Genus Rhodeus
Agassiz, 1832

The bitterlings comprise about 5 species in Europe, Asia Minor, the Caspian Sea basin, China, Japan and Korea with 1 species in Iran.

They are small fishes with deep, compressed bodies, an incomplete lateral line (about 10 pored scales or less), large to moderate-sized scales, females with an ovipositor, males larger than females (unusual in cyprinid fishes), brightly coloured and tuberculate when spawning, pharyngeal teeth in 1 row and not or only slightly serrated, mouth small, oblique and subterminal, no barbels, dorsal fin short to moderately long and spineless, anal fin of similar length, gill rakers short, intestine long and spirally coiled, and peritoneum black.

Rhodeus ocellatus
(Kner, 1866)

Reported from the Karakum Canal and Kopetdag Reservoir in Turkmenistan (Shakirova and Sukhanova, 1994; Sal'nikov, 1995) as an exotic from China. May eventually be found in the Tedzhen (= Hari) River and Caspian Sea basins of Iran. No Iranian record.

Rhodeus amarus
(Bloch, 1782)

Common names

ماهي مخرج لوله اي (= mahi-ye makhraj lulehi or mahi-e-makhraj looleei, meaning tube-like vent fish), rodeus.

[karka in Azerbaijan; gorchak in Russian; bitterling, European bitterling].

Systematics

Holčík and Duyvené de Wit (1964) reviewed the systematic status of Rhodeus sericeus (Pallas, 1776) in Europe and western Asia (but not Iran) in comparison to the Chinese populations of this species. They refer European and western Asian populations to Rhodeus sericeus amarus (Bloch, 1782) and Iranian populations were long regarded as this subspecies. Cyprinus sericeus was described from Dauriya; Cyprinus amarus was described from the Elbe basin, Germany and no types are known (Eschmeyer et al., 1996). Later, Holčík and Jedlička (1994) consider subspecies not to be warranted as the key characters used in distinguishing them (pored lateral line scales, scales in lateral series, gill rakers) showed clinal variation with longitude and the number of segments was also related to latitude, elevation, mean annual air temperature, and fish size. Bohlen et al. (2006) consider Rhodeus from the Vistula to the Volga to belong to the R. amarus eastern clade based on cytochrome b sequences.

Kottelat (1997) considers Rhodeus amarus to be a distinct species since it is diagnosable (although differences with Rhodeus sericeus are slight and largely overlap), and it is separated by 2-4 million years in time and 4000 km in space. However he does admit that the immense distributional gap may be a source of bias. Holčík in Bănărescu (1999) considers amarus to be synonymous with sericeus. Bogutskaya and Komlev (2001) found no characters to clearly confirm the specific status of R. amarus. The name amarus is retained here as an indication that the taxa are geographically isolated. Van Damme et al. (2007) refer the Caspian bitterling to a species as yet undescribed.

This species was described from Lake Müggelsee near Köpenik, Berlin, Germany and 3 syntypes are in the Museum für Naturkunde, Humboldt-Universität zu Berlin (or Zoologisches Museum Berlin, ZMB 3393).

Key characters

The presence of an ovipositor in females, the flank stripe and few pored scales are distinctive.

Morphology

Dorsal fin with 2-4, usually 3, unbranched and 7-11, usually 9, branched rays, anal fin with 2-4, usually 3, unbranched and 6-12, usually 9, branched rays, pectoral fin branched rays 10-13, and pelvic fin branched rays 4-8, usually 6-7. Pored lateral line scales 0-11, usually 4-6, along the flank 28-45, usually about 30-32 in some reports but 32-38 in Abdurakhmanov (1962), 37-40 in Holčík and Jedlička (1994), 30-38 in Pipoyan (1996b) and 35-40 in Holčík in Bănărescu (1999). Gill rakers 9-16, usually 10-14, reaching the raker below when appressed. Vertebrae 33-39. Pharyngeal teeth 5-5, rarely 5-4, 4-5 or 4-4. Teeth are elongate and narrowly compressed with a slight to strong hook at the tip and a very long, narrow and concave grinding surface below the tip. The gut has numerous coils. The chromosome number is 2n=48 (Klinkhardt et al., 1995).

Meristic values for Iranian specimens are:- dorsal fin branched rays 8(4), 9(52), 10(1) or 11(1); anal fin branched rays 8(18), 9(39) or 10(1); pectoral fin branched rays 10(3), 11(24), 12(29) or 13(2); pelvic fin branched rays 4(1), 6(3), 7(53) or 8(1); scales in lateral series 32(1), 33(2), 34(22), 35(29) or 36(4); pored lateral line scales 3(1), 4(7), 5(37), 6(11) or 7(2); total gill rakers 10(3), 11(14), 12(27), 13(10) or 14(4); pharyngeal teeth 5-5(20); and total vertebrae 34(9), 35(36), 36(12) or 38(1). Holčík and Jedlička (1994) give ranges in their Iranian sample of 33-41 for lateral series scales, 0-6 pored scales and 9-14 for gill rakers, in general agreement with data here.

Sexual dimorphism

Males develop a triangular or crescent-shaped patch of 7-20 tubercles on each side of the snout and small tubercles are found above the eyes. The female develops an ovipositor near the genital opening and it may be longer than the body. The flank stripe is longer and about one half wider in males compared to females, and male colouration is distinctive. Males are generally larger than females.

Colour

Males are particularly colourful in the spawning season: the top of the head and back are olive to bright green, reddish or dark violet, the iris is bright red, flanks are iridescent with violet and steel-blue colours most evident, the throat and belly are orange to blood-red, dorsal and anal fins are bright red and margined with black, the caudal fin is green at the base and yellow distally, and pectoral and pelvic fins are yellowish. Females are more yellowish and less iridescent than males in the spawning season. Outside the breeding season both sexes are similar in colour with a grey-green back, silvery flanks and yellowish belly. A grey-green to greenish-blue stripe originates under the dorsal fin and extends back to the tail base, broadening posteriorly. The dorsal fin is blackish and other fins reddish to yellowish. The dorsal, and sometimes the anal fin, has a dark interrupted stripe. The iris is silvery or yellowish. The peritoneum is dark.

Size

Reaches a reputed 18.0 cm but usually not more than 7.0-9.0 cm.

Distribution

Found from western Europe north of the Pyrenees and Alps to the Caspian Sea basin. In Iran, it is recorded from Astara to the Gorgan River including the Anzali Talab (Derzhavin, 1934; Holčík and Oláh, 1992; Abbasi et al., 1999; Kiabi et al., 1999; Abdoli, 2000). Also probably in the Araks River of Armenia (Pipoyan, 1996b). They may have been introduced into the Zarrineh River of Azarbaijan-e Gharbi based on photographs by Saber Shiri (pers. comm., 14 June 2008).

Zoogeography

Bohlen et al. (2006) assumed a continuous distribution of Rhodeus from Europe through Siberia to east Asia during the Pliocene, loss of the Siberian population in the late Pliocene or early Pleistocene, subsequent isolation, and later post-glacial expansion from several refugia in the Euro-mediterranean zoogeographic subregion. The Caspian Sea populations were not examined but seem to belong to R. amarus although the authors suggest a revisionary study is required for European bitterlings. Van Damme et al. (2007) consider this species was restricted to Ponto-Caspian and Aegean regions and its presence in western and central Europe is associated with the spread of Cyprinus carpio cultivation, and more recently, anthropogenic alterations to habitats and temperature changes.

Habitat

This species favours heavily vegetated areas of small lakes, ponds and slow-moving rivers, rarely in faster water. It is found in the lower reaches of rivers on the Caspian coast of Iran (Jolodar and Abdoli, 2004). The bottom is usually a fine sand or a thin layer of mud. Swan mussels (Anodonta) and freshwater clams (Unio) share this kind of habitat and are necessary for reproduction. Other genera of clams include Pseudanodonta, Cristaria, Margaritifera and Dahurinaia (Smith et al., 2004). Spawning occurs at water temperatures of 12-24°C, although 15-21°C is optimal (Holčík in Bănărescu, 1999), Van Damme et al. (2007) giving 23°C as optimal. Its distribution is limited by the 16°C July isotherm (Van Damme et al., 2007).

Age and growth

Maximum life span is 5-8 years, the higher values being uncertain (Holčík in Bănărescu, 1999). Maturity is attained during the second or third year, the life span of most individuals. Rarely some fish may mature as early as before the age of 1 year or as late as the fourth year. Growth is faster in ponds than in rivers. Males outnumber females at a ratio of 1.2-1.5:1, especially in spawning areas, although females apparently outlive males (Holčík in Bănărescu, 1999).

Food

Food consists of diatoms and detritus with aquatic insects and crustaceans being mostly accidental inclusions. They also take eggs of Rutilus rutilus, Cyprinus carpio and Rutilus frisii, and also their own eggs which fail to be deposited in the clam or mussel. Most gut contents in Iranian fish examined were plant fragments, filamentous algae, detritus and sand grains.

Reproduction

Reproduction takes place mainly in April and May, but can run from the end of February (in Azerbaijan) to August. The female develops an ovipositor from the genital opening, up to 6 cm long. In Iranian fish the best developed ovipositor was seen in a fish collected on 12 May when it extended back two-thirds along the caudal fin length. Eggs in this fish were 2.2 mm. Fish taken in September, October, November and January had short ovipositors progressively increasing in length with time. A fish taken on 4 July had an ovipositor extending only half way along the anal fin but no large eggs. Spring spawning is indicated but an ovipositor can be seen in varying degrees of development year round in adult females. Holčík in Bănărescu (1999) reports ovipositor length up to 126.5% of standard length in the Anzali Mordab in April.

The ovipositor lays eggs inside freshwater clams and mussels, using the excurrent siphon as the entry route. Apparently the flow of water and a high oxygen content out of this siphon encourage egg laying. Before egg laying, the female nudges the clam repeatedly to accustom the mollusc to stimulus so that it does not close up its shell. In the absence of clams, the bitterling does not become sexually mature. Clams and mussels with high numbers of bitterling larvae or filled with glochidia are avoided, as is Anodonta cygnaea, a mussel which is able to eject eggs and larvae and has low oxygen levels in its excurrent siphon (Kottelat and Freyhof, 2007). Males select and defend a particular clam against other males. They may headbutt each other or strike flanks, dislodging scales. Sneaking occurs despite this. The female deposits eggs 1-2 at a time and the male sheds sperm which are sucked into the clam on its feeding current. This process may be repeated with the same or different females. The female deposits about 40-100 eggs at each spawning and can spawn at least 5 times a day. The movement of the ovoid eggs through the ovipositor can be clearly seen as they are somewhat larger than the distensible ovipositor. Spawning bouts last 1-3 days with intervals of 5-7 days, variable with feeding conditions and temperature (Smith et al., 2004). Fecundity is up to 22,136 eggs and maximum egg diameter to 3.1 mm with width up to 1.52 mm. Eggs hatch 2-5 weeks later and the young leave the clam after 2 days when the yolk sac has been absorbed. Young fish leave the clam singly or in pairs. The fish gain the advantage that the eggs and young are protected inside the clam, even should the shore area dry out since the clam will move to deeper water. The clam is unharmed and is able to disperse its own young or glochidia by their attachment to the fins of the adult fish. Bitterlings seem however to have an immunological response to glochidia, having far fewer than other fishes that are less intimately associated with clams. Circumstantial evidence laid out by Smith et al. (2004) involving inhibition of free water circulation by the fish embryos, damage to clam gills, and increased consumption of oxygen by clams, indicate the relationships is a parasitic rather than a commensal one.

Smith et al. (2004) give a detailed account of reproduction, behaviour and development in this species.

Parasites and predators

None reported from Iran.

Economic importance

Robins et al. (1991) list this species as important to North Americans. Importance is based on its use in textbooks and aquaria and because it has been introduced outside its natural range. Van Damme et al. (2007) regard it as a parasite on freshwater mussel populations in western and central Europe outside its native range, escaping glochidia infection and having low egg ejection rates.

Conservation

Lelek (1987) classifies this species as rare to vulnerable in Europe. Vulnerable in Turkey (Fricke et al., 2007).Kiabi et al. (1999) consider this species to be of least concern in the south Caspian Sea basin according to IUCN criteria. Criteria include medium in numbers, widespread range (75% of water bodies), absent in other water bodies in Iran, and present outside the Caspian Sea basin.

Further work

Although well-studied elsewhere, the biology of this species in Iran has not been investigated in detail.

Sources

Iranian material:  CMNFI 1970-0510, 21, 34.5-47.5 mm standard length, Gilan, Golshan River (37º26'N, 49º40'E); CMNFI 1970-0512, 25, 26.6-43.9 mm standard length, Gilan, Shalman River (37º08'N, 50º15'E); CMNFI 1970-0514, 2, 36.6-38.3 mm standard length, Gilan, Shafa River estuary (37º35'N, 49º09'E); CMNFI 1970-0520, 7, 28.9-45.0 mm standard length, Gilan, Astara River (ca. 38º25'N, ca. 48º52'E); CMNFI 1970-0526, 4, 30.7-43.2 mm standard length, Gilan, Safid River below Astaneh Bridge (37º19'N, 49º57'30"E); CMNFI 1970-0579, 8, 32.6-49.0 mm standard length, Gilan, Old Safid River estuary (37º23'N, 50º11'E); CMNFI 1970-0580, 5, 35.8-53.8 mm standard length, Mazandaran, river near Iz Deh (36º36'N, 52º07'E); CMNFI 1979-0265, 9, 16.1-47.4 mm standard length, Gilan, Anzali Mordab at Abkenar (37º28'N, 49º20'E); CMNFI 1979-0472, 6, 37.7-47.7 mm standard length, Mazandaran, stream west of Mahmudabad (36º37'N, 52º12'E); CMNFI 1980-0117, 3, 42.2-47.8 mm standard length, Gilan, Golshan River (37º26'N, 49º40'E); CMNFI 1980-0127,9, 32.6-43.0 mm standard length, Gilan, Caspian Sea near Hasan Kiadeh (37º24'N, 49º58'E).

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