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STATE OF THE MARINE ECOSYSTEMS ALONG THE BULGARIAN
BLACK SEA COAST
TSONKA KONSULOVA
Institute of Oceanology, BAS, P.O.Box 152, 9000, Varna, Bulgaria,
e-mail: [email protected]
ABSTRACT
In the present paper, the ecological vulnerability of the Black Sea, one of the most isolated seas in
the world, is documented. The evolution of the pelagic and benthic ecosystems along the Bulgarian
Black Sea coast are characterized by the following three periods – pristine (up to 70s), disturbed (up
to the 1992), and partially rehabilitated (after 1993). An assessment of the impact of some
commercial activities on the marine environment, habitat and biodiversity is made and suggestions
for setting up protected sites and putting in practice environmentally friendly mariculture activities.
Keywords: Euthrophication, Pelagic ecosystem, Benthic ecosystem, Mariculture.
1. INTRODUCTION
The Black Sea is a unique part of the world oceans because of a number of reasons.
 Of all the inland European seas, such as the White Sea, the Baltic Sea, and the Mediterranean
Sea, the Black Sea is the most isolated. Its only link with other seas is with the Mediterranean
through the Bosphorus Strait (average 1.3 km width and 60 m depth) and with the Azov Sea
through the Kerch Strait (45 km length and average 7 m depth) (Figure 1). Such a significant
degree of isolation, together with low salinity and low water temperature, has been a decisive
factor in shaping the Black Sea flora and fauna.
 The extensive drainage basin and the great number of incoming rivers contribute to the unique
water balance of the Black Sea. The largest rivers Danube, Dniester and Dnieper are located in
the northwestern part and provide over 70% of all freshwater entering the sea (Figure 2). Since
the sea receives more freshwater than it loses by evaporation, the salinity of the waters (18‰) is
quite low compared to other marginal seas.
 The Black Sea is hereditarily burdened of hydrogen sulfide gas, which consists of 87% of its
volume. If you do not understand this part, I will rephrase: the very steep and deep profile, the
slow rate of replenishment from the Mediterranean and the very large freshwater input has lead
to a stable hydrographic environment in which wind, solar and wave energies are insufficient to
completely mix lighter fresh surface water with underlying denser seawater mass. This feature,
coupled with a high oxygen demand from decaying organic matter also resulted in a marine
ecosystem whose basin waters are permanently anoxic below a depth of 150 m (Figure 1)
[Zaitsev&Mamaev, 1998; Topping & Mee, 1998].
These peculiarities give the Black Sea a very different profile compared to other water bodies in the
world oceans and characterize it as one of the most fragile and vulnerable seas. The complex
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relationships between living organisms and the environment includes the human activities that
frequently cause pollution. In fact, the degree of incompatibility between the living conditions
necessary for the development of various organisms and those that are forced upon them can have
physical, chemical, biological, social and economic consequences [Konsulov at all., 1998].
Figure 1. Profile of hydrogen sulfide zone in the Black Sea [Zaitsev. Yu.,&V. Mamaev, 1997].
Figure 2. Major river catchments in the Black Sea basin [Kotlyakov & Mandych, 1996].
The most devastating consequence of pollution in the Black Sea is the high rate of euthrophication,
with increased levels of organic matter both in the water mass and on the sea bottom.
Euthrophication, combined with other acute forms of marine pollution has produced a decrease in
biological diversity in coastal and open sea areas, leading to a destabilization of pelagic and bottom
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ecosystems. Based on the level of anthropogenic euthrophication and the biota response to it, the
time interval from the 1950s to the late 1980s can be subdivided into two periods [Moncheva &
Krastev, 1997; Shtereva et al., 1999]. The first one, up to 1970, is considered as a background in an
ecological sense, a relatively pristine period, with a natural variability of the ecosystem. The second
one (1970-1992) is a period of intensive anthropogenic euthrophication, including dramatic
"biological noise" in the ecosystem - alterations in the phytoplankton communities, structure and
succession, increase in the total phytoplankton biomass and blooms, resulting in the deterioration of
the Black Sea ecosystem [Moncheva et al., 1995]. The recent period (after 1993) is a priori
assumed to be a period of decrease in the level of pollution pressure, mainly due to the collapsing
economy and related cutbacks in the industrial and agricultural production. Similar trends are
marked for the Danube river input, being the main source of anthropogenic euthrophication for the
northwestern and the western Black Sea area [Cociasu et al., 1997].
The aims of this paper are to present the main trends in the evolution of the pelagic and benthic
ecosystems, to define the ecological effects of some commercial marine activities and to
recommend appropriate measures for the stabilization and recovery of the coastal ecosystems.
2. THE PELAGIC ECOSYSTEM
During the 1980s, the period of high euthrofication, dramatic changes were observed in the pelagic
communities (phytoplankton, zooplankton and fish), and follwing the intrusion of new exotic
species in the Black Sea (Fig 3.- source: Zaitsev, Mamaev, 1997). To overview the alterations in the
Black Sea pelagic ecosystem, a long term data series is discussed, including the following
parameters: *Phytoplankton: data set 1967-1995 [Moncheva, S., 1991; Moncheva, S., Krastev, A.,
1997] and unpublished data (1996-1998). *Zooplankton:data set 1967-1995 [Konsulov,A.,
L.Kamburska,1998] and unpublished data (1996-1998).*Flagellates: Noctiluca scintillans long-term
spring-summer abundance (1967-1998) [Konsulov,A, L.Kamburska,1997].*Jellyfish/Ctenophora:
Mnemiopsis leidyi and Beroe ovata abundance and distribution-published [ Kideys,E.A.,et al.,1998;
Konsulov,A.,L.Kamburska,1998] and unpublished data.*Anchovy total biomass and total Black Sea
catch: long-term data (1967-1997) published [Prodanov, K. et al., 1997] and unpublished data.
The onset of anthropogenic euthrophication in the 1970s marked the inversion of the dominance of
major phytoplankton taxonomic groups, especially in spring-summer opportunistic dinoflagelates
dominating diatoms. During the 1980s, increasing euthrophication induced further dramatic changes
in phytoplankton communities’ structure, abundance and biological cycle, with increased
phytoplankton bloom phenomena. The enhanced outbursts of dinophytes and chrysophytes and the
intensification of bloom frequency, duration and densities in spring-summer, as well as the
diversification of the bloom species became the main features of phytoplankton dynamics
(Figure4 C – source: Kamburska et al., 2003).
The zooplankters copepods Anomalocera pattersoni, Pontella mediterranea, Centropages kroyeri
and Oithona nana were common in 1970s and rare in 1980s. During 1973-1989, the average
biomass of O. nana and C. kroyeri was 1.46 mg.m-3 and 2.37 mg.m-3 respectively, almost 6 times
lower than that in the early 1970s. On the contrary, N.scintillans, an indicator species of
euthrophication, became dominant with frequent and massive blooms. In 1967-1975, its average
abundance was low - 1364 ind.m-3, while in the period of intensive euthrophication (1978-1988) it
increased about 7 fold with a higher range of spring/summer oscillations. Two extremely high
maxima are evident-in 1977 (125 619 ind.m-3) and in 1989 (123 424 ind.m-3) (Figure4 A). The
decrease of fodder zooplankton biomass during the 80-ies is concurrent with the intensification of
phytoplankton blooms and increased anchovy total biomass, irrespective of the increased catches,
due to the planned high fishing activity (Figure4 B, C). After the depression in 1989-1991 (critically
low total and spawning biomass and respectively total catch) the anchovy biomass reached
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637.1 thousand tons in 1993, followed by a very high anchovy catches in the recent period 19941997 (285.2 thousand tons), close to that found during 1977-1988 (Figure4 B). The critically low
biomass at the end of the 1980s could well be attributed to a M. leidyi explosion and overfishing
and predation by Mnemiopsis, an introduced Ctenophore. Food competition pressure is suggested to
play an important role in the sharp decline of Black Sea pelagic fisheries.
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140000
700
A
600
500
3
100000
400
60000
300
40000
200
20000
100
0
1967
0
1972
1977
1982
1987
1992
1997
year
zooplankton biomass [mg.m-3]
1600
B
1400
1200
2000
1800
1600
800
800
600
600
400
[g.m–2]
1400
1200
1000
1000
2]
400
200
0
200
tons
anchovy biomass in thousand tons
N.scintillans [ind.m-3]
0
1967
[mg.m-3]
m
80000
3]
[ind.m -3 ]
120000
1972
Catches
1977
1982
Total biomass
1987
1992
1997
year
M.leidyi wet weight [g.m-2]
300
C
200
]
150
100
[1x10
N [1x106 cells/l]
250
50
0
1983
1985
1987
1989
Bacillariophyceae
Euglenophyceae
1991
1993
1995
1997
year
Dinophyceae
Chrysophyceae
Figure 4. Long-term dynamic of: A. Average spring-summer fodder zooplankton biomass [mg.m-3]
and N.scintillans abundance [ind.m-3] at 3 miles station off cape Galata; B. Total anchovy biomass
and catch in Black Sea [Prodanov, K. et al., 1997], average M.leidyi biomass [g.m-2] in Black Sea
[Kideys,E.A.,et.al.,2000]; C. Average spring-summer phytoplankton bloom abundance
[1x106 cells/l] at 3 miles station off cape Galata including Varna Bay [Kamburska et all., 2003].
The introduction of both Ctenophora exotic species M.leidyi and B. ovata into the Black Sea are
probably due to ships' ballast waters, most likely transferred from the estuaries along the North
Antlantic Ocean where the species are tolerant to lower salinity. It has been reported that B. ovata
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feeds only on M. leidyi [Nelson, T.C.,1925; Swanberg N.,1970;Burrell, V.G.Jr., Van Engel,
W.A.,1976, In: Kamburska et al., 2003]. As it was hypotesized for M. leidyi (GESAMP,1997), it is
quite possible that Beroe has been introduced earlier into the Black Sea basin where, after a period
of adaption, it successfully naturalized to produce the recent outbursts.
During the recent period (the 1990s), the Black Sea ecosystem emerged from the state of critical
ecological instability - into a phase of relative recovery. Most likely the collapse of industrial and
agricultural production of all Black Sea countries during the early 1990s has contributed
considerably to ecosystem improvement [Kamburska et al., 2003]. As our results reveal, possibly
the 1991-1992 marked a breakdown of the interaction pattern in the pelagic food web typical for the
1980s, the changed predator-prey interactions evolving to the degree of an important controlling
factor during the 1990s. Thus, under these conditions the introduction of the new ctenophore and
the prey-predator coupling M. leidyi/B. ovata could at least exacerbate the Black Sea ecosystem
ecological state.
Figure 5. Structure of the classic Black Sea food web before and after registration of M. leidyi in the
Black Sea up to 1995 [Yu. Zaitsev – unpublished data].
Regarding the general impact of the exotic species Mnemiopsis leidyi on the Black Sea marine food
web, a scheme is presented in Figure 5. Compared to the 1950s, in the 1970s (the beginning of
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enhanced euthrophication) the phytoplankton biomass increased tenfold. The latter led to an
increase of the biomass of herbivorous and detritivorous zooplankters and jellyfish respectively.
The stock of pelagic fishes also increased; the reduction of dolphins is due to intensive catch. In the
end of 1980s and the beginning of 1990s, when a maximum of M. leidyi was registered, the
zooplankton biomass, being the main food source of the predatory ctenophore, decreased. Fish
stocks also decreased significantly due to the predatory pressure of M. leidyi – as a competitor in
fish feeding and a consumer of fish eggs and larvae. The dolphin population was not able to recover
during that period mainly because fish stocks were decreasing. With the decrease of M. leidyi’s
biomass during 94-95, as a result of the decrease of its prey, a gradual restoration of the fish stocks
started, as well as an increase of the abundance of dolphins. Coastal birds abundances also depend
on the changes in the biomass of their main food – fish.
3. THE BENTHIC ECOSYSTEM
Zoobenthic communities have long been studied as a tool to measure environmental quality. Since
most macrofauna species are relatively long-living (over 1 year) and sessile, they act as integrators
of the effect of environmental stress, whether or not the stress is natural or anthropogenic.
Zoobenthos species composition in the Bulgarian Black sea area is comparatively well studied. The
data obtained up to the 1960s showed a total number of 1370 zoobenthic species belonging to 12
groups (Protozoa, Porifera, Coelenterata, Plathelminthes, Nemathelminthes, Nemertini, Annelida,
Arthropoda, Mollusca, Tentaculata, Echinodermata, Chordata). Outstanding in species diversity
are Arthropoda - 492 species, with a major contribution of Harpacticoida - totalling 204. Ranking
second and third are Nematoda with 109 species and Polychaeta with 102 species [Marinov, 1990].
In biocenological terms, as a result of the detailed investigations carried out during 1954-1960
[Kaneva-Abadjieva et al., 1960], the main zones along the Bulgarian Black sea area - supralittoral,
mediolittoral and sublittoral, have been subdivided into 4 general types of zoocenoses (sandy,
coastal mud, Mytilus mud and Phaseolina mud zoocenoses). Zoobenthos was studied with regard to
the species composition, quantity prevalence and spatial distribution (Figure. 6). The sandy
sublittoral zone that showed the richest species diversity (142 species), followed by the Mytilus
mud zoocenosis (90 species), Phaseolina mud (60 species) and coastal mud zoocenosis (47 and 42
species for both subcenoses respectively) (Table 1) [Source: Marinov, 1990].
Table 1. Characteristic of separate zoocenoses in the soft sublittoral bottom
Zoocenoses and Subcenoses
1. Sand bottom - total
2. Coastal mud
3. Mytilus mud
4. Phaseolina mud
Number
of
species
142
42-47
Average
density
(ind/m2)
1484
256-564
90
60
666
853
Average Depth
biomass
(m)
(g/m2)
136.4 11-28
40.915-48
76.3
134.3 13-80
44.0
63-184
Two categories of introduced species were distinguished: far-sea species (occasional) and
Mediterranean immigrants [Cvetkov, Marinov, 1986]. Far-sea species are mainly benthic animals
brought by ships: Balanus improvisus, Balanus eburneus, Blackfordia virginica, Bougainvillia
megas, Mercierella enigmatica, Rhitropanopeus harrisii, Rapana thomasiana, Mya arenaria,
Scapharca inaequivalvis.
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Figure 6. Distribution of the zoobenthos cenoses in front of the Bulgarian Black Sea coast [KanevaAbadjieva, Marinov, 1960].
Two crabs - Homarus gammarus and Alpheus dentipes - are considered as new Mediterranean
immigrants, the latter being considered an already fully integrated species.
The reduced benthic diversity and the degradation of communities to opportunistic species and
predictable responses to environmental stress are well documented [Gray, 1989]. It has been
verified that the euthrophication and the recurrent phytoplankton “blooms”, the subsequent organic
enrichment of the sediments and hypoxia in the near-bottom water layers are major stresses for the
macrozoobenthic communities in the North-Western part of the Black Sea, including the Bulgarian
coast, resulting in mass mortality of benthic invertebrates, extinction of sensitive species and
decreased diversity [Konsulov et al., 1998; Konsulova et al., 1991; Zaitsev, 1993].
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Changes in the contribution of the major taxonomic groups to the total number of species is an
alternative indication of euthrophication impact.This is due to differences in tollerance between
mollusks, crustaceans and polychetes and their ability to adapt to an altered environment and to
hypoxia in particular. Most vulnerable to hypoxia are the crustaceans – oxygen concentration below
1.5 – 2.0 ml/l are lethal. Polychaetes are the most tolerant – they survive concentrations as low as
0.5 ml/l [Zaitsev,&Mamaev, 1997]. Many bivalve species are able to close their shells tightly and
use the oxygen reserves retained in their tissues, which makes them tolerant to harsh environmental
conditions, hypoxia included. Evidently, the relative diversity decrease of crustacean species is a
consequence of their weak physiological resistance to low oxygen concentration, while the relative
increase in number of molluscs is due to their hypoxia tolerance. These conditions favor the
invasion of exotic mollusc species Mya arenaria and Scapharca inaequivalvis, while sensitive
decapod crustaceans, e.g. Upogebia pusilla and the crab Macropipus holsatus became very rare
[Konsulova et al., 1991].
A comparison of the relative contribution of the three major taxonomic groups to the total
macrofauna composition for the periods 1954-57, 1982-85 and 1996-1997 shows a decreasing
trend in crustaceans : from 37% in 1954-57 to 28% in 1982-85 and to 25% in 1996-1997. An
opposite trend is noticeable for the share of the mollusks (Figure 7 A). Another evidence for
euthrophication is the outburst of polychaete abundance (Figure 7 B). In contrast to pelagic
communities, in which signs of recovery have been recognized, the bottom inhabiting communities
currently appear to be even more disturbed in 1996-97 than in the 1980s. This is due to the fact that,
as a response to the improvement of the environmental conditions in the water masses, benthic
communities need longer time for a full restoration and stabilization..
B
A
100
% share in the average abudance
100
% share in the number of taxa
90
80
70
60
50
40
30
20
10
90
80
70
60
50
40
30
20
10
0
0
1954-1957
Polychaeta
1982-1985
1996-1997
Mollusca
Crustacea
1954-1957
1982-1985
Polychaeta
Mollusca
1996-1997
Crustacea
Figure 7. Trend in the percentage share of the major zoobenthic taxonomic groups in the total
number of taxa (A) and average abundance (B) [Todorova et al., 2000].
The lower biodiversity of zoobenthos (about 4 fold lower in comparison with the Mediterranean
Sea) and the higher sensitivity of the Black Sea fauna to unfavorable conditions impose exclusively
careful exploitation of the marine resources. One of the most significant problems, which have to be
solved by marine ecologists today, is to assess the effect of commercial activities at sea and their
environmental friendly or non-friendly impacts. One of the most important hindrances for the
normal course of the rehabilitation processes in the benthic communities along the Bulgarian coast
during the last years is bottom trawling for Rapana thomasiana.
During the pristine period of the Black Sea (to the end of the 1960s) the mussel beds ensured the
coastal ecosystem's balance, due to a powerful water clearance capacity. Since the 1970s, the
population of M. galloprovincialis has reduced significantly as a result of the invasion of the alien
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predatory gastropod Rapana thomasiana, mass mortality due to oxygen deficiency at the bottom
layers in the post-blooming periods and silting by suspended sediments following bottom trawling
for sprat [Zaitsev & Mamaev, 1997; Zaitsev, 1993].
Commercial harvesting of Rapana thomasiana in the Black Sea has developed rapidly since 1990
and has become a new threat to the mussel beds. Initially, the gastropod were collected by divers .
During the last 6-7 years, the harvesting along the Bulgarian coast has been intensified by means of
illegal bottom trawling of the mussel beds, which are the feeding grounds of R. thomasiana. The
number of trawling vessels has increased by approximately three since 1996, which resulted in
three-fold increase in catches in 2000 (Figure 8).
1400
140
1191
1200
120
889
Tons
1000
729
800
600
100
668
636
642
80
60
427
400
40
200
20
0
0
1996
1997
1998
1999
2000
2001
2002
Years
Meat yeild in tons
Number of trawlers
Figure 8. Total meat yield (t) and number of trawlers per years (according to the data from National
Custom Agency and National Agency of Fisheries).
Overcatch was followed by a significant decrease in yields in 2001 and 2002 (about two times
lower – Figure8), indicating a serious decline of the R. thomasiana population. A disruption of
mussel beds was also observed. Large quantities of bycatched injured mussels have been discarded
back to the seabed, where their decay contributed to recurrent hypoxia and mass mortality of
benthic invertebrates and fish during 1999-2001. Currently, bottom trawling for Rapana
thomasiana represents a significant hindrance to the recovery of zoobenthic communities along the
Bulgarian Black Sea shelf, already degraded due to the other anthropogenic euthrophication
[Todorova, Konsulova, 2000].
A
B
Figure 9. Sonar image of the protected site (A) and trawled site (B) [Konsulova et al., 2002].
In 1999, an experiment for the protection of the seabed against bottom trawling was initiated. In
compliance with the artificial reefs method implemented along the Mediterranean coast, a protected
area was created near Varna Bay in November 1999 by means of specially designed concrete
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blocks. An intensively trawled area at the depth of 18 m with a surface of 648 ha was covered
chess-like by 45 concrete pyramids with a surface of 1,53 m2 each, accommodated by metal spikes
and oval concavities that provide shelter for juvenile marine organisms. An area of 400 m2 was
covered for sampling and assessment of the protection effect. The implementation of the seabed
protection method has reduced the trawling impact and has fostered the recovery of the mussel
beds: two years after the start of the project, the percentage cover of mussel patches at the protected
site (Figure 9-A) was 4-fold higher than at the trawled site (Figure 9-B).
30000
60
40
30
15
3
3
14
15
14
13
12
9
7
19
17
15
20
10
20000
2
-2
50
25000
ind . m
Species number
4
15000
10000
5000
19
0
PS-MP
Vermes
PS-SP
Crustacea
A
TS-MP
Mollusca
TS-SP
Varia
0
PS-MP
Vermes
PS-SP
Crustace
a
TS-MP
Mollusca
TS-SP
Varia
B
Figure 10. Total and per group average number of species (A) and biomass (B) of macrofauna in
mussel patches (MP) and silt patches (SP) at the protected site (PS) and trawled site (TS).
The total number of species was higher at the protected site (n=64) than at the trawled site (n=50).
As evident from Figure 10-A, the highest number of species was observed at the mussel patches of
the protected site (n=52) and the lowest - at the silt patches of the trawled site (n=38). The species
number decrease at the trawled sited is due mainly to absence of crustaceans. The encountered
crustaceans are typical inhabitants of mussel beds, hence their decrease is deemed to follow the M.
galloprovincialis population decline at the trawled site. The average abundance of the macrofauna
was highest at trawled site-Mussel patches (TS-MP- 24180 ind.m-2) and lowest at protected site-silt
patches (PS-SP - 14459 ind.m-2), due to the dominance (90.6 %) of opportunistic worms that
usually take advantage of environmental stress, developing in excessive numbers (Figure10-B).
Mussel beds are inhabited by a diverse macrofaunal assemblage that is disturbed by bottom trawling
directly as well as through the impact on key species M. gallorpovincialis.
Data show that bottom trawling causes a serious threat to bottom living fauna resulting in a
disturbed recruitment of the M. galloprovincialis population, a decline of community diversity,
especially crustacean richness and a further threat to several Decapod species already threatened by
extinction, habitat alteration: a relative increase of fine silt/clay fraction and degradation of benthic
community from "mussel bed" type to "silt" type dominated by opportunistic polychaetes and
oligochaetes. The implementation of our seabed protection method has reduced the trawling impact
and has fostered the recovery of mussel beds [Konsulova et al., 2002].
As a result of this research on the negative impact on the environment of bottom trawling, the Law
of Fisheries and Aquaculture banned this type of commercial activity in 2000. However, inadequate
control leads to the necessity to set up large protected areas at the most intensively trawled regions
as an insurance against illegal bottom trawling.
145
Photo 1. Collector with commercial production
of cultivated mussels in the region of Sozopol.
Figure 11. Storm-proof “star” type installation
in cape Kaliakra region [Konsulov,1980].
M. galloprovincialis is the only Mollusk species consumed by the population of the Black Sea
countries. From an ecological viewpoint, due to their high bio-filtering capacity, mussel cultivation
can also be a good method, helping in the restoration of the biological balance in the coastal
ecosystems.
A new benthic community is formed on farms for cultivated mussels, which are similar to the
Mytilus zoocoenosis with regard to species diversity (Photo 1; Figure 11). The high quality
production does not endanger human health and correspond to the requirements for sustainable use
of the living marine resources. In 1984, as a result of detailed biological investigations, the
complete normative documentation was created [Konsulova, 1984].
A national strategy for the development of mariculture in Bulgaria, recommends setting up mussel
cultivations as an alternative to the devastation to life on the sea floor caused by bottom trawling.
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