Genus Hypophthalmichthys
Bleeker, 1859

The silver carp genus contains 3 species with a native distribution in eastern Asia. Two species have been widely introduced for food in aquaculture and for phytoplankton control.

The genus is characterised by an elongate and compressed body, very small scales (usually over 100 in the lateral line), eyes low on the head with their lower margin below the mouth corner level, a terminal mouth, no barbels, gill rakers long and thin, a very long gut, branchiostegal membranes joined and free of the isthmus, a short dorsal and elongate anal fin, both spineless, pharyngeal teeth in 1 row, and a ventral keel from the throat or pelvic fins to the anus.

Hypophthalmichthys molitrix
(Valenciennes in Cuvier and Valenciennes, 1844)

Common names

فيتوفاگ (= fitofag or phytophag, i.e. phytophage or plant eater), كپور نقره اي (= kopur-e noqrehi or kapoor-e-noghreie, meaning silver carp), آزاد پرورشي (= azad-e parvareshi meaning free farmed).

[silver carp, thickforehead, white thickforehead; belyi tolstolobik, tolpyga and maksun in Russian].

Systematics

Leuciscus molitrix was originally described from China. Populations in the Anzali Mordab are hybrids with Hypophthalmichthys nobilis (J. Holčík, in. litt., 1989).

Key characters

The abdomen has a compressed keel extending from the breast to the vent, the eyes are positioned low such that they are visible from the underside of the head, and scales are minute. The similar bighead (H. nobilis) can be distinguished by the long pectoral fins which extend past the origin of the pelvic fins, a shorter keel (pelvic fins to anus), and gill raker structure (free, no spongy root mass).

Morphology

Dorsal fin with 2-3 unbranched rays followed by 6-7 branched rays, anal fin with 2-3, usually 3, unbranched rays and 11-15 branched rays, pectoral fin branched rays 17, and pelvic fin branched rays 7. Lateral line scales 85-125 Scales are rounded to oval with a posterior focus and very few posterior radii. Total vertebrae 36-40. Pharyngeal teeth 4-4, well-developed, compressed and with striated grinding surfaces. Gill rakers exceed 650 and are longer than the gill filaments. The left and right sides of the gill arches are united by a mucous membrane to form a continuous band; the gill rakers are distinguishable distally but the roots form a spongy mass. The gut is long and complexly coiled. The diploid chromosome number is 48 (Klinkhardt et al., 1995; Varasteh et al., no date). There were 6 pairs of metacentric, 14 pairs of submetacentric and 4 pairs of acrocentric chromosomes in the latter study.

Sexual dimorphism

Unknown.

Colour

Overall colour is silvery, the back bluish to grey-black with upper flanks olivaceous but silver laterally and ventrally, and the fins red or immaculate.

Size

Reaches 1.42 m and 56 kg.

Distribution

The natural distribution is from the Amur River in the former U.S.S.R. southward to southern China. In Iran, it has been introduced to the Sistan basin including the Hamun Sabari and the canal flowing into Chahnimeh (Ahmadi and Wossughi, 1988; Mansoori, 1994; J. Holčík, in litt., 1996), the Voshmgir Reservoir on the Gorgan River (Petr, 1987) as well as widely stocked in Mazandaran and Gorgan provinces in reservoirs and lakes by both governmental agencies and private companies. It is also introduced to the Anzali Mordab and its outlets (Holčík and Oláh, 1992), the Gorgan, Tajan, Aras, and Safid rivers, and the Anzali Mordab (Kiabi et al., 1999; Abbasi et al., 1999), Lake Zaribar, Kordestan (Abzeeyan, 5(5):III, 1994), reservoirs and fish farms in Khuzestan, Mahabad Dam (Abdi, 1999; www.mondialvet99.com, downloaded 31 May 2000).

Abdoli (2000) records this species generally from the Kavir, Yazd, Sistan and Jaz Murian basins; from the middle and lower Kor River and the Pulvar River in the Kor River basin; from the middle and lower Zayandeh River in the Esfahan basin; from the Khersan River, lower Karun River, the lower Jarrahi river, the lower Dez River the upper Karkheh River and the lower Kashkan River in the Tigris River basin; the middle and lower Qareh Su and Qom rivers, the lower Karaj and Shur rivers in the Namak Lake basin; the lower Zarrineh river and the middle and lower Talkheh River in the Orumiyeh basin; the middle Kashaf River in the Tedzhen basin; the middle and lower Atrek and Gorgan rivers, the lower Babol, Heraz, Chalus, Tonekabon and Safid rivers, the Anzali Talab and the Caspian coast generally in the Caspian Sea basin.

This species is also recorded from the Karakum Canal and Kopetdag Reservoir in Turkmenistan (Shakirova and Sukhanova, 1994; Sal'nikov, 1995) and may eventually reach Iranian waters in the Tedzhen (= Hari) River and Caspian Sea basins. It is pond-cultured in Iraq and is known from open waters such as the Shatt al Arab and Tigris River (Al-Hassan, 1994).

Zoogeography

This species is an exotic, introduced to Iran from a variety of sources. It may become established in the large river systems of southern Iran and Iraq from escapees (Al-Hassan, 1994).

Habitat

This species is a riverine fish in its native habitat, or is found in water bodies connected to rivers, but is extensively cultivated in ponds for food throughout Asia. Silver carp can live in the Caspian Sea at salinities of 5-8‰ although a few are found at 10-12‰. It enters rivers to spawn (Abdusamodov, 1986). Temperatures in the range 0-40ºC are tolerated although 26-30ºC or 30-34ºC is preferred in different studies. It is more cold-tolerant than bighead carp. This species can be difficult to catch as it will jump over nets, to a height of about 2 m, and when frightened by noise has been known to jump into boats. Malek Nedjad and Parivar (1993) consider that the level of lead pollution in the Anzali Mordab (average 0.124 p.p.m. in surface waters, 0.1956 p.p.m. in deeper waters) caused 8% mortality in fertilised eggs and nearly 18% of eggs are useless for fisheries work.

Age and growth

Terek River silver carp first mature at 4 years for males and 5 years for females. About 15% of females mature at 4 years but 87% of the females and 85% of the males are in the 5-7 age groups (Abdusamadov, 1986). Maturity varies with locality, at 2-8 years, with males maturing a year earlier than females. Silver carp can reach 18-23 kg in 4-5 years. Life span is at least 20 years. Abdolmalaki (2004) examined the fishery for this carp in the Mahabad Reservoir, Iran and found mean fork length was 51.15 cm and mean weight was 2272.1 g. The length-weight relationship was W = 0.013L^3.04. The von Bertalanffy growth parameters were L_∞ = 150 cm, K = 0.128, instantaneous rate of total (Z), natural (M) and fishing (F) mortality were 1.68/year, 0.22/year and 1.46/year. The exploitation rate (E) was calculated to be 0.82. The biomass was 158.5 t with a maximum sustainable yield estimated at 68 t. A decreased fishing effort was recommended as the annual catch in 1998-1999 was 101,123.5 kg.

Food

The gill rakers form a very fine, sponge-like mesh used to filter small planktonic food, aided by the epibranchial organ that produces mucus to trap very small particles. This species is a pump filter feeder, taking smaller particles than bighead carp. Food in Lake Kinneret, Israel is phytoplankton from February to August and predominately zooplankton from September to January, a response to a decrease in phytoplankton biomass in summer-fall (Spataru and Gophen, 1985). Cladocerans and cyclopoid copepods dominate the biomass of zooplankton taken. The ability to take cyclopoids is due to the large mouth, strong sucking power and the high filtration rate when feeding. Food is taken passively rather than selectively.

Reproduction

Silver carp require cool, flowing water to breed. The spawning migration begins at the end of April in the Terek River of Dagestan at 16-17°C, with a peak between the middle of May and the beginning of June. Generally spawning occurs between 18 and 26°C. Fecundity reaches 1,340,500 large, greyish eggs (and in the Kara-kum Canal 1,525,000 eggs; elsewhere to 5.4 million eggs). Water hardened eggs are 4.9-5.6 mm, smaller than those of bighead carp. Spawning takes place after a sharp rise in water level and current speed. Spawners chase each other near the water surface where eggs and sperm are shed. Eggs are first found in the drift in the second week of June and hatch 34-70 hours later depending on temperature. Some larvae reach rice fields and live there until autumn when the fields dry up where some are lost, others migrating. Other larvae are carried into the Caspian Sea where they are sensitive to the prevailing salinity at 1-1.5 days old (Abdusamadov, 1986). It does not breed in the wild in Iran.

Parasites and predators

Mokhayer (1989) reports metacercariae of the eye fluke, Diplostomum spathaceum from this species in Iran, which can cause complete blindness and death in commercially important species, as well as black-spot, Posthodiplostomum cuticola. Jalali and Molnár (1990b) record the monogenean Dactylogyrus hypophthalmichthys from this species at fish farms in Iran. Masoumian and Pazooki (1998) surveyed myxosporeans in this species in Gilan and Mazandaran provinces, finding Myxobolus pavlovskii. Akhlagi (1999) reports that high temperatures (up to 32°C) stresses this species and leaves it open to infection with Aeromonas hydrophila. Safari and Khandagi (1999) record Clostridium botulinum from 1.1% of fresh and smoked samples of this species in Mazandaran Province. Ebrahimzadeh Mousavi and Khosravi (1999; www.mondialvet99.com, downloaded 31 May 2000) record the toxigenic fungi Aspergillus flavus, Alternaria, Penicillium and Fusarium from this species and the pond water at a fish farm in northern Iran. Akhondzadeh Basti and Zahrae Salehi (2003) show that the psychotropic pathogen Listeria monocytogenes is found in market and fish farm samples of this species. Naem et al. (2002) found the following parasites on the gills of this species from the western branch of the Safid River, namely the protozoans Ichthyophthirius multifilis and a Trichodina species and the  monogenean trematode Dactylogyrus hypophthalmichthys. Jalali et al. (2002) and Jalali and Barzegar (2006) record several parasites from this species in Lake Zarivar, namely Dactylogyrus hypophthalmichthys, D. suchengiaii, Diplostomum spathaceum, two species of Argulus, and myxosporean plasmodia. Jalali et al. (2005) summarise the occurrence of Gyrodactylus species in Iran and record G. sprostonae from Safid River fish. Araghi Soureh and Jalali Jafari (2006) recorded Dactylogyrus hypophthalmichthys and D. suchengtaii from this species in the Mahabad River of the Lake Orumiyeh basin, the latter species being a new record for Iran.

Economic importance

This species is the most productive freshwater fish in the world, with 3.1 million metric tons produced in 1997 (versus 2.2 million mt for Cyprinus carpio).

Holčík and Oláh (1992) report a total catch of 6585 kg in the Anzali Mordab in 1990, at 8.8% of the total fish catch being the third largest catch. This species is used in polyculture with common and grass carps and comprises 50-63% of the fishes. They are fed through pond fertilization without supplementary feeding (Emadi, 1993b). Silver carp in oil are packaged in northern Iran (http://www.netiran.com/business.html, downloaded 31 October 2003). They are also found in fish stores in Ahvaz, Khuzestan (personal observations, September 1995). Iran shares with Uzbekistan the most production of this species among North African and Near Eastern aquaculture; the Iranian catch increasing from nothing in 1989 to 24,720 tonnes in 1994 (Food and Agriculture Organization, Fisheries Department, 1996). Bartley and Rana (1998b) however give a production of 15,228 t for 1995. Market price in 1995 was about U.S.$1.00/kg in 1995, lower than for grass carp at about $2, but silver carp have the higher stocking ratio (Rana and Bartley, 1998a). Kals and Bartels (2004) give some recommendations for improving silver carp farming in Iran.

Abdolmalaki (2004) reported that 67.3% of the 150,261 kg of fishes caught in Mahabad Reservoir in the1998-1999 fishing season were this species. The fishing effort was 69 beach seine hauls and 2530.7 fishing effort units with 7-15 cm gill nets, each unit being 100 m of gill net for 24 hours.

Robins et al. (1991) list this species as important to North Americans. Importance is based on its use in aquaculture and food. The food of this species being phytoplankton it has been introduced to areas lacking filter feeders such as Europe and Israel in efforts to control algal blooms associated with eutrophication. The results in Israel were controversial and difficult to interpret because of chemical treatments for nuisance dinoflagellates and introductions of other fish species (Opuszynski and Shireman, 1995). In some cases the effects of the introduction were negative because the silver carp fed from September to January on zooplankton which themselves reduce algal blooms. There was also competition with a more valuable native species of cichlid for the same zooplankton resource and the native cichlid was a more efficient consumer of the nuisance dinoflagellate. Elsewhere, the consumption of plankton may remove food for native, larval fishes.

This species has been studied extensively as a commercial species in various parts of the world. Studies specific to Iran include Javadian et al. (2003) on the effect of ice storage on lipid and other chemical changes, moisture and texture and appearance; Moradian et al. (2003) on the effects of the hormone thyroxine on the survival of early growth stages (the ratio of hatched eggs in 0.5 p.p.m. thyroxine was highest); Kashani Sabet et al. (2004) on inducing ovulation with hormones combined with dopamine antagonists; Alavi Talab (2007) on use of skins and fins for gelatin extraction, etc.

This fish can be dangerous to boaters as it leaps out of the water (Kolar and Lodge, 2002). Akhondzadeh Basteh et al. (2006) found the bacterial pathogens Listeria monocytogenes in fresh and smoked H. molitrix, Staphylococcus aureus in smoked H. molitrix, Escherichia coli and Salmonella dublin in fresh H. molitrix and Vibrio haemolyticus in smoked H. molitrix.

Conservation

Krasznai (1987) and Petr (1987) give details of fish farms propagating this species in Iran. For example, 30 million fish were produced by the Safid Rud Fish Farm in 1986. 20 million carp, silver carp and grass carp fingerlings were produced in the Shahid Rajaae Hatchery in Sari for release across Iran in reservoirs and dams (Abzeeyan, Tehran, 4(7):VII, 1993). Piri and Ordog (1999) describe the effects of herbicides and insecticides on this species. These chemicals are used extensively on rice fields in Gilan where aquaculture is widely developed.

Hybridisation (presumably with H. nobilis) has led to poor growth and a decline in the fishery (Shehadeh, 1997).

Further work

The biology of this species in Iran needs investigation in relation to its effects on native fishes and its distribution monitored.

Sources

Opuszynski and Shireman (1995) summarise the biology and culture of this species.

Comparative material: CMNFI 1977-0590, 3, 120.3-135.5 mm standard length, Israel, Kibbutz `En Hamifraz (32º59'N, 35º05'E).

Hypophthalmichthys nobilis
(Richardson, 1844)

Common names

sar gondeh or sargundeh (= bighead) in the Caspian basin, كپور سرگنده (= kopur-e sargondeh, meaning bighead carp), mahi kopur sar gondeh, fitofag.

[pestryi tolstolobik in Russian; bighead, painted thickforehead].

Systematics

Leuciscus nobilis was originally described from Canton, China. Eschmeyer et al. (1996) give the date of publication as 1845, Reshetnikov et al. (1997) as 1846.

Howes (1981) reaffirms the placement of this species in Hypophthalmichthys Bleeker, 1860, considering that the characters of abdominal keel length, pharyngeal dentition and gill raker form are insufficient to place this species in the distinct genus Aristichthys Oshima, 1919. Other authors disagree (see Eschmeyer, 1990; Reshetnikov et al., 1997).

Populations in the Anzali Mordab are hybrids with Hypophthalmichthys molitrix (J. Holčík, in litt., 1989).

Key characters

The similar silver carp (H. molitrix) can be distinguished by the short pectoral fins which do not extend past the origin of the pelvic fins, a longer keel (throat to anus), and gill raker structure (continuous band uniting both sides, roots fused into a spongy mass).

Morphology

Dorsal fin unbranched rays 3 followed by 7 unbranched rays, anal fin unbranched rays 3 with 11-14 branched rays, pectoral fin branched rays 16-19, and pelvic fin branched rays 7-9. Lateral line scales 92-115. Scales are a rounded oval with a slightly posterior focus, very few posterior radii and numerous fine circuli. Total vertebrae number 36-41. Pharyngeal teeth 4-4, with smooth grinding surfaces. Gill rakers are very numerous. The gut is elongate and convoluted. The diploid chromosome number is 48 (Klinkhardt et al., 1995).

Sexual dimorphism

Males have a sharp edge along the dorsal surface of several anterior pectoral fin rays.

Colour

Overall colour is silvery and the body has numerous scattered small black spots which makes some fish speckled or darker in overall colour. A few larger blotches may be present. The head is often darker and contrasts with the silvery body. Fins are greyish and similar to the adjacent body colour with the caudal fin darkest, sometimes reddish.

Size

Attains 1.46 m in length and over 50 kg.

Distribution

This species is a native of China and was first introduced to Iran in 1966 from a hatchery in the Krasnodar region of the former U.S.S.R. (Anonymous, 1970b). It is reported from fish farms in the Caspian Sea basin and is stocked in reservoirs throughout Iran (Coad and Abdoli, 1993b). Introduced to the Kor River in Fars (A. Alamdari, in litt., 1997) and reported from the Gorgan, Tajan, Aras, and Safid rivers, and the Anzali Mordab (Abbasi et al., 1999; Kiabi et al., 1999; Jalali et al., 2005). Abdoli (2000) records it generally from the Sistan, Hormuz, Kor, Yazd, Kavir, Esfahan, Namak, Tigris, and Orumiyeh basins and from the lower Gorgan, Neka, Babol, Haraz, Chalus and Tonekabon rivers, the Gorgan and Anzali mordabs and along the Caspian coast.

Also reproducing naturally in the Karakum Canal and recorded from the Kopetdag Reservoir in Turkmenistan (Shakirova and Sukhanova, 1994; Sal'nikov, 1995) and may eventually reach Iranian waters in the Tedzhen (= Hari) River basin. Introduced to Iraq for fish farming.

Zoogeography

An exotic introduced to Iran.

Habitat

In their natural habitat, bigheads are found in large rivers and associated floodplain lakes. They migrate upstream to spawning grounds when water levels rise, moving to flooded land afterwards, and returning to the river channel as water levels fall. Bigheads can live in the Caspian Sea at salinities of 5-8 p.p.t. although a few are found at 10-12 p.p.t.. They can adjust gradually to salinities of 15-20 p.p.t. They enter rivers to spawn (Abdusamodov, 1986) but are known to spawn in the Karakum Canal of Turkmenistan. Preferred temperatures for feeding and reproduction are within the general range 20-30°C. Activity almost ceases at 10°C and the critical thermal maximum is 38.8°C.

Age and growth

Males achieve first maturity at age 5 and males of 5-7 years and 81-90 cm make up 90% of the run in the Terek River. Most females mature at 6 years and 81% of the females on the spawning run are 6-7 years old and 75-100 cm (Abdusamodov, 1986). Males mature at 2-4 years and females at 3-5 years (and 10 kg) in Turkmenistan. Sexual maturity varies widely with environmental conditions, 2-6 years for males and a year later for females. Life span is up to 16 years. Growth is rapid, attaining 18-23 kg in 4-5 years.

Food

Zooplankton is almost exclusively the food of this species. Phytoplankton and detritus may be taken when zooplankton biomass is low. Most feeding occurs during summer and peaks daily in the range 1200 to 2000 hours. This species is both a pump feeder, using the buccal pump to push food-laden water through the gill rakers, and a ram feeder, swimming with the mouth open to force water through the gills, with intermittent gulps. Feeding often occurs at the water surface, in contrast to silver carp, as well as in the water column and on the bottom.

Reproduction

A spawning migration of this species enters the Terek River in the second week of May at water temperatures of 18-19°C, numbers increasing until the end of June. Spawning takes place after a sharp rise in water level and current speed. Males actively chase females near the water surface, occasionally butting the female's belly, and sometimes leaping out of the water. Eggs and sperm may be cast into the air. Fecundity attains 1,860,800 eggs. Unswollen eggs are 1.4-1.5 mm in diameter and water hardened eggs are 5.7-6.2 mm. Eggs are first found in the drift in the second week of June and hatch 34-70 hours later depending on temperature. Some larvae reach rice fields and live there until autumn when the fields dry up where some are lost, others migrating. Other larvae are carried into the Caspian Sea where they are sensitive to the prevailing salinity at 1-1.5 days old (Abdusamadov, 1986).

Parasites and predators

Jalali and Molnár (1990b) record the monogeneans Dactylogyrus aristichthys and D. nobilis from this species in Iranian fish farms. Naem et al. (2002) found the following parasites on the gills of this species from the western branch of the Safid River, namely the protozoan Trichodina sp., monogenean trematodes Dactylogyrus nobilis, D. aristichthys, and Gyrodactylus sp.. Jalali et al. (2005) summarise the occurrence of Gyrodactylus species in Iran and record G. sprostonae and G. sp. in fish from the Safid River. Masoumian and Pazooki (1998) surveyed myxosporeans in this species in Gilan and Mazandaran provinces, finding Myxobolus pavlovskii.

Economic importance

Holčík and Oláh (1992) report a catch of 466 kg in the Anzali Mordab in 1990. Aquaculture production in 1995 was 1269 tonnes (Bartley and Rana, 1998b). Marjan Iran Company was selling 1500-1800 g fish for U.S.$1.90/kg in August 2003 (http://groups.yahoo.com/groups/hilsa/message/25).

Robins et al. (1991) list this species as important to North Americans. Importance is based on its use in aquaculture and food. It ranks fourth on world aquaculture production. This species has been used in Israel to reduce zooplankton populations in reservoirs in an effort to improve water quality (Opuszynski and Shireman, 1995). It has a higher net production in culture systems than H. molitrix and Ctenopharyngodon idella. The consumption of plankton may remove food for native, larval fishes, and affect the diet of piscivorous fishes and birds. This species can also cause habitat alteration, increasing turbidity, and introduce diseases and parasites. In Iran, it has been used in aquaria for investigations on the effect of lead nitrate on blood serum electrolytes (Jamili et al., 2006).

Conservation

Krasznai (1987) and Petr (1987) give some details of propagation of this species in Iran. Some populations are hybrids (see above) and there is a danger of loss of genetic purity in fish farm stocks should breeding adults be captured in the wild. As an exotic, there is no need for conservation.

Further work

The biology of this species in relation to native species should be investigated for Iran.

Sources

Jennings (1988), Opuszynski and Shireman (1995) and Kolar et al. (2005) summarise the biology and culture of this species.

Comparative material: CMNFI 1980-0530, 2, 230.6-255.8 mm standard length, Japan, pond cultured (no other locality data).

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