Journal of Marine Biology

Volume 2013 (2013), Article ID 134263, 7 pages

http://dx.doi.org/10.1155/2013/134263

Research Article

List of Zooplankton Taxa in the Caspian Sea Waters of Iran

Siamak Bagheri,¹ Jalil Sabkara,¹ Alireza Mirzajani,1,2 Seyed Hojat Khodaparast,¹ Esmaeil Yosefzad,¹ and Foong Swee Yeok³

¹Inland Waters Aquaculture Institute, Iranian Fisheries Research Organization (IFRO), Anzali 66, Iran

²Faculty of Natural Resources, University of Tehran, P.O. Box 4314, Karaj 31587-77878, Iran

³School of Biological Sciences, Universiti Sains Malaysia, 11800 Penang, Malaysia

Received 26 June 2012; Revised 15 September 2012; Accepted 14 October 2012

Academic Editor: E. A. Pakhomov

Copyright © 2013 Siamak Bagheri et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract.

A total of 61 zooplankton taxa were found in the southwestern Caspian Sea between 1996 and 2010. Thirteen of them were meroplankton taxa and forty-eight were holoplankton taxa. The occurrence of 14 freshwater taxa indicated the influence of the Anzali wetland and river inflows. The decrease in zooplankton taxa was detected since 1996-1997 and continued till 2010. Pleopis polyphemoides, the only one out of the nine recorded Cladocera species in 1996-1997, was found after 2001. Similarly, of the five Copepoda species recorded in 1996-1997, only one, Acartia tonsa, was found abundant during the 2001–2010 sampling period. It was striking that many species which were abundant in the Caspian Sea in 1996-1997 were not found after 2000. Many reasons could have contributed to the changes in the zooplankton composition of the southern Caspian Sea, notably the serious environmental degradation since the early 1990s. It is also possible that invasive species might play a role in wiping out some sensitive endemic species.

1. Introduction

The Caspian Sea is a large inland water body. It is called a sea even though not being directly connected to any marine system due to its large size [1]. Water is mainly sourced from the big river Volga in the north (almost 76.3% of the total), and other rivers like Kura, Ural, Terek, and Sefidrood [2]. In the Iranian coast, the Sefidrood river is the largest river pouring into the Caspian Sea with 67,000 km² of catchment area and an average discharge of 4,037 million m³ per year [3, 4]. The Caspian Sea has undergone significant ecological alteration during the past 30 years. This could be linked to dramatic changes in the southern Caspian Sea due to increased pollution: sewage, industry effluent, and agricultural waste water discharges into the river as well as deforestation of the river’s watersheds [5, 6].

Zooplankton is recognized among the best indicators to be particularly useful to investigate and document environmental changes [7]. Main zooplankton taxa have short life cycle and the community structure is able to reflect real-time scenario as it is less enforced by the stability of individuals from previous years [8]. Besides this, zooplankton is also the food of choice for many fishes and as such plays a very significant role in pilaring the upper stages of the food chain [9].

Bagirov [10] reported that the number of zooplankton taxa was almost 200 in the northern Caspian Sea with 70 taxa of Protista, 50 taxa of Rotatoria, 30 taxa of Cladocera, and 20 taxa of Copepoda. Meroplankton, represented mainly by larvae of bivalves and crustaceans, contributed to the biodiversity of plankton communities in the North. Whereas in the South of Caspian Sea, Hossieni et al. [11] documented that zooplankton community consisted of 36 taxa, including Cladocera (24 taxa), Copepoda (7 taxa), and meroplankton (2 taxa) along the Iranian coastal area of the Caspian Sea in 1996. Subsequently in 1999, Sabkara et al. [12] reported over 50 zooplankton taxa with holoplankton comprising >80% of the taxa sampled and Rotifera (22 species) dominating. Meroplankton accounted for the remaining diversity. Recently, Roohi et al. [13] noted that only 18 zooplankton taxa were observed in the southern Caspian Sea, of which five taxa belonged to holoplankton (four Copepoda and one Cladocera) and 13 to meroplankton.

In recent years, few studies have been conducted on the distribution and abundance of zooplankton in the southern Caspian Sea [11–14], while there was hardly any work done to look at the composition of zooplankton taxa. In order to investigate the state of ecological condition of the Caspian Sea, an eleven-year study of the zooplankton community in the Caspian Sea waters of Iran was compiled between 1996 and 2010.

2. Materials and Methods

2.1. Study Area

The area under investigation is located at the southwestern corner of the Caspian Sea. The identification of zooplankton taxa was carried out along three transects along the mouth of the Anzali wetland, Lisar and Sefidrood rivers. The sampling was performed at 5 m, 10 m, 20 m, and 50 m depths during 1996–2010 (Figure 1). Table 1 shows the seasonal sample collection done in between 1996–2010. In some years, sampling was unable to be carried out due to logistic problems. In total, a collection of 132 samples were carried out during these periods (Table 1).

Table 1: “×” denotes sampling done based on season in the Caspian Sea waters of Iran during 1996–2010.

Year
Season

Winter
Spring
Summer
Autumn

1996

×
×
×

1997
×

2001
×

×
×

2002
×
×
×
×

2003
×

×

2004
×
×
×
×

2005
×
×
×
×

2006
×

×
×

2008
×
×
×
×

2009

×
×

2010
×
×

×

Figure 1: Study sites sampled 1996 to 2010 in the Caspian Sea waters of Iran. L = Lisar, A = Anzali, S = Sefidrood, 5 m (L1, A1, S1), 10 m (L2, A2, S2), 20 m (L3, A3, S3), and 50 m (L4, A4, S4).

2.2. Data Collection

Zooplankton was sampled using a Juday net (opening diameter: 36 cm, mesh size: 100 μm). At every station, a vertical haul with a Juday net was carried out from bottom to surface using a handle pulley for heaving the net. Zooplankton samples were preserved in neutral 4% formaldehyde and analyzed in the laboratory. Samples were divided into subsamples using a 1 mL Hensen-Stempel pipette and transferred to a Bogorov chamber for identification. At least 100 individuals were counted per sample and identified to species, and life-cycle stages were determined using an inverted microscope [15]. Zooplankton taxonomic classification was performed based on Birshtain et al. [16], Kasimov [17], and James and Covich [18].

3. Results

A total of 61 zooplankton taxa belonging to 48 taxa of holozooplankton were found in the area of investigation (Tables 2 and 3). Fourteen of them, Pleroxus trigenellus O.F. Mueller, Chydorus sp. Leach, Moina sp. Baird, all Cladocera, the copepod Cyclops sp. Risso, Cyclops sp. nauplii and the rotifers Filinia sp. Vincent, Keratella cochlearis, Lecane sp. Nitzsch, Notholca acuminate Ehrenberg, Philodina sp. Ehrenberg, Polyarthera dolichoptera Idelson, Testudinella patina Hermann, Trichocerca sp. Lamarck, and Trichocerca caspia Tschugunoff are freshwater species in the area.

Table 2: Checklist of zooplankton taxa in the Caspian Sea waters of Iran during 1996–2010.

Holoplankton taxa
After appearance of Mnemiopsis leidyi

1996-1997
2001
2002
2003
2004
2005
2006
2008
2009-2010

Macrozooplankton

    Ctenophora:

        *Mnemiopsis leidyi A. Agassiz, 1865
−
+
+
+
+
+
+
+
+

Mesozooplankton

    Cladocera:

        Cercopagis pengoi Ostroumov, 1891
+
−
−
−
−
−
−
−
−

        Cercopagis prolongata G.O. Sara, 1897
+
−
−
−
−
−
−
−
−

        Chydorus  Leach, 1843
−
−
−
−
−
−
−
+
−

        Evaden anonyx G.O. Sars, 1897
+
−
−
−
−
−
−
−
−

        Moina  Baird, 1850
−
−
−
−
−
−
−
+
−

        Pleroxus trigonellus  O.F. Muller, 1785
−
−
−
−
−
−
−
+
−

        Podonevadne Gibitz, 1922
−
−
−
−
−
−
−
+
−

        Podonevaden angusta G.O. Sars, 1902
+
−
−
−
−
−
−
−
−

        Podonevaden camptonyx G.O. Sars, 1897
+
−
−
−
−
−
−
−
−

        Podonevaden trigona G.O. Sars, 1897
+
−
−
−
−
−
−
−
−

        Podon intermedius Lilljeborg, 1853
+
−
−
−
−
−
−
−
−

        *Pleopis polyphemoides Leuckart, 1859
+
−
+
−
+
+
+
+
+

        Polyphemus exiguus G.O. Sars, 1897
+
−
−
−
−
−
−
−
−

    Copepoda:

        *Acartia tonsa nauplii
+
+
+
+
+
+
+
+
+

        *Acartia tonsa Dana, 1849
+
+
+
+
+
+
+
+
+

        *Calanipeda aquae dulcis nauplii
+
−
−
−
−
−
−
−
−

        *Calanipeda aquae dulcis Kritchagin, 1873
+
−
−
−
−
−
−
−
−

        Cyclops nauplii
−
−
−
−
−
−
−
+
−

        Cyclops  Risso, 1826
+
+
−
+
+
+
−
+
+

        Eurytemora grimmi nauplii
+
−
−
−
−
−
−
−
−

        Eurytemora grimmi G.O. Sars, 1897
+
−
−
−
−
−
−
−
−

        Halicyclops sarsi Akatova, 1935
+
−
+
−
−
−
−
−
+

        Ectinosoma concinnum Akatova, 1935
+
−
−
−
−
−
−
+
−

        Limnocalanus grimaldii grimaldii nauplii
+
−
−
−
−
−
−
−
−

        Limnocalanus grimaldii grimaldii Guerne, 1886
+
−
−
−
−
−
−
−
−

    Rotifera:

        Brachionus Pallas, 1766
−
−
−
−
+
+
−
−
−

        Brachionus angularis Gosse, 1851
−
+
+
−
−
−
−
−
−

        Brachionus calyciflorus Pallas, 1766
−
−
+
−
+
+
+
−
+

        Brachionus plicatilis Muller, 1786
−
+
+
−
−
−
−
+
+

        Filinia Bory de St. Vincent, 1824
−
−
+
−
−
−
−
−
−

        Keratella cochlearis Gosse, 1851
−
+
+
+
−
−
−
+
+

        Lecane  Nitzsch, 1827
−
+
−
−
−
−
−
−
−

        Notholca acuminata Ehrenberg, 1832
−
−
+
−
−
−
−
−
−

        Philodina Ehrenberg, 1830
−
−
−
−
−
−
−
−
+

        Polyarthera dolichoptera Idelson, 1925
−
−
+
−
−
−
−
−
+

        Synchaeta Ehrenberg, 1832
+
+
+
+
+
+
+
−
+

        Synchaeta stylata Wierzejski, 1893
+
−
−
−
−
−
−
−
−

        Synchaeta vorax Rousselet, 1902
+
−
−
−
−
−
+
−
−

        Testudinella patina Hermann, 1783
−
−
−
−
−
−
−
−
+

        Trichocerca Lamarck, 1801
−
−
+
−
−
−
−
−
−

        Trichocerca capica Tschugunoff, 1921
−
−
+
−
−
−
−
−
−

Microzooplankton

    Ciliata:

        Codonella Haeckel, 1873
−
−
+
−
−
−
−
−
−

        Codonella relicta Minikiewich, 1905
−
+
+
−
−
−
−
−
+

        Tintinnopsis Stein 1867
−
+
+
−
−
−
−
−
−

        Tintinnopsis karajacensis Brandt, 1896
−
+
−
−
−
−
−
−
−

        Tintinnopsis tubulosa Levander, 1900
−
+
+
+
+
+
−
+
+

Meroplankton taxa (Mesozooplankton)

Arachnida Larvae Cuvier, 1812
+
−
−
−
−
−
−
+
+

Cirripedia:

    *Balanus sp. cypris Costa, 1778
+
+
+
+
+
+
+
+
+

    *Balanus sp. nauplii Costa, 1778
+
+
+
+
+
+
+
+
+

Crustacea:

    *Rhithropanopeus harrisii Gould, 1841
+
−
−
−
−
−
−
−
−

Foraminifera larvae
+
+
+
−
+
+
−
−
+

Bivalvia larvae Linnaeus, 1758
+
+
+
+
+
+
+
+
−

Nematoda larvae
−
−
−
−
+
+
+
+
+

Ostracoda larvae Latreille, 1802
−
−
+
−
−
−
−
−
−

Pisces larvae
+
+
+
−
+
+
+
+
+

Pisces ovae
+
+
−
−
+
+
+
+
+

Polychaeta:

    Hypania Ostroumouw, 1897
−
−
−
−
−
−
−
+
−

    Hediste diversicolor O.F. Muller, 1776
−
+
+
+
+
+
+
+
+

Porifera:

    Asteromeyenia Weltner, 1913
−
−
−
−
−
−
−
+
−

Cumacea:

    Pseudocuma G.O. Sars, 1865
+
−
−
−
−
−
−
−
−

*Alien taxa; bold font: freshwater taxa indicated the influence by river inflow.

Table 3: Zooplankton number of taxa (holomeroplankton) in the Caspian Sea waters of Iran during 1996–2010.

Zooplankton taxa
After appearance of Mnemiopsis leidyi
Number of taxa

1996-1997
2001
2002
2003
2004
2005
2006
2008
2009-2010

Ctenophora
0
1
1
1
1
1
1
1
1
1

Ciliata
0
4
4
1
1
1
0
1
2
5

Cladocera
9
0
1
0
1
1
1
5
1
13

Copepoda
11
3
3
3
3
3
2
5
4
12

Rotifera
3
5
10
2
3
3
3
2
7
17

Total holoplankton
23
13
19
7
9
9
7
14
15
48

Arachnida
1
0
0
0
0
0
0
1
1
1

Cirripedia
2
2
2
2
2
2
2
2
2
2

Crustacea
1
0
0
0
0
0
0
0
0
1

Foraminifera
1
1
1
0
1
1
0
0
1
1

Bivalvia
1
1
1
1
1
1
1
1
0
1

Nematoda
0
0
0
0
1
1
1
1
1
1

Ostracoda
0
0
1
0
0
0
0
0
0
1

Pisces
2
2
1
0
2
2
2
2
2
2

Polychaeta
0
1
1
1
1
1
1
2
1
1

Porifera
0
0
0
0
0
0
0
1
0
1

Pseudocuma
1
0
0
0
0
0
0
0
0
1

Total meroplankton
9
7
7
4
8
8
7
10
8
13

Total zooplankton
32
20
26
11
17
17
14
24
23
61

Thirteen meroplankton taxa consisted of individuals of water spiders (Arachnida), crab (Rhithropanopeus harrisii Gould), Foraminifera, Ostracoda larvae, Asteromeyenia sp. Weltner, Pseudocuma sp. G.O. Sars, and larvae of Bivalvia, Nematoda, Polychaeta (Hediste diversicolor O.F. Muller, Hypania sp. Ostroumouw), Pisces (egg and larvae), and multitudinous Cirripedia (Balanus sp. Costa) represented by nauplii and cypris larvae (Table 2).

Thirty-four holoplankton taxa belong to Ctenophora (Mnemiopsis leidyi A. Agassiz), Ciliata (Codonella sp. Haeckel, Codonella relicta Minikiewich, Tintinnopsis sp. Lamarck, Tintinnopsis karajacensis Brandt, and Tintinnopsis tubulosa Levander), Rotifera (Brachionus sp. Pallas, Brachionus angularis Gosse, Brachionus calyciflorus Pallas, Brachionus plicatilis Mueller, Synchaeta sp. Ehrenberg, Synchaeta stylata Wierzejski, and Synchaeta vorax Rousselet), Cladocera (Cercopagis pengoi Ostroumov, Cercopagis prolongata G.O. Sars, Evaden anonyx Sars, Podonevadne sp. Gibitz, Podonevaden angusta G.O. Sars, Podonevaden camptonyx G.O. Sars, Podonevaden trigona G.O. Sars, Podon intermedius Lilljeborg, Pleopis polyphemoides Leuckart, and Polyphemus exiguus G.O. Sars), and Copepoda (Acartia tonsa Dana, Calanipeda aquae dulcis Kritchagin, Eurytemora grimmi G.O. Sars, Halicyclops sarsi Akatova, Ectinosoma concinnum Akatova, and Limnocalanus grimaldii grimaldii Guerne).

The Copepoda (Eurytemora grimmi, Limnocalanus grimaldii grimaldii, Acartia tonsa, Ectinosoma concinnum, and Halicyclops sarsi), Cladocera (Podonevaden trigona, Pleopis polyphemoides, Polyphemos exiguus), Cirripedia (Balanus sp.), Polychaeta (Hediste diversicolor), Bivalvia larvae, and Ctenophora (Mnemiopsis leidyi) dominated the zooplankton taxa in all seasons in the southwestern Caspian Sea (Table 4).

Table 4: Seasonal list of zooplankton taxa in the Caspian Sea waters of Iran during 1996–2010.

Group
Zooplankton taxa
Season

Winter
Spring
Summer
Autumn

Arachnida
Arachnida larvae
+
−
−
+

Bivalvia
Bivalvia larvae
+
+
+
+

Ciliata
Codonella sp.
+
−
−
−

Ciliata
Codonella relicta
+
−
−
−

Ciliata
Tintinnopsis sp.
+
−
−
−

Ciliata
Tintinnopsis karajacensis
+
−
−
+

Ciliata
Tintinnopsis tubulosa
+
−
+
+

Cirripedia
Balanus sp. cypris
+
+
+
+

Cirripedia
Balanus sp. nauplii
+
+
+
+

Cladocera
Cercopagis pengoi
−
−
−
+

Cladocera
Cercopagis prolongata
−
−
−
+

Cladocera
Chydorus sp.
+
−
−
−

Cladocera
Evaden anonyx
−
+
−
+

Cladocera
Moina sp.
−
−
−
+

Cladocera
Pleroxus trigonellus
−
−
−
+

Cladocera
Podonevadne sp.
−
+
−
−

Cladocera
Podonevaden angusta
+
−
−
+

Cladocera
Podonevaden camptonyx
−
+
−
−

Cladocera
Podonevaden trigona
+
+
+
+

Cladocera
Podon intermedius
+
−
−
−

Cladocera
Pleopis polyphemoides
+
+
−
+

Cladocera
Polyphemus exiguus
+
+
+
+

Copepoda
Acartia tonsa nauplii
+
+
+
+

Copepoda
Acartia tonsa
+
+
+
+

Copepoda
Calanipeda aquae  dulcis nauplii
+
+
+
+

Copepoda
Calanipeda aquae  dulcis
+
+
+
+

Copepoda
Cyclops nauplii
+
−
−
+

Copepoda
Cyclops sp.
+
−
−
+

Copepoda
Eurytemora grimmi nauplii
+
+
+
+

Copepoda
Eurytemora grimmi
+
+
+
+

Copepoda
Halicyclops sarsi
+
+
+
+

Copepoda
Ectinosoma concinnum
+
+
+
+

Copepoda
Limnocalanus grimaldii grimaldii nauplii
+
+
+
+

Copepoda
Limnocalanus grimaldii grimaldii
+
+
+
+

Ctenophora
Mnemiopsis leidyi
+
+
+
+

Crustacea
Rhithropanopeus harrisii
+
−
−
+

Cumacea
Pseudocuma sp.
−
−
−
+

Foraminifera
Foraminifera larvae
−
+
+
−

Nematoda
Nematoda larvae
+
+
−
+

Ostracoda
Ostracoda larvae
+
−
−
−

Pisces
Pisces larvae
+
−
+
−

Pisces
Pisces ovae
+
+
−
−

Polychaeta
Hypania sp.
−
−
+
+

Polychaeta
Hediste diversicolor
+
+
+
+

Porifera
Asteromeyenia sp.
−
+
−
+

Rotifera
Brachionus sp.
+
+
−
+

Rotifera
Brachionus angularis
+
+
−
+

Rotifera
Brachionus calyciflorus
+
+
−
+

Rotifera
Brachionus plicatilis
+
+
−
+

Rotifera
Filinia sp.
+
−
−
−

Rotifera
Keratella cochlearis
+
−
−
−

Rotifera
Lecane sp.
+
−
−
−

Rotifera
Notholca acuminata
+
−
−
−

Rotifera
Philodina sp.
−
+
−
−

Rotifera
Polyarthera dolichoptera
−
+
−
−

Rotifera
Synchaeta sp.
+
+
−
−

Rotifera
Synchaeta stylata
+
+
−
+

Rotifera
Synchaeta vorax
+
+
−
+

Rotifera
Testudinella patina
−
−
−
+

Rotifera
Trichocerca sp.
+
+
−
−

Rotifera
Trichocerca capica
+
−
−
−

Bold font: freshwater taxa indicated the influence by river inflow.

4. Discussion

In comparison with earlier surveys by Hossieni et al. [11] and Roohi et al. [13] which were carried out in the southern Caspian Sea, major changes in zooplankton community became obvious after 2000 (Tables 2 and 3). During the present study, 26 taxa including Codonella sp. and Codonella relicta (Ciliata); Tintinnopsis sp., Tintinnopsis karajacensis, and Tintinnopsis tubulosa (Ciliata); Brachionus sp., Brachionus angularis, Brachionus calyciflorus, and Brachionus plicatilis (Rotifera); Filinia sp. (Rotifera), Keratella cochlearis (Rotifera), Lecane (Rotifera), Notholca acuminata (Rotifera), Philodina (Rotifera), Polyarthera dolichoptera (Rotifera), Synchaeta sp. (Rotifera), Synchaeta stylata, Synchaeta vorax (Rotifera), Testudinella patina (Rotifera), Trichocerca (Rotifera), and Trichocerca capica; Podonevadne sp. (Cladocera); Rhithropanopeus harrisii (Crustacea); Asteromeyenia sp. (Porifera); Pseudocuma sp. (Cumacea) and Hypania larvae (Polychaeta) were documented. Hossieni et al. [11] and Roohi et al. [13] listed none of these taxa. Hossieni et al. [11] did not list the following species, which were sampled in subsequent years: Ostracoda larvae, Arachnida larvae, Harpacticoida (Ectinosoma concinnum), Nematoda larvae, and Hediste diversicolor. Roohi et al. [13] listed Chironomidae, Nematidae, and Mysidacaea ( in 2006), which were not observed in this study.

Hossieni et al. [11] listed 24 Cladocera species in the southern Caspian Sea (cited by Roohi et al., [13]). Three of these taxa were repeated twice under different names as Apagis cylindrata (Cercopagis cylindrata), Apagis longicaudata (Cercopagis longicaudata), and Apagis ossiani (Cercopagis ossiani). Additionally fourteen taxa cited were not recognized as validly published taxa by CSBP (Caspian Sea Biodiversity Project), ITIS (Integrated Taxonomic Information System), MarBEF (Marine Biodiversity and Ecosystem Functioning), and WoRNS (World Register of Marine Species), while there were nine Cladocera listed in the present study in 1996-1997 and only two of them (Pleopis polyphemoides and Podonevadne sp.) could be found after 2000. Five Copepoda species were present in 1996 [11] and the present study, but they were either absent or found in very low numbers during 2001 to 2010 (Table 2): Calanipeda aquae dulcis, Limnocalanus grimaldii, Eurytemora minor, and Eurytemora grimmi.

It was striking that many species which were abundant in the Caspian Sea since 1996-1997 were not found after 2000 (Tables 3 and 4). However, a similar drastic decline in species numbers was not observed in other invaded seas [19]. Possible reasons could be twofold: the endemic Caspian Sea fauna is very sensitive to disruptions of invaders [5, 20], or it a results of serious environmental degradation which started since the beginning of the 1990s [5]. Rodionov [21], Bilio and Niermann [22], and Polonskii et al. [23] theorized that hydrobiological changes in the Caspian Sea, Black Sea, and Baltic Sea during the 1990s and 2000s could definitely be correlated to these changes. Recent remarks on other seas indicated that the shifting plankton communities can also be related to climatic inconsistency [7, 24–26].

The survey helped to characterize the composition of the zooplankton taxa in the southwestern Caspian Sea between 1996 and 2010. In comparison with previous publications, the multiyear composition of zooplankton taxa was estimated for the first time. We call for a standardization in the result presentation during future studies in this area. A comprehensive database including international participation should be launched to facilitate long-term comparisons of planktonic species to monitor anthropogenic and climatic effects on the Caspian Sea ecosystem.

Acknowledgments

The authors are grateful to Peter Boyce for improving the English of the draft paper. They would like to thank the Inland Waters Aquaculture Institute and Iranian Fisheries Research Organization (IFRO) for financially supporting this project. They deeply appreciate the assistance received from F. Maddadi, Y. Zahmatkesh, M. Sayad-Rahim, A. Sedaghat-Kish, H. Norouzi, and M. Iran-Pour in this study.

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