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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 135 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 136 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 137 637.1 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. 138 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 139 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 140 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. 141 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]. 142 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 143 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 144 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. 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