species are Feodosiya on the Black Sea, all considered as endangered by this collecting for curios, medicines synonyms of S. abaster. However, Naseka & and aquaria. Bogutskaya (2009) and Esmaeili et al. (2010, 2014) recognised S. caspius as the species in the Caspian Genus Syngnathus Linnaeus, 1758 Sea and this is followed here. Kiryukhina (2013) used Members of this genus are found in all seas and there cytochrome b mtDNA and found Black and Caspian are about 31 species. A single species is found in the Sea populations represent genetically isolated Caspian Sea and Iranian waters. Coad (1987, 1998) groups. and Coad & Abdoli (1996) place the species in Key characters: The extremely thin, elongate body context with the Iranian ichthyofauna. encased in bony rings is unique in Iranian fresh and The genus is characterised by a brood pouch in brackish waters. the caudal area of males, running forward to about Morphology: Dorsal fin rays 22-43, the count the origin of the dorsal fin. The eggs develop in increasing with age, anal fin rays 3, pectoral fin rays isolation from the sea, oxygen diffusing from the 9-15, and total caudal fin rays 8-11. Trunk rings 14- "pregnant" male. Dorsal, caudal, anal and pectoral 18, tail rings 28-42, and rings under the dorsal fin 5- fins are present. The caudal fin is very small. 12. A dorsal ridge ends near the rear of the dorsal fin and a continuation of the mid-lateral ridge becomes Syngnathus caspius Eichwald 1831 the dorsal ridge posteriorly. A mid-belly ridge (Figs. 5-6) extends back to the anus where it terminates. As a Common names: Ney mahi or naymahi (= reed fish, result the anterior part of the body from the dorsal fin i.e., as thin as a reed), ney mahi darya-ye Khazar (= forward has 7 longitudinal ridges, reduced to 4 141 Iranian Journal of Ichthyology (September 2015), 2(3): 133-147

posteriorly. Size: Reaches 23.0cm total length. Meristic values for Iranian specimens are: 30(3), Distribution: Found in the Caspian Sea and, in Iran, 31(6), 32(9), 33(18), 34(13), 35(7), 36(1), 37(1), it is recorded from the Anzali Talab (= Mordab) and 39(2), 40(4), 41(3) or 43(1), anal fin rays uniformly neighbouring rivers such as the Sowsar Roga and Pir 3, pectoral fin rays 11(14), 12(22), 13(10), 14(8) or Bazar Roga and at Ab Kenar village, at Bandar-e 15(1), and total caudal fin rays 9(1), 10(51) or 11(2). Anzali and Anzali beach, the Amirkelayee Lagoon Trunk rings 15(46), 16(18) or 17(4), tail rings 33(3), near Lahijan, Boojagh Wetland, Gorgan Bay and 34(7), 35(28), 36(13), 37(5), 38(6), 39(4) or 40(2), Gorgan River, lower reaches of Caspian Sea rivers rings under the dorsal fin 6(1), 7(28), 8(24) or 9(2), such as the Safid, Rud-e Sera, Kargan, Talar, Safid, and brood pouch rings 15(1), 17(2), 18(3), 19(1), Shafa, Haraz, Langrud, Sheikan, , Lalarud 20(3), 21(1), 22(2) or 23(1). Total vertebrae 52(3), and Babol, the southeast Caspian Sea, southwest 53(2), 54(2), 55(4), 58(1) or 59(1). Caspian Sea and south-central Caspian Sea, Sexual dimorphism: Males have a brood pouch under including the deltas of some rivers (Derzhavin 1934; the tail. Holčík & Oláh 1992; Paateemaar 1993; Nejatsanatee Colour: Overall colour is brown to green with dark or 1994; Karimpour 1998; Kiabi et al. 1999; Nazari light spots and bars arranged in a reticulate fashion 2002; Jolodar & Abdoli 2004; Khara et al 2004, on each ring. Pigment is best developed on the dorsal 2005; Naderi & Abdoli 2004; Nezami & Khara 2004; half of the head and body. The ventral part of the tail Mostafavi 2007; Abdoli & Naderi 2009). becomes darkest posteriorly near the tail fin. The Zoogeography: Berg (1948-1949) contends that this reticulate pattern of darker pigment can form a species entered the Caspian from the Black Sea in consistent pattern of arcs bounding the plate post-glacial times while most other Caspian fishes junctions along both the upper and lower flank such are relicts of earlier transgressions or migrants from that a double row of dark ovals with light centres is northern waters. apparent. Behind the dorsal fin where there is no Habitat: This pipefish can live and reproduce in water central ridge on the flank, there is a single dark oval at a salinity of 59.5‰ (Zenkevitch 1963) and is at each plate junction. While some fish have this euryhaline. It is found over sandy or muddy bottoms regular pattern of dark ovals, others are more usually where there is vegetation or detritus, down to irregular with the ovals filled in with pigment leaving about 5m. only very small clear patches in the centre. Various Age and growth: Growth is faster in the first year of other patches of clearer or lighter pigmentation form life as in the second year energy is used for part of the general reticulate pattern. Additionally, reproduction. Life span is slightly over one year in large dark spots or pigment concentrations may be the related (and presumably similar) S. abaster in present along the edge of the uppermost ridge northwest Sicily (Campolmi et al. 1994; 1996) and anteriorly and small dark spots may be scattered 17 months in the Po River Delta, Italy (Franzoi et al. along the back and flanks. 1993), or up to 4 years generally. Maturity of The dorsal fin base can be darkly spotted or S. abaster in the Mauguio Lagoon in southern France striped. The fin itself may be almost immaculate but is reached as early as 3-4 months and almost all a few melanophores line the rays. The pectoral fin individuals are mature after their first winter base has a dark line of merged spots and the rest of (Tomasini et al. 1991). Heydarnejad (2009) gave the the fin is almost immaculate although the rays can be length-weight relationship for an Iranian sample as very lightly lined with melanophores. The anal fin is W=0.0099TL3.543. immaculate. The caudal fin is dark on the rays and Food: Food is zoobenthos such as harpacticoids, membranes, in particular on the central part. gammarids and caprellids and isopods. Prey hidden 142 Coad-Review of the Sticklebacks and Pipefishes of Iran

in vegetation may be taken on account of the short population is unknown rendering an assessment of its and conical snout which is less effective than the conservation status difficult. Kiabi et al. (1999) longer snout of other species which feed on more consider this species to be of least concern in the active pelagic prey. south Caspian Sea basin according to IUCN criteria. Reproduction: Reproductive behaviour in closely- Criteria include abundant in numbers, widespread related species (S. abaster) starts with mutual range (75% of water bodies), absent in other water flickering movements in fish observed in Portugal. bodies in Iran, and present outside the Caspian Sea This is comprised rapid and vigorous bends of the basin. The IUCN (2014) lists it as of Least Concern body with both males and females approaching the (as S. abaster). opposite sex (Silva et al. 2006). If the opposite Sources: Paateemaar (1993) gives an account of this flickered in response, the next phase was rapid side- species in Iran in Farsi. Data were taken from Lueken by-side movements while swimming more or less (1967) and Dawson in Whitehead et al. (1984-1986). parallel. Flickering increased in frequency and the Further details on collections examined can be found female's genital papilla protruded. The distended in the museum catalogues. genital papilla is placed in the anterior area of the Iranian material: CMNFI 1970-0507, 1, 91.3mm marsupium of the male, the folds in this area being standard length, Gilan, Caspian Sea at Hasan Kiadeh separated and swollen. The mated pair then ascend (37º24'N, 49º58'E); CMNFI 1970-0508, 1, 89.4mm slowly in the water column, vibrating the dorsal fin standard length, Gilan, Safid River at Hasan Kiadeh and rotating a few times. Eggs are transferred and the (37º24'N, 49º58'E); CMNFI 1970-0531, 1, 108.1mm female retreats to the substratum while the male standard length, Mazandaran, Larim River mordab continues swimming with violent body contractions (36º46'N, 52º58'E); CMNFI 1979-0535, 1, 126.3mm - these help pack the eggs in the posterior end of the standard length, Gilan, Shara River estuary (37º35'N, marsupium. Later, spawning occurs again up to three 49º09'E); CMNFI 1970-0543A, 5, 104.6-144.8mm times by the same pair although females may mate standard length, Gilan, Caspian Sea at Hasan Kiadeh with up to 3 different males in less than 30 minutes. (37º24'N, 49º58'E); CMNFI 1970-0554, 13, 40.4- Broods are found in males from Iran collected on 95.6mm standard length, Gilan, Pir Bazar Roga 4 May, the same sample having males with eggs and (37º21'N, 49º33'E); CMNFI 1970-0563, 1, 134.9mm males with minute young pipefish. A sample from 22 standard length, Gilan, Caspian Sea, Kazian Beach September has eggs just about to hatch while males (ca. 37º29'N, ca. 49º29'E); CMNFI 1970-0567, 7, taken on 3 August, 28 September and 17 December 52.9-99.5mm standard length, Gilan, Pir Bazar Roga contain neither eggs nor young. Females with large (37º21'N, 49º33'E); CMNFI 1970-0575, 1, 94.3mm eggs have been caught in Iran on 17 April and 7 July standard length, Gilan, Pir Bazar Roga (37º21'N, while on 3 August, 19 September, and 12 and 17 49º33'E); CMNFI 1970-0587, 3, 131.6-140.0mm December females had only small eggs. The 17 April standard length, Mazandaran, Babol River near sample contained eggs of dissimilar sizes. Iranian Babolsar (36º43'N, 52º39'E); CMNFI 1971-0343, 3, fish appear to have a similar breeding season to 104.6-109.0mm standard length, Gilan, Langarud at closely-related species from other localities and Chamkhaleh (37º13'N, 50º16'E); CMNFI 1979-0077, probably have batch spawning too. 8, 128.4-149.2mm standard length, Mazandaran, Parasites and predators: The Caspian seal, Pusa Caspian Sea beach at Now Shahr (36º39'N, 51º31'E); caspica, is a predator on this species (Krylov 1984). CMNFI 1980-0130, 9, 59.3-97.8mm standard length, Economic importance: None. Mazandaran, river near Iz Deh (36º36'N, 52º07'E); Conservation: The ecology of this species has not CMNFI 1980-0136, 16, 76.6-100.5mm standard been studied in detail in Iranian waters and its length, Mazandaran, Fereydun Kenar River estuary 143 Iranian Journal of Ichthyology (September 2015), 2(3): 133-147

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