The dramatic changes were encountered in the Black Sea ecosystem during the 1980s and 90s due to combination of (i) eutrophication, (ii) overfishing, (iii) population explosion of alien gelatinous carnivore species Mnemiopsis leidyi, and Beroe ovata (iv) abrupt decadal cooling and warming events and associated changes in the hydro-meteorological properties (Oguz, 2005a, b). Here, using the time series data from different trophic levels shown, we examine the last 4 decades of the ecosystems transformations under four distinct phases. 

Pre-eutrophication phase: The period up to 1970 represents an oligotrophic regime of the ecosystem with maximum nitrate and phosphate concentrations of ~2.0 and ~0.2 µM, respectively, in the upper layer water column, maximum phytoplankton and fodder mesozooplankton biomass of ~5.0 g m^-2 (Fig. 1b,c), surface chlorophyll concentration 0.1 gm^-3 (Fig. 1b), small pelagic fish catch of <200 kilotons (Fig. 1e).

Early-eutrophication phase: It comprises the mizotrophic regime of the 1970s at which the Black Sea started showing a sign of deterioration in response to increasing anthropogenic nutrient and pollution influxes, removal of large predator piscivorous fishes (e.g., bluefish, bonito) and dolphins.  The phytoplankton and fodder mesozooplankton biomass started varying around 5-10 g m^-2, summer-autumn surface chlorophyll concentration 0.1-0.15 gm^-3, small pelagic fish catch ~400 kilotons. Both the pre-eutrophication and early-eutrophication phases were characterized by the warm and mild winters with typical winter average temperatures of the basin around 8.5-9.0 ^oC (Fig. 1a). 

Intense eutrophication phase: It signifies the 1980-1995 period of significant changes.  Climatically, this period coincides with the strong positive phase of the North Atlantic Oscillation-NAO (Oguz, 1995b), which brought extremely cold, dry and severe winters into the Black Sea region as evident in Fig. 1a by approximately 1.5-2.0 ^oC drop in the winter-mean SST.  In particular, the period 1985-1993 represented the coldest SSTs of the last century. During this period, peak nitrate concentration increased from about 2 µM of the previous phase to ~6-7 µM within the chemocline layer immediately below the euphotic zone (Konovalov and Murray, 2001).  Relatively higher rate of nitrate was supplid into the euphotic zone by strong upwelling associated with the intense basinwide cyclonic circulation system as well as strong wind and buoyancy-induced mixing. They supported more enhanced primary and secondary production with changes in phytoplankton biomass from 10 to 25 g m^-2, and in fodder mesozooplankton biomass from 5 to 15 g m^-2 (Fig. 1b, c). The variations of May-November mean surface chlorophyll concentration from about 0.1 mg m^-3 during the early eutrophication phase up to 0.5 mg m^-3 during the coldest period of the intense eutrophication phase (Fig. 1b) also supported enhanced primary production. 

The period 1977-1984 corresponded to the rapid increase of small pelagic (mainly anchovy) stocks due to the loss of their top predators. As a result, their total catch rose up to ~700 kilotons (Fig. 1e). Such relatively high small pelagic stocks exerted stronger grazing pressure on fodder mesozooplankton community, and thus contributed positively to the increase of phytoplankton biomass (Fig. 1b). Following a few years of stability, as they were continued to be overfished, the catch finally exceeded a sustainable level in 1987/1988, and collapsed to less than 200 kilotons in 1989-1990 (Daskalov, 2002; Gucu, 2002). The weaker grazing pressure associated with reduction in the small pelagic stocks was responsible for the gradual increase of fodder mesozooplankton biomass to its maximum values during this phase (Fig. 1c).

As the small pelagic fish stocks were exploited by uncontrolled fishing, and their eggs and larvae were consumed efficiently by gelatinous and opportunistic species, the niche vacated by small pelagics was gradually replaced first by jellyfish Aurelia aurita reaching a biomass of 1.5 kg m^-2 during the mid 1980s, and then the ctenophore Mnemiopsis leidyi attaining the peak value of about 2.5 kg m^-2 at the end of the decade (Fig. 1d). Thus, the intense eutrophication phase and the period of massive exploitation of small pelagics have also been characterized by pronounced increase in the gelatinous carnivore biomass from its negligible values during the early 1970s up to 2.5 kg m^-2 at the end of the 1980s.

The period of collapse of small pelagic fish stocks was accompanied with the sharp drops in the biomass of fodder mesozooplankton and Mnemiopsis during 1991-1993. Even though both bottom-up and top-down conditions were quite favourable for maintenance of their biomass level of the previous several years, the surface mixed layer temperatures as low as 5-6^oC due to prevailing severe winter conditions (Oguz et al., 2003) affected adversely their overwintering and subsequent efficient spring production. The early 1990s thus reflected a state of catastrophy with complete breakdown of the biological life in major part of the Black Sea except some limited activities in coastal-shelf regions around the periphery of the basin.  Some improvements however took place as soon as the adverse impact of exceptional cooling was relaxed during 1994-1995.

Post-eutrophication phase: The Black Sea entered into so-called post-eutrophication phase after 1995. One particular sign of this new phase was considerable reduction in the anthropogenic nutrient and pollutant load (Cociasu and Popa, 2002) and subsequent erosion at the subsurface nitrate accumulation from 6-7 µM of the previous decade to 5-6 µM (Konovalov and Murray, 2001). The other distinct signature of this phase was due to an abrupt switch of the NAO index from strongly positive to strongly negative values, and the subsequent cycle with warm and mild years (Oguz et al., 2003). The warming was indicated in Fig. 1a by the continuous trend of increase of the SST from about 7.2 ^oC at 1993 to about 9.0 ^oC at 2000. By 1995, the Black Sea maintained a similar level of warming prior to 1980. The spring phytoplankton bloom was either lost completely or weakened considerably depending on the hydro-meteorological conditions of each particular year after 1995 (Oguz et al., 2003).  The loss of spring phytoplankton bloom was reflected as reduced phytoplankton biomass and surface chlorophyll concentration (Fig. 1b), and reduced stocks of higher trophic levels (Fig. 1c-e). The Black Sea ecosystem was switched back to a reletaively low productive state similar to that encountered previously in the first half of the 1970s. A short-term population increase of Beroe ovata towards the end of the 1990s (Shiganova et al., 2003) further contributed to stabilization of the ecosystem by their predation on Mnemiopsis population, and thus recovery of fodder mesozooplankton community.  

“Regime shift” refers to a transition between two quantifiable, quasi-equilibrium states (or regimes), when resilience declines and an ecosystem becomes vulnerable to low frequency, high-amplitude changes in multiple trophic levels introduced by external forcing (Collie et al., 2004). The ecosystem then alters its regime by top-down forcing (e.g., removal of functional groups by means of overfishing, introduction of alien species), bottom-up forcing (e.g. nutrient and pollutant inputs), climate change (Scheffer et al., 2001; Steele, 2004).

The dramatic changes were encountered in the Black Sea ecosystem during the 1980s and 90s (see the figure below) due to combination of (i) eutrophication, (ii) overfishing, (iii) population explosion of alien gelatinous carnivore species Mnemiopsis leidyi, and Beroe ovata (iv) abrupt decadal cooling and warming events and associated changes in the hydro-meteorological properties (Oguz, 2005a, b). The idealized representations of the control variables (e.g. indices for eutrophication, fishing pressure, climate) corresponding to three external forcing, and of the response variables of the ecosystem at different trophic levels (e.g. phytoplankton, mesozooplankton biomass, fish stocks, etc.) are shown below.

Signature of regime shifts at higher trophic level

The regime shift is diagnosed by examining small pelagic catch variations with respect to the fishing pressure (FP).  This plot suggests three different groups of catch-fishing pressure pairs. The state S1 encompasses the catches from about 100 to 300 kilotonnes over the fishing pressure values from 0.2 in the 1960s to 0.60 at the mid-1970s. When large pelagics were withdrawn from the system at the mid-1970s, the same amount of small pelagic fishes (~350-400 kilotonnes) was caught with much reduced fishing pressure (about 0.35) because of an apparent increase in the stock.  This implies a switch to the alternative state from 1973 to 1978.  The new state S2 signifies the so-called intense eutrophication phase of the ecosystem in the 1980s and is characterized by gradually increasing catch values up to about 700 kilotonnes over a range of increasing fishing pressure values (up to ~0.9) associated with continual overexploitation of stocks.  At low fishing pressure levels (<0.3) and below a critical catch value (350-400 kilotonnes), the system was at the low stock state.  At high fishing pressure (>0.55) and above the critical catch, the system moved into the high stock state.  For intermediate fishing pressure values between 0.3 and 0.55, the system was unstable with two alternative equilibria. As the system continued to be perturbed by means of strong overfishing (suggested by FP values greater than 0.7), it was not able to maintain its high catch state S2 any longer and shifted abruptly to a new low catch state at the end of 1980s.  This new state was an alternative to the high catch state for the FP range between 0.55 and 0.7; e.g. note two different catch values of approximately 650 at 1980 and 200 kilotonnes at 1990 for FP~0.6. In state S3, below this threshold, in response to the reduction in fishing pressure up to 0.3 due to lower catchability of the system under reduced fish population, the catch increased gradually up to 300-400 kilotonnes range. Following the definitions adopted and the George Bank example of haddock stocks discussed by Collie et al. (2004), the transitions from S1 to S2 and from S2 to S3 are identified as “discontinuous regime shift” events.

Signature of regime shifts at lower trophic level

Phytoplankton biomass variations were controlled concomitantly by climate, eutrophication and overfishing as described by Oguz (2005a,b). According to the data provided by Sorokin (2002) the anthropogenic-based nitrogen load, being the main limiting nutrient for most part of the Black Sea ecosystem (Oguz 2005a), was ~150 kilotonnes y^-1 in the 1960s, increased almost linearly up to ~600 kilotonnes y^-1 in the mid-1980s and later decreased to ~300 kilotonnes y^-1 in the 1990s.  While the nitrogen load is the primary forcing variable related to eutrophication, the sea surface temperature time series data may be used to diagnose simultaneous impact of the climatic cooling/warming on the long term variations of phytoplankton biomass.  Its original and smoothed variations represented by straight lines are shown in Fig. 8a.  

The phase diagrams representing phytoplankton biomass versus nitrogen load  also demonstrate hysteresis as in the case of the small pelagic catch data.  For the load rate increasing from 150 to 600 kilotonnes y^-1, phytoplankton biomass remained at its low biomass state S1 with values less than 7 g m^-2. This period covered the pre-eutrophication and early-eutrophication periods prior to the 1980s.  Only after the early 1980s, with the onset of a new cooling phase and the maximum nitrogen load level of 600 kilotonnes y^-1, the biomass increased abruptly and the system moved into the high biomass state S2 with values around 20 g m^-2. This state was also maintained during the 1987-1995 period of decreasing load up to the critical level of 150 kilotonnes y^-1 and SST range of 7.2-8.4^oC.  Thus, multiple equilibria were held for nitrogen load greater than ~300 kilotonnes y^-1 and SST less than ~8.5^oC. Thereafter, the system was transformed quasi-linearly to a new low biomass state S3 identified by relatively low nutrient load (<300 kilotonnes y^-1) and high SSTs (>8.5 ^oC). According to Collie et al. (2004), this transition may be identified as “smooth regime shift”.  This implies that the type of transition between the states S2 and S3 is fundamentally different for phytoplankton biomass and small pelagic fish catch.