Int. J. Aquat. Biol. (2015) 3(5): 282-289
E-ISSN: 2322-5270; P-ISSN: 2383-0956
Journal homepage: www.ij-aquaticbiology.com
© 2015 Iranian Society of Ichthyology
Review Article
Review of the Silversides of Iran (Family Atherinidae)
Brian W. Coad*1
Canadian Museum of Nature, Ottawa, Ontario, K1P 6P4 Canada.
Article history:
Received 2 May 2015
Accepted 27 July 2015
Available online 2 5 October 2015
Keywords: Atherina, Biology, Morphology, Caspian Sea.
Abstract: The silversides are found in coastal areas of temperate to tropical seas and in fresh water.
There are about 14 genera and 68 species with only one native species in the Caspian Sea basin,
Atherina caspia. In this review, the systematics, morphology, distribution, biology, economic
importance and conservation of the Caspian silverside of Iran are described, the species is illustrated,
and a bibliography on this fish in Iran is provided.
Introduction
The freshwater ichthyofauna of Iran comprises a
diverse set of families and species. These form
important elements of the aquatic ecosystem and a
number of species are of commercial or other
significance. The literature on these fishes is widely
scattered, both in time and place. Summaries of the
morphology and biology of these species were given
in a website (www.briancoad.com) which is updated
here for one family, while the relevant section of that
website is now closed down. Other families will also
being addressed in a similar fashion.
Family Carcharhinidae
The silversides or sand smelts are found in coastal
areas of temperate to tropical seas and in fresh water.
There are about 14 genera and 68 species (Nelson,
2006; Eschmeyer and Fong, 2011) with only one
reported from the Caspian Sea and Iran. Coad (1987,
1998) and Coad and Abdoli (1996) place this species
in context with the Iranian ichthyofauna. Most are
small fishes with a maximum length of 60 cm.
These small, silvery fishes have a moderately
elongate body, usually cycloid and moderately large
scales, no lateral line but sometimes a pit on each
* Corresponding author: Brian W. Coad
E-mail address: bcoad@mus-nature.ca
scale, small teeth in the jaws and sometimes on the
roof of the terminal, upwardly-directed mouth, wide
gill openings with branchiostegal membranes free of
the isthmus, 5-6 branchiostegal rays, gill rakers
usually long and slender, two well-separated dorsal
fins, the first with 3-10 unbranched but flexible rays,
and the second with 1-2 unbranched and the rest
branched rays, anal fin long, pectoral fins high on the
flank, no pyloric caeca, egg membranes with
filamentous outgrowths, back bluish to greenish with
small melanophores but translucent, and a silvery
stripe along the flank, often distinctively outlined
with black.
Silversides can occur in vast schools in inshore
waters and are an important item in the diet of other
fishes. They have been used as bait but are too bony
to be much used as food. Their food is plankton.
Eggs are large and greenish. The sticky egg filaments
entangle with plants, rocks or sand as anchors until
hatching.
Genus Atherina Linnaeus, 1758
Members of this genus are found in fresh and
brackish waters with a single representative in Iran.
The record of Atherina hepsetus Linnaeus, 1758 in
the Caspian Sea by Quignard and Pras in Whitehead
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Coad/Silversides of Iran
et al. (1984-1986) is an error (Vasil'eva, 1994).
The body is compressed with a rounded belly, the
mouth large and terminal, jaws large, reaching back
to the anterior eye level or beyond, sides of the upper
jaw are straight and premaxillaries protractile, the
dentary bone has a high central portion, a
preopercular notch is absent, rows of setiform teeth
on the jaws, vomer and palatines, cycloid scales
extending onto the head, short pectoral fins, vent
nearer the pelvic fin origin than the anal fin,
numerous gill rakers, 5-10 flexible rays in the first
dorsal fin, and the second dorsal fin is similar in
length to the anal fin with its origin above the anal
fin.
Atherina caspia Eichwald, 1831
(Figs. 1-2)
Common names: Shisheh mahi (= glass fish), gol
azin mahi (= flower decoration fish), atrinka (from
the Russian). [aterinka or xazar aterini in Azerbaijan;
kaspi aterinasy in Turkmenian; Kaspiiskaya aterinka
or Caspian silverside in Russian; Caspian silverside,
Caspian sand smelt, big-scale sand smelt].
Systematics: Formerly called Atherina mochon
pontica natio caspia Eichwald, 1831 or Atherina
mochon caspia in Caspian Sea literature.
Atherina mochon Cuvier, 1829 was described
originally from Ivasa and Atherina presbyter pontica
Eichwald, 1831 from near Odessa, Ukraine. The
Caspian Sea taxon was also known as Atherina
boyeri Risso, 1810. Atherina boyeri was originally
described from the sea shore and lower course of
rivers in the Département du Var, France.
Reshetnikov et al. (1997) give the date for this
species as 1826.
Atherina presbyter var. caspia Eichwald, 1831
described from "in Caspii maris littore australiore,
sinu balchanensi" (i.e., southern shore of the Caspian
Sea, Balkhan Bay) was considered a synonym of
Atherina boyeri. Naseka and Bogutskaya (2009)
consider caspia to be a full species and this is
followed by Esmaeili et al. (2014).
Syntypes of A. boyeri are in the Muséum national
d'Histoire naturelle, Paris under MNHN A-4342 (2)
and MNHN B-860 (1) (Eschmeyer's "Catalog of
Fishes", downloaded 29 August 2007). No types are
known for Atherina presbyter var. caspia.
Bamber and Henderson (1985) demonstrated how
the morphology of Atherina presbyter around Britain
varies according to temperature and salinity during
embryonic development. Isolation of populations
results in local selection and random genetic drift
and thus recognisable morphologies but these were
not recognised as distinct. Kottelat (1997) reviewed
literature reports of variation in this species in the
Mediterranean and Black seas and neighbouring
fresh waters and concludes that lacustrine
populations should be called A. boyeri while marine
populations are A. mochon. The status of Caspian
populations was not commented on. These studies
showed how variable these related silversides are
and why the definition and limitation of species has
been varied.
The silverside in the Caspian Sea was referred to as
Atherina boyeri caspia by Savenkova and Asanov
(1991) and by Vasil'eva (1994, 1996) and this
seemed a reasonable step as the population is
isolated from other populations in the Atlantic Ocean
and Mediterranean Sea. The subspecies was
Figure 1. Line drawing of Atherina caspia by S. Laurie-Bourque.
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Int. J. Aquat. Biol. (2015) 3(5): 282-289
characterised by a reduced number of infraorbital
bones (3 bones in Caspian Sea fish as opposed to 4
in Black Sea fish; apparently infraorbital bones 2 and
3 fuse), a reduced number of gill rakers (generally
19-27 as opposed to 27-37), and the form of the
maxilla (the inferior margin in Caspian Sea fish is
always smooth while in the Black Sea and Sea of
Azov a "wing" is usually developed). However,
Kiener and Spillman (1972) allocated Caspian
populations to this subspecies on the basis of larger
size, hardly an adequate criterion. Vasil'eva (1994)
makes the allocation based on a reduced number of
gill rakers, reduction of the number of bones around
the eye to three (preorbital, infraorbital and
postorbital) and a smooth lower margin to the
maxilla without a wing protuberance.
Dobrovolov and Ivanova (1999) studied two non-
enzymatic proteins and 11 enzymes for putative
Atherina boyeri and A. mochon pontica. They
concluded that these are distinct species and indeed
the Black Sea fish are a distinct species, A. pontica.
They diverged 2.316 MYA. These authors did not
examine Caspian Sea material. Miller in Miller
(2003) followed a conservative approach, regarding
the various named and wide-ranging populations as
representing a single polymorphic species.
Key characters: The two dorsal fins, cycloid scales,
pectoral fin high on the flank and the vent remote
from the anal fin are characteristic.
Morphology: First dorsal fin spines 5-10, second
dorsal fin with 1-2 spines and 8-15 soft rays, anal fin
with 1-2 spines and 9-18 soft rays, pectoral branched
rays 10-17, usually 12-15, pelvic fin with 1 spine 5-
7, usually 5, branched rays, lateral series scales 37-
53 (possibly to 61, see Vasil'eva (1994)), total gill
rakers 19-29 in the Caspian Sea, spinulose on the
interior surface, and long and reaching about 7 rakers
along the arch when appressed, and vertebrae 39-52.
Note narrower ranges for all preceding meristic
characters for Iranian material given below. The
anus is 4-5 scales in advance of the anal fin. Scales
are higher than broad, with slight indentations on the
otherwise straight dorsal and ventral margins, a
rounded posterior margin, and a wavy to rounded
anterior margin with a protuberant central point.
There are no radii. Circuli are restricted to the
anterior third of the scale with a central and vertical
roughened area posterior to the circuli, presumably
made up of fragmented circuli. The focus is central.
The lower jaw symphysis fits into a notch in the
upper jaws. The haemal arches of the anterior 4-7
caudal vertebrae are expanded around the gas
bladder. The gut is s-shaped. The chromosome
number is 2n=48 (Klinkhardt et al., 1995).
Meristic values for Iranian specimens are: first dorsal
fin spines 8(28), 9(5) or 10(1); second dorsal fin soft
rays 11(10), 12(21), 13(2) or 14(1), anal fin soft rays
13(7), 14(15), 15(9) or 16(3), pectoral fin branched
rays 12(1), 13(12), 14(14) or 15(6), pelvic fin
branched rays 5 (34), caudal fin branched rays 13(1),
15(30), 16(2) or 17(1), lateral series scales 50(1),
51(10), 52(5), 53(3), 54(8), 55(3), 56(3) or 57(1),
predorsal scales 17(1), 18(2), 19(12), 20(8), 21(3),
22(3), 23(1), 24(3) or 26(1), caudal peduncle scales
12(31), 13(2) or 14(1), transverse scales from anal
fin antero-dorsally 10(2), 11(6), 12(23) or 13(3),
total gill rakers 24(3), 25(4), 26(14), 27(8), 28(4) or
29(1), and total vertebrae 45(1), 46(19), 47(7) or
Figure 2. Atherina caspia, Anzali Shore, December 2009, courtesy of K. Abbasi.
285
Coad/Silversides of Iran
48(7).
Sexual dimorphism: Females tend to be larger than
males and there are some differences in
morphometrics and meristics (Ghoorbanalidoost et
al., 2003).
Colour: General colour is given in the family
account. The lateral band is strongly developed and
bright in Caspian Sea specimens. The belly is white,
fins are pale to translucent grey. Lagoon specimens
are brownish or grey-brown on the back. The
peritoneum is brown to black, eggs being encased in
a black peritoneum while the abdomen wall is a light
brown.
Size: Reaches 11.8 cm and 17.6 g in the Atrak River
(Savenkova and Asanaov, 1991), to 14.5 cm
standard length in the Caspian Sea basin generally
(Henderson and Bamber, 1987). Kiener and
Spillman (1972) found a maximum of 15.4 cm in
their Caspian Sea sample and Patimar et al. (2009)
found 12.8 cm total length for their sample of 2256
fish in the Gomishan Wetland.
Distribution: Found in the Caspian Sea and the
Uzboi Valley of Turkmenistan. In Iran, it is reported
along the whole Caspian Sea coast, and from the
Safid, Tajan, Tonekabon, Havigh, Karkan, Chalus,
Farahabad, Langarud, Siahrud, Sheikan, Shafa, Talar
and Atrak rivers, Gomishan Lagoon or Wetland,
Boojagh Wetland, Anzali Lagoon and the Sowsar
Roga outlet of the lagoon seasonally, the Caspian
Sea at Bandar Anzali breakwater and beach, Hasan
Kiadeh, Kazian Beach and west of Chalus, Gorgan
Bay, Alma-Gol, Adji-Gol and Ala-Gol (Savenkova
and Asanov, 1991; Holčík and Oláh, 1992; Roshan
Tabari, 1997; Karimpour, 1998; Abbasi et al., 1999;
Kiabi et al., 1999; Afraie and Lalooie, 2000; Khara
et al., 2004; Abbasi, 2006; Patimar, 2008b; Abdoli
and Naderi, 2009; Patimar et al., 2009; Esmaeili et
al., 2014).
Zoogeography: This species probably entered the
Caspian Sea from the Black Sea during Khvalyn
transgression (10-70,000 years B.P.) via the Kumo-
Manych Depression (Kosarev and Yablonskaya,
1994). Berg (1948-1949) contends that it entered the
Caspian from the Black Sea in post-glacial times
while most other Caspian fishes are relicts of earlier
transgressions or migrants from northern waters.
Habitat: The Caspian silverside is a schooling fish
found at depths exceeding 100 m but is concentrated
at 10-20 m. Salinity tolerance is high, up to 77‰
(Miller in Miller, 2003), up to 60‰ in the Atrak
River (Savenkova and Asanov, 1991). Reproduction
can occur up to 42‰ while preferred levels are 3-
12‰. A wide temperature range is tolerated, 0-31ºC
(Miller in Miller, 2003). It is also found in lagoons
and river mouths, and enters rivers to spawn, against
currents up to 1.2 m/sec. It is the dominant species in
the Gomishan Wetland in spring, summer and
autumn (Patimar et al., 2009). Holčík and Oláh
(1992) report its apparent recent occurrence in the
Anzali Lagoon in response to increased salinity
there. It is also known from fresh water in Lenkoran.
It can rapidly adjust its life history to a range of
environments, from fresh water to coastal water.
Age and growth: Maturity is attained in the first year
and life span varies from 1 to 5 years, 4-5 years
usually in the Caspian Sea basin (Henderson and
Bamber, 1987). Ghoorbanalidoost et al. (2003)
found populations in the south Caspian Sea to be
73.82 mm long on average and 3.15 g in weight, with
age groups 1-3 years, average 1.7 years, total length
and length-weight relationship W=0.00000615L3.02
and a sex ratio of male:female=0.47:0.53.
Heydarnejad (2009) gave the length-weight
relationship for an Iranian sample as
W=0.0326TL3.033. Patimar (1995) and Patimar et al.
(2009) found 2256 fish from the Gomishan Wetland
had a 4-year life cycle (to age 4+ years). Length-
weight relationships were W=0.0053TL3.0181 for
males and W=0.0050TL3.063 for females, both
allometrically positive. The von Bertalanffy
equation was Lt=155.17[1-exp-0.28(t+0.738)] for
males and Lt=162.77[1-exp-0.27(t+0.727)] for
females. The sex ratio was male:female 1:1.3 and
females dominated in the older age classes. Amri
Sahebi et al. (2015) examined 191 fish from the
southeast coast of the Caspian Sea and found an
average fork length of 7.7 cm, weight 3.64 g and age
2 years.
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Int. J. Aquat. Biol. (2015) 3(5): 282-289
Food: Savenkova and Asanov (1991) report
plankton, eggs and juvenile fishes to be food items
in the Atrak River of Turkmenistan. Some
populations also eat benthic organisms such as
amphipods, worms and molluscs. Some Iranian
specimens contained encysted cladocerans and
beetles in their guts. It has a trophic plasticity,
adapting to whatever conditions obtain (Miller in
Miller, 2003). Amri Sahebi et al. (2015) examined
this fish in the southeast coastal waters of the
Caspian Sea, finding it to be an opportunistic and
carnivorous fish and a relatively voracious feeder.
Benthic Gammarus and the zooplankton Daphnia
were favoured foods and various other cladocerans
along with copepods, ostracods, nematodes and
dipterans were taken.
Reproduction: Spawning in this species is
intermittent and occurs along the coast from May to
July, peaking in mid-May to mid-June (Savenkova
and Asanov, 1991) or from April to August
(Henderson and Bamber, 1987). Preserved Iranian
fish samples have relatively large eggs from April to
September, e.g., 1.4 mm on 27 April, 1.6 mm on 14
May. Savenkova and Asanov (1991) also studied the
annual spawning migration into the Atrak River
(lower reaches in Turkmenistan, upper reaches
shared with Iran). Fish are caught in a fish ladder 18-
19 km from the sea and in the river. The first schools
appear in the Atrek mouth as early as mid-February
at water temperatures of 8-10°C but the mass
migration takes place in mid to late March and the
first half of April at 14-22°C. Spawning occurs in
March, April and May but most intensively in April
at flood water temperatures of 13.7-23.0°C. There is
a larger migration in high-water years. Sex ratio is
about 1:1. A female may be able to spawn 5-6 times
in one season so that egg numbers and diameters
vary within each individual for different generations
of eggs. Egg deposition in the Caspian Sea is
associated with the alga Cladophora to which the
eggs are attached or entangled by long filaments (up
to 15) and this plant is present in the Atrak. Egg
diameters may reach up to 2.0 mm and the light
yellow eggs number up to 5500 (Caspian Sea
Biodiversity Database, www.caspianenvironment.o-
rg) presumably total seasonal fecundity. Only one
gonad develops. Larvae are pelagic but may school
close to shore. Patimar et al. (2009) for their
Gomishan study found the reproductive season was
March-July, peaking in March. Average absolute
and relative fecundities were 2976 eggs and 784 eggs
g-1 of body weight respectively (874 in the abstract).
Maximum fecundity was 10,188 eggs for a 4+ fish.
Mean oocyte diameter was 0.68 mm.
Parasites and predators: The Caspian seal, Pusa
caspica, is a predator on this species (Krylov, 1984)
as are the larger fishes such as Stenodus leucichthys
and Alosa saposchnikowii (Lönnberg, 1900) and the
sturgeons Acipenser persicus and A. stellatus
(Haddadi Moghadam et al., 2009).
Economic importance: This species is food for a
number of other fishes including such economic
species as sturgeons, Sander and the predacious
shads. It has been caught as a by-catch in kilka seine
nets and used in fishmeal production. In Europe, the
related A. boyeri has been sold fresh or canned, and
in Turkey has been investigated as a food in the form
of fish chips (Izci et al., 2011).
Conservation: Kiabi et al. (1999) consider this
species to be of least concern in the south Caspian
Sea basin according to IUCN criteria. Criteria
include abundance in numbers, widespread range
(75% of water bodies), absent in other water bodies
in Iran, and present outside the Caspian Sea basin.
The IUCN (2014) has not assessed this species.
Sources: Further details on collections examined can
be found in the museum catalogues.
Iranian material: CMNFI 1970-0507, 11, 22.2-56.3
mm standard length, Gilan, Caspian Sea at Hasan
Kiadeh (37º24'N, 49º58'E); CMNFI 1970-0509, 5,
49.5-101.7 mm standard length, Gilan, pond at
Hasan Kiadeh (37º24'N, 49º58'E); CMNFI 1970-
0543A, 7, 52.9-83.1 mm standard length, Gilan,
Caspian Sea at Hasan Kiadeh (37º24'N, 49º58'E);
CMNFI 1970-0563, 18, 39.8-112.5 mm standard
length, Gilan, Kazian Beach (ca. 37º29'N, ca.
49º29'E); CMNFI 1970-0581, 5, 47.6-54.8 mm
standard length, Caspian Sea near Hasan Kiadeh
287
Coad/Silversides of Iran
(37º24'N, 49º58'E); CMNFI 1970-0586, 7, 33.4-84.9
mm standard length, Mazandaran, Gorgan Mordab at
Ashuradeh-ye Kuchak (36º50’N, 53º56’E); CMNFI
1971-0343, 2, 65.9-72.5 mm standard length, Gilan,
Langarud at Chamkhaleh (37º13'N, 50º16'E);
CMNFI 1979-0081, 3, 74.1-77.3 mm standard
length, Mazandaran, Caspian Sea, 3 km west of
Chalus (36º41'N, 51º24'E); CMNFI 1980-0127, 6,
39.7-44.4 mm standard length, Gilan, Caspian Sea
near Hasan Kiadeh (37º24’N, 49º58’E); CMNFI
1980-0146, 4, 92.1-103.6 mm standard length,
Mazandaran, Gorgan Mordab at Ashuradeh-ye
Kuchak (36º50'N, 53º56'E); and CMNFI 1980-0160,
2, 49.2-73.8 mm standard length, Iran, Caspian Sea
basin (no other locality data); CMNFI 1993-0144, 1,
75.3 mm standard length, Mazandaran, Neka Power
Plant (36º51’48”N, 53º23’24”E); CMNFI 2008-
0105, 1, 87.6 mm standard length, Gilan, Bandar
Anzali breakwater (37º26’N, 49º29’E).
Acknowledgements
I am indebted to the Department of Biology, Shiraz
University and the Canadian Museum of Nature,
Ottawa for funding of research. Numerous
colleagues and co-authors assisted in developing the
website on Iranian fishes, providing specimens, data
and photographs and are listed at
www.briancoad.com.
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Int. J. Aquat. Biol. (2015) 3(5): 282-289
E-ISSN: 2322-5270; P-ISSN: 2383-0956
Journal homepage: www.ij-aquaticbiology.com
© 2015 Iranian Society of Ichthyology
چکیده فارسی
(Atherinidae)خانواده ایران گل آذین ماهیانمروری بر
برایان کد
نادا.، کاK1P 6P4انتاریو، ، موزه تاریخ طبیعی کانادا، اتاوا
چکیده:
گونه در این خانواده 86جنس و 41شوند. حدود معتدله تا گرمسیری و آبهای شیرین یافت میدر نواحی ساحلی دریاهای ماهیان آذین گل
شناسی، یستماتیک، ریختشود. در این مقاله مروری، سدر دریای خزر یافت می Atherina caspiaوجود دارد که تنها یک گونه بومی بنام
هرستفشود. همچنین یک شده و به تصویر کشیده میایران توصیف گونه گل آذین خزری شناسی، اهمیت اقتصادی و حفاظت پراکنش، زیست
گردد.در مورد این ماهی در ایران ارائه میمنابع
.دریای خزرشناسی، شناسی، ریختزیست ،Atherina :کلمات کلیدی