Ichthyofauna in the Lower Course of the Sazliyka River, Southern Bulgaria: Composition, Diversity, Seasonal Dynamics and Conservation Significance

Abstract

Abstract: The species diversity and seasonal dynamics of the ichthyofauna in the lower course of the Sazliyka River,
a left tributary of the Maritsa River, are presented. The stretch of the river from the village of Lyubenovo
to the mouth was studied for a period of four years. The composition of the ichthyofauna of the river consisted
of 21 fish species of eight families. The family Cyprinidae had the highest number of species – 12,
with a total of 7631 captured individuals; this family included the most abundant species captured in this
river: Carassius gibelio – 3414, Alburnus alburnus – 2562, Squalius orpheus – 620 and Rutilus rutilus –
531 individuals. The ichthyofauna in the lower course of the river included 18 permanently inhabiting species.
Spawning migration from the Maritsa River was proven for two species (Chondrostoma vardarense
and Vimba melanops), while one species (Ctenopharyngodon idella) has accidentally entered the river.
Out of the four studied sampling sites, the greatest was the fish diversity at the confluence of the Sokolitsa
River (after Galabovo) and at the mouth of the Sazliyka River. Seventeen species are considered of conservation
significance according to the referred national and international sources. A total of three species
are listed in the Bulgarian Biodiversity Act (Annexes 2 and 4), one in the Bulgarian Red Data Book, one
in the Black Sea Red Data Book, three in the Bern Convention (Annex 3), 17 are in the IUCN Red List
and three are in the annexes of the Habitat Directive (92/43/EEC).

Full text

331
ACTA ZOOLOGICA BULGARICA
Acta zool. bulg., 70 (3), 2018: 331-338
*Corresponding author: zhivko-m@uni-plovdiv.bg
Zoogeography and Faunistics
Research Article
Introduction
Anthropogenic pollution of surface waters at the
end of the previous and the beginning of the pre-
sent century has become an environmental prob-
lem in global scale. To survey the mechanism of
the formation, functioning and stability of such
aquatic ecosystems is one of the biggest challenges
in modern ecology. The ichthyofauna in such water
bodies is directly damaged to the greatest extent.
-
ble when the anthropogenic impact and the adap-
tive capacity of the species are both known. This
would allow both identifying indicator species for
Ichthyofauna in the Lower Course of the Sazliyka River,
Southern Bulgaria: Composition, Diversity, Seasonal
Dynamics and Conservation Signicance
Zhivko M. Zhelev1*, Angel G. Tsekov2, Georgi S. Popgeorgiev3, Mladen V. Angelov4,
Peter S. Boyadzhiev5 & Tihomir R. Stefanov3
1Department of Human Anatomy and Physiology, Faculty of Biology, University of Plovdiv “Paisii Hilendarski”, 24 Tsar Assen
Street, 4000 Plovdiv, Bulgaria
2Department of Ecology, Faculty of Biology, University of Plovdiv “Paisii Hilendarski”, 24 Tsar Asen Street, 4000 Plovdiv 4000,
Bulgaria
3
4Basin Directorate, 35 Yanko Sakazov Street, 4000 Plovdiv, Bulgaria
5Department of Zoology, Faculty of Biology, University of Plovdiv “Paisii Hilendarski”, 24 Tsar Assen Street, 4000 Plovdiv,
Bulgaria
Abstract: The species diversity and seasonal dynamics of the ichthyofauna in the lower course of the Sazliyka River,
a left tributary of the Maritsa River, are presented. The stretch of the river from the village of Lyubenovo
to the mouth was studied for a period of four years. The composition of the ichthyofauna of the river con-

with a total of 7631 captured individuals; this family included the most abundant species captured in this
river: Carassius gibelioAlburnus alburnusSqualius orpheusRutilus rutilus
531 individuals. The ichthyofauna in the lower course of the river included 18 permanently inhabiting spe-
cies. Spawning migration from the Maritsa River was proven for two species (Chondrostoma vardarense
and Vimba melanops), while one species (Ctenopharyngodon idella) has accidentally entered the river.

River (after Galabovo) and at the mouth of the Sazliyka River. Seventeen species are considered of con-

are listed in the Bulgarian Biodiversity Act (Annexes 2 and 4), one in the Bulgarian Red Data Book, one
in the Black Sea Red Data Book, three in the Bern Convention (Annex 3), 17 are in the IUCN Red List
and three are in the annexes of the Habitat Directive (92/43/EEC).
Key words: Fish community, spatial distribution, species richness, Sazliyka River, catchment area of the Maritsa
River, anthropogenic pollution

332
Zhelev Z. M., A. G. Tsekov, G. S. Popgeorgiev, M. V. Angelov, P. S. Boyadzhiev & T. R. Stefanov
biomonitoring investigations and implementing
restoration activities.
Sazliyka is a typical Bulgarian internal river.
It belongs to the rivers of the Aegean Sea catch-
ment area whose ichthyofauna includes 13 endem-
ic species (   2010). The
Sazliyka River is exposed to an intense anthropo-
genic impact, which worsens the parameters of its
environment (Executive Environmental Agency
Bulgaria http://eea.government.bg). The entire eco-
system of the Sazliyka River (from the source to the
mouth) is classed by order RD-970/28.07.2000 as
an environmentally sensitive area under Directive
91/271/EEC. It is also a protected area included
in the Ecological Network NATURA 2000 (code
BG0000425) under Directive 92/43/EEC as well as
in the Plan for river basin management in the East
Aegean region, 2010-2015. In 1997, the Rozov
Kladenets Reservoir and some lands on its shores
were established as an Important Bird Area (in the
list of Bird Life International). It is located in the
region of the town of Galabovo and it is connected
with the Sazliyka River. In 1998, the reservoir was
declared a CORINE place because of its European
importance for the preservation of rare and endan-
gered bird species. In 2008, it was declared a pro-
tected area by NATURA 2000, code BG0002022.
The objective of this work is to examine the
      
        
and downstream to the mouth of the river. This is the

lower course of Sazliyka River to be published.
Materials and Methods
Studied area
The source of the Sazliyka River is at an altitude
of 651 m a. s. l. in Sredna Gora Mountain, north
of the Kazanka Village. Initially the river is called
Toplicite (Vurbitsa) and, when it reaches Stara
Zagora Mineral Baths, it is known as Banyanska
River. There it passes through the Rakitnitsa
Village (as Syutliyka or Rakitnitsa) and after the
    
         -
luvial valley under the name Sazliyka. Its two larg-
est left tributaries, the Blatnitsa (54 km long) and
        
town of Radnevo. One of the bigger left tributar-
ies, the river Ovcharitsa (71.5 km), has had its bed
changed since the 1990s by the coal mining conces-
sionaire Maritsa East Mines EAD in the town of

mouth, south of the village of Lyubenovo, where
 
stopped. The total length of the Sazliyka River is
145.4 km with a catchment area of 3300 km2. The
      
is 18.0 m3/s. The Sazliyka River is connected to the
technological process in the thermal power plants
Brikel and AES Galabovo. Water is diverted to the
Rozov Kladenets Reservoir, then it is pumped out
as raw water for cooling the turbines of the thermal
power plants and it is brought back in the reservoir.
Waste water, coming from the lake-sedimentation
-
fore the town of Galabovo.
Our study was carried out in 2009-2012 at
four sampling sites (labelled A, B, C and D) located
    
        
         
        
        -
Fig. 1. Geographical location of the studied water sites on
the Sazliyka River: Site A
water to TPP Brikel; Site B
River, south of the town of Galabovo; Site C  -
stream the village of Kalugerovo; Site D  
of the Maritsa River, south of the town of Simeonovgrad.

Ichthyofauna in the Lower Course of the Sazliyka River, Southern Bulgaria...
333
        
Simeonovgrad (Fig. 1).
The studied river area was 40 km long in
straight line. Locations A, B, C and D were 10-12
km apart from each other down on the river cur-
rent. The locations were chosen to be approximately
evenly spaced; site A was in located next to the in-
dustrial pollution source (TPP Brikel) and site D was
the most distant point.
The area of the Sazliika River is hydromorpho-
        
 
   

-
     
of the main river, the area is corrected in the middle of
the 20th century. On the main river there are two trans-
-
-

Plan in the East-Aegean Region 2016-2021).
Fish sampling
The material was collected in the period 2009-
2012, from April to October of each year. Catches
-
        
      
dragnet (seine net) and cast net. In the caches with

features, each stretch we covered was approximate-
ly 1-2 km long (repeated on each sampling occa-
sion) following  (1966) and 
(2000). Due to the strong current the best results
were obtained using a cash net. After identifying
the species, according to   
       
       
were also annalysed.
Statistical analysis
The Shannon index (entropy) was used to assess
the species diversity in each of the surveyed sites
according to the formula:
where ni is the number of individuals of taxon i.
Fisher’s alpha diversity index was calculated
using the formula S=a*ln (1+n/a) where S is num-
ber of taxa, n is number of individuals and a is the
Fisher’s alpha ( 1999). A given community
A is truly more diverse than community B if the
      
     
        
          


The calculations were performed using PAST,
version 3.0 ( et al. 2001).
Fig. 2. A
B
the town of Galabovo; CD  
mouth of the Maritsa River, south of the town of Simeonovgrad.

334
Zhelev Z. M., A. G. Tsekov, G. S. Popgeorgiev, M. V. Angelov, P. S. Boyadzhiev & T. R. Stefanov
Table 1. Species composition, numbers and conservation status of the ichthyofauna in the lower course of the Sazliyka River for
the entire study period 2009-2012.
Family Species Sites Total
A B C D
Esocidae Esox lucius (Linnaeus, 1758)
•IUCN (LC) 8 3 1 4 16
Cyprinidae
Alburnus alburnus (Linnaeus, 1758)
•IUCN (LC) 751 1123 267 421 2562
Barbus cyclolepis (Heckel, 1840)
•BBA (II, IV); HD (V); IUCN (CR) 5 47 4 3 59
Carassius gibelio (Bloch, 1782)
•IUCN (LC) 1356 777 478 803 3414
Chondrostoma vardarense (Karaman, 1928)
•IUCN (LC) 119   119
Cyprinus carpio (Linnaeus, 1758)
•IUCN (VU) 1 9 1 19 30
Ctenopharyngodon idella (Valenciennes, 1844)
•Alien 7 2 14 23
Gobio bulgaricus Drensky, 1926
•IUCN (LC) 4 8 2 15
Squalius orpheus (Kottelat & Economidis, 2006)
•IUCN (LC) 69 393 53 105 620
Pseudorasbora parva (Temminck & Schlegel, 1846)
•Alien - 3 - - 3
Rhodeus amarus (Bloch, 1782)
•BBA (II); HD (II); IUCN (LC) 3 8 2 13
Rutilus rutilus (Linnaeus, 1758)
•IUCN (LC) 45 407 6 73 520
Vimba melanops (Heckel, 1840)
•IUCN (DD) 253   253
Cobitidae Cobitis strumicae (Karaman, 1955)
•BBA (II); BC (III); HD (II); IUCN (LC) 3 8 2 13
Siluridae Silurus glanis (Linnaeus, 1758)
•BC (III); IUCN (LC) 2 4 1 6 13
Poeciliidae Gambusia holbrooki (Girard, 1859)
•Alien 4 35 4 11 54
Centrarchidae Lepomis gibbosus (Linnaeus, 1758)
•Alien 95 46 27 82 250
Percidae
Gymnocephalus cernua (Linnaeus,1758)
•Translocated 28 52 3 83
Perca uviatilis (Linnaeus, 1758)
•IUCN (LC) 33 41 4 23 101
Sander lucioperca (Linnaeus, 1758)
•IUCN (LC) 84 84 30 46 246
Gobiidae Proterorhinus semilunaris (Heckel, 1837)
•BSRBD (EN); BC (III); IUCN (LC) 1 4   5
Legend: Site ASite B
the mouth of the Sokolitsa River, south of the town of Galabovo; Site C
of Kalugerovo; Site D    
BBA-
servation requires the designation of protection areas for their habitat conservation; IV: Species under conservation and
regulated nature usage; BSRDBBC
on the conservation of European wildlife and natural habitats (Bern Convention), Annex III (Protected species); HD

Directive), Annex II (Animal and plant species of community interest whose conservation requires the designation
of special areas of conservation); BRDBIUCN  
International Union of Conservation the Nature (Categories: CRNTEN
endangered; VUDDLC

Ichthyofauna in the Lower Course of the Sazliyka River, Southern Bulgaria...
335
Results

caught during the whole study period 2009-2012
(Table 1).
The family Cyprinidae was the richest in spe-
cies in the surveyed river stretch: 12 species with
7631 individuals. The most common species of this
family were Carassius gibelio, Alburnus alburnus,
Squalius orpheus and Rutilus rutilus. Of the family
Percidae, we recorded three species: Sander lucio-
perca, Perca uviatilis and Gynnocephalus cernuus.
The other six families were represented by only one
species. Some species were presented by single indi-
viduals only: Esox lucius (Esocidae), Pseudorabora
parva (Cyprinidae), Cobitis strumicae (Cobitidae),
Silurus glanis (Siluridae) and Proterorhinus
semilunaris (Gobiidae). The alien Lepomis gib-
bosus (Centrarchidae) and Gambusia holbrooki

The data obtained during the four-year period
revealed that the number of species caught at sites
located in the upper course of the river (in the area of

Galabovo, site A and at the mouth of the Sokolitsa
River, site B), was higher than at the river mouth
(site D). In the course of the studied river stretch,
two species were the most numerous: C. gibelio and
A. alburnus       

C. idella does not permanently live in the river but
        
in the spring of 2008-2009, when the dykes of the
  -
aged.
The highest species diversity was registered at
site B, where a total of 21 species were found. The
      
Fig. 3. Seasonal dynamics and catch number of the most widely presented species and the ongoing migration breeding
species in the lower course of the Sazliyka River. The presented results are aggregate values by month for the entire
study period (2009-2012). Legend: AB-
zliyka River at the mouth of the Sokolitsa River, south of the town of Galabovo; C
village of Kalugerovo; D
Table 2.  
of the Sazliyka River. Legend: Sites: Site A    
Site BSite C
River downstream the village of Kalugerovo; Site D
the town of Simeonovgrad.
Sites Mean Lower Upper
A 1.291 1.245 1.336
B 1.981 1.943 2.014
C 1.23 1.163 1.303
D 1.539 1.479 1.595

336
Zhelev Z. M., A. G. Tsekov, G. S. Popgeorgiev, M. V. Angelov, P. S. Boyadzhiev & T. R. Stefanov

(Table 2, Fig. 2).
The data on the seasonal dynamics showed the
following features of the most common and predom-
inant species: S. orpheus had the highest presence
during the period from April to June at site B, which
coincided with the breeding period of the species; R.
rutilus was equally common in all years and months,
with higher numbers at site B; A. alburnus highest
presence was during the period May-July (the breed-
ing season); C. gibelio was very common mainly at
sites A and B. Two species, Chondrostoma varda-
rense and Vimba melanops, have likely entered from
the Maritsa River at site B in early spring (in April),
which is a typical spawning migration (Fig. 3).
Discussion
Monitoring and control of the Sazliyka River sur-
face water is performed by the National System
for Environmental Monitoring (NSEM). Based on
data from the annual report on the environmental
status for the period 2001-2012 from the Executive
Environmental Agency (http://eea.government.bg)
and the data on the physical and chemical parametres
of the Sazliyka River for 2001-2012 in the newslet-
ters of the Basin Directorate of Water Management
in the East Aegean Sea, Plovdiv (http://www.bg-ibr.
org), the river is considered one of the most polluted
in Bulgaria. The contamination exceeds the allowed

-
ly polluted) and Water Category III (moderately pol-
-
cators and standards for running waters in Bulgaria.
The main pollutants are nitrite nitrogen, phosphates
and suspended solids. Two “hot spots”, which are
of national importance, are marked along the river.


second one is after the town of Radnevo at the con-
 
Blatnitsa Rivers are polluted with domestic waste
waters and industrial discharge. A 12 km stretch
of the river in the area of Stara Zagora is extreme-
        
Zagora is also highly polluted. Near the town of
Radnevo, the wastewaters from the production site
of Remotex-Radnevo EAD are the major pollutant
of the Blatnitsa River. Since April 2011, a modern
wastewater treatment plant was put into operation at
the end of Stara Zagora. It has a three-stage treat-
ment system: mechanical, biological and tertiary
treatment for nitrogen and phosphorus. There are
facilities for anaerobic sludge treatment managing
the entire load of the Bedechka River. At the end of
Nova Zagora and Radnevo, the treatment facilities

nor phosphorus removal systems. This is the main
reason why the Blatnitsa River is considered a major
pollutant of the Sazliyka’s middle course (Regional
Development Strategy of the Stara Zagora Region
2014-2020).
The wastewaters from the processes in the sed-
        
     

  -
ment facilities. The chemical composition of this

site A are constantly isolated from the upstream part
of the river by sluices which are opened only during
freshets, but due to the strong current it is impossible
       
     -
jected to a great stress. In our view, namely the spo-
-

In a recent study conducted in the Maritsa River
downstream of Dimitrovgrad (north of the mouth of
the Sazliyka River),  (2005)

the family Cyprinidae was represented by 11 species
(A. alburnus, Aspius aspius, B. cyclolepis, Carassius
carassius Linnaeus, 1758, C. gibelio, Chondrostoma
nasus C. vardarense), G. go-
bio, R. rutilus, L. cephalus  
Scualius orpheus), R. amarus and V. malanops. The
family Centrarchidae was represented by Lepomis
gibbosus. The authors mention that during previous
research conducted in 1996-1997 and 2001 in the
same area of the Maritsa River, three more species
of the family Cyprinidae were found: Cyprinus car-
pio, Pseudorasbora parva and Scardinius erytroph-
thalmus, and one species of each of three families:
Cobitis taeniaЕ. lucius and
  G. holbrooki. In earlier studies from
th Century in the lower course
of the Maritsa River, several other species were also
mentioned; these were Anguilla anguilla, Abramis
brama, Barbus barbus (this species is mentioned by
some authors in the past but the contemporary au-
thors do not consider it a part of the ichthyofauna
of the Maritsa River and it has been never found
recently), Tinca tinca, Sabanejewia balcanica, S.
glanis, P. semilunaris, P. uviatilis and S. lucioperca
( 1921,  1931,  1939,
 1951,  1961,  1965).

Ichthyofauna in the Lower Course of the Sazliyka River, Southern Bulgaria...
337
Out of the species caught during the period
1996-2004 in the Maritsa’s lower course, we found
14 species in the Sazliyka River: A. alburnus, B.
cyclolepis, C. gibelio, C. vardarense, C. carpio, Е.
lucius, G. holbrooki, G. bulgaricus, S. orpheus, R.
amarus, R. rutilus, V. malanops, P. parva and L.
gibbosus. Three previously reported species were
not found by us: A. aspius, C. carassius and S. ery-
trophthalmus. Other two species, G. cernuus and C.
idella, were found in the Sazliyka River by us, while
they have not been reported by the last survey of the
Maritsa River (   2005). As
it was mentioned before, Ctenopharyngodon idella
has accidentally entered the river, as it is a species
unable to spawn and establish populations in natural
conditions; therefore, we cannot recognise it as a part
of the natural ichthyofauna of the Sazliyka River.
The comparative analysis of the literature sourc-
   
 
 
in the second half of the 20th century that the species
A. anguilla has been occasionally entering the lower
course of the Sazliyka River from the Maritsa River.
-
formation about A. aspius and A. brama being caught
there. It is also interesting that the invasive species
G. cernuus found by us in the Sazliyka River is still
not found in the Maritsa River. This is a species with
low economic importance, which was transferred in
-
rial. It is very likely that it has entered the Sazliyka
River through one if its left tributaries, the Ovcharitsa
River, which is connected to the reservoir. This spe-
cies also occurs in another reservoir connected to the
   
of documented catches of G. cernuus, we assume that
it occurs in the lower course of the Maritsa River as
well. At the site at the mouth of the Sazliyka River,
for the whole study period 2009-2012, a considerable
number of individuals were caught (Table 1.) Another
-
cies from the family Cyprinidae: crucian carp (C. car-
assius) and gibel carp (C. gibelio). According to our
previous (unpublished) catches in the last century and
C. carassius used to
be a common species with high numbers in the lower
stretch of the river. The results of this study showed a
complete lack of the species in this part of the Sazliyka
River for the entire four-year study period.
Regarding conservation issues, the composi-
tion of the ichthyofauna in the lower course of the
         
most of the other rivers in Bulgaria ( et

included in the Bulgarian Biodiversity Act (Annexes
2 and 4), one in the Bulgarian Red Data Book, one
in the Black Sea Red Data Book, three in the Bern
Convention (Annex 3), 17 in the IUCN Red List and
three in the Habitat Directive (92/43/EEC).
Our results show the great need of modern
wastewater treatment facilities in Nova Zagora,
Radnevo and Galabovo as well as a strict control on
the pollution from the thermal power plants Brikel
and AES Galabovo. This would help not only to im-
prove the overall ecological condition of the river,
-
pogenically damaged river, the biota has been able to
survive in reduced numbers by developing adaptive
mechanisms. It has kept its potential for a rapid pro-
gress in improved living conditions.
Conclusions
The results of this study showed that in conditions of
constant anthropogenic pollution (with varying inten-
sity) the composition of the ichthyofauna at the lower
         -
cies from eight families. The data obtained during the
four-year period reveals that the number of species
caught at sites located in the upper course of the river,
          
Brikel and AES Galabovo (site A) and at the mouth
of the Sokolitsa River (site B), is higher than at the
river mouth (site D). This indicates that the species do
not just temporary enter from the Maritsa River but
form a permanent ichthyofauna species composition
in the lower course of the Sazliyka River (18 perma-
nently inhabiting species). Seventeen species are con-
 
referred national and international sources. A total of
three species are listed in the Bulgarian Biodiversity
Act (Annexes 2 and 4), one in the Bulgarian Red Data
Book, one in the Black Sea Red Data Book, three in
the Bern Convention (Annex 3), 17 in the IUCN Red
List and three in the annexes of the Habitat Directive
(92/43/EEC).
Acknowledgements: This article is published with the assis-
     
“Paisii Hilendarski”, project No PP18-BF-001
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Received: 03.04.2017
Accepted: 02.05.2018