BLACK OCEANOGRAPHY Impacts of Invasive Ctenophores on the Fisheries of the and

Figure 1b. Th e ctenophore ovata of the Black Sea. Th is specimen has no food Figure 1a. Th e ctenophore leidyi of (i.e., Mnemiopsis leidyi) in its stomach, which is most of the body cavity (compare the Black Sea. Photo by Ahmet E. Kideys. with Figure 1c and 1d where the organisms have food in their stomachs). Mouth of B. ovata, which is half closed, is along the entire width.

Th is article has been published in Oceanography, Volume 18, Number 2, a quarterly journal of Th e Oceanography Society. Copyright 2005 by Th e Oceanography Society. All rights reserved. Reproduction of any portion of this article by photo- 76 Oceanography Vol.18, No.2, June 2005 copy machine, reposting, or other means without prior authorization of Th e Oceanography Society is strictly prohibited. Send all correspondence to: [email protected] or Th e Oceanography Society, PO Box 1931, Rockville, MD 20849-1931, USA. BY AHMET ERKAN KIDEYS, ABOLGHASEEM ROOHI, SIAMAK BAGHERI, GALINA FINENKO, AND LYUDMILA KAMBURSKA

Gelatinous zooplankton are known to have a substantial effect on pelagic food webs by exerting top- down control on their ecosystems (Purcell and Decker, 2005), but their impact could be even greater when they invade other . The effects of zooplankton invasions have been well documented for the Black Sea and very recently for the Caspian Sea. Until the , three species of gelatinous macrozooplankton were present in the Black Sea: two scyphozoan medusae ( pulmo and Aurelia aurita) and only a single ctenophore species ( pileus) (Kideys and Romanova, 2001). Then, in the early 1980s, the ctenophore Mne- miopsis leidyi (Figure 1a), already known as a voracious zooplankton feeder (Reeve et al., 1978), was transported (likely via ballast waters) to the Black Sea from its native waters of the western Atlantic . Achievement of peak biomass levels of this ctenophore at the end of the 1980s caused the onset of striking adverse ecological events in the Black Sea, such as abnormal oscillations in dy- namics (Kideys et al., 2000) and, most notably, a sharp decrease in the pelagic fi shery (Kideys, 1994). By the end of the 1990s, the accidental introduction of another ctenophore to the Black Sea, Beroe ova- ta (already known to feed exclusively on other ctenophores) (Figure 1b, 1c, 1d), coincided with another set of striking events, but this time it was benefi cial for the ecosystem and the fi shery.

Figure 1c. Th e ctenophore Beroe ovata of the Black Sea with a Figure 1d. Th e ctenophore Beroe ovata just swallowed a Mnemiopsis half-digested Mnemiopsis leidyi specimen in its stomach. leidyi specimen in the Black Sea. Photo by Ahmet E. Kideys.

Oceanography Vol.18, No.2, June 2005 77 Invasion of these ctenophores and et al., 1978). Such high growth rates can et al., in press). M. leidyi has also been their contribution to the decline of the only be achieved with a very high feeding shown to feed on the eggs and larvae of entire Black Sea’s ecosystem in general, rate. The abundance of Mnemiopsis has fi shes both in its native and in the and on its fi shery in particular, has been been observed to fl uctuate throughout Black Sea (Mutlu, 1999). questioned. Other factors, such as over- the year. In the Narragansett (off- In the Black Sea, M. leidyi (as well as fi shing (Gücü and Oguz, 1998; Gücü, Rhode Island, USA), for example, Aurelia aurita and Beroe ovata) are con- 2002) and climate change (see Oguz, this Kremer and Nixon (1976) found that fi ned to surface (and mainly coastal) issue) may also be to blame. All of these while the overwintering population of waters above the (in the factors could be acting simultaneously Mnemiopsis was extremely low (1 to 2 warm seasons) (Mutlu, 1999; Kideys and on the ecosystem, however, pinpoint- per 104 m3), they could reach a Romanova, 2001) coincident with the ing the major ones is very important for peak density of over 50 individuals per greatest abundance of zooplankton (due understanding sensitive ecosystems that m3 in summer. Although highest abun- to smaller copepod and cladoceran spe- are increasingly exposed to anthropo- dances occur in summer (and early au- cies as well as young stages of other im- genic effects and for using the experience tumn), unlike in native regions, relatively portant forage zooplankton). These ge- obtained from the Black Sea case study high concentrations of this ctenophore latinous zooplankton are separated from to predict, and possibly mitigate, future were present during other seasons in the the native ctenophore Pleurobrachia rho- ecosystem decline. One immediate prac- Black Sea (Mutlu, 1999; Kideys and Ro- dopis, which dwells in deeper (below the tical benefi t of such knowledge would manova, 2001). It is worth noting that thermocline at around 30 m in summer) be for helping to stem the decline of the Mnemiopsis’s summer spawning and offshore waters. neighboring Caspian Sea, a unique and period coincides with that of the ancho- fertile ecosystem, which is presently ex- vy in the Black Sea. LONGTERM DISTRIBUTION OF periencing similar adverse events, but on Mnemiopsis has long been reported M. LEIDYI IN THE BLACK SEA an even greater scale. as an effective predator on zooplankton. The biomass of the offshore- (and deep-) Reeve et al. (1978) state that perhaps dwelling ctenophore Pleurobrachia rho- BIOLOGY OF MNEMIOPSIS the most signifi cant aspect of the feed- dopis varies less over time (Kideys and LEIDYI IN ITS NATIVE AND ing behavior of Mnemiopsis is that their Romanova, 2001) than Aurelia aurita INTRODUCED REGIONS ingestion rate is proportional to food and M. leidyi. Figure 2 shows long-term Mnemiopsis () has certain concentration. Because of this, concomi- changes in the biomass of only M. leidyi biological characteristics that enable this nant with their appearance, a dramatic and Aurelia aurita (biomass changes of species to signifi cantly affect its ecosys- decrease in the number or biomass of the most recent ctenophore Beroe ovata tem. Main (1928 cited in Vinogradov et copepods and other food zooplankton is are discussed separately later). In this al., 1989) points out that, although most often observed in the native region. For fi gure, the values obtained until 1991 medusae are microphages (consume mi- example, Burrell (1968, cited in Kremer, croscopic prey), Mnemiopsis is a macro- 1979) suggested that by M. Ahmet Erkan Kideys ([email protected]. phage capable of consuming fairly large leidyi was responsible for a large frac- edu.tr) is Associate Professor, Institute of prey (up to 1 cm or more in length). tion (73 percent) of total zooplankton Marine Sciences, Erdemli, . Abol- Mnemiopsis, like all other ctenophores, mortality in the York of ghaseem Roohi is Research Associate, are hermaphroditic. Ctenophores, partic- the (offshore Virginia, Mazandaran Fisheries Research Center, Sari, ularly members of the genus Mnemiopsis, USA). Finenko and Romanova (2000) . Siamak Bagheri is Research Associate, have a very high reproductive capacity. calculated that on a daily basis, about Guilan Fisheries Research Center, Anzali, Mnemiopsis mccradyi is able to produce 20 percent of total forage zooplankton Iran. Galina Finenko is Senior Research 8,000 eggs within 23 days—after only 13 was being eaten by this ctenophore in Associate, Institute of Biology of the South- days of its own birth. The growth rate the summer of 1995. Similar high values ern , , . Lyudmila of this species is comparable to that of were found by other scientists studying Kamburska is Senior Research Associate, (daily doublings) (Reeve the Black Sea and Caspian Sea (Finenko Institute of Oceanology, Varna, .

78 Oceanography Vol.18, No.2, June 2005 25 belong to Russian investigators (mainly 25 (a) Bulgaria 20 20 from the western and northern Black 15 15

Sea), and after 1991, to Turkish investi- 10 10 gators (from the southern Black Sea). It 5 5 should be noted that, although the Turk- 0 0 1970 1975 1980 1985 1990 1995 2000 ish data were from a higher number of 25 25 (b) stations, Kideys and Romanova (2001) 20 20 ) -2 suggested these values were too low be- 15 15 cause their nets were not as effi cient (had 10 10 a coarser mesh) as the Russians’. Because 5 5 of this, the Russian values were effi cien- 0 0 cy-corrected (multiplied by 2 to 3 based 1970 1975 1980 1985 1990 1995 2000 on the net most often used), though 25 500 (c) Former USSR Countries those from the southern Black Sea (af- 20 400 ter 1991) were reported as uncorrected, 15 300 fish catch (thousand tons) Total 200 raw values. As seen in Figure 2, after the 10 Forage zooplankton biomass (g wet wtForage m 5 100 famous peak values of 1989, biomass 0 0 values for M. leidyi as high as 485±34 g 1970 1975 1980 1985 1990 1995 2000 2 25 WW/m (wet weight per meters squared) (d) Turkey 500 20 were obtained in 1995 (uncorrected, raw 400 15 300 data from March, which is not the main 10 200 development season of this ctenophore!) 5 100 from a dense station grid (107 stations) 0 0 1970 1975 1980 1985 1990 1995 2000 in the southern Black Sea (Mutlu, 1999). 2000 . 2000 1500 These data clearly show that the Rus- 1600 1430 1200 900 biomass sian (corrected) values of 1.5 to 2 kg ) 800 -2 WW/m2 obtained for early autumn 1989 Mnemiopsis leidyi

(Vinogradov et al., 1989) are reasonable aurita A. 400 Aurelia aurita (g wet wt m as opposed to Gücü and Oguz’s (1998) and statement that, “neither carrying capac- 0 ity nor the trophodynamic structure of M. leidyi 1970 1975 1980 1985 1990 1995 2000 the Black Sea support such high biomass Figure 2. Long-term changes in the biomass of fi sh, forage zooplankton, and gelatinous mac- value of Mnemiopsis sp.” rozooplankton in the Black Sea. Fish catch data for each country is from www.seaaroundus. com. Th e forage zooplankton data (from Kideys et al. [2000], except for Romania) are for (a) It has been suggested that, since the from the off shore western Black Sea, (b) from the coastal waters off Romania (from A. Pe- 1970s, the population of A. aurita has tran and M. Moldoveau, National Institute for Marine Research and Development “Grigore been increasing, reaching peak values in Antipa” Constanta, unpublished data, 2005), (c) from the coastal northwestern shelf (+) and off shore waters of the northeastern region, and (d) from off shore waters off Turkey. Gelati- the 1980s (Figure 2). After the explosive nous zooplankton data before 1991 belong to the northern Black Sea (Russian values), and development of M. leidyi in 1989, the after 1990 belong to the southern Black Sea (Turkish values, after Kideys et al. [2000]). Note abundance of A. aurita dropped precipi- the blue rectangular area where the fi rst peak of Mnemiopsis leidyi occurred, when there were sharp decreases in the fi sh catches and forage zooplankton in diff erent regions. tously (Figure 2), indicating a potential for intense competition between these species. One should note here that, given the same biomass, M. leidyi would exert in their physiological rates (e.g., feeding, reported in 1982 in the western Black a much higher impact on the ecosystem reproduction, and growth). Sea (Konsulov and Kamburska, 1998) compared to A. aurita due to differences The fi rst appearance of M. leidyi was and its biomass peaks in 1988 to 1989,

Oceanography Vol.18, No.2, June 2005 79 six years later. Considering the extremely the distribution of this ctenophore in the calculations suggest a minimal role of fast reproduction and growth capability Black Sea (Kideys and Romanova, 2001). gelatinous species on the decline of the of this ctenophore, this period is long. In fact, this is the lowest average biomass fi sh stocks, contrary to the general belief. However, since M. leidyi is known to value recorded for M. leidyi since its More interestingly, the model results in- prefer higher temperatures for repro- mass development in the southern Black dicate that the decline in the fi sh stocks duction, such a delay may be due to the Sea. This clear decreasing trend (Figure was as a consequence of overfi shing...” unusually cold temperatures observed 2) and the strong seasonality (Figure 3) We disagree with this statement. It would in the Black Sea occurring during those observed after 1998 appears to follow the be too much of a coincidence that all years (Oguz, this issue). arrival of the M. leidyi predator Beroe countries overfi shed during the same pe- After the highest values were reported ovata to the Black Sea (more on this in riod. One expects that overfi shing, if any, between 1988 and 1991, the biomass of later sections). should be at its lowest level for the Soviet M. leidyi oscillated at more moderate block countries during this time; at the levels, with a secondary peak in 1995. THE ROLE OF MNEMIOPSIS end of the 1980s, they were experiencing Given the lack of predators (until 1997) LEIDYI ON THE DECREASE OF the worst economic (and political) insta- and parasites, one of the most important CATCHES bility of the last several decades. factors for the decrease in the biomass Fish-catch data are some of the most One could argue that while most of of M. leidyi was likely to have been food important indicators of an ecosystem’s the fi sh species are non-migratory, the limitation: glycogen storage is the main condition. Therefore, the analysis of fi sh- anchovy may be migrating and hence mechanism for energy accumulation in catch data presents important clues to any potential overfi shing by Turkish fi sh- ctenophores. Under conditions of star- understanding the role of different fac- ermen may have an effect at the basin vation, glycogen levels in these animals tors in ecosystem change. The anchovy scale. There are two subspecies of ancho- decrease. Data on the body glycogen (Engraulis encrasicolus) is the most im- vy in the Black Sea: Engraulis encrasicolus content of M. leidyi from the offshore portant fi sh species in the Black Sea, ponticus, which mainly dwells in and waters in September 1996 recorded levels both in terms of biomass as well as in around the Sea area, and Engrau- between 21 and 44 µg/g wet weight (An- economic terms. Between 1950 and 2001, lis encrasicolus maeticus, which is found ninsky et al., 1998). Thus, the condition more than 60 percent of the total catch in throughout the Black Sea. E. e. ponticus is of M. leidyi obtained from fi eld samples the Black Sea had been that of reported to undertake basin-scale migra- corresponded to that expected after a (more information available at http:// tions between different regions in the sea two-day fasting period (determined ex- www.seaaroundus.org). Turkey and the (Ivanov and Beverton, 1985); however, perimentally), implying that the cteno- former were the two ma- spawning data from the entire Black Sea phores were starving. The decrease in M. jor fi shing nations in the Black Sea until coastal region (Niermann et al., 1994) leidyi after its major peak also could have the late 1980s. Since then, Turkey’s fi sh indicates that this anchovy could well been infl uenced by the cooler climatic catch has been the highest in this region be a non-migratory fi sh. It should also period observed between 1992 and 1995 (Kideys, 1994), which has defi ned an be noted that catches of other small pe- (Oguz, this issue), as this ctenophore Exclusive Economical Zone for each ri- lagic fi sh species (e.g., Sprattus sprattus, prefers warm temperatures for spawning. parian country. One interesting aspect is Clupeonella cultriventris, and Trachurus One important aspect of the temporal the sharp decreases in anchovy catches mediterraneus) also plummeted sharply distribution of M. leidyi until 1998 was observed at the end of the 1980s for all during this period (Kideys, 1994). Even that relatively high biomass values of this countries. These decreases in fi shing lev- the catch of all small pelagic fi sh species ctenophore could still be obtained by els in most bordering countries correlate from the showed the cruises during the colder months. How- well with the peak levels of the intro- sharpest decrease in 1989. This sea was ever, the very low average biomass value duced ctenophore M. leidyi (Figure 2). likely also invaded by the ctenophore of 12 g/m2 observed in the main spawn- Despite such a correlation, follow- M. leidyi during the same period as the ing month of September 1999 was very ing an ecological modeling exercise, Black Sea; strong surface currents ex- striking for the scientists investigating Gücü (2002) claimed that, “The budget change water between these species.

80 Oceanography Vol.18, No.2, June 2005 Two of the major indicators of over- 800 ) fi shing are related to fi shing effort and -2 400 B. ovata mean size of the fi sh. During the pe- 30 M. leidyi riod of sharp decrease in anchovy catch, Zooplankton there was no sharp increase in the effort (a) spent fi shing for anchovies (see Figure 3 20 in Gücü [2002]). In 1988, the very large mean size of an anchovy was 11.3 cm just 10 before the fi shery collapsed. This large size is a good indication that the southern 0 Black Sea was not signifi cantly overfi shed. 800 There was, however, a sharp decrease in mean size of anchovies caught after 1988 400

(down to 7.4 cm in 1990) (Figure 4), 40

along with total catch. However, this size ) Specimens Abundance (m (b) -2 decrease is mystifying. Rather than over- 30 fi shing, this decrease must be mainly due 20 to the invasion of M. leidyi. While the anchovy population was declining due 10 to malnutrition (M. leidyi were eating Biomass (g m their way through the anchovies’ normal 0

prey), fi shermen were trying to maintain ) 2.0 -2 the fi sh catches they had secured in the (c) previous few years (i.e., mid 1980s). Ap- 1.5 plying the same fi shing effort to a smaller 1.0 fi sh stock would inevitably result in a decrease of the mean fi sh size as was sug- 0.5

gested by Bingel et al. (1993). So, if there Zooplankton (g m were no M. leidyi in the ecosystem, the 0.0 9 101112 1 2 3 4 5 6 7 8 9 101112 1 2 3 4 5 6 7 8 9 1011 mean size of the anchovies caught would Months not necessarily decrease sharply. 1999 2000 2001 Another piece of evidence (and pos- Figure 3. (a) Abundance and (b) biomass of M. leidyi and B. ovata, and (c) zoo- sibly the most important) against the plankton biomass in in 1999-2001 (from Finenko et al., 2003). Note the predation impact of B. ovata on M. leidyi and of M. leidyi on forage overfi shing hypothesis is the sharp de- zooplankton particularly in 2000 and 2001. crease in the mesozooplankton popu- lation, the food of both planktivorous small pelagic fi sh and the ctenophore M. leidyi. If there was a signifi cant level levels were seen only in one data set, off- These species are also well adapted to of overfi shing, one would expect an in- shore of the northern Black Sea (Figure large temperature variations, as high as crease in the biomass of mesozooplank- 2c). In the Black Sea, there are a limited 15 degrees C in a 24-hour period, be- ton during this cold period when more number of forage zooplankton species, cause of their vertical migration capabil- nutrients are pumped from deeper wa- many of which are well adapted to cold ities. There is no evidence that an overall ters, leading to higher productivity in the temperatures (e.g., the chategnath Sa- decrease of about 1.8 degrees C in winter surface waters for the entire basin (Oguz, gitta setosa, and the copepods Calanus temperatures from 1980 to 1993 would this issue). Yet, high mesozooplankton euxinus and Pseudocalanus elongatus). be detrimental for forage zooplankton as

Oceanography Vol.18, No.2, June 2005 81 12 Oguz, 2005) are also due to the very low levels of zooplankton biomass (con- 11 sumed by the invasive ctenophore). Sim- 10 ilarly, high chlorophyll levels in the Cas- pian Sea during March 2001 are shown 9 to be due to M. leidyi predation on me- 8 sozooplankton (Kideys et al., in press).

Mean size of anchovy (cm) The economic losses were substantial 7 from the decreased fi sh catches particu- 1986 1988 1990 1992 1994 1996 1998 larly during 1989 to 1993. Assuming a Years costs of about 1 USD per kilogram of Figure 4. Changes in the mean sizes of anchovy catch population in the southern Black Sea. fi sh, the minimum economic loss for Data of 1988 to 1994 are from Bingel et al. (1993) and 1996 to 1997 from Mutlu (2000). Turkey alone would be more than 1 bil- lion USD. Recognizing the large-scale impact of the invasive ctenophore, the United Nations Environmental Program implied by Oguz (this issue). this issue), the biology of the dominant became involved in order to fi nd a solu- Long-term changes in forage zoo- mesozooplankton species, and the dis- tion to the negative impact of M. leidyi plankton biomass show that during the tribution of M. leidyi (mainly inshore) on the Black Sea ecosystem. After re- initial peak years (1988 to 1991) of M. (Kideys and Romanova, 2001) and its viewing the situation, the Group of Ex- leidyi biomass, forage zooplankton bio- feeding strategy. Anninsky et al. (1998), perts on the Scientifi c Aspects of Marine mass was generally the lowest for differ- after analyzing fi eld data, suggested that Environmental Protection (GESAMP) ent regions of the Black Sea (Figure 2). the impact of the M. leidyi predation recommended biocontrol as the only vi- Fisheries biomass was also at its lowest on small copepods, cladocerans, and able method of dealing with the M. leidyi levels, or had declined sharply, during younger stages of Calanus euxinus was problem and, furthermore, suggested this time period. These data correspond stronger. They explained the high levels another ctenophore, Beroe ovata, as the well with data on the mean size of fi shes. of mesozooplankton in 1989 and 1990 best biocontrol agent to be used. The only exception to these trends was were due to late stages of the large cope- the mesozooplankton of the offshore pod C. euxinus, which usually constitutes THE CTENOPHORE BEROE waters of the northern Black Sea, where an important portion of the total meso- OVATA AND ITS IMPACT IN high levels of mesozooplankton were still zooplankton biomass. In later years, due THE BLACK SEA present until 1990, after which they also to consumption of the younger stages of The new alien ctenophore, B. ovata (Fig- declined sharply. Note that coastal re- this copepod (i.e., recruitment failure), ure 1b), fi rst appeared in the Black Sea gions are generally known to have higher this copepod population also declined in October 1997 (Konsulov and Kam- productivity and hence larger fi sh stocks; sharply. It is also interesting that during burska, 1998), possibly arriving in the the biomass decline seen in the inshore the second highest peak of M. leidyi in ballast waters of . During their 1999 mesozooplankton of northern Black Sea 1995 (about 500 g WW/m2 for the south- cruise, Kideys and Romanova (2001) (Figure 2) should have played a greater ern Black Sea and as high as a few kg noted for the fi rst time the occurrence role in the decline of former Soviet values for the northern regions) (Kova- of this M. leidyi predator in the south- Union fi sheries through malnutrition of lev and Piontkovski, 1998), secondary ern Black Sea with an average biomass adults and, particularly, younger fi sh. decreases in the fi sheries of all riparian value of 12 g/m2. Immediate labora- The high forage mesozooplankton countries (except Romania) and meso- tory experiments (combined with fi eld biomass values in offshore regions in zooplankton occurred (Figure 2). data) designed specifi cally to assess the 1989 and 1990 could be due to increased We suggest that the high chlorophyll outcome of this new productivity of the ecosystem (Oguz, levels seen between 1988 and 1992 (see concluded that B. ovata could effec-

82 Oceanography Vol.18, No.2, June 2005 tively control the M. leidyi population, ranged from 17 to 53 percent of the zoo- the bulk of individuals (85.5 percent) in particular, and help the dynamics and plankton stock during July-October 1995 were less than 10 mm in length (much structure of the pelagic community as a (Finenko et al., 2003). smaller than the Black Sea population, whole (e.g., Finenko et al., 2001; Kideys, After Beroe ovata’s arrival, many other perhaps due to lower of the Cas- 2002). One important aspect of B. ovata positive developments were reported in pian Sea). The average and maximum is that it is observed, both in the labora- the Black Sea ecosystem, including in- biomasses of M. leidyi were calculated tory and fi eld, to feed exclusively on M. creases in mesozooplankton numbers as 120 and 351 g WW/m2, respectively. leidyi (Kideys et al., 2004). Note that the from different regions, in numbers of These fi gures showed that this cteno- other ctenophore species of the Black fi sh larvae and eggs, in meroplankton phore population expanded much faster Sea, Pleurobrachia rhodopis, is separated quantities, and even in increased dolphin in the Caspian Sea compared to the from B. ovata by depth (the latter being appearances (Shiganova et al., 2004). Black Sea, which could be related to the also confi ned to above the thermocline). warm period during those years (Oguz, Even the larva of B. ovata has been - M. LEIDYI IN THE CASPIAN SEA this issue). While the highest biomasses served to feed on M. leidyi (either on its The possibility of M. leidyi introduction were observed in the western and cen- tissue or larva). into other sensitive, neighboring ecosys- tral Middle Caspian Sea, hot-spot re- Figure 3 shows the abundances, bio- tems, notably the Caspian Sea, had been productive areas were present along the masses, and population structures of the mentioned during the GESAMP meet- coasts of the western Caspian Sea, with two introduced ctenophore species M. ing in 1994. As expected, this ctenophore abundance values of up to 2285 ind./m2 leidyi and B. ovata, and mesozooplank- was reported to be present in the Cas- (Kideys and Moghim, 2003). The impact ton, in inshore waters of the northern pian Sea by November 1999 (Ivanov et of such high densities of M. leidyi is sug- Black Sea (i.e., Sevastopol Bay and adja- al., 2000). Ivanov et al. (2000) suggested gested to be signifi cant for the pelagic cent regions), from 1999 to 2001, follow- that this ctenophore was transported ecosystem of the Caspian Sea. ing B. ovata’s arrival. Unlike to the previ- via ballast water taken aboard either in Since 2000, several monitoring sta- ous years, very low abundances and bio- the Black Sea or the (where tions were set up along the Caspian mass values of M. leidyi were observed M. leidyi occurs in the warm months) coasts with the support of the Caspian during most of the year, with a sudden and released after ballast-loaded ships Environment Program (CEP) and na- increase in summer to early autumn, but had passed through the Ca- tional funding from several riparian only for about a two-month period. The nal and the shallow, freshwater areas of states. Long-term data from the southern B. ovata bloom during the peak M. leidyi the northern Caspian Sea into the saltier Caspian revealed a seasonal distribution biomass resulted in the biomass of the central or southern Caspian waters. This in M. leidyi quantity, with the highest latter falling sharply to extremely low species invasion was the start of one of values in warmer months (Figure 5). values. These data show that the intro- the most important anthropogenic prob- Finenko et al. (in press) calculated the duction of B. ovata to the Black Sea has lems the Caspian Sea ecosystem has ever seasonal impact of M. leidyi on zoo- considerably reduced the numbers M. seen. This event can be classifi ed among plankton, which was highest in summer leidyi present. Subsequently, the predato- the largest impacts from an invasive spe- due to higher water temperatures and ry impact of M. leidyi on prey zooplank- cies in any of the world’s seas. the population size structure; at this ton was found to be reduced signifi cantly Several basin-wide surveys were un- time, juvenile ctenophores, with mean in this period compared with pre-Beroe dertaken to understand the distribution lengths of 2 to 5 mm, accounted for most ovata appearance. The daily energy re- of M. leidyi in the Caspian Sea (Shi- of the population. From winter through quirements of M. leidyi accounted for 29 ganova et al., 2001; Kideys and Moghim, spring, these ctenophores were found to 39 percent of the zooplankton stock 2003). In August 2001, a comparison of to consume the available stock of zoo- only in September 2000 and August 2001 data from different depths revealed that plankton in three to eight days, whereas (period of maximum Mnemiopsis bio- M. leidyi were generally confi ned to sur- in summer, total population consump- mass); for other months they accounted face waters. The maximum size of the tion took only one day. Finenko et al. for less than 1 percent. These values ctenophore was only 41 to 45 mm, and (in press) suggested that such a high

Oceanography Vol.18, No.2, June 2005 83 abundance of ctenophores, if sustained, Caspian Sea due to top-down effects of carried out in the Black Sea, Beroe ovata would maintain the non-gelatinous zoo- M. leidyi consumption of zooplankton, seems the obvious solution for the Cas- plankton biomass at very low quantities which was observed to have decreased pian Sea problem. To evaluate the po- and, consequently, no recovery could be substantially between 1998 and 2001 tential success of Beroe establishment in expected in this pelagic fi shery. (A. Roohi et al., Mazandaran Fisheries this environment, several physiological The Caspian Sea, is similar to the Research Center, Sari, Iran, unpublished aspects (feeding, respiration, growth, and Black Sea in many respects, including data, 2004). Many of the endemic cla- reproduction rates) of B. ovata in Cas- sustaining a large pelagic fi shery, the doceran species are no longer present in pian waters were investigated by either main fi sh of which is the kilka (three the samples obtained from the monitor- transporting B. ovata from the Black Sea species of Clupeonella). Similar to the ing stations. Some large predators that into the Khazerabad Fisheries Research Black Sea, the most visible impact of M. feed on kilka, such as the white Laboratory on the Caspian coast of leidyi was on the pelagic fi shery (Figure (Huso huso) and the endemic Caspian Iran, or by transporting Caspian water 5). For example, the kilka (Clupeonella seal (Phoca caspica), are now considered to Sinop (Turkey), southern Black Sea spp.) catches of Iran initially dropped to to be highly endangered in the Caspian (Finenko et al., 2003; Kideys et al., 2004). 64 thousand tonnes in 2000 to 45 thou- Sea (Kideys and Moghim, 2003). There The studies’ fi ndings showed that after sand tonnes in 2001, from earlier 1988 have already been reports of mass mor- gradual adaptation, B. ovata were able and 1989 values of 82 and 85 thousand tality events for the Caspian seal (H. to adapt to the Caspian Sea’s low salin- tonnes, respectively. Further decreases Dumont, Laboratory of Ecology, ity (maximum value of 13). B. ovata only were observed during 2002 to values of Ghent University, Belgium, pers. comm, consumed M. leidyi. The feeding rate of less than 24 thousand tons. So, within 2004). Although seal mortality is often B. ovata ranged from 14 to 765 percent three years, more than 70 percent de- related to viral infections, we believe that of body wet weight and was highest for crease in the kilka catches of Iranian the decrease in the kilka populations smaller individuals (i.e., 13 to 16 mm). fi shermen occurred, with a minimum contributed to such mortalities. It has Over the measured weight range, the of 125 million USD in economic losses. also been reported that the percentage weight-specifi c respiration rate was in- Similarly, Azerbaijan and Russian kilka of pregnant females among seal popu- dependent of weight. The daily specifi c catches also plummeted strikingly dur- lations decreased signifi cantly in 2001 growth rate of adult B. ovata was 7 to ing 2000 to 2003 (Figure 5). (Shiganova et al., 2001), which could be 11 percent of body wet weight. B. ovata During 2000 to 2003, several other related to malnutrition. spawned, and their eggs were hatched, in adverse events must have occurred in the After the events and investigations Caspian Sea water. Although the larvae

Iran 100 Azerbaijan Mnemiopsis 80 160 Figure 5. Sharp decrease in 800 24 the kilka (Clupeonella spp.) 60 120 fi shery of some Caspian 20 600 states and annual/seasonal 40 changes in the biomass of 80 16 Mnemiopsis leidyi (stars) from 20 400 monitoring stations along the 40 12 southern Caspian Sea. Th e 0 thick red line in November 200 0 8 1999 shows the fi rst appear- ance of this ctenophore in

Kilka catch (thousand tons) 4 0 the Caspian Sea.

1995 1996 1997 1998 1999 2000 2001 2002 2003 2004

84 Oceanography Vol.18, No.2, June 2005 survived for only a few hours in the 2002 Bingel, F., A.E. Kideys, E. Ozsoy, S. Tugrul, and T. Oguz. fyan, M.T. Rostamian, H. Rostami, and H. Negar- 1993. Stock assessment studies for the Turkish estan. 2004. Physiological characteristics of the experiments, during the 2003 experi- Black Sea Coast. NATO-TU Fisheries Final Report. ctenophore Beroe ovata in the Caspian Sea water. ments, the larvae survived and subse- Middle East Technical University, Institute of Ma- Marine Ecology Progress Series 266:111-121. rine Sciences, Erdemli, Turkey, 96 pp. Kideys, A.E., N. Soydemir, G. Ekingen, E. Eker, V. Vlad- quently grew over a two-month period. Finenko, G.A. and Z.A. Romanova. 2000. The popu- ymyrov, and N. Kochisarli. In press. Phytoplankton Based on these physiological data, it was lation dynamics and energetics of ctenophore distribution in the Caspian Sea during March 2001. Mnemiopsis leidyi in Sevastopol Bay. Oceanology Hydrobiologia. suggested that in the Caspian Sea, B. ova- 40:677-685. Konsulov, A.S. and L.T. Kamburska. 1998. Ecological ta will be able to ingest M. leidyi inten- Finenko, G.A., B.E. Anninsky, Z.A. Romanova, G.I. determination of the new ctenophora - Beroe ovata Abolmasova, and A.E. Kideys. 2001. Chemical invasion in the Black Sea. Oceanology [Bulgaria] sively (Kideys et al., 2004) and help the composition, respiration and feeding rates of the 2:195-198. ecosystem to recover signifi cantly. Such new alien ctenophore, Beroe ovata, in the Black Sea. Kovalev, A.V. and S.A. Piontkovski. 1998. Interannual Hydrobiologia 451:177-186. changes in the biomass of the Black Sea gelatinous a fi nding is very important for dealing Finenko, G.A., Z.A. Romanova, G.I. Abolmasova, B.E. zooplankton. Journal of Plankton Research 20:1377- with the invasive ctenophore M. leidyi Anninsky, L.S. Svetlichny, E.S. Hubareva, L. Bat, 1385. and A.E. Kideys. 2003. Ingestion, growth and re- Kremer, P. 1979. Predation by the ctenophore Mne- problem in the Caspian Sea or other re- production rates of the alien Beroe ovata and its miopsis leidyi in Narragansett Bay, Rhode Island. gions in future. impact on plankton community in Sevastopol 2:97-105. Bay, the Black Sea. Journal of Plankton Research Kremer, P. and S. Nixon. 1976. Distribution and abun- The ongoing discussion as to the rea- 25:539-549. dance of the ctenophore, Mnemiopsis leidyi in Nar- sons of major ecosystem changes in the Finenko, G.A., A.E. Kideys, B.E. Anninsky, T.A. Shi- ragansett Bay. Estuarine and Coastal Marine Science ganova, A. Roohi, M.R. Tabari, H. Rostami, and S. 4:627-639. Black Sea should not be seen as futile. Bagheri. In press. Invasive ctenophore Mnemiopsis Mutlu, E. 1999. Distribution and abundance of cteno- Such an exercise in pinpointing the ma- leidyi in the Caspian Sea: Feeding, respiration, phores, and their zooplankton food in the Black reproduction and impact on zooplankton commu- Sea. II. Mnemiopsis leidyi. Marine Biology 135:603- jor causes could be extremely important, nity. Marine Ecology Progress Series. 613. for example, in dealing with the invasive Gücü, A.C. 2002. Can overfi shing be responsible for Mutlu, C. 2000. Characteristics of anchovy popula- the successful establishment of Mnemiopsis leidyi tions (Engraulis encrasicolus, Linnaeus 1758) and species problem of the Caspian Sea. The in the Black Sea? Estuarine, Coastal and Shelf Sci- application of analytical methods in stock estimate. available data presented here suggest that ence 54:439-451. Ph.D. Thesis, Karadeniz Technical University, Trab- Gücü, A.C. and T. Oguz. 1998. Modeling trophicin- zon, Turkey, 112 pp. the invasive ctenophores are major in- terrelationship in the Black Sea. Pp. 359-371 in Niermann, U., F. Bingel, A. Gorban, A.D. Gordina, A.C. fl uences driving the striking ecosystem NATO TU-Black Sea Project: Ecosystem Modeling Gücü, A.E. Kideys, A. Konsulov, G. Radu, A.A. Sub- as a Management Tool for the Black Sea, Sympo- botin, and Z.E. Zaika. 1994. Distribution of ancho- changes taking place in the Black and sium on Scientifi c Results, L. Ivanov and T. Oguz, vy eggs and larvae (Engraulis encrasicolus Cuv.) in Caspian Seas. eds. Kluwer Academic Publishers, Dordrecht, The the Black Sea in 1991-1992. ICES Journal of Marine Netherlands. Science 51:395-406. Ivanov, P.I. and R.J.H. Beverton. 1985. The Fisheries Purcell, J.E. and M.B. Decker. 2005. Effects of cli- ACKNOWLEDGEMENTS Resources of the Mediterranean. Part Two: The Black mate on relative predation by scyphomedusae Sea. Studies and Reviews, 60, General Fisheries and ctenophores on copepods in Chesapeake Bay We thank the Caspian Environment Pro- Council for the Mediterranean, Food and Agricul- during 1987-2000. Limnology & Oceanography gramme (CEP) for their support of our ture Organization of the UN (FAO), Rome, , 50(1):376-387 135 pp. Reeve, M.R., M.A. Walter, and T. Ikeda. 1978. Labora- studies in the Caspian Sea, to T. Oguz Ivanov, P.I., A.M. Kamakim, V.B. Ushivtzev, T. Shi- tory studies of ingestion and food utilization in for making his unpublished manuscript ganova, O. Zhukova, N. Aladin, S.I. Wilson, G.R. lobate and tentaculate ctenophores. Limnology and Harbison, and H.J. Dumont. 2000. Invasion of Cas- Oceanography 23(4):740-751. available to us, and to E. Eker-Develi pian Sea by the comb jellyfi sh Mnemiopsis leidyi Shiganova, T.A., A.M. Kamakin, O.P. Zhukova, V.B. for her various help in preparing the (Ctenophora). Biological Invasions 2:255-258. Ushivtzev, A.B. Dulimov, and E.I. 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