**4. General aspect of** *Mnemiopsis*

176 Ecosystems Biodiversity

dealing with the problem in the Black Sea, due to risk of unexpected problems: What if *B.* 

A warning that *M. leidyi* might also invade the Caspian Sea had been voiced during the Geneva meeting as well as by Dumont (1995). Unfortunately, at the end of the 1990s the invasion of *M. leidyi* in the Caspian Sea was already being reported (Esmaeili et al., 2000; Ivanov et al., 2000; Roohi, 2000). It must have also been transported in the ballast waters of ships traveling from the Black Sea (salinity 18 ppt) to the Caspian Sea (max. salinity 13-14 ppt) through the Volga Don Canal. Investigations in the Caspian Sea showed by September 2000, it was found everywhere including the northern Caspian where the salinity can be as

The impact of *M. leidyi* on the Caspian Sea ecosystem has been even worse than in the Black Sea due to the greater sensitivity of this enclosed basin. Adverse impacts from *M. leidyi*

1. Again the fish collapse was the most apparent problem in the ecosystem. Striking decreases were observed in the pelagic (mainly sprat *Clupeonella* spp.) fishery of all countries bordering the Caspian Sea: almost a 50% decrease in the kilka catches of both Iranian, Azerbaijan and Russian fisheries had occurred during 1999 and 2001. During spring and summer of 2001, mass (estimated as 250,000 tons, or 40% of the population) mortalities of sprat were reported at the sea surface (Davis et al., 2003). The fish catch value was halved again in 2002, resulting in great economic losses (Kideys et al., 2004, 2005). Fishermen even stopped fishing during most part of 2003, due to lack of fish

2. Sharp decrease in fish catch became a big problem for thousands people earning livelihood from sprat fishery. The economical loss from sprat fishery alone is hundreds million Euros per year. Most of the fishermen in Iran, who once took loans from banks for starting to a business with promising outlook, cannot now pay their debts and may even end up in prison. Their problem was even at headlines on BBC World TV in 23rd

3. Not only pelagic fishes, but also some large predators feeding on these fish such as white sturgeon *Huso huso* and the endemic Caspian seal *Phoca caspica* are also suffering from significant population decrease. As reported by the media, the mass deaths of Caspian seals (*Phoca caspica*) occurred in the northern Caspian Sea during the spring of 2000. There is strong evidence that the epizootic disease observed in seals during the spring of 2000 was caused by under nourishment (Davis et al., 2003). Significantly decreased pregnancy and fat content inseal population were also reported. The white sturgeon, that is famous for the quality of its caviar, mainly depend on sprat as food

4. Biodiversity of the Caspian is important as most of species occur only in this sea all over the world (i.e. endemic). Not only the quantity of zooplankton is reported to decrease sharply, but also the number of species. For example, number of zooplankton (copepod and cladocerans) species during 2001-2002 was only 3 compared to 22 species in 1995 or 1996!. The consequences of such reduction could be very significant for the ecosystem

5. Due to decreased levels of zooplankton, eutrophication (to much plant production) started to be a significant problem for this ecosystem. Global chlorophyll distribution

*ovata* start feeding on other species rather than *M. leidyi?.* 

low as 4 ppt (Shiganova et al., 2001a).

could be listed as the following:

(Fazli and Roohi 2003).

(Hashemian and Roohi 2004).

(Roohi et al., 2010)

July 2001.

*Mnemiopsis leidyi* - is the lobate ctenophore. Two oral lobes are derivatives of the ctenophore body (spherosome). Four smaller lobes -auricules are situated under the principal two oral lobes. During their movements the lobes in fold completely its buccal orifice. The oral lappets carry tentacular rings. Its central part is situated above the lips of the mouth crevice. Both "lips" are extremely contractible (Agassiz, 1860; Seravin, 1994, plate 3). *Mnemiopsis* **characteristics** in a glance are as follows:

*Mnemiopsis leidyi* photo by ROOHI, A.

Plate 3. *Mnemiopsis leidyi* images of the Caspian Sea

**Luminescence-** *Mnemiopsis* is remarkably phosphorescent. The seat of the phosphorescence is confined to the rows of locomotive flappers.

**Ecological group-** Macrozooplankton

**Origin:** North American species might be brought into the Black Sea with ballast water by Russian tankers driving oil to the ports at eastern coast of USA. From the Black Sea Mnemiopsis might be transferred into the Caspian Sea also by tankers driving oil though the Volga-Don Canal.

**World distribution:** The native habitat of the ctenophore, *Mnemiopsis*, is in temperate to subtropical estuaries along the Atlantic coast of North and South America (Harbison et al., 1978). In the early 1980s, it was accidentally introduced to the Black Sea (Vinogradov et al., 1989), where it flourished and expanded into the Azov, Marmara, eastern Mediterranean, and Caspian Seas (Studenikina et al., 1991, Shiganova et al, 2001a, Shiganova et al, 2001b).

*Mnemiopsis leidyi* Invasion and Biodiversity Changes in the Caspian Sea 179

Ctenophore samples were collected with an METU (Medalist Technology University) net having a mouth opening of 0.2 m2 and a screen with a mesh size of 500 m, from the same depths as the Juday net (Vinogradov et al., 1989; Kideys et al., 2001). On completion of each tow, the cod end was immediately passed into a container and ctenophores counted by eye. The body length of each individual with lobes was measured lying flat (out of water) onboard, and the density of *Mnemiopsis leidyi* (per m2 and m3) was calculated from the net diameter and tow depth. The ctenophores were sorted in length groups of 5-mm intervals to determine the abundance of different size groups. Length measurements were converted to wet weight using an appropriate equation (Kideys et al., 2001). Samples of M*nemiopsis* were collected from 20001 along few semi- transects perpendicular to the Iranian coast of the

Fig. 1. Distribution of sampling stations in the southern Caspian Sea.

Caspian Sea (Fig. 1).

**Habitat:** *Mnemiopsis leidyi* inhabits coastal areas and surface layers (above thermocline) open sea. Some large ctenophores can spread deeper and even can be found near the bottom in the coastal areas of the Caspian Sea.

**Migrations:** Transferred with the currents. Dial vertical migrations were not recorded, although it is more abundant near the surface at night where they feed and reproduce

**Relation to salinity:** Euryhalinic species. Salinity range from 2 to 38 (Kremer, 1993). In the seas of Mediterranean basin *M .leidyi* occurs in waters with salinities ranging from 3 in the Sea of Azov to 39 in the eastern Mediterranean. In the Caspian Sea its distribution is limited isohalines of 4 ‰.

**Relation to temperature:** Eurythermic species. Temperatures range from 0оC in northern native locations in the winter, to 32оC in the southern estuaries during the summer.

**Feeding type:** Heterotrophic, carnivorous

**Feeding behavior:** The larvae of *Mnemiopsis* can retract entirely their two tentacles into the tentacular sheaths on either side of the body, between the oral and aboral poles.

**Reproduction type:** *Mnemiopsis leidyi*- is a self-fertilizing hermaphrodite

**Relation to environmental factors:** The main factors, which are important for reproduction, are temperature and food concentration

#### **5. Highlights of** *Mnemiopsis* **monitoring data in the Caspian**

Invasion of the Caspian Sea by the comb-jelly *Mnemiopsis leidyi* (ML) since late 1990s has become one of the main environmental issue of this unique ecosystem. The adverse effects of this ctenophore was first visible on the pelagic fishery but also evident on other major compartments of the ecosystem, including, phytoplankton, zooplankton, benthos, Caspian Seal and even on some sturgeon species. Some endemic zooplankton species appear to have completely disappeared from samples of ongoing monitoring programs. ML invasion has had major impact on fisheries industry causing considerable economic damage, mostly to the coastal communities which depend on pelagic fisheries for their livelihood. The case of ML in the Caspian Sea is one of the largest invasion impacts ever occurred in a marine ecosystem all over the world.

#### **6. A review of Mnemiopsis investigations of the Caspian Sea over the last decade**

After *Mnemiopsis* invasion into the Caspian Sea via the ballast water from the Black Sea and/or the Sea of Azov in 1999 (Roohi et al., 2008a), some objectives of this alien ctenophore was taken into account in several local or national projects such as follows:


*Mnemiopsis* monitoring with the spatial and temporal investigations were conducted along the inshore and offshore of the Caspian Sea in Iran- Russia- Azerbaijan and Turkmenistan coasts. Fortunately, the main two countries (Iran and Russia) had established the favorable framework of the jelly study and achieved the appropriate results in which most of the discussion were based on two countries data analysis.

**Habitat:** *Mnemiopsis leidyi* inhabits coastal areas and surface layers (above thermocline) open sea. Some large ctenophores can spread deeper and even can be found near the bottom in

**Migrations:** Transferred with the currents. Dial vertical migrations were not recorded, although it is more abundant near the surface at night where they feed and reproduce **Relation to salinity:** Euryhalinic species. Salinity range from 2 to 38 (Kremer, 1993). In the seas of Mediterranean basin *M .leidyi* occurs in waters with salinities ranging from 3 in the Sea of Azov to 39 in the eastern Mediterranean. In the Caspian Sea its distribution is limited

**Relation to temperature:** Eurythermic species. Temperatures range from 0оC in northern

**Feeding behavior:** The larvae of *Mnemiopsis* can retract entirely their two tentacles into the

**Relation to environmental factors:** The main factors, which are important for reproduction,

Invasion of the Caspian Sea by the comb-jelly *Mnemiopsis leidyi* (ML) since late 1990s has become one of the main environmental issue of this unique ecosystem. The adverse effects of this ctenophore was first visible on the pelagic fishery but also evident on other major compartments of the ecosystem, including, phytoplankton, zooplankton, benthos, Caspian Seal and even on some sturgeon species. Some endemic zooplankton species appear to have completely disappeared from samples of ongoing monitoring programs. ML invasion has had major impact on fisheries industry causing considerable economic damage, mostly to the coastal communities which depend on pelagic fisheries for their livelihood. The case of ML in the Caspian Sea is one of the largest invasion impacts ever occurred in a marine

**6. A review of Mnemiopsis investigations of the Caspian Sea over the last** 

was taken into account in several local or national projects such as follows:

Zooplankton and phytoplankton changes after ML invasion

discussion were based on two countries data analysis.

After *Mnemiopsis* invasion into the Caspian Sea via the ballast water from the Black Sea and/or the Sea of Azov in 1999 (Roohi et al., 2008a), some objectives of this alien ctenophore

Distribution and abundance of *Mnemiopsis leidyi* in the Caspian Sea (Iran- Russia –

 Feeding, respiration, reproduction of *Mnemiopsis leidyi* in the Caspian Sea- in 2001-2009 Comparative feeding study of *Mnemiopsis leidyi* and Kilka in the Caspian Sea- in 2003 -

*Mnemiopsis* monitoring with the spatial and temporal investigations were conducted along the inshore and offshore of the Caspian Sea in Iran- Russia- Azerbaijan and Turkmenistan coasts. Fortunately, the main two countries (Iran and Russia) had established the favorable framework of the jelly study and achieved the appropriate results in which most of the

native locations in the winter, to 32оC in the southern estuaries during the summer.

tentacular sheaths on either side of the body, between the oral and aboral poles. **Reproduction type:** *Mnemiopsis leidyi*- is a self-fertilizing hermaphrodite

**5. Highlights of** *Mnemiopsis* **monitoring data in the Caspian** 

the coastal areas of the Caspian Sea.

**Feeding type:** Heterotrophic, carnivorous

are temperature and food concentration

ecosystem all over the world.

2004 and 2008/9

Azerbaijan)- in 2001-2004 and 2009

**decade** 

isohalines of 4 ‰.

Ctenophore samples were collected with an METU (Medalist Technology University) net having a mouth opening of 0.2 m2 and a screen with a mesh size of 500 m, from the same depths as the Juday net (Vinogradov et al., 1989; Kideys et al., 2001). On completion of each tow, the cod end was immediately passed into a container and ctenophores counted by eye. The body length of each individual with lobes was measured lying flat (out of water) onboard, and the density of *Mnemiopsis leidyi* (per m2 and m3) was calculated from the net diameter and tow depth. The ctenophores were sorted in length groups of 5-mm intervals to determine the abundance of different size groups. Length measurements were converted to wet weight using an appropriate equation (Kideys et al., 2001). Samples of M*nemiopsis* were collected from 20001 along few semi- transects perpendicular to the Iranian coast of the Caspian Sea (Fig. 1).

Fig. 1. Distribution of sampling stations in the southern Caspian Sea.

*Mnemiopsis leidyi* Invasion and Biodiversity Changes in the Caspian Sea 181

Fig. 3. Seasonal distribution of Mnemiopsis leidyi abundance (depth averages of available months) in the Southern Caspian Sea during 2001–2006. (A) Spring. (B) Summer. (C)

Autumn. (D) Winter.

The ctenophore *Mnemiopsis leidyi* was found at all stations from 2001–2009. There was a seasonal succession of ctenophore densities every year, the maximum being observed in August and September, and the minimum density in the winter months. A significant correlation was found between the water temperature and the abundance of Mnemiopsis leidyi (P <0.005). The highest summer– autumn average of Mnemiopsis leidyi abundance was observed in 2002 (760 ± 1148 ind.m3), although the biomass during this period (23.2 ± 23.3 g.m3) was lower than in 2001 (41.5 ± 44.3 g.m3). In terms of monthly averages, October 2001 was the month of the maximum abundance and biomass (1157 ± 1614 ind.m3 and 58.9 ± 40.0 g.m3).

Fig. 2. Spatial and depth means of *Mnemiopsis leidyi* abundance and biomass in the Southern Caspian Sea during summer–autumn 2001–2006

In terms of spatial distribution, in spring the maximum abundance of *Mnemiopsis leidyi* (141 ind.m3) was recorded in the coastal area of the southeastern Caspian Sea (Amirabad) and the minimum (3–14 ind.m3) in waters 100 m deep. In summer, the highest abundance was again noted in the southeastern Caspian Sea, with values 763 ind.m3. Likewise, in autumn, the maximum abundance was in the southeast at Babolsar (at the shallowest station of 5 m depth), with a value of 1235 ind.m3. In addition, abundance was high at a station with a depth <20 m (500–700 ind.m3. In winter the maximum abundance was recorded in the Anzali region, with a value of 653 ind.m3 (Fig. 3).

In the Northern Caspian, *M. leidyi* was first found only in September 2000; its abundance increased in October, but values were not high: 108 ±65 ind. m-2 (21.6 ±9 ind. m-3), biomass 140.4 ±42 g m-2 (28.1 ±8 g m-3).

In May 2001, *M. leidyi* was recorded only in the Southern Caspian (Fig. 6A), where its abundance was 1972 ± 683 ind. m-2 (100 ± 34 ind. m-3) and biomass 128 ± 57.5 g m-2 (6.4 ± 2 g m-3) and in the southwestern part of the Middle Caspian, up to 43° N, abundance was 230 ± 144 ind. m-2 (12 ± 20 ind. m-3)and biomass was 20.0 ± 37 g m-2 (1.4 ± 2 g m-3) (Fig. 4). *M. leidyi*  was most abundant in the western and middle areas of the Southern Caspian, with maximum abundance at the Apsheron Swell and in the western slope waters. Mean size was

The ctenophore *Mnemiopsis leidyi* was found at all stations from 2001–2009. There was a seasonal succession of ctenophore densities every year, the maximum being observed in August and September, and the minimum density in the winter months. A significant correlation was found between the water temperature and the abundance of Mnemiopsis leidyi (P <0.005). The highest summer– autumn average of Mnemiopsis leidyi abundance was observed in 2002 (760 ± 1148 ind.m3), although the biomass during this period (23.2 ± 23.3 g.m3) was lower than in 2001 (41.5 ± 44.3 g.m3). In terms of monthly averages, October 2001 was the month of the maximum abundance and biomass (1157 ± 1614 ind.m3 and 58.9 ±

Fig. 2. Spatial and depth means of *Mnemiopsis leidyi* abundance and biomass in the Southern

In terms of spatial distribution, in spring the maximum abundance of *Mnemiopsis leidyi* (141 ind.m3) was recorded in the coastal area of the southeastern Caspian Sea (Amirabad) and the minimum (3–14 ind.m3) in waters 100 m deep. In summer, the highest abundance was again noted in the southeastern Caspian Sea, with values 763 ind.m3. Likewise, in autumn, the maximum abundance was in the southeast at Babolsar (at the shallowest station of 5 m depth), with a value of 1235 ind.m3. In addition, abundance was high at a station with a depth <20 m (500–700 ind.m3. In winter the maximum abundance was recorded in the

In the Northern Caspian, *M. leidyi* was first found only in September 2000; its abundance increased in October, but values were not high: 108 ±65 ind. m-2 (21.6 ±9 ind. m-3), biomass

In May 2001, *M. leidyi* was recorded only in the Southern Caspian (Fig. 6A), where its abundance was 1972 ± 683 ind. m-2 (100 ± 34 ind. m-3) and biomass 128 ± 57.5 g m-2 (6.4 ± 2 g m-3) and in the southwestern part of the Middle Caspian, up to 43° N, abundance was 230 ± 144 ind. m-2 (12 ± 20 ind. m-3)and biomass was 20.0 ± 37 g m-2 (1.4 ± 2 g m-3) (Fig. 4). *M. leidyi*  was most abundant in the western and middle areas of the Southern Caspian, with maximum abundance at the Apsheron Swell and in the western slope waters. Mean size was

Caspian Sea during summer–autumn 2001–2006

Anzali region, with a value of 653 ind.m3 (Fig. 3).

140.4 ±42 g m-2 (28.1 ±8 g m-3).

40.0 g.m3).

Fig. 3. Seasonal distribution of Mnemiopsis leidyi abundance (depth averages of available months) in the Southern Caspian Sea during 2001–2006. (A) Spring. (B) Summer. (C) Autumn. (D) Winter.

*Mnemiopsis leidyi* Invasion and Biodiversity Changes in the Caspian Sea 183

of other seas. This was shown to be due mainly to malnutrition of larvae. One of the most striking changes in the Ichtyoplankton has been the shift in the spawning areas of the main fish species in Caspian Sea. Even the invading ctenophore *Mnemiopsis* were found to be starving. The condition of other species (*Calanipeda aquae dulcis* and *Limnocalanus grimaldii*) disclosed the fact that cyclonic regions where chlorophyll and nutrient concentrations are

A total of 18 zooplankton species (mero- and holozooplankton) were found. Among them there were 13 species of merozooplankton and only five species of holozooplankton. The latter belonged to Copepoda (four species) and Cladocera (one species) (Table 2). The only Cladocera species was *Podon polyphemoides*. Four copepod species were found, with the predominant calanoid *Acartia tonsa* present in all stations and every season. In 2006, a slightly higher diversity of Copepoda was seen; *Eurytemora grimmi*, absent in 2001–2005, was then observed for the first time at 50 m depth of the 100-m-deep station off Anzali (49N and

Table 2. Species number of zooplankton before and after *Mnemiopsis leidyi* invasion in the

In general, low zooplankton abundance and biomass (wet weight) were observed in summer months from 2001 to 2006. The highest abundance and biomass of zooplankton along the whole water column were not regularly found in the same season each year (Fig. 5). The maximum abundance recorded was 22,088 ± 24,840 ind.m3 (average of stations and depths) in December 2001, whereas the highest biomass was 64.1 ± 56.8 mg.m3 (average of stations and depths) in August 2004. Monthly variations of zooplankton biomass were similar to the fluctuations in abundance except in some summer–autumn periods when large-sized specimens dominated. The minimum zooplankton abundance and biomass were 397 ± 567 ind.m3 and 1.8 ± 2.6 mg.m3, respectively, in September 2002. The annual mean zooplankton abundance varied between 3361 and 8940 ind.m3 during 2001–2006. The

high provide better nutrition than anticyclonic regions.

**8. Species composition of zooplankton** 

37E) in 2006.

Southern Caspian Sea.

**9. Zooplankton frequency** 

very small: up to 3.6 mm in the Southern Caspian and 4.2 mm in the Middle Caspian. It is well known that *Mnemiopsis* shrinks in unfavorable conditions; here, salinity, food, or a combination of both may have been strongly suboptimal.

In May, a few eggs and larvae were found in the Southern and Middle Caspian, but mass reproduction did not start yet because of scarcity of reproducing adults and probably, low spring temperatures (16°C in the Southern and 15°C in the Middle Caspian) (Fig.4).

In June 2001, *Mnemiopsis leidyi* began to reproduce and continued its expansion towards the north: in the Southern and south Middle Caspian (Fig. 4), its average abundance was 680 ± 16.8 ind. m-2 (34 ± 2 ind. m-3), and biomass 88.3 ± 7.78 g m-2 (4.3 ± 1 g m-3) (Fig. 4). The highest abundance and biomass, found in the Southern Caspian, represented values of 2005 ± 1248 ind. m-2 (100 ± 62 ind. m-3) and 230 ± 197.66 g m-2 (10.2 ± 9 g m-3), respectively (Shiganova et al., 2004).

Fig. 4. Seasonal distribution of the Caspian population of *Mnemiopsis leidyi* (ind.m3) in 2003 (shiganova et al., 2004)

#### **7. A review of zooplankton investigations of the Caspian**

Investigations performed in the last decade indicate that there have been important changes in the zooplankton composition and structure in the Caspian Sea. However, contrasting events taking place in different regions of the Caspian Sea indicate a non-uniform structure of its ecosystem. Several fodder zooplankton species have either disappeared from or substantially decreased in number at different sampling sites of the Caspian Sea over the last decade. Some other species adapted to thrive in eutrophic conditions have either appeared or increased in quantity especially meroplankton. Meanwhile the biomass of the fodder zooplankton has also fluctuated considerably through the years. However, there seems to be a reverse trend in the long-term variation of fodder zooplankton between the shallow western and deep eastern areas. Over the last decade the abundance of fish larvae has decreased significantly when compared either to past records or with larval abundances of other seas. This was shown to be due mainly to malnutrition of larvae. One of the most striking changes in the Ichtyoplankton has been the shift in the spawning areas of the main fish species in Caspian Sea. Even the invading ctenophore *Mnemiopsis* were found to be starving. The condition of other species (*Calanipeda aquae dulcis* and *Limnocalanus grimaldii*) disclosed the fact that cyclonic regions where chlorophyll and nutrient concentrations are high provide better nutrition than anticyclonic regions.
