The New Invader Beroe Ovata Mayer 1912 and Its Effect on the Ecosystem in the Northeastern Black Sea

Home , Beroe (ctenophore), Beroe cucumis, Beroe ovata, Mnemiopsis, Pleurobrachia, Pleurobrachia pileus

The new invader Beroe ovata Mayer 1912 and its effect on the ecosystem in the northeastern Black Sea

Tamara A. Shiganova1, Yulia V. Bulgakova1, Stanislav P. Volovik2, Zinaida A. Mirzoyan2 & Sergey I. Dudkin2 1P. P. Shirshov Institute of Oceanology, Russian Academy of Sciences, 36 Nakhimovskiy Pr., Moscow, 117851, Russia E-mail: [email protected] 2State Unitary Enterprise Research, Institute of the Azov Sea Fishery Problems 21/2 Beregovaya, Rostov-on-Don, 344007, Russia

Key words: Azov Sea, Mnemiopsis leidyi, feeding, respiration, ichthyoplankton, zooplankton

Abstract The abundance, biomass and distribution of the ctenophore, Beroe ovata Mayer 1912 were assessed along with several parameters associated with composition, respiration and feeding. Digestion time of B. ovata feeding on other ctenophores ranged from 4–5.5 h for Mnemiopsis leidyi A. Agassiz to 7–8 h for Pleurobrachia pileus (O. F. Müller). Daily ration was estimated as 20–80% of wet weight based on ﬁeld observations of feeding frequency coupled with digestion time. Calculations indicate that the measured population of B. ovata ingested up to 10% of the M. leidyi population daily. A marked decrease in M. leidyi density was recorded. The abundance of zooplankton increased about 5-fold and ichthyoplankton about 20-fold compared with the same season in previous years following the M. leidyi invasion.

Introduction abundance, the biomass of trophic mesozooplankton, its main food, sharply declined (Vinogradov et al., The invasion of alien species has become a great prob- 1989). The stocks of zooplanktivorous fish (anchovy, lem for many seas of the world due to increasing Mediterranean horse mackerel and sprat) dropped, international commerce combined with the use of bal- presumably due to competition with M. leidyi for last water on ships. The discharge of ballast water has food and predation by M. leidyi on fish eggs and lar- resulted in the transfer of species to regions where they vae (Tzikhon-Lukanina et al., 1993; Shiganova et al., are not indigenous. 1998; Shiganova & Bulgakova, 2000). As a rule, the invasion of alien species has a In response to this situation, a group of ex- damaging effect on ecosystems. For example, the perts from the international commission of the Joint introduction of the ctenophore, Mnemiopsis leidyi, Group of Experts on the Scientific Aspects of with ballast water from ships at the beginning of the Marine Pollution (GESAMP) (IMO/FAO/UNESCO- 1980s was a real catastrophe for the Black and Azov IOC/WMO/WHO/IAEA/UN/UNEP) (GESAMP, 1997) Seas (Vinogradov et al., 1989; Volovik et al., 1993). proposed the introduction of potential predators for These ecosystems were already damaged due to hy- Mnemiopsis leidyi. Among suggested species was drological and hydrochemical changes resulting from another ctenophore, Beroe ovata. Although this sug- decreased river discharge, eutrophication and overfish- gestion was not intentionally implemented, Beroe sp. ing (Ivanov & Beverton, 1985; Caddy & Griffiths, nevertheless appeared in the Black Sea in 1997 for the 1990; Zaitzev & Aleksandrov, 1997). The invasive M. first time. During 1997–1998, Beroe sp. occurred in leidyi demonstrated explosive development in 1989, some coastal areas in the northern part of the Black when its total biomass reached 1 billion tons for the Sea (Konsulov & Kamburska, 1998; Nastenko & Pol- entire Black Sea. Co-incident with high ctenophore ishchuk, 1999; N. Lupova, (Saint Petersburg Univer- 188 sity, Russia) pers. com.; Prof. M. Gomoiu, (Institute of ctenophore or 2–3 small ctenophores per container. Geoecology, Constanta, Romania) pers. com.). By late The duration of the experiments was 4 h; temper- August 1999, Beroe sp. spread throughout the north- atures ranged from 24.6 to 26.1◦C. Metabolic rates eastern Black Sea (Shiganova et al., 2000a,b) and was were estimated as differences between oxygen con- also found in the northwestern and southern regions centration in the container without (control) and with (Finenko et al., 2000a,b). In October 1999, Beroe sp. ctenophores. Oxygen concentrations were determined was observed in the Sea of Azov for the first time by the Winkler method (Romanenko & Kuznetzov, (Shiganova et al., 2000b). 1974). The oxygen concentration in the experimental bottles decreased to 78–89% of the initial oxygen concentration during the incubation. Twenty-one meas- Material and methods urements were made at a salinity of 18 and another 3 measurements at a salinity of 10.8 after the 1 h ac- Investigations of the ctenophore, Beroe ovata, were climation period. The experiments for tolerance to low ◦ conducted from 27 August to 15 September 1999. oxygen were carried out at 21 C. Ctenophores were They included experimental studies in both the labor- kept in closed containers until they died. atory of the Southern Branch of the P. P. Shirshov Beroe ovata was studied in laboratory and by in Institute of Oceanology, Russian Academy of Sci- situ observations. Feeding rate, digestion time, prey ences and the laboratory of the Novorossiisk research selection and behavior were conducted in the labor- station, and also field surveys in the northeastern Black atory from 27 August to 6 September and on 7–13 Sea on 17–24 August, 7–15 September 1999 and 12– September on board R/V ‘Akvanavt’. The freshly 19 April 2000. In addition, long-term field data of the caught specimens of B. ovata and their potential prey authors were used for comparison. – Mnemiopsis leidyi, Aurelia aurita (L), Pleurobra- The dry weight (DW) was determined for 31 chia pileus, fish larvae and Acartia clausi Giesbrecht specimens (length range 40–112 mm), of them, 6 (Copepoda) were placed in aquaria. To avoid dam- specimens were weighed individually and additional aging the ctenophores being used in experiments, weights were determined for groups of ctenophores weights were estimated using a length-weight rela- with mean lengths of 50, 75 and 105 mm. All anim- tionship based on 43 specimens (Fig. 1a). Weights als had empty guts. Length was measured for each of Mnemiopsis leidyi used in the feeding experiments animal, then excess moisture was removed by blot- were estimated using the equation ting before individuals were weighed (wet weight, y = 0.0056x1.85, WW). Ctenophores were dried at 60 ◦C constant to obtain a dry weight. Twenty five ctenophores (lengths where x is the length in mm and y is the wet weight in 40–110 mm) were analyzed for lipids by the Swahn grams. method (Swahn, 1953), for protein by the Lowry The study of the spatial and vertical distribution method (Pushkina, 1963), and for carbohydrates by of Beroe ovata, other gelatinous plankton, zoo- and the Orcin method. ichthyoplankton was conducted aboard the R/V ‘Ak- Tolerance to different salinities of Beroe ovata was vanavt’ by Institute of Oceanology, Russian Academy also studied using 3 l containers, with a single cteno- of Sciences. An additional ichthyological survey was phore in each container. Water of different salinity was carried out on 17–24 August by the Institute of the prepared by diluting Black Sea water with distilled Azov Sea Fishery Problems, and those ichthyoplank- water. Experiments were carried out with gradual sa- ton data were included in our study. Gelatinous linity changes from 18 to 15, 18 to 13.5, 18 to 10.8, plankton and ichthyoplankton were sampled with a 18 to 7.2, 18 to 4.5. Each experiment was conducted Bogorov-Rass net (square net opening of 1 m2,mesh for 1 h. Freshly collected ctenophores were used for size 500 µm) in vertical hauls from 150 m to the sur- every experiment after a 1 h acclimation period. After face in deep water and from the bottom to the surface the experiment testing B. ovata tolerance to different in shallow areas. A Juday net (square net opening of salinities, ctenophores were moved to a salinity of 18 0.1 m2, mesh size 200 µm) with a closing device was for 1 h rehabilitation. The experimental temperature used for depth-stratified hauls from the thermocline to was kept at 25–26 ◦C. the surface (15–25 to 0 m), from the pycnocline to the Respiration rate was determined in closed con- thermocline (60–80 m to 15–25 m) and from the an- tainers (volume 1.5 l) using 1 freshly collected large oxic layer to the pycnocline (120–200 m to 60–80 m). 189

Figure 2. Oxygen consumption of Beroe ovata. (a) – dependent on wet weight; (b) – dependent on the dry weight.

Figure 1. (a) Dependence of wet weight on length of Beroe ovata, appearance of a beroid in the Black Sea, the question (b) – dry weight as percentage of wet weight: 1-individual measure- of species identification was relevant. Some scient- ments; 2- group measurements. ists of the Black Sea countries identified this invasive species as Beroe cucumis (Zaitzev, 1998), introduced During bad weather, only two hauls were made per with ballast waters from the North Atlantic, others station. A total of 50 stations were occupied and 148 identified the ctenophore as Beroe ovata (in Konsu- hauls were made in September 1999 and 42 stations, lov & Kamburska, 1998; Shiganova et al., 2000a, b). 84 hauls were made in April 2000. Analyses of morphology, conducted by Prof. L. N. Seravin (Saint Petersburg University, Russia) determined it to be Beroe ovata Mayer, 1912 (Seravin et al., Results 2001) which was transferred with ballast waters from northern atlantic area. Taxonomy, body structure, size and chemical The ctenophores generally have a pink colour, and composition of Beroe ovata the largest were coloured with a brown tint. The body of this ctenophore is oval, wider at the oral end and At least two species of beroid ctenophores inhabit the tapered but not pointed at the aboral end. The me- Mediterranean Sea – Beroe ovata Esch and Beroe for- ridian canals have anostomoses between them, which skalii Chun (in Tregouboff & Rose, 1957). Of these are characteristic for Beroe ovata (in Seravin, 1998). species, only Beroe ovata has been identified in the The young specimens are wider in both the oral and Sea of Marmara (Shiganova et al., 1994). With the aboral ends of the body. 190

The relationship between length (L) and wet weight (WW) for Beroe ovata wasexpressedbya power regression: WW = 0.01 L 1.78 (R2= 0.79, n = 43, p < 0.001, std. error = 0.0092) (Fig. 1a). We collected mostly moderate to large B. ovata (60–162 mm) in offshore waters. Small specimens (16–18 mm) were found only in coastal areas with shallow depths of 2– 4 m. The most common sizes of B. ovata collected were 70–90 mm for specimens from Blue Bay, and 80–100 mm for specimens from the open sea. In the coastal area, the examined adult specimens were mature with both male and female gonads. Egg production was observed in a single ﬁeld-collected specimen. Eggs have a round shape. Hatched larvae were beroid type larvae without tentacles. The occur- rence of small individuals (16–18 mm) in the coastal area along with larger sizes supports the conjecture that Beroe ovata can both grow and reproduce in the Black Sea. Dependence of dry weight (DW) on the length was expressed by the equation: DW = 0.0016L1.36 (R2 = 0.93, n =9,p < 0.01). The proportion of DW to wet weight (WW) decreased with an increase in Beroe ovata size (Fig. 1b). Mean ratio of DW to WW for 31 specimens (40–112 mm) was 2.4 ± 0.3%. Mean protein content was 2.47 mg g−1, lipid content was 0.28 mg g−1, carbohydrates were 0.54 mg g−1 of WW. The mean caloriﬁc value of B. ovata tissue was determined from the known energetic standards of protein (5.7 cal mg−1), lipid (9.45 cal mg−1)and carbohydrate (4.10 cal mg−1) as 18.8 cal g−1 of WW. The carbon composition of B. ovata specimens from the Black Sea was 7.8% of DW, higher than in ocean waters (2–6%) (Kremer et al., 1986). This relatively high percentage of carbon per unit dry weight and the relatively low ratio of dry to wet weight can be explained by the lower salinity of Black Sea water compared with other regions where B. ovata has been studied.

Tolerance to salinity

Results of experiments showed that behaviour of ctenophores did not change when the salinity was decreased from18 to13.5. When ctenophores were moved from a salinity of 18 to a salinity of 15, they first stopped beating their cilia. However, in approximately 15 min, the cilia beating recovered and the ctenophores were again very active. When Beroe ovata Figure 3. Spatial distribution of ctenophores in the northeastern was moved from the Black Sea water (salinity 18) to Black Sea in September 1999: (a) – Beroe ovata;(b)–Mnemiopsis water of salinity 13.5, it sank down to the bottom, leidyi in September 1999; (c) – Mnemiopsis leidyi in April 2000. 191 made some movements there with actively beating with the mouth closed 5–10 cm from the surface. Less cilia, but did not go to the surface. Then the ctenophore often B. ovata was 30–50 cm from the surface with its began to produce mucus, but later it recovered act- body oriented horizontally. ive movements. In the water with salinity of 10.8, B. Of the specimens found near the shore, only 2.5% ovata sank down to the bottom, cilia beating ceased for of them had Mnemiopsis leidyi in the gut contents. 15 min but then the ctenophore completely recovered Further from shore in depths of 2–4 m, approximately active movements and natural behaviour. 20% of B. ovata had M. leidyi in the gastrovascular With the treatment at salinity of 7.2, Beroe ovata cavity. About 2% of B. ovata had fish larvae in the sto- laid on the bottom almost without any movements. Its modeum or a larva was attached on the body outside body grew turbid, but in 20–30 min. the ctenophore close to the mouth. began to move and its behaviour was the same as in In initial observations, Beroe ovata with newly previous experiments. In a salinity of 4.5 the cten- ingested Mnemiopsis leidyi, Aurelia aurita,orMedi- ophore sank to the bottom without movement, body terranean horse mackerel (Trachurus mediterraneus density decreased and its tissue turned a whitish color ponticus Aleev) and mullet (Mugil saliens Risso) fry and began to disintegrate. Later some recovery of were placed individually in aquaria (20 l). On one oc- movement was observed. When B. ovata was moved casion, the mullet larva, which was on the external side from Black Sea water (salinity 18) to the water with of B. ovata escaped and survived in the aquarium. In salinity 3 it immediately sank to the bottom and laid a few other occasions, larvae attached on the external there without any movements and no recovery. These part of the body were observed already dead with dam- data are preliminary but showed that B. ovata can aged skin. One ingested A. aurita (diameter 32 mm) tolerate short-term salinity shocks. was alive in the B. ovata (size 80 mm) stomodeum, and continued to make swimming movements. The Respiration rate mouth of B. ovata was closed and it kept the medusa in its stomodeum for 8 h before A. aurita was ejected Oxygen consumption by Beroe ovata was measured at and survived. Once a specimen of B. ovata tried to 2 salinities, 18 and 10.8. In the first case, the respir- envelop another one in the aquarium, but the swal- ation rate Q (ml ind−1h−1)varied nearly linearly with lowed B. ovata was finally egested. B. ovata also did wet weight (WW) where Q = 0.02WW0.86 (R2 = 0.78, not consume the copepod A. clausi and if swallowed, it n p < = 21, 0.001). Two of three measurements in egested A. clausi. In aquaria, non-feeding B. ovata ori- water with salinity 10.8 gave higher estimates than ented vertically near the surface with the closed mouth in experiments with salinity of 18 (Table 1, Fig. 2a). upwards or near the bottom of the tank with the mouth When the respiration rate was expressed in terms of turned towards the bottom. DW (Fig. 2b), no regression was significant. The oxy- During digestion observations on the R/V ‘Ak- gen consumption ranged from 0.25 to 0.71, with a vanavt’, newly collected Beroe ovata and their prey, mean of 0.54 ± 0.131 ml g WW−1 h−1. Mnemiopsis leidyi, Pleurobrachia pileus and Aurelia Our results of metabolic rate, re-calculated for ◦ aurita, were measured and placed in an aquarium (250 standard temperature (20 C) according to the normal l). B. ovata were very active and swallowed M. leidyi Krogh’s curve, were close to results of Finenko et al. in two ways – either enveloping them gradually or (2000 a, b; 2001), but were two times higher than res- opening the mouth widely, bending their body and Beroe ovata ults obtained for in the Bahamas (Kremer rapidly sucking in the entire prey. Biting off parts of et al., 1986) (Table 1). This difference probably was the M. leidyi body with macrocillia was not observed. due to salinity differences in the habitats, and there- During digestion, the prey was gradually macerated fore on the dry weight, of B. ovata. If the results are and advanced with stomodeum cilia to the aboral pole expressed in terms of body C, we obtain 6.9 ml O2g −1 −1 where it accumulated in whitish clumps near the prein- C h , which is similar the value re-calculated from fundibular complex. Then whitish material entered the Kremer et al. (1986) of 7.3 ml O gC−1 h−1. 2 preinfundibulum in fractions and passed in meridional canals and excreted with moisture though the pores. In Feeding addition to M. leidyi, B. ovata ingested P. pileus.One In situ observations in the coastal area of the Blue Bay B. ovata caught as many as three P. pileus or small M. showed Beroe ovata swam near the surface when not leidyi and P. pileus at the same time. B. ovata did not feeding. Most of the time it was oriented vertically, consume A. aurita in these experiments. Once B. ovata 192 ◦ Table 1. Beroe ovata oxygen consumption at experimental temperatures, and recalculated to standard temperature (20 C)

◦ Author DW Duration Temperature ( C) Salinity Oxygen consumption Oxygen consumption − − ◦ − − (g) (h) (ml g DW 1 h 1)at20C(mlgDW 1 h 1)

Kremer et al. (1986) 0.01–0.56 3–5 25 35 0.27 0.19 Finenko et al. (2000 a, b) 0.01–0.9 17–18 21 18 0.35–0.44 0.34 Shiganova et al. (2000a, b) 0.31–1.04 4 24.6–26 18 0.25–0.71 (0.54±0.131) 0.37 10.8 0.47–0.83 (0.66) 0.46

swallowed two P. pileus which had Calanus euxinus areas and only in small numbers in late August–early Hulsemann in their gut contents. P.pileus was digested September. by B. ovata,butC. euxinus was egested through the After the arrival of Beroe ovata, the sharpest drop mouth. Digestion times for M. leidyi prey were 4–5.5 among other gelatinous species was observed for both h at 21–26◦ C, for P. pileus were 7–8 hours at 25 ◦ C biomass and density of the ctenophore Mnemiopsis (Table 2). leidyi in 1999 compared with late summer data during We estimated daily ration by two methods. First, the previous ten years. In September 1999, the average the cost of respiration at 24–26 ◦C equalled 2.4 cal g abundance was only 17.3 ind. m−2, and the biomass DW−1 h−1. Consequently the minimum daily ration was155gm−2 (Fig. 4). The proportions of size groups of B. ovata (assimilation rate = 0.7) would be about 80 of M. leidyi greatly changed, too. Previously, there cal g DW−1 d−1 or about 2 cal g WW−1 d−1. Feeding had been intensive reproduction in August–September on Mnemiopsis leidyi (caloricity = 10 cal g WW−1 resulting in an abundance of small specimens of M. (Vinogradov et al., 1989)), the minimum daily ration leidyi (<10 mm) (Shiganova, 1997). By contrast, in of B. ovata should be about 20% of its wet weight. September 1999, small M. leidyi made up only 11.7% Second, if B. ovata were assumed to feed continuously of the population inshore and 16.4% in the open sea. on M. leidyi, one at a time, then the digestion time The most intensive reproduction usually occurs in the measurements suggest that the daily rations would inshore waters, but during August–September 1999, range from 80 to 400% measured as wet weight of the small M. leidyi were proportionally less abundant both predator B. ovata and prey M. leidyi. Such rates in the inshore waters than in the open sea. During our are unlikely in situ. Our observations in situ during survey in April 2000, M. leidyi was found only in the August-September 1999 indicated that approximately warmest locations and its density was 1.2 ind. m−2 20% of B. ovata contained M. leidyi. Therefore, we es- andbiomasswas28gWWm−2, but there were no timate that during this period, daily ration of B. ovata individuals of B. ovata at all (Fig. 3c). was in the range of 16–80% of its wet weight. By contrast, populations of gelatinous species not eaten much by Beroe ovata were unaffected. The bio- Distribution and abundance of the main components mass of the medusa Aurelia aurita was comparable in −2 of the Black Sea ecosystem both September 1998 and 1999 (Fig. 4): 283.6 g m in 1999 and 305 g m−2 in 1998. The biomass and In late August–early September 1999, Beroe ovata oc- density of the ctenophore Pleurobrachia pileus re- curred throughout the northeastern part of the Black mained practically unaltered relative to the previous −2 Sea above the seasonal thermocline (15–25 m). The year, the biomass was 83 g m in 1999 and 86.2 −2 −2 average abundance was 0.62 ind. m−2 in the inshore gm in 1998, density comprised 176.6 ind. m in −2 watersand1.27ind.m−2in the open sea, with an 1999, and 183.3 ind. m in 1998 (Fig. 4). The abund- average abundance in the whole investigated area of ance of the dinoﬂagellate, Noctiluca scintillans Kofoid 3 1.1 ind. m−2, and an average WW biomass of 31 & Swezy, decreased markedly from 30 to 37 × 10 −2 3 −2 gm−2 (Fig. 3a). The most abundant aggregations of ind. m in September 1998 to 9–10 × 10 ind. m B. ovata generally coincided with areas where Mnemi- in 1999 (Fig. 5). opsis leidyi was also abundant (Fig. 3a,b). In the open The biomass of zooplankton was several times sea, there were only moderate to large sized B. ovata, higher than observed in the same season during all while small specimens were found only in the coastal years since the Mnemiopsis leidyi invasion. The mean 193

Figure 4. Biomass of gelatinous animals in August–September in the Black Sea 1 – Pleurobrachia pileus;2–Aurelia aurita;3–Mnemiopsis leidyi (Data from 1989–1992 in Vinogradov et al. (1989, 1992, 1993) and Khoroshilov (1993). biomass of zooplankton was about 11g m−2 in the followed by the eggs of Trachurus mediterraneus open sea and about 13 g m−2 in the inshore waters ponticus (average 11.1 eggs m−2), and the eggs of in early September 1999. Compared with1998, bio- Mugil saliens and Diplodus annularis (Linne) (aver- masses of Calanus euxinus and Pseudocalanus elong- age 1.2 eggs m−2). Until these collections such high atus Boeck remained approximately constant in 1999, densities of E. encrasicolus and T. mediterraneus eggs but biomass of other copepods increased more than had not recorded since the Mnemiopsis leidyi invasion three fold and reached 1.4 g m−2 and >4 × 104 (Fig. 6a). ind m−2 between these periods (Fig. 5). The density of Sagitta setosa Muller also increased substantially to 6–15 × 103 ind. m−2 and the density of meroplank- Discussion ton also went up. The most conspicuous increase in mesozooplankton was for Cladocera, which increased In late August–early September 1999, Beroe ovata oc- up to 150–300 × 103 ind. m−2. The most abundant curred everywhere in the northeastern Black Sea, both cladoceran species was Penielia avirostris Dana. After in the deep sea and in the inshore waters. Our ob- many years of absence from the Black Sea zooplank- servations demonstrated that B. ovata consumes both ton samples species such as Pontella mediterranea other species of ctenophores in Black Sea, Mnemiopsis Claus appeared and Centropages ponticus Karaw was leidyi and Pleurobrachia pileus, primarily feeding on found in the 1999 samples in large numbers. the more available M. leidyi. Our observations indic- In 1999, twenty-four species of ﬁsh eggs and larvae ated that B. ovata did not digest crustacean zooplank- were selected as part of this study (Fig. 6a, b). The ton, the medusa A. aurita or ﬁsh larvae, although they eggs of the anchovy Engraulis encrasicolus ponticus were caught occasionally. Our results for digestion Aleksandrov predominated (average 323 eggs m−2), times were similar with other researchers (Table 2). B. ovata digested large Bolinopsis in 4–5 h at 24–25◦ C 194

Table 2. Digestion times of Beroe spp. feeding on lobate ctenophores. Numbers in parentheses are means

Author Temp. Predator Prey Length (mm) Weight (g) Digestion ◦ ( C) predator prey predator prey time (h)

Kamshilov (1960) B.cucumis Bolinopsis 30–40 15–20 3 Swanberg (1974) 24–25 B. ovata Bolinopsis 12–40 (27) 12–90 (50) 4.5 Finenko et al. (2000b) 21 B. ovata Mnemiopsis 1.4–59 0.25–14 0.5–5.5 Shiganova et al. (2000a, b) 21–26 B. ovata Mnemiopsis 50–98 30–88 11–37 3–22 4–5.5

In Great Bahama Bank, the specimens were observed from12to40mm(x = 27 mm) (Swanberg, 1974). Specimens of B. ovata within the size range 10–50 mm were found in the Bahamas (Kremer et al., 1986). It is not clear the reasons for the size difference between locations. We suppose that B. ovata in the Black Sea reach a larger size due to the abundance of available food, Mnemiopsis leidyi. The metabolic rate estimated in our experiments was very close to the value of Finenko et al. (2000a,b, 2001) for the northwestern Black Sea in 1999 (Table 1), but significantly higher on a dry weight basis than for the same species from the northern At- lantic (Kremer et al., 1986). Most of this difference can be explained by salinity differences if we assume Beroe ovata composition is in isotonic equilibrium with its surrounding water, where the Black Sea is approximately half the salinity of the water of the Bahamas. The minimum daily ration for Beroe ovata estimated from our metabolic data was about 20% of its wet weight. The observed digestion rate suggests that if B. ovata fed continuously, they could consume and digest 5–8 specimens of Mnemiopsis leidyi daily. In the field in August–September 1999, we observed about 20% B. ovata with M. leidyi in their guts, equivalent to an Figure 5. Density of zooplankton in the northeastern Black Sea in ingestion rate of 1–1.6 M. leidyi per day. During this September 1998–1999. period, mean B. ovata biomass was 31 g WW m−2 (1.1 ind. m−2)andM. leidyi biomass was 155 g WW m−2 (17.3 ind. m−2). Consumption by B. ovata that we (Swanberg, 1974). B. cucumis Fabricius from the Bar- calculated from field and experimental feeding rates ents Sea digested small Bolinopsis in3h(Kamshilov, amounted to a daily removal of 6.5–10% of the M. 1960 a, b). In our experiments the larger lobates, M. leidyi population. About 4% of the M. leidyi popula- leidyi, were digested considerably faster than smaller tion would need to be ingested per day to meet the cydippid P. pileus. metabolic requirement of the B. ovata population as Maximum size of Beroe ovata collected in the estimated from measured respiration rates of B. ovata. Black Sea was larger than for collections it in their A sharp decrease in the density and biomass of native regions. B. ovata reaches 115 mm near the At- Mnemiopsis leidyi in the northeastern Black Sea in lantic coast of North America (Mayer, 1912) as well as September 1999, as compared to September of prein the Mediterranean Sea (Tregouboff & Rose, 1957). vious years (Fig. 4), implicates Beroe ovata as a po- 195

Figure 6. Long-term dynamics of ichthyoplankton density in the northeastern Black Sea in July–August. (a) – eggs; (b) – larvae. Data from 1962 in Dekhnik (1973). 1 – anchovy; 2 – Mediterranean horse mackerel, 3 – others. tentially important source of mortality. The M. leidyi from the previous year. This may be because Beroe population usually increases in spring after a warm ovata inhabits the surface layer while P. pileus pre- winter (Shiganova, 1998); considering that the 1998– dominantly inhabits the cold intermediate layer and 1999 winter was warm and that water temperature below. Possibly, B. ovata ingests some P. pileus at increased by 1.5–2 ◦C in June–July 1999 (data of Hy- night, however, only a small part of the P. pileus popu- drophysical laboratory of the Southern Branch of the P. lation ascends into the surface layer (Vinogradov et al., P. Shirshov Institute of Oceanology, Russian Academy 1987). The population of the medusa Aurelia aurita of Sciences), a high density of M. leidyi would have was also similar in 1999 to the 1998 level (Fig. 4), and been expected in August–September, as observed in slightly higher than average levels for the past 5 years previous years (Purcell et al., 2001). In addition, M. (Shiganova et al., 1998), suggesting that its population leidyi usually actively reproduces at that time (Shigan- also was not affected by B. ovata. ova, 1997, 1998). By contrast, in September 1999, The density and biomass of mesozooplankton and we observed an unusually low abundance of M. leidyi its species diversity greatly increased in September and low numbers of small specimens relative to the 1999, after the appearance of Beroe ovata, and were previous September (Shiganova et al., 2000 b). Prob- similar to values observed prior to the Mnemiopsis ably B. ovata initially grazed small specimens in the leidyi invasion (Shiganova, 1998). The species in- inshore waters, due to the availability and accessibility habiting cold intermediate layer (Calanus euxinus, of young M. leidyi as prey. Pseudocalanus elongatus) did not change in density Observations of previous years showed that sea- and biomass, while the density of copepods inhabiting sonal population dynamics of Mnemiopsis leidyi were surface layer greatly increased. The density of Clado- similar in the Black and Azov Seas (Shiganova et al., cera, mainly Penilia avirostris, inhabiting the sur- 2001). In September 1999, however, biomass of M. face layer also greatly increased. In addition, several leidyi was very high in the Sea of Azov (Fig. 7), while Mediterranean species (Copepoda: Euchaeta marina the population in the Black Sea was the lowest in 10 Pustandrea, Rhyncalanus nasutus Giesbrecht, Pleur- years (Fig. 6). This circumstantial evidence implicates omamma gracilis Claus, and Ostracoda Philomedes B. ovata as a major predator of M. leidyi in the Black globosa) were found in the northeastern region for Sea. the ﬁrst time (E. I. Musaeva, P. P. Shirshov Institute The abundance of the ctenophore Pleurobrachia of Oceanology, Russian Academy of Sciences, pers. pileus in late summer 1999 was essentially unchanged com.). 196

Figure 7. Long-term dynamics of Mnemiopsis leidyi density in Sea of Azov in August.

Species diversity and total numerical abundance of neither mesozooplankton nor endemic gelatinous spe- ichthyoplankton were unusually high for the north- cies (Aurelia aurita, Pleurobrachia pileus) should be eastern region in late August 1999. The density of affected directly. Due to its feeding preference and eggs of both Engraulis encrasicolus ponticus and vertical distribution, B. ovata should primarily impact Trachurus mediterraneus ponticus increased to levels the population of Mnemiopsis leidyi and indirectly comparable to those before the Mnemiopsis leidyi in- affect mesozooplankton. vasion (Fig. 6a). The density of larvae was still low We demonstrated that Beroe ovata can live in water in August after the introduction of Beroe ovata.Un- with rather low salinity, and therefore may be able to like the collected eggs, which were spawned only one penetrate into the Sea of Azov, however, it is unknown day before sampling, when B. ovata was present and if B. ovata could live and reproduce in the Sea of Azov, M. leidyi density was low, the larvae possibly were if it would be a constant or temporary inhabitant there, from spawnings before B. ovata was present. Thus, or if it could influence the recovery of its ecosystem. the 1999 data suggest the appearance of B. ovata in the Black Sea decreased the abundance of M. leidyi sufficiently to modify populations of other zooplankt- References ivores. All effects of B. ovata may not be positive, however. Preliminary observations indicate that fish Caddy, J. F. & R. C. Griffiths, 1990. A perspective on recent fishery- larvae, although not ingested by B. ovata,maybe related events in the Black Sea. Studies and Reviews. GFCM 63: killed though occasional direct contact with B. ovata. 43–71. Dekhnik, T. V., 1973. Ichthyoplankton of the Black Sea. Naukova Certainly, all the above improvements were not Dumka: 234 pp merely the results of the invasion by Beroe ovata. Finenko, G. A., Z. A. Romanova & G. I. Abolmasova, 2000 a. New Since the first decrease of Mnemiopsis leidyi dens- settler into the Black Sea – ctenophore Beroe ovata. In Matishov, ity in 1993, some improvements in parameters of the G. G. (ed.), Thesis of the Report at Scientific Seminar “Species - Invaders in the European Seas of Russia”, Murmansk, 27–28 ecosystem and recovery of biodiversity were recorded January 2000: 95–96 (in Russian). (Shiganova et al., 1998). But it was not until 1999, Finenko, G. A., Z. A. Romanova & G. I. Abolmasova, 2000 b. with the advent of B. ovata, that there was a sharp in- The ctenophore Beroe ovata is a recent invader to the Black Sea. crease in the density and diversity of mesozooplankton Ecologiya morya 50: 21–25 (in Russian). Finenko, G. A., B. E. Anninsky, Z. A. Romanova, G. I. Abolmasova and ichthyoplankton. & A. E. Kideys, 2001. Chemical composition, respiration and Our data demonstrate that Beroe ovata can re- feeding rates of the new alien ctenophore, Beroe ovata,inthe produce, feed and grow in the northeastern Black Black Sea. Hydrobiologia 451 (Dev. Hydrobiol. 155): 177–186. Sea. The same conclusions were made for the north- GESAMP (IMO/FAO/UNESCO-IOC/WMO/WHO/IAEA/UN/ UNEP Joint Group of Experts on the Scientific Aspects of western area (Finenko et al., 2000 a, b, 2001). If Marine Environmental Protection), 1997. Opportunistic settlers B. ovata continues to be found in the Black Sea, and the problem of the ctenophore Mnemiopsis leidyi invasion in the Black Sea. Rep. Stud. GESAMP 58: 84 pp. 197

Ivanov, L. & R. J. H. Beverton, 1985. The fisheries resources of the Shiganova, T. A., Yu. V. Bulgakova, P. Yu. Sorokin & Yu. F. Mediterranean. Part two. Black Sea. GFCM FAO, Rome: 70 pp. Lukashev, 2000a. Preliminary results of investigations of Beroe Kamshilov, M. M., 1960a. Feeding of ctenophore Beroe cucumis ovata, a new invader into the Black Sea, and its effect on the Fab. Dokl. Acad. Nauk SSSR 130: 1138–1140 (in Russian). pelagic ecosystem. In Matishev, G.G. (ed.), Thesis of the Report Kamshilov, M. M., 1960b. The dependence of ctenophore Beroe at Scientific Seminar “Species - Invaders in the European Seas of cucumis Fab sizes from feeding. Dokl. Acad. Nauk SSSR 131: Russia”, Murmansk: 105–108 (In Russian). 957–960 (in Russian). Shiganova, T. A., Y. V. Bulgakova, P. Yu. Sorokin & Yu. F. Khoroshilov, V. S., 1993. Sesonal dynamics of the Black Sea Lukashev, 2000b. Investigations of new settler Beroe ovata in population of ctenophore Mnemiopsis leidyi. Oceanology 33: the Black Sea. Biol. Bull. 2: 247–255. 558–562. Shiganova, T. A., U. Niermann, A. C. Gucu, A. Kideys & V. S. Konsulov, A. & L. Kamburska, 1998. Ecological determination of Khoroshilov, 1998. Changes of species diversity and their abund- the new Ctenophora - Beroe ovata invasion in the Black Sea. Tr. ance in the main components of pelagic community after Mne- Ins. Oceanology, Varna: 195–197. miopsis leidyi invasion. In Ivanov, L. & T. T. Oguz (eds), Kluwer Kovalev, A. V., S. Besiktepe, J. Zagorodnyaya & A. Kideys, Academic Publishers, Dordrecht, The Netherlands: 171–188. 1998. Mediterraneanization of the Black Sea zooplankton is con- Shiganova, T. A., I. A. Mirzoyan, E. A. Studenikina, S. P. Volovik, tinuing. In Ivanov, L. & T. Oguz (eds), Ecosystem Modeling I. Siokoi-Frangou, S. Zervoudaki, E. D. Christou, A. Yu. Skirta, as a Management Tool for the Black Sea. Kluwer Academic & H. J. Dumont, 2001. Development of the Ctenophore Mnemi- Publishers, Dordrecht 47: 199–207. opsis leidyi (A. Agassiz) in the Black Sea and in the other seas Kremer, P., M. F. Canino & R. W. Gilmer, 1986. Metabolism of of the Mediterranean basin. Mar. Biol. In press. epipelagic tropical ctenophores. Mar. Biol.: 403–412. Swahn, B., 1953. Method identification of lipids. Scand. J. Clin. Mayer, A. G., 1912. Ctenophores of the Atlantic coast of North Lab. Inv. 5: 9. America. Publs. Carnegie Inst. 162: 1–58. Swanberg, N., 1974. The feeding behavior of Beroe ovata.Mar. Nastenko, E. V. & L. M. Polishchuk, 1999. The comb jelly Beroe Biol. 24: 69–76. (Ctenophora: Beroida) in the Black Sea. Dopovidi Nazionalnoi Tregouboff, G. & M. Rose, 1957. Manuel de Planctonologie Akademii Nauk, Ukraine11: 159–161. Mediterraneenne. Centre Nat. de la Rech. Sci. Paris 1: 1–587. Pushkina, N. I., 1963. Biokhimicheskie metody issledovanii. Bio- Tzikhon-Lukanina, E. A., O. G. Reznichenko & T. A. Lukasheva, chemical methods of investigations. Moscow, MedGIZ: 63 pp. 1993. Ecological variation of combjelly Mnemiopsis leidyi Purcell, J. E., T. A. Shiganova, M. B. Decker & E. D. Houde, 2001. (Ctenophora) in the Black Sea. J. obschei biologii 6: 713–721 The ctenophore Mnemiopsis in native and exotic habitats: U. S. (in Russian). estuaries versus the Black Sea basin. Hydrobiologia, this volume. Vinogradov, M. E., M. V. Flint & G. G. Nikolaeva, 1987. Vertical Romanenko, V. I. & S. I. Kuznetzov, 1974. Opredelenie rastvoren- distribution of mesoplankton in the open Black Sea in spring. nogo v vode kisloroda po metody Winklera. Determination of In Musaeva, E. I. (ed), Sovremennoe sostoyanie ecosystemy dissolved oxygen according to Winkler method. Ekologia mik- Chernogo morja. Nauka, Moscow: 144–186 (in Russian). roorganizmov presnikh vodoemov, Leningrad, Nauka: 176–177. Vinogradov, M. E., V. V. Sapozhnikov & E. A. Shushkina, 1992. Seravin, L. N., 1998. Ctenophora. Dobrovol’sky, A. (ed.), Omsk The Black Sea Ecosystem. Nauka, Moscow: 112 pp. Biological Scientific Institute, St.-Petersburg: 1–84. Vinogradov, M. E., E. A. Shushkina & G. G. Nikolaeva, 1993. The Seravin, L. N., Shiganova, T. A., Lupova, N. E., 2001 The history of state of zoocenosis in the open Black Sea in the end of summer study of ctenophore Beroe ovata (ctenophora, atentaculata, ber- 1992. Oceanology 33: 382–387. oida) and some peculiarities of morphology of the representative Vinogradov, M. E., E. A. Shushkina, E. I. Musaeva & P. Yu. Sorokin, from the Black Sea. Zoologichesky jour. in press. 1989. Ctenophore Mnemiopsis leidyi (A. Agassiz) (Ctenophora: Shiganova, T. A., 1997. Mnemiopsis leidyi abundance in the Black Lobata) – new settlers in the Black Sea. Oceanology 29: 293– Sea and its impact on the pelagic community. Sensitivity of the 298. North, Baltic Sea and Black Sea to Antropogenic and Climatic Volovik, S. P., I. A. Mirzoyan & G. S. Volovik, 1993. Mnemiopsis Changes. In Ozsoy, E. & A. Mikaelyan (eds), Kluwer Academic leidyi: biology, population dynamics, impact to the ecosystem Publishers, Dordrecht, The Netherlands: 117–130. and fisheries. ICES. Statutory meeting C. M. 1993/L:69: 1–12. Shiganova, T. A., 1998. Invasion of the Black Sea by the ctenophore Zaitsev, Yu. P., 1998. Marine hydrobiological investigations of Mnemiopsis leidyi and recent changes in pelagic community National Academy of Science of Ukraine during the 1990s in structure. Fish. Oceanogr. GLOBEC Special Issue: 305–310. XX century: shelf and coastal water bodies of the Black Sea. Shiganova, T. A. & Y. V. Bulgakova, 2000. Effect of gelatin- Hydrobiol. Zhurnal 6: 3–21 (in Russian). ous plankton on the Black and Azov Sea fish and their food Zaitsev, Yu. P. & B. G. Aleksandrov, 1997. Recent man-made resources. ICES J. mar. Sci. 57: 641–648. changes in the Black Sea ecosystem. In Ozsoy, E. & A. Mi- Shiganova, T. A., B. Ozturk & A. Dede, 1994. Distribution of the kaelyan (eds), Sensitivity of North Sea, Baltic Sea and Black ichthyo-, jelly- and zooplankton in the Sea of Marmara. FAO Sea to Anthropogenic and Climatic Changes. Kluwer Academic Fisheries report 495: 141–145. Publishers, Dordrecht, The Netherlands: 25–32.