ATTACHMENT 16.

Invader in the Caspian Sea, Ctenophora Mnemiopsis, and preliminary results of study of its impact on pelagic ecosystem

V.P.Ivanov, T.A.Shiganova, E.I.Musaeva, L.A.Zykov, A.F.Sokilsky

Caspian Scientific-ReSearch Institute of Fisheries
1 Savushkina st., Astrakhan, 414056
Shirshov Institute of Oceanology Russian Academy of Sciences
36 Nakhimov prospect, Moscow, 117997

During the last 30 years the environmental status of the Caspian Sea significantly altered under the impact of various factors where sea level changes and pollution from different toxicants were dominant (Ivanov, 2000; Salmanov, 1999). Besides, there is another important source of impact such as biological pollution - introduction of flora and fauna from ballast waters of vessels which entered the Caspian.

Early in November 1999 underwater video taken at banks of the Middle and South Caspian recorded two gelatinous species previously not found in the Caspian, which were identified as Ctenophora Mnemiopsis and jelly fish Aurelia aurita. They were found at two stations at 29-332 m (40^o 54 N 52 ^o 50 E and 39 ^o 50 N 51 ^o 50 E), water temperature was 16.5-19.5⁰C, salinity 11.76-13.07‰. In 1998 fishermen found some gelatinous species in nets in deep water in the South and Middle Caspian.

The Ctenophora Mnemiopsis originates from the coastal waters, bays and estuaries of North America. However, in the early 1980’s Ctenophora Mnemiopsis leidyi Agassiz was introduced into the Black Sea from ballast water (Vinogradov et al., 1989). Mnemiopsis adapted to the Black Sea conditions and made significant damage to its ecosystem by eating out zooplankton, eggs and fish larvae which became a menace to the food base of fish feeding on plankton and its reserves (Tsikhon-Lukanina et al. 1991; Vinogradov et al., 1992; Shiganova et al., 1998; Shiganova and Bulgakova, 2000). From the Black Sea it was introduced into the Azov Sea, Sea of Marmora and is periodically found in the eastern part of the Mediterranean Sea (Studenikina et al., 1991; Shiganova et al. 1994, Shiganova et al., 2000).

Jellyfish Aurelia aurita (L) is wide spread all over the world, it is found in different areas of the world’s oceans, it is a resident of the Black and Mediterranean Seas and occasionally found in the Azov Sea.

In July-October 2000 a specific survey was arranged in order to study the biology and morphology, distribution and abundance of the introduced species in the Caspian Sea.

MATERIAL AND METHODS

The surveys were carried out in the North, Middle and South Caspian and included 4 offshore surveys of a scientific-reSearch vessel of CaspSRIF (see Table 1).

Gelatinous species and ichtyo plankton were caught by IKS-80 net (gas 500 m m, inlet 0.5 m²) in the surface mixed layers; zooplankton sampling was carried out by Jedi net (gas 200 m m, inlet 0.1 m²) in the North Caspian in July and October by total vertical catch from bottom to surface. Trawl nets were used in all surveys (30 feet and 15 feet juvenile trawls) in bottom layers at low vessel speed.

Table 1. Survey dates and locations, 2000, Caspian Sea

Coefficient of low catch (2) was used to calculate abundance and biomass of Mnemiopsis (Vinogradov et al, 1989).

Distribution of Mnemiopsis

Mnemiopsis was not found during the first survey early in July in the North Caspian (Fig.1). Late in July a survey was carried out in the Middle Caspian and north part of the South Caspian. Mnemiopsis was abundant in the Middle Caspian along the Kazakhstan and Turkmenistan coast (Fig.1) at a depth of 2-=170 m, temperature 24.6-26.6^o C and salinity 11-13‰. Both large specimens up to 6.4 cm with lobes and small specimens of 0.5-1.1 cm were abundant.

Concentration of Mnemiopsis increased to the south, the species was the most abundant in deep-water areas at the border of the Middle and South Caspian and in the north part of the South Caspian where its abundance reached 100 ind.m^-2. Small specimens dominated, which was the evidence of intensive reproduction. Average abundance for the area was 24 ind.m^-2, average biomass was ind.m^-2, average individual weight of Mnemiopsis was 2.46 g.

Visual observation in the South Caspian at a depth of 20-25 m showed vertical distribution of Ctenophora. The species were mainly concentrated in the surface layer 4 m thick, small specimens prevailed. Mnemiopsis was not found in deeper areas but large specimens were sparsely distributed at the bottom.

In September a survey was carried out only in the North Caspian (Fig. 3A). Mnemiopsis was first found in the south-east part of the North Caspian at a depth of 5-6 m in Belensky Canal where salinity ranged from 4.0 to 6.4‰ which is close to the values of the Volga delta. Water temperature in surface layers varied from 22 to 24.4^o C. Mnemiopsis size was in the range from 2 to 4.5 cm, no small specimens were found. Average individual weight was 2.94 g, average abundance was 6 ind.m^-2 (2 ind.m^-3), biomass was 36.6 g.m^-2 (13 g.m^-3). Mnemiopsis was not found in north-west part of the North Caspian (Fig.3A).

In October a survey was carried out in the south-east part of the North Caspian where Mnemiopsis was previously found in September. The habitat of Mnemiopsis increased (Fig.3B), the abundance and biomass increased. Average abundance in the survey area was 108 ind.m^-2 (23 ind.m^-3), biomass was 140.4 g.m^-2 (30 g.m^-3). Average individual weight decreased up to 1.3 g due to the high amount of small specimen (Fig.2). Mnemiopsis was the most abundant at Maly Zemchuzny island (170 ind.m^-2). Specimens found at the farthest northern stations with salinity 4.27‰ were in bad condition, morphological structures were unmacerated, but the specimens were alive although their lobes and cilia were partially or totally damaged. The highest amount of specimens at the station was found at the bottom, and at the bottom they were in a better condition, possibly due to a higher salinity – 4.83‰. Mnemiopsis was not found in the areas with the lower salinity. Obviously, there is 4‰ salinity limit for Mnemiopsis in the Caspian where salinity range is different from other marine water bodies.

Distribution of other gelatinous species

Unlike in 1999, jellyfish Aurelia aurita was found only once in July 2000 at the border of the Middle and South Caspian in the area adjacent to Kara-Bogaz-Gol bay (41^o00’ N 52^o 30' E).

Jellyfish Blackfordia virginica Mayer, diameter of bell 0.6-1.0 cm was found among other gelatinous. This is also the species introduced from Azov-Black Sea basin. The abundance was low, 2 specimens per catch were found at two stations in the North Caspian and 2 specimens per catch were found at two stations in the Middle Caspian.

Zooplankton studies

Zooplankton food base was rich in the North Caspian early in July. Average biomass was 3579 m g.m^-2 (715.8 m g.m^-3), abundance was 292440 ind.m^-2 (58601 ind.m^-3). Copepoda dominated (Fig.5). The most abundant was Acartia tonsa, next abundant were Calanipeda aquae dulcis, Eurytemora grimmi and E.minor. Cladocera were insignificantly less abundant than Copepoda, Bosmina longicornis, Alone rectangula, Podonevadne trigona were the most dominant. The third abundant were Rotatoria. Asplanchna priodonta were the most abundant species of Rotifera. At northern stations Rotifera were dominating both in abundance and species distribution; 6 species were found, but A. Priodonta was also dominant. Meroplankton (larvae of bottom species) was also abundant, it was represented by larvae of Bivalvia and nauplii of Cirripedia. In October abundance and biomass of zooplankton reduced, biomass reduced by a factor of 6 to 578 mg.m^-2 (115.6 mg.m^-2), abundance reduced by a factor of 5.3 to 55110 mg.m^-2 (11022 mg.m^-2). The reduction of Copepoda was the most significant: the abundance reduced by a factor of 8 (Fig.5) though normally the amount of Copepoda increases by August and reaches maximum in August-September, and reduces in late October (Lesnikov, Matveeva, 1959). Species distribution is similar to July: A.tonsa and C. aquae dulcis were dominant but the abundance reduction of the species in October was more significant than for other species. The abundance of A.tonsa reduced 11 times, the abundance of C. aquae dulcis reduced almost 20 times though under normal conditions this most abundant representative of North Caspian plankton reaches its extreme in August-September and its biomass is high even in November (Kun, 1965). Seasonal reduction of abundance and biomass of other communities of Caspian plankton is typical for this time of year due to reduction or complete disappearance of summer thermophilic species of Cladocera and Rotatoria, as well as benthos larvae (L.A.Lesnikov, Matveeva, 1959; Kun, 1965). In October Cladocera were represented only by two species, Evadne anonyx prevailed but its abundance was low (Fig.5). The abundance of Rotifera in October did not reduce so significantly compared to July, it was represented by five species, Asplanchna priodonta was again dominant.

80-100% of Mnemiopsis caught in the survey area of North Caspian at the end of the day had food in the gastrovascular cavity. The amount of food substances varied from 5 to 35, Copepoda were dominant; small specimen had eggs and nauplii of Calanoida and Cirripedia.

DISCUSSION

In July 2000, Mnemiopsis was already wide spread in both Middle and South Caspian, but it was not found in the North Caspian. No surveys were carried out in August. First large adult specimens (2.2-4.8 cm) of Mnemiopsis in the North Caspian were found in September, at a depth of 5.5-6.6 m. In October Mnemiopsis was already wide spread in the North Caspian at a depth of 2.7-6.0 m. Different size specimens were found, including small 0.2-0.5 cm which is evidence of successful reproduction of the species; it also proves that the conditions of the North Caspian are appropriate for Mnemiopsis. Isohaline 4‰ is probably limiting for Caspian Mnemiopsis, as it was not found in the areas with salinity below 4‰.

The result of the 2000 survey allow to initially conclude that the basic habitat of Mnemiopsis formed in the Middle and South Caspian; currents carry Mnemiopsis to the North Caspian. The main current direction at Kazakhstan coast of the Middle Caspian is north, to the areas where Mnemiopsis was found.

However, considering that the North Caspian is often covered with ice in winter, Mnemiopsis cannot live there in cold seasons; the population of Mnemiopsis winters in the Middle and South Caspian.

Jellyfish Aurelia aurita was found only once, unlike last year when the abundance of Mnemiopsis and Aurelia was pretty similar. Probably Mnemiopsis, as a more successful competitor, suppressed the development of Aurelia as in the Black and especially the Azov Seas (Shiganova et al., 2001).

Further changes in the ecosystem were recorded in 2000. In the North Caspian the abundance and biomass of zooplankton reduced during the period from July till October, 5.3 times and 6 times accordingly. The most significant was the reduction of Copepoda abundance.

We carried out preliminary calculations of the average use of zooplankton by Mnemiopsis for minimal support of metabolism. On the basis of data on zooplankton biomass (578 m g/m^-2) and Mnemiopsis (140.4 m g/m^-2) in the North Caspian in October 2000 and the equation of metabolism of Caspian Mnemiopsis we calculated that Mnemiopsis requires 7% of zooplankton biomass per 24 hours to support metabolism (i.e. if calorie content of zooplankton is 0.7 cal/g of dry substance, assimilability of Mnemiopsis at 0.7, Mnemiopsis will require 0.9 mg/24 hours). Besides, Mnemiopsis needs additional food resources for growth and reproduction, so the actual percentage of grazing would be much higher.

What could be the consequences of Mnemiopsis invasion in the Caspian?

In the South and Middle Caspian, where Mnemiopsis is most abundant, the first species to suffer were fish feeding on plankton: common kilka Clupeonella delicatula caspia and anchovy kilka Clupeonella engrauliformes that inhabit the surface layers up to 70 m depth during warm Seasons (see Table 2). In 2000 and 2001 especially size/weight ratio of kilka of all age groups deteriorated. Condition factor decreased, too. The catch of anchovy kilka for 6 months in 2001 reduced by a factor of 2 compared to previous years. Big-eyed kilka C.grimmi inhabits deeper areas but at night it moves to higher layers. It migrates vertically for plankton, its main food. Juvenile kilka inhabits higher layers and migrates to feed to surface layers. There is also a possibility of reduction of big-eyed kilka population.

Table 2. Average length (cm), weight (g) and condition factor (K) (Fulton) for anchovy kilka in 1997-2000

Some species of herring that winter in the South Caspian also feed on plankton but not to a great extent (10-20% of ration). Some species spawn in the Volga but their juvenile feed on plankton in the open sea; one such species is black back shad Alosa kessleri kesleri, Agrachanka shad A. Brashnikovi agrachanica and Dolginka shad A.brashnikovi brashnikovi. Black back shad and Agrachanka shad spawn in south-west part of the North Caspian in spring and summer. There is a possibility that their eggs and larvae will be eaten by Mnemiopsis as it is the most abundant in summer.

90% of stomach content of herring and kilka in particular contains Copepoda. In 2000 Anchovy kilka was provided with only 25% of their usual food base. In the North Caspian small fish that feed on plankton provide the main food base (Ivanov, 2000). In 2000 nutrition of roach lacked mollusk larvae; common kilka disappeared from beluga ration.

The seal Phoca caspica is the highest trophic link in the Caspian. The seal feeds mainly on kilka (80% of its ration), in the Middle and South Caspian in particular, where the seals feed during warm seasons (Khuraskin, Zakharova, 2000).

It is essential to take measures to reduce the abundance of the introduced species. The experience of the Black Sea shows that introduction of Ctenophora Beroe ovata can be an effective measure, as adult specimens feed mainly on Ctenophora and on Mnemiopsis in particular. After its introduction in 1999 its abundance suddenly increased of and the biomass of Mnemiopsis significantly reduced. The biomass of zooplankton and the amount of fish eggs increased to the previous levels (Shiganova et al, 2000a, 2000b). However, B.ovata develops well in the Black Sea only in late August and lives till late November – early December. The rest of the year the abundance of Mnemiopsis increases and Mnemiopsis exhausts plankton stocks. However, Mnemiopsis in spite of its high biomass does not reduce zooplankton biomass to the level of 1989-91. As salinity limit for B.ovata is 7.2 (Shiganova et al., 2000b), it will probably live in the Middle and South Caspian and will not spread to the North Caspian. Nevertheless, the main habitat of Mnemiopsis is in the Middle and South Caspian where B.ovata can live and control the abundance of Mnemiopsis.

LIST OF REFERENCES

Vinogradov, M.E., Sapoznikov, V.V, and E.A. Shushkina, Ekosistema Chernogo moria (The Black Sea Ecosystem), Moscow, Nauka, 1992.

Vinogradov, M. E., Shushkina, E.A., Musaeva, E.I., and P. Yu. Sorokin, A New Black Sea Invader-Ctenophore Mnemiopsis Leidyi (A. Agassiz) (Ctenophora: Lobata), Oceanologiya, 1989, vol. 29, no. 2, pp. 293-299.

Kkun M.S. Plankton of the Caspian Sea in the conditions of controlled Volga discharge// Chage of biological structures of the Caspian Sea during last decades. M: Nauka. 1965. page 54-97.

Lesnitov L.A., Matveeva R.P. Character of Volga discharge impact on zooplankton of the North Caspian.

Salmanov M.A. Ecology and biological reproduction of the Caspian Sea. Edited by U.I.Sorokin. Baku. 1999. page 397

Studenikina E.I., S.R.Volovik, Z.A.Mirzoyan and G.I.Luts Ctenophore Mnemiopsis leidyi in the Azov Sea. Okeanologiya 1991. v.31 No 5 page 722-725.

Khuraskin L.S. Zakharova N.A. Modern conditions of formation of biological resources of Caspian Seal population// B. Sea mammals of Golarctics. Arkhangelsk. Internation conferece. 2000. p.464

Tsikhon-Lukanina E.A., Reznichenko O.G., Lukasheva T.A. Quantitative aspects of nutrition of Ctenophore Mnemiopsis leidyi in the Black Sea// Okeanologiya. 1991. v.31 No2. page 272-276

Shiganova T.A., U.V.Bulgakova, P.U.Sorokin, U.F.Lukashev. Results of study of the new invader Beroe ovata in the Black Sea// Izv ISR. Ser.Biology 2000a No 2 page 248-256

Shiganova T.A. U.V.Bulgakova, S.P.Volovik, Z.A.Mirzoyan, S.I.Dudkin New invader Beroe ovata and its impact on the ecosystem of Azov-Black Sea basin in August-September 1999// Ctenophore Mnemiopsis leidyi (A.Agassiz) in Azov and Black Seas and consequences of its introduction. Editd by S.P.Volovik. Rostov-na-Donu. 2000b. page 432-449

Finenko G.I. Abolmazova G.I. Romanova Z.A. Nutrition, oxygen use and growth of Ctenophore Mnemiopsis leidyi in relation to food concentration// Marine biology. 1995 v 21 No 5 page 315-320

Kremer, P. Population dynamics and ecological energetics of a pulsed zooplankton predator, the ctenophore Mnemiopsis leidyi. // Ed. M. L. Wiley, Estuarine Processes. Academic Press, City 1976. N 1. P. 197-215.

Shiganova T A. Mnemiopsis leidyi abundance in the Black Sea and its impact on the pelagic community // Sensivity of the North, Baltic Sea and Black Sea to antropogenic and climatic changes"// 1997. Sp. Volume. Ed. Ozsoy . E. and Mikaelyan A.. Kluwer Acad. Pub. P.117-130.

Shiganova T. A. Invasion of the Black Sea by the ctenophore Mnemiopsis leidyi and recent changes in pelagic community structure // Fisheries Oceanography – GLOBEC Special Issue. 1998. Ed. Steeve Coombs. P. 305-310.

Shiganova T.A. ,Ozturk B., Dede A. Distribution of the ichthyo-, jelly- and zooplankton in the Sea of Marmara // FAO Fisheries report. 1994. No 495. P.141-145.

Shiganova, T. A. & Y. V. Bulgakova, Effect of gelatinous plankton on the Black and Azov Sea fish and their food resources // ICES J. mar. Sci. 2000. 57: 641-648.

Shiganova T. A .,. Mirzoyan Z. A , Studenikina E. A. , Volovik S. P. , Siokou-Frangou I. , Zervoudaki S., Christou E. D., Skirta A. Y., and Dumont H. J. The invasion of the ctenophore Mnemiopsis leidyi ( A.Agassiz) on the Black Sea and on other Seas of the Mediterranean basin. // Marine biology. 2001. In press

List of figures

Fig. Stations location and distribution of Mnemiopsis (ind.m^-2) in the North (stations are marked by squares) Middle and South Caspian (stations are marked by circles) in July

Fig.2 A Stations location and distribution of Mnemiopsis (ind.m^-2) in the North Caspian in September

B Stations location and distribution of Mnemiopsis (ind.m^-2) in the North Caspian in October

Fig.3 Abundance and rate of main groups of zooplakton in July (A) and in October (B) in the North Caspian (ind.m^-2)

1-Copepoda; 2-Cladocera; 3-Rotatoria; 4 meroplankton; 5 other (including demersal plankton).

An invader in the Caspian Sea ctenophore Mnemiopsis and its initial effect on pelagic ecosystem.

Distribution of a new invader Mnemiopsis in the Caspian Sea were studied.. Data of distribution Mnemiopsis in Northern, Middle and Southern Caspian Sea, its density and biomass, seasonal dynamics in 2000 were presented for the first time. In July Mnemiopsis was widely distributed in the Middle and northern part of Southern Caspian Sea. In Northern Caspian it was not found. In September Mnemiopsis was first found in the Northern Caspian. In October its area of distribution became wider and biomass increased in 3.5 times, density in some areas reached 170 ind.?^-2 . Distribution to the north was limited izohaline 4 ‰. Comparative analyses of species composition, density and biomass mesozooplankton in the Norhern Caspian was conducted in July and October.Decrease of density of zooplankton in 5.3 times and biomass in 6 times was recorded in October comparing with July, decline of density of Copepoda was the most considerable.