Abstract

The impact of the introduced ctenophore Beroe ovata on its prey Mnemiopsis leidyi, another invader ctenophore voraciously feeding on mesozooplankton, and consequently on the mesozooplankton community, was evaluated by undertaking both laboratory and field studies in the northern Black Sea. Ingestion and growth rates as well as the gross growth efficiency of B. ovata were estimated from laboratory experiments. The daily ration of ctenophores was related to food abundance within a wide range of prey concentration and never reached saturation. Beroe ovata required high food rations (not less than 20% of body weight per day) for growth. The abundances, biomasses and population structures of these two introduced ctenophore species were also monitored, along with mesozooplankton, in inshore waters of the northern Black Sea (i.e. Sevastopol Bay and adjacent regions) over a period of 3 years (1999–2001) which is after B. ovata’s arrival. The annual dynamics of the M. leidyi population were similar for the last 3 years: very low abundances and biomass values were observed during most of the year (unlike the previous years), with a sudden increase in summer–early autumn, but only for about a 2 month period. The B. ovata bloom during the peak M. leidyi biomass resulted in the M. leidyi biomass falling sharply to extremely low values. The predatory impact of M. leidyi on prey zooplankton was found to be reduced during the period of study compared with before.

INTRODUCTION

The accidental introduction of the northwestern Atlantic ctenophore Mnemiopsis leidyi in the early 1980s radically affected the Black Sea ecosystem (Vinogradov et al., 1992; Shiganova, 1998; Shiganova et al., 1998). Pronounced changes in plankton community structure took place during the peak occurrence of this ctenophore in the late 1980s. The Aurelia aurita biomass fell sharply because of competition for food with M. leidyi. The previously abundant zooplankton species like the copepod Oithona nana and the chaetognath Sagitta setosa were not found in samples taken in 1989; the abundance of the copepod Paracalanus parvus and cladocerans Penilia avirostris and Pleopis polyphemoides decreased dramatically while the copepod Acartia clausi became dominant in inshore waters. The total biomass of microzooplankton fell by 5- to 10-fold and mesozooplankton 6-fold (Kovalev et al., 1998).

Mnemiopsis consumed a considerable proportion of the zooplankton (Finenko and Romanova, 2000) that had been the food for pelagic fish and their larvae in the years before the arrival of M. leidyi. In 1989 the fish catches decreased sharply for all the countries around the Black Sea (Kideys, 1994). Despite speculation about different possible reasons, e.g. climatic and hydrological fluctuations as well as anchovy population cycles (Niermann et al., 1999), overfishing (Gücü, 1997) and anthropogenic pollution of the sea (Zaitsev and Alexandrov, 1997), the invasion of the exotic ctenophore M. leidyi might be considered as the main factor (Zaika, 1994).

The lack of natural predators feeding on M. leidyi resulted in temperature and food conditions being the only factors controlling the distribution and abundance of its population. In the Black Sea Mnemiopsis showed the typical pattern of a new colonizer: after its mass development in 1989 and 1990 (∼2 kg m−2 biomass in the offshore waters) with a secondary increase in 1995,M. leidyi number and biomass fell to moderate (but still significant) levels of ∼200 g m−2 (Mutlu et al., 1994; Shiganova, 1998; Mutlu, 1999; Kideys and Romanova, 2001). During these years some positive changes in the pelagic ecosystem of the Black Sea occurred: the zooplankton biomass in the central Black Sea has been recovering since 1992, some species (O. nana and S. setosa) appeared again in inshore waters (Zagorodnyaya et al., 2001). However, it is worth noting that during the second increase of M. leidyi levels in 1995, mesozooplankton biomass was again very low in the coastal waters of the Black Sea (Kovalev et al., 1998).

The appearance of a new invader ctenophore Beroe, a known feeder on Mnemiopsis in native waters (Kremer, 1976), at the end of the 1990s in the Black Sea caused further improvements in the planktonic community. The consequence of this new invasion was positive for the recovery of the Black Sea ecosystem.

In autumn 1999 the first estimation of the predatory impact of B. ovata on the M. leidyi population was carried out in the Sevastopol and Blue Bays, the northern Black Sea. The B. ovata population appeared to graze from 5 to 80% of the M. leidyi population biomass daily and was found to be very effective in controlling the M. leidyi population in inshore waters of the Black Sea (Finenko et al., 2000, 2001; Shiganova et al., 2000; Shushkina et al., 2000; Vostokov et al., 2001). By analyzing the long-term distribution of Mnemiopsis, it has already been observed that the biomass of this ctenophore has been decreasing sincethe arrival of its predator Beroe in both Sevastopol and Blue Bays as well as in the southern Black Sea (Shiganova et al., 2000, 2001; Finenko et al., 2001; Kideys and Romanova, 2001). A reduction in the Mnemiopsis biomass and therefore decreased food competition with fish would result in future improvements of food conditions particularly for pelagic fish and hence fisheries.

The quantification of the top-down control mechanism exerted by B. ovata is important to understand ecosystem changes occurring in the pelagic ecosystem of the Black Sea. Therefore this investigation aimed (i) to study seasonal and inter-annual dynamics (1999–2001) of abundance, biomass and population structure of M. leidyi and B. ovata in Sevastopol Bay and adjacent water regions; (ii) to measure ingestion, growth and reproduction rates of B. ovata and the effects of food concentration and body weight on these parameters; and (iii) to estimate the grazing impact of B. ovata and M. leidyi on their prey populations.

METHOD

Abundance, biomass and population structure

Ctenophores (M. leidyi and B. ovata) were collected either monthly (in the winter–spring period) or twice a month (in summer–autumn) during the daytime with a Bogorov-Rass net (500 μm mesh size and 80 cm diameter) (Kiselev, 1969) at seven stations in Sevastopol Bay (stations 1–7) and at five stations in adjacent water regions (stations 7a–11) during September 1999–November 2001(Figure 1). The Bay is 7 km long and on average 850 m wide with an average depth of 12 m. As in the Black Sea, the salinity of the Bay is ∼18‰.

Maximum depths at stations 2–9 (except 6) varied from 10 to 18 m, at stations 10 and 11 depth reached 50 and 45 m. At stations 1 and 6, having a depth of <9 m, only horizontal samples were taken for analysis of population structure. At all other stations the standard layer of10–0 m was sampled by vertical tows. There was a thermocline at the two deep stations (i.e. 10 and 11) during June–August, the upper boundary of which (10–12 m) coincided with the lower boundary of our sampling. There was not any halocline at these stations (Gordinaet al., 2001). The surface temperature was measured at each station.

Immediately upon retrieval, samples were examined, the ctenophores were counted and their lengths (total length of B. ovata and oral–aboral length without lobes of M. leidyi) were measured to the nearest 1 mm; the abundance of the ctenophores of different size groups (with intervals of 10 mm) was estimated.

The biomass was calculated from the abundance and the mean wet weight of each group using related regression equations (Finenko et al., 1995, 2001):

 

\[\mathit{B.\ ovata}:\ \mathit{W}\ =\ 0.85\ \mathit{L}^{2.47}\ 10\ {<}\ \mathit{L}\ {<}\ 120\]
 
\[\mathit{M.\ leidyi}:\ \mathit{W}\ =\ 1.07\ \mathit{L}^{2.76}\ 2\ {<}\ \mathit{L}\ {<}\ 10\]

 

\[\mathit{M.\ leidyi}:\ \mathit{W}\ =\ 1.31\ \mathit{L}^{2.49}\ 11\ {<}\ \mathit{L}\ {<}\ 65\]

where L is length in millimeters and W is wet weight in milligrams. The total biomass was computed as the sum of biomass of all size groups. Significant variability of ctenophore abundance could be observed between the stations in some cases but the annual dynamics was the same at all stations, so data obtained from all stations were integrated to calculate average number and biomass of ctenophores. The mesozooplankton samples were collected at similar time intervals from one monitoring station (station 7) using a Juday net (opening diameter37 mm, mesh size 120 μm) by vertical hauls from near the bottom to the surface (10–0 m). At this station, zooplankton investigations have been undertaken during the last three decades by the IBSS and this enabled us to compare our data from previous years. Immediately after transportation to the laboratory, the samples were processed under a binocular microscope in Bogorov’s counting chamber (Kiselev, 1969) for determining the abundance of each species and stage or size group. The biomass of total mesozooplankton was calculated by taking into account the abundance and weight of each of these groups (Petipa, 1957). Fodder zooplankton is evaluated separately without taking into account gelatinous species or the dinoflagellate Noctiluca scintillans.

The data from long-term (1976, 1989–1990 and 1995–1996) observations of zooplankton abundance and species composition in Sevastopol Bay were used for comparison (Gubanova et al., 2001). The samples were collected at the same station (station 7 in our study) twice per month with the same sampling and calculation methods as we used. The annual averages were calculated by averaging the monthly means from January to December for each year.

Estimation of ingestion, growth and reproduction rates

The long-term experiments (8–11 days) with adult B. ovata were conducted to estimate digestion time, ingestion, growth and reproduction rates. Undamaged animals after careful selection were measured, weighed and placed in 5 l vessels containing 112 μm filtered seawater. The lengths and wet weights of B. ovata in the experiments ranged from 16 to 65 mm or from 0.55 to 40 g. Mnemiopsis leidyi specimens of 5–10 mm length (5–30 individuals per container) or 10–35 mm (1–7 individuals per container) were offered as food. Water in the containers was changed daily, the number of uneaten M. leidyi was counted and new prey specimens were added to maintain the specified food concentration. The B. ovata specimens were measured and weighed every 2–3 days. To examine the reproduction rate, water from each experimental vessel was filtered through a 112 μm mesh daily, and eggs (with a size of 830 ± 0.80 μm) retained on the mesh were transferred into 100 ml glass Petri dishes and counted in Bogorov’s counting chamber under a binocular microscope. The Beroe feeding was tested at three food concentrations: I, 0.75; II, 1.40; III, 2.4 g wet wt l−1. The consumption rates (R, g wet wt ind.−1 day−1) were calculated from the measured difference in concentration and total weight at the beginning and the end of observations. Digestion time was studied in the same experiments. Once ingestion occurred the B. ovata specimens were monitored every 15 min until defecation was complete and the gut was empty.

The average specific growth rates (μ, day−1) were estimated assuming exponential growth:

 

\[\mathit{W}_{t}\ =\ \mathit{W}_{0}\ e^{{\mu}t}\]

where Wt and W0 are final and initial weights in mg, and t = time in days.

All experiments were conducted at a temperature of 18 ± 1°C.

To calculate the gross growth efficiency of Mnemiopsis and Beroe the dry:wet weight ratios of 0.022 and 0.024, caloricity of 0.64 and 0.68 cal mg−1 dry weight and carbon content of 6.5 and 6.6% of dry weight were taken, respectively (Anninsky, 1994, 2000; Finenko and Romanova, 2000; Finenko et al., 2000).

RESULTS

Abundance, biomass and population structure of ctenophores

The annual dynamics of the M. leidyi population were similar during the 3 years: usually very low abundance and biomass during the winter–spring period and a sharp increase in summer–early autumn (early September in 2000 and mid-July–early August in 2001) (Figure 2A and B). Maximum biomasses on average were as large as 211.5 g m−2 in 2000 and 790.3 g m−2 in 2001. The appearance of Beroe during high levels of M. leidyi resulted in a sharp decrease of Mnemiopsis biomass down to 0.20 g m−2 in 2000 and to 0.02 g m−2 in 2001 and remained at this level for the next few months. After the disappearance of B. ovata in late autumn the M. leidyi biomass displayed a secondary peak, which was lower than the major one. In 1999 a summer peak of M. leidyi biomass was not found (it appeared to have occurred before sampling began), but in September–October, when B. ovata was still present in the plankton, the M. leidyi biomass (2.1–8.1 g m−2) was lower than in previous years (Finenko and Romanova, 2000) but higher than secondary peaks in the next 2 years.

Beroe ovata was found in the plankton of Sevastopol Bay during 3 months: from September to November in 1999–2000 and from August to October in 2001. It appeared ∼2 weeks after the maximum M. leidyi biomass (Figure 2A and B). In late September 1999, when B. ovata was first found in Sevastopol Bay the population consisted of animals measuring from <10 to 110 mm in length, whilst ctenophores of 10–50 mm size range were dominant (54%) (Figure 3). Reproduction was almost complete by this time. In September 2000, juvenile Beroe of <10 mm were the only size group, whilst in October–November ctenophores of 10–50 mm dominated (97 and 70% of total number). In August 2001, 90% of the population consisted of individuals of <10 mm, most of which were as large as 10–30 mm in September.

The abundance characteristics of Beroe were consistent from year to year with maximum values occurring at the beginning of population development. In 2001, B. ovata abundance and biomass were much higher than in the previous 2 years.

The annual dynamics of the prey zooplankton biomass in 1999–2001 were characterized by one summer–autumn maximum (1.9–2.0 g m−2) generated by the copepoda Acartia clausi, a few cladoceran species (60–90% of total biomass) and meroplankton (especially nauplii of Balanus) (Figure 2C). The increase in mesozooplankton biomass by late autumn with the sharp decrease in M. leidyi was particularly notable for the year 2000.

Digestion time, ingestion, growth and reproduction rates of B. ovata

Digestion time of adult B. ovata at 19 ± 10°C varied from 0.75 to 5 h at the tested wet weight range of both ctenophores (Beroe 0.55–27.5 g, Mnemiopsis 0.39–6.88 g). Beroe ovata of every size consumed both large and smallM. leidyi, and the ratio between weight of prey and predator (p) affected the digestion time (DT) (Figure 4). The relationship between these values could be expressed as:

 

\[\mathit{DT}\ =\ 2.956\ \mathit{p}^{0.59}\ (\mathit{n}\ =\ 17,\ \mathit{r}^{2}\ =\ 0.61,\ \mathit{P}\ {<}\ 0.01)\]

for a prey–predator weight ratio range of 0.03–3.24.

Specific daily ration of adult ctenophores (SDR, %) in the experiments with food concentration 1.8 g wet wt l−1 ranged from 15 to 460% of body wet weight (W, g) from the largest to the smallest animals and could be described as (Figure 5)

 

\[\mathit{SDR}\ =\ 259\ \mathit{W}^{{-}0.703};\ (\mathit{n}\ =\ 64,\ \mathit{r}^{2}\ =\ 0.70,\ \mathit{P}\ {<}\ 0.01)\]

The clearance rate (the water volume swept clear during a time period per unit body weight) did not depend on the density of M. leidyi in the range of 0.8–6.2 ind. l−1 or 0.47–7.36 g l−1 but the negative correlation between clearance rate (CR, l g−1 wet wt h−1) and the wet weight of ctenophores (W, g) was evident (Figure 6); the equation describing this relationship was as follows:

 

\[\mathit{CR}\ =\ 0.105\ \mathit{W}^{{-}0.939}\ (\mathit{n}\ =\ 36,\ \mathit{r}^{2}\ =\ 0.59,\ \mathit{P}\ {<}\ 0.01)\]

At exponential growth that is characteristic of ctenophores (Zaika, 1972), the specific growth rate does not depend on the size but on the specific ration. In our experiments the specific growth rate increased from –0.05 to 0.20 while the ration increased from 27 to 150% of body weight (Figure 7). The same relationship was observed for gross growth efficiency (K), which was negative (∼–0. 26) at the ration value <27% of wet weight (Figure 8). As can be seen from Figure 5, under these food conditions large Beroe lost some weight. Increasing the ration improved growth efficiency.

In our experiments B. ovata started reproduction at a body length of 12–13 mm. Separate determinations of egg wet weight yielded a value of 0.153 mg egg−1. Under controlled food conditions during 10 days when daily weight-specific rations averaged 20–108% of B. ovata wet weight, they had 4–6 clutches and the total number of eggs laid by one ctenophore ranged from 2066 to 4220 (Table I) or from 0.2 to 1.6% of body weight (0.02–0.16% per day).

Predatory impacts of M. leidyi on zooplankton and B. ovata on the Mnemiopsis population

Based on M. leidyi abundance, the individual wet weight of ctenophore in the population over the year and its clearance rate (CR, ml ind.−1 h−1) measured in laboratory experiments for animals of different wet weight (W, g), according to:

 

\[\mathit{CR}\ =\ 53.08\ \mathit{W}^{0.405}\]

at 22°C (Finenko and Romanova, 2000), the predatory impact of M. leidyi populations on zooplankton have been estimated. Being almost a non-selective predator Mnemiopsis could consume all types of zooplankton and remove 4–6% of the biomass daily in August–September 2000 and ∼16% in early August 2001 when abundance peaks of the M. leidyi population occurred. Laterthe Mnemiopsis population was devastated due to the predation of B. ovata and the predatory effect became low (below 1% per day).

DISCUSSION

Population dynamics

The ability of Mnemiopsis to adapt successfully to seasonal fluctuations in food abundance and temperature enables them to increase their population density very rapidly. Although the Mnemiopsis peak biomass is suggested to be governed by temperature in the northwestern Atlantic (Purcell et al., 2001), in the past, high biomass and abundance values were often reported even in winter in the Black Sea. For example, studying distribution of M. leidyi in eight different cruises during 1991–1995, Mutlu (Mutlu, 1999) found peak values of biomass and abundance between January and March when the range of surface temperatures was 6.5–10°C in the southern Black Sea. Although monthly or more intensive data on M. leidyi are scarce, in the northern Black Sea, it shows a more seasonal distribution with lower values in winter (Shiganova, 1998). However, before the appearance ofB. ovata the period in which M. leidyi notably occurs was wider: for example values >200 g m−2 were present from May till November (accounting for more than half a year) in 1995 in Sevastopol Bay (Finenko and Romanova, 2000). However, as revealed in this study, after the B. ovata invasion, occurrence of M. leidyi biomass is limited to only 2 months (i.e. July and August, Figure 2A and B). When it reaches peak values in a month or so,B. ovata starts to increase sharply and in the following 2 weeks this predator controls the levels of M. leidyi very effectively. In the southern Black Sea, too, in the last few years M. leidyi has not occurred until summer (A. E. Kideys, personal observation). Probably higher temperatures in summer 2001 resulted in the earlier seasonal maximum of Mnemiopsis (Figure 2A and B). The maximum biomass value increased from 1999 to 2001, being 211.5 g m−2 in 2000 and 790.3 g m−2 in 2001. Beroe ovata seemed to act even quicker in 2001 in reducing the M. leidyi peak. A similar event was also observed for 2002 (our personal observation).

After the disappearance of B. ovata in late autumn, the M. leidyi biomass again increased, but at a lower level than in previous years. Probably the better food provision of this over-wintering not numerous population produced fast growth and high fecundity so that in early summer the maximum abundance and biomass values of M. leidyi exceeded those in the years prior to the appearance of Beroe. In Narragansset Bay the annual population dynamics of Mnemiopsis were similar to those in Sevastopol Bay: the pattern of seasonal dynamics was identical during 3 years (1971, 1972, 1974) but differences in the timing and maximum biomass values occurred. In 1974 the population fell dramatically in September, whilst high biomasses were observed in this month in the other 2 years (Kremer, 1976). A reduction of the Mnemiopsis biomass coincided with an increase in Beroe abundance. Density of the Mnemiopsis population appeared to be a function of food abundance and the role of Beroe consisted in a reduction of prey biomass in autumn but not in a limitation of the maximum biomass.

The introduction of B. ovata to the Black Sea has considerably shortened the time of M. leidyi availability in large numbers in the plankton and hence its predatory impact on the zooplankton.

Digestion time, ingestion, growth and reproduction rates of B. ovata

The digestion time in Beroe in the present study is comparable with those determined by other authors for ctenophores. The digestion times of Mnemiopsis mccradyi and M. leidyi feeding on copepods varied from 0.33 to 3.5 h depending on temperature and prey number in the stomadeum (Reeve and Walter, 1978; Reeve, 1980; Larson, 1987). According to Shiganova et al. (Shiganova et al., 2000) the digestion time of B. ovata varied from 3 to 5 h at 24–26°C. Digestion times of B. ovata feeding onM. leidyi at 21 ± 1°C in our previous experiments varied within a wider range from 0.5 to 5.5 h depending on the prey–predator weight ratio (0.01–2.0) (Finenko et al., 2001). In this study digestion time ranged from 0.75 to5 h at 18°C when the prey–predator weight ratio changed from 0.03 to 3.24.

Like other gelatinous predators Beroe ingest their prey in proportion to the widely ranging prey concentrations (Reeve and Walter, 1978; Reeve et al., 1978). In conditions of high food abundance ingested food could reach >400% of body wet weight per day. Such a high ingestion rate could produce a high growth rate of ctenophores. However, the maximum daily specific growth rate for adult Beroe in our experiments was ∼0.2. This value is rather low compared with the values of 0.76 and 0.78 day−1 for M. mccradyi (Reeve and Baker, 1975) and Pleurobrachia bachei (Reeve and Walter, 1976), but close to Miller’s value (0.25) for M. leidyi in a range of temperatures up to 20°C, at which the fastest growth rates were observed (Reeve and Walter, 1978). The M. leidyi growth rate was found to range from 0.06 to 0.38 per day, being dependent on the ctenophore weight (Finenko and Romanova, 2000). Greve (Greve, 1970) reported the maximum daily growth rate for Beroe cucumis as 0.4 and for Bolinopsis infundibulum as 0.2. The lowest ctenophore growth rates (0.02–0.04 day−1) were reported by Kamshilov (Kamshilov, 1960) in the Barents Sea for B. cucumis at low temperatures.

In Sevastopol Bay in August 2001 under conditions of maximum prey concentration and high temperature, the maximum daily growth rate of the B. ovata population computed from field biomass data varied between 0.66 and 0.37. The maximum growth efficiency of adultB. ovata in our experiments was ∼0.3–0.35 under a high specific daily ration value and was comparable with those of other gelatinous predators (Fraser, 1969; Reeve et al., 1989). Beroe ovata demands both high food rations (not less than 20% of body weight per day) and a high prey biomass for growth. Probably the low prey abundance in late autumn is a major reason for the disappearance ofB. ovata from the plankton.

Predatory impact of M. leidyi on zooplankton and B. ovata onMnemiopsis population

During the first 2 years (1999–2000) after the arrival of Beroe in Sevastopol Bay its effect on the plankton community was very pronounced: the mean summer–autumn Mnemiopsis biomass fell by a factor of 4.6 in comparison with 1995 (Finenko and Romanova, 2000) when Beroe was absent (230 g m−2 in 1995 and 50 g m−2 in 2000). The predatory impact of M. leidyi on the forage zooplankton diminished sharply: even whenM. leidyi were at their peak biomass, they were found to remove 4–6% of zooplankton standing stock daily, throughout most of the year this value was below 1% per day.

In 2001 the mean summer–autumn M. leidyi biomass (160 g m−2) was close to that in 1995 (230 g m−2) as well as its predatory impact on zooplankton (maximum daily grazing rates were 16 and 20% of the zooplankton biomasses in 2001 and 1995, respectively), but a very short Mnemiopsis bloom in 2001 resulted in high average annual zooplankton biomass values.

A decrease in the predatory impact of Mnemiopsis on zooplankton during the last 3 years is confirmed by the comparison of minimum food requirements of the Mnemiopsis population with its food supply (biomass of zooplankton, cal m−2) (calorific content of zooplankton was taken as 4 cal mg−1 dry weight, dry:wet weight ratio as 0.2, and 1 ml of O2 is assumed to be equal to 4.86 cal). Food requirements were calculated for station 7, where zooplankton and ctenophore have been sampled, from the relationship between oxygen consumption rate and mean weight of ctenophores in the population at different temperatures (Abolmasova, 2001). The daily energy requirements accounted for 29–39% of the zooplankton stock only in September 2000 and August 2001 (period of maximum Mnemiopsis biomass), for other months they were below 1%. In July 1995 these values ranged from 172 to 284% of the zooplankton stock, being in the range of 17–53% during the longest period (July–October). Another conclusion from these findings is that the Mnemiopsis in the bay might experience a lack of food, especially during the period of intensive growth in summer when fodder zooplankton biomass cannot meet their energy requirements. Either the animals fed in micropatches of zooplankton, or they had additional food sources. Two different mechanisms of prey encounter that are functioning simultaneously (directing the food into the mouth by using lobes or transport of prey through food canals along the body) enable them to capture a wide range of prey with different swimming speeds such as ciliates, copepod nauplii and bivalve larvae (Waggett and Costello, 1999). Stoecker et al. (Stoecker et al., 1987) have shown that planktonic ciliates and copepod nauplii are preyed on by larval and post-larval Mnemiopsis and that they may be particularly important as food for newly hatched ctenophore larvae. In Sevastopol Bay M. leidyi larvae (wet weight 0.296 g) comprised up to 80% of population abundance on 1 August 2001 (the peak of Mnemiopsis biomass) and biomass of microzooplankton (infusoria and copepod nauplii) was 0.92 g m−2 (T. Pavlovskaya, unpublished data). If the clearance rate of the larvae was 1 l g−1 wet wt day−1 at 20°C (Stoecker et al., 1987), the ctenophore population could remove ∼4% of the microzooplankton biomass daily and cover 20% of their respiration requirements from that (microzooplankton caloricity is 0.5 cal mg−1 wet wt) (Khlebovich, 1979).

The predatory impact of the B. ovata population in Sevastopol Bay, calculated from data on Beroe respiration rate (Svetlichny et al., 2003), its size structure and abundance, could amount to 60% of M. leidyi biomass per day in October–November 2001. The minimal food requirements of the Beroe population in August–September 2001 far exceeded the energy content of their prey population.

In October 1999 the values of predatory impact ranged from 2 to 53% (Finenko et al., 2001). In the northeastern Black Sea in September 1999 the Beroe population consumed 0.7–5.7% of M. leidyi biomass daily (Shiganova et al., 2000). According to the calculations of Shushkinaet al. (Shushkina et al., 2000), the potential predatory impact of Beroe on a Mnemiopsis population in the same region could be as high as 30–80% of the biomass daily. The huge potential pressure of B. ovata on the M. leidyi population is supported by experimental data on the feeding behavior and ingestion rate of ctenophores. The daily ration of ctenophores grows in parallel with the food abundance within a wide range of prey concentrations and does not achieve any saturation (Reeve and Walter, 1978; Reeve et al., 1978). In the sea in conditions of patchy prey distribution when the average biomass could be exceeded several times, Beroe are able to feed very intensively and thus reduce the Mnemiopsis population sharply for a short period. A keen decrease in M. leidyi abundance during the period of B. ovata availability in the bay supports the hypothesis that the predatory impact of this invader is an important factor determining the structure and functioning of the plankton community in inshore waters of the Black Sea.

Intensive predation on Mnemiopsis by Beroe should cause an increase in zooplankton biomass. In fact the mean annual prey zooplankton biomass (1.10 ± 0.65 g m−2) in 2000–2001 increased by >2-fold compared with 1995 (0.42 ± 0.38 g m−2). This difference is statistically significant at P < 0.05 (Student’s t-test). Considerable increases in mean annual copepod abundance as a whole (Figure 9) and some species (Acartia clausi, Paracalanus parvus, Centropages ponticus) in particular (Figure 10) were also observed in the last 2 years as compared with previous years when Mnemiopsis bloom occurred and Beroe was absent. It means that the predatory impact of Mnemiopsis on prey zooplankton was reduced in the years of Beroe availability. The effectiveness of the ctenophore B. ovata in controlling high levels of the voracious plankton consumer M. leidyi and hence improvements in the pelagic ecosystem including the increase in the quantity of mesozooplankton presents an important step in dealing with invasive pelagic ctenophores, not only for the Black Sea but for other regions having similar problems.

Table I:

Fecundity of B. ovata inlong-term feeding experiments

No. of bottle Beroe wet wt, (g) Specific daily ration, (% wet wt) Total egg number 
4.68 108.3 ± 33.0 4007 
10.7 97.7 ± 43.2 2066 
17.0 70.1 ± 27.2 4220 
21.8 20.1 ± 8.4 2525 
No. of bottle Beroe wet wt, (g) Specific daily ration, (% wet wt) Total egg number 
4.68 108.3 ± 33.0 4007 
10.7 97.7 ± 43.2 2066 
17.0 70.1 ± 27.2 4220 
21.8 20.1 ± 8.4 2525 
Fig. 1.

Sampling locations 1–11 in Sevastopol Bay and adjacent water area.

Fig. 1.

Sampling locations 1–11 in Sevastopol Bay and adjacent water area.

Fig. 2.

(A) Abundance and (B) biomass of M. leidyi and B. ovata, (C) zooplankton biomass and (D) temperature (°C) in Sevastopol Bay in 1999–2001.

Fig. 2.

(A) Abundance and (B) biomass of M. leidyi and B. ovata, (C) zooplankton biomass and (D) temperature (°C) in Sevastopol Bay in 1999–2001.

Fig. 3.

Size structure of B. ovata population in 1999–2001 in Sevastopol Bay.

Fig. 3.

Size structure of B. ovata population in 1999–2001 in Sevastopol Bay.

Fig. 4.

Relationship between digestion time (h) and prey–predator wet weight ratio in B. ovata.

Fig. 4.

Relationship between digestion time (h) and prey–predator wet weight ratio in B. ovata.

Fig. 5.

Relationship between weight-specific daily ration (%) and wet weight (g) in B. ovata.

Fig. 5.

Relationship between weight-specific daily ration (%) and wet weight (g) in B. ovata.

Fig. 6.

Relationship between clearance rate (l g−1 h−1) and wet weight (g) in B. ovata.

Fig. 6.

Relationship between clearance rate (l g−1 h−1) and wet weight (g) in B. ovata.

Fig. 7.

Effect of specific daily ration (% mean wet weight) on specific growth rate (day−1) in adult B. ovata.

Fig. 7.

Effect of specific daily ration (% mean wet weight) on specific growth rate (day−1) in adult B. ovata.

Fig. 8.

Effect of specific daily ration (% mean wet weight) on gross growth efficiency (K1) at two food concentrations: 1.68 ± 0.47 g l−1 (diamonds), 2.54 ± 0.80 g l−1 (circles).

Fig. 8.

Effect of specific daily ration (% mean wet weight) on gross growth efficiency (K1) at two food concentrations: 1.68 ± 0.47 g l−1 (diamonds), 2.54 ± 0.80 g l−1 (circles).

Fig. 9.

Inter-annual dynamics of Copepoda abundance in Sevastopol Bay during 1976–1996 (Gubanova et al., 2001) and 2000–2001 (our data; vertical bars denote SE).

Fig. 9.

Inter-annual dynamics of Copepoda abundance in Sevastopol Bay during 1976–1996 (Gubanova et al., 2001) and 2000–2001 (our data; vertical bars denote SE).

Fig. 10.

Mean annual abundance of copepod species (ind. m−3) during 1995–1996 (shaded columns) (Gubanova et al., 2001) and 2000–2001(open columns) (our data; vertical bars denote SE). A.c., Acartia clausi + A. tonsa; P.e., Pseudocalanus elongatus; P.p., Paracalanus parvus; C.p., Centropages ponticus; O.s., Oithona similis.

Fig. 10.

Mean annual abundance of copepod species (ind. m−3) during 1995–1996 (shaded columns) (Gubanova et al., 2001) and 2000–2001(open columns) (our data; vertical bars denote SE). A.c., Acartia clausi + A. tonsa; P.e., Pseudocalanus elongatus; P.p., Paracalanus parvus; C.p., Centropages ponticus; O.s., Oithona similis.

This work was supported by Linkage Grant EST.CLG.976805 from NATO. We would like to thank Dr T. Yuneva, Dr P. Nival and an anonymous reviewer for their valuable comments on the manuscript and Mrs Alison Kideys for correcting the English of the text.

REFERENCES

Abolmasova, G. I. (2001) Effect of temperature and food conditions on energy metabolism in Mnemiopsis leidyi. Hydrobiol. J., 37, 90–96 (in Russian).
Anninsky, B. E. (
1994
) Organic matter composition of the jelly-fish Aurelia aurita and two species of ctenophores from the Black Sea.
Biol. Morya
 ,
20
,
291
–295 (in Russian).
Anninsky, B. E. (
2000
) The proximate chemical composition and energy content of the ctenophore Beroe ovata.
Ecol. Morya
 ,
51
,
25
–29 (in Russian).
Finenko, G. A. and Romanova, Z. A. (
2000
) Population dynamics and energetics of ctenophore Mnemiopsis leidyi in Sevastopol Bay.
Oceanologia
 ,
40
,
677
–685.
Finenko, G. A., Abolmasova, G. I. and Romanova, Z. A. (1995) Consumption, respiration and growth rates of Mnemiopsis mccradyi in relation to food conditions.
Biol. Morya
 ,
21
,
315
–320 (in Russian).
Finenko, G. A., Romanova, Z. A. and Abolmasova, G. I. (2000) The ctenophore Beroe ovata is a recent invader to the Black Sea.
Ecol. Morya
 ,
50
,
21
–25 (in Russian).
Finenko, G. A., Anninsky, B. E., Romanova, Z. A., Abolmasova, G. I. and Kideys, A. E. (
2001
) Chemical composition, respiration and feeding rates of the new alien ctenophore, Beroe ovata, in the Black Sea.
Hydrobiologia
 ,
451
,
177
–186.
Fraser, J. H. (
1969
) Experimental feeding of some medusae and chaeto-gnaths.
J. Fish. Res. Board Can.
 ,
26
,
1743
–1762.
Gordina, A. D., Pavlova, E. V., Ovsyany, E. I., Wilson, J. G., Kemp, R. B. and Romanov, A. S. (
2001
) Long-term changes in Sevastopol Bay (the Black Sea) with particular reference to the ichthyoplankton and zooplankton.
Estuarine Coastal Shelf Sci.
 ,
52
,
1
–13.
Greve, W. (
1970
) Cultivation experiments on North Sea ctenophores.
Helgol. Wiss. Meeres.
 ,
20
,
304
–317.
Gubanova, A. D., Prusova, I. Yu., Niermann, U., Shadrin, N. V. and Polikarpov, I. G. (
2001
) Dramatic change in the copepod community in Sevastopol Bay (Black Sea) during two decades (1976–1996).
Senckenbergiana marit.
 ,
31
,
17
–27.
Gücü, A. C. (1997) Role of fishing in the Black Sea ecosystem. In Örsoy, E. and Mikaelyan, A. (eds), Sensitivity to Change: Black Sea, Baltic Sea and North Sea. Klüwer Academic Publishers, Dordrecht, pp. 149–162.
Kamshilov, M. M. (1960) Size of ctenophore Beroe cucumis Fabricius.
Dokl. Akad. Nauk USSR
 ,
131
,
957
–960 (in Russian).
Khlebovich, T. V. (1979) Respiration rate in Infusoria. In Winberg, G. G. (ed.), General Basis for Aquatic Ecosystems Study. Nauka, Leningrad, pp. 25–30 (in Russian).
Kideys, A. E. (
1994
) Recent dramatic changes in the Black Sea ecosystem: the reason for the sharp decline in Turkish anchovy fisheries.
J. Mar. Syst.
 ,
5
,
171
–181.
Kideys, A. E. and Romanova, Z. A. (
2001
) Distribution of gelatinous macrozooplankton in the southern Black Sea during 1996–1999.
Mar. Biol.
 ,
139
,
535
–547.
Kiselev, I. A. (1969) Plankton of Seas and Continental Reservoirs. Nauka, Leningrad, Vol. 1, 658 pp. (in Russian).
Kovalev, A. V., Gubanova, A. D., Kideys, A. E., Melnikov, V. V., Niermann, U., Ostrovskaya, N. A., Prusova, I. Yu., Skryabin, V. A., Uysal, Z. and Zagorodnyaya, Ju. A (1998) Long-term changes in the biomass and composition of fodder zooplankton in coastal regions of the Black Sea during the period 1957–1996. In Ivanov, L. I. and. Oguz, T. (eds), Ecosystem Modeling as a Management Tool for the Black Sea. Klüwer Academic Publishers, Dordrecht, Vol. 1,pp. 209–219.
Kremer, P. (1976) Population dynamics and ecological energetics of a pulsed zooplankton predator, the ctenophore Mnemiopsis leidyi. In Wiley, M. (ed.), Estuarine Processes. Academic Press, New York, Vol. 1, pp. 197–215.
Larson, R. J. (
1987
) In situ feeding rates of the ctenophores Mnemiopsis mccradyi.
Estuaries
 ,
10
,
87
–91.
Mutlu, E. (
1999
) Distribution and abundance of ctenophores, and their zooplankton food in the Black Sea. II. Mnemiopsis leidyi.
Mar. Biol.
 ,
135
,
603
–613.
Mutlu, E., Bingel, F., Gücü, A. C., Melnikov, V. V., Niermann, U., Ostrovskaya, N. A. and Zaika, V. E. (
1994
) Distribution of the new invader Mnemiopsis sp. and the resident Aurelia aurita and Pleurobrachia pileus populations in the Black Sea in the years 1991–1993.
ICES J. Mar. Sci.
 ,
51
,
407
–421.
Niermann, U., Kideys, A. E., Kovalev, A. V., Melnikov, V. V. and Belokopytov, V. (1999) Fluctuations of pelagic species of the open Black Sea during 1980–1995 and possible teleconnections. InBesiktepe, S., Unluata, U. and Bologa, A. (eds), Environmental Degradation of the Black Sea: Challenges and Remedies. Klüwer Academic Publishers, Dordrecht, pp. 147–173.
Petipa, T. S. (
1957
) On average weight of the main zooplankton forms in the Black Sea.
Proc. Sevastopol Biol. Stn
 ,
9
,
39
–57 (in Russian).
Purcell, J. E., Shiganova, T. A., Decker, M. B. and Houde, E. D. (
2001
) The ctenophore Mnemiopsis leidyi in native and exotic habitats: U.S. estuaries versus the Black Sea basin.
Hydrobiologia
 ,
451
,
145
–176.
Reeve, M. R. (
1980
) Comparative experimental studies of feeding of chaetognaths and ctenophores.
J. Plankton Res.
 ,
2
,
381
–393.
Reeve, M. R. and Baker, L. D. (
1975
) Production of two planktonic carnivores (chaetognath and ctenophore) in south Florida inside waters.
Fish. Bull. US
 ,
73
,
238
–247.
Reeve, M. R. and Walter, M. A. (1976) A large-scale experiment on the growth and predation potential of ctenophore populations. In Mackie, G. (ed.), Coelenterate Ecology and Behavior. Plenum Publishing Company, New York, pp. 187–199.
Reeve, M. R. and Walter, M. A. (
1978
) Nutritional ecology of ctenophores—a review of recent research.
Adv. Mar. Biol.
 ,
15
,
249
–258.
Reeve, M. R., Sims, M. A. and Ikeda, T. (
1978
) Laboratory studies of ingestion and food utilization in lobate and tentaculate ctenophores.
Limnol. Oceanogr.
 ,
23
,
740
–751.
Reeve, M. R., Sims, M. A. and Kremer, P. M. (
1989
) Growth dynamics of a ctenophore (Mnemiopsis) in relation to variable food supply. I. Carbon biomass, feeding, egg production, growth and assimilation efficiency.
J. Plankton Res.
 ,
11
,
535
–552.
Shiganova, T. A. (
1998
) Invasion of the Black Sea by the ctenophore Mnemiopsis leidyi and recent changes in pelagic community structure.
Fish. Oceanogr.
 ,
7
,
305
–310.
Shiganova, T. A., Kideys, A. E., Gucu, A. C., Niermann, U. and Khoroshilov, V. S. (1998) Changes in species diversity and abundance of the main components of the Black Sea pelagic community during the last decade. In Ivanov, L. and Oguz, T. (eds), NATO TU-Black Sea Project: Ecosystem Modeling as a Management Tool for the Black Sea, Symposium on Scientific Results. Klüwer Academic Publishers, Dordrecht, Vol. 1, pp. 171–188.
Shiganova, T. A., Bulgakova, Yu. V., Sorokin, P. Yu. and Lukashev, Yu. F. (
2000
) Investigation of a new settler Beroe ovata in the Black Sea.
Biol. Bull.
 ,
27
,
202
–209.
Shiganova, T. A., Bulgakova, Yu. V., Volovik, S. P., Mirzoyan, Z. A. and Dudkin, S. I. (
2001
) The new invader Beroe ovata Mayer 1912 and its effect on the ecosystem in the northeastern Black Sea.
Hydrobiologia
 ,
451
,
187
–197.
Shushkina, E. A., Musaeva, E. I., Anokhina, L. L. and Lukasheva, T. A (
2000
) Role of the gelatinous macroplankton: jellyfish Aurelia and invading ctenophores Mnemiopsis and Beroe in the plankton commun-ities of the Black Sea.
Oceanologya
 ,
40
,
859
–866 (in Russian).
Stoecker, D. K., Verity, P. G., Michaels, A. E. and Davis, L. H. (
1987
) Feeding by larval and post-larval ctenophores on microzooplankton.
J. Plankton Res.
 ,
9
,
667
–683.
Svetlichny, L. S., Abolmasova, G. I., Hubareva, L. S., Finenko, G. A., Bat, L. and Kideys, A. (2003) Metabolic rates of Beroe ovata in the Black Sea. Mar. Biol. (in press).
Vinogradov, M. E., Sapoznikov, V. V. and Shushkina, E. A. (1992) The Black Sea Ecosystem. Nauka, Moscow, 112 pp. (in Russian).
Vostokov, S. V., Arashkevich, E. G., Drits, A. V. and Lukashev, Yu. F. (
2001
) Ecological and physiological characteristics of the ctenophore Beroe ovata in the coastal waters of the Black Sea: quantity, biomass, size distribution, hunting behaviour, feeding and metabolism.
Oceanologia
 ,
41
,
109
–115 (in Russian).
Waggett, R. and Costello, T. H. (
1999
) Capture mechanisms used by the lobate ctenophore, Mnemiopsis leidyi, preying on the copepod Acartia tonsa.
J. Plankton Res.
 ,
21
,
2037
–2052.
Zagorodnyaya, Y. A., Kovalev, A. V. and Ostrovskaya, N. A. (
2001
) Quantitative data and seasonal dynamics of Black Sea zooplankton near the Crimean coast in 1994–1995.
Ecol. Morya
 ,
55
,
17
–22 (in Russian).
Zaika, V. E. (
1972
) Growth of ctenophores and medusae.
Zool. J
 .,
51
,
179
–189 (in Russian).
Zaika, V. E. (1994) The drop in anchovy stock in the Black Sea: Result of biological pollution? Report of the Second Technical Consultation on Stock Assessment in the Black Sea. Ankara, Turkey, 15–19 February 1993. Rome, Italy, FAO, No. 495 78–83.
Zaitsev, Yu. P. and Alexandrov, B. G. (1997) Recent man-made changes in the Black Sea ecosystem. In: Örsoy, E. and Mikaelyan, A. (eds), Sensitivity to Change: Black Sea, Baltic Sea and North Sea. Klüwer Academic Publishers, Dordrecht, pp. 25–31.