Invaders in the Caspian Sea

INV ADERS IN THE CASPIAN SEA

NIKOLAI V. ALADIN*, IGOR S. PLOTNIKOV & ANDREI A. FILIPPOV

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Zoological Institute, Russian Academy ofSciences, St.Petersburg, Russia *Corresponding author aral@zin.ru

Abstract The Caspian Sea is the largest lake in the world. All its resident species can be considered as invaders with various time of introduction. The most ancient invaders are regarded as indigenous species. The glacial relicts invaded the Caspian 1-1.5 million years BP. There are also "Atlantic species" and those of fresh-water origin. Human-mediated introductions started in the beginning of 20th century. The construction of the Volga-Don Canal facilitated invasion many-fold. A deliberate introduction of fishes and invertebrates has exerted essential influence on the biodiver­sity of the Caspian in the 1930s-1970s. The impact of introduced species on indigenous biota can be either positive or negative. The invasion of the comb jelly Mnemiopsis leidyi and the bivalve Mytilaster lineatus had negative consequences while deliberate accIimatisation as weil as a num­ber of accidental introductions of other aquatic organisms had positive effects. The concIusion was drawn that the most ancient representatives of the Caspian flora and fauna should be pro­tected against any negative impact, incIuding the impact of newly introduced species.

1 Introduction

The Caspian Sea, a lake without outlets, washes the shores of five countries; Azerbaijan, Iran, Turkmenistan, Kazakhstan and Russia, and two continents, Europe and Asia (Fig. 1). It is the largest lake in the world. The sea level ofthe Caspian Sea is 25-29 m lower than the mean sea level; it fluctuates depending on the water balance, rising when the balance is positive and lowering when it is negative. Due to the instable water levels, the surface area is also varying. The Caspian is elongated: its length from the north to the south is 1,204 km (Zenkevich 1963) and the greatest width is 566 km. The surface ofthe Caspian is 436,000 km2, its watershed area is 3.1-3.5 million km2 and total vol­urne about 77,000 km3• The Caspian Sea is divided into three parts of approximately equal dimension: North, Middle and South. Only apart ofthe Northem Caspian belongs to Europe, while both Middle and Southem parts are on the Asian side of the sea. The average depth of Northem Caspian is 6 m maximal depths do not exceed 10m. The mean and greatest depths of Middle and Southem parts are 175-790 and 300-1,025 m, respectively.

A shallow (max depth < 10 m) gulf Kara-Bogaz-Gol lies approximately 3-4 m lower than the sea level and due to this the sea constantly drains into it, making the gulf a large evaporator of the Caspian. Presently, 200-300 m3 per second of Caspian water is discharged into Kara-Bogaz-Gol carrying some 130-150 million tons of salt from the sea. Average salinity of the N orthem Caspian is 5-10 PSU, of the Middle part 12.7, of the Southem part 13 and of the gulf Kara-Bogaz-Gol up to 300-359 PSU. Caspian wa­ters differ from oceanic waters by their salt composition, which is rather poor with so­dium and chlorine ions and rich with ions of calcium and sulphates.

Each of the four areas of the Caspian has its own features of the temperature regime. In the Northem Caspian, in the middle of a summer, the average water temperature is

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E. Leppäkoski et al. (eds.), Invasive Aquatic Species of Europe, 351-359. © 2002 Kluwer Academic Publishers.

352 N. V. Aladin, I. S. Plotnikov & A. A. Filippov

24°C; in the winter this part of the Caspian freezes. Water temperature under iee ean drop down to -O.5°C. In the Southem Caspian the temperature never drops below 13°C in wintertime; in summertime it usually inereases up to 25 and even 30°C. Constant temperature is maintained at depths ofthe Caspian Sea both in winter and summer. The water of the Caspian Sea is eharaeterized by high transpareney with maximums ob­served in the open parts of the Southem Caspian. As a result of good turbulent mixing the deep waters have no dead zone and are rieh with dissolved oxygen. On the surfaee the amount of oxygen is elose to saturation all over the Sea.

Figure 1. Caspian Sea water area (with isohalines) and drainage basin (by Zenkevich 1963 and Rodionov 1994).

All present resident speeies in the Caspian Sea ean be deseribed as invaders. The only differenee is the time of introduetion. Aeeording to the time of appearanee in the Cas-

Invaders in the Caspian Sea 353

pian the speeies can be divided into four groups. (i) The most ancient invaders, which can be regarded as indigenous and are often called "living fossils". (ii) Early invaders from the Arctic seas, the glaeial relicts. The ancestors ofthese species invaded the Cas­pian 1-1.5 million years BP during the period of melting of the ice sheet that covered almost all Europe, Arctic and coastal areas ofthe Baltic and White Seas. (iii) Introduced species from the Black and Mediterranean Seas. The most ancient of these "Atlantic invaders" were introduced into the Caspian about 50,000 years ago when the ancient Caspian was connected with the Azov-Black Sea basin through the Manych canal. (iv) Invaders from fresh waters. The most ancient ones are the Caspian gastropods that originated from fresh waters of Pliocene. They probably invaded the ancient Caspian approximately 2-5 million years BP when the sea was most desalinated.

2 Native fauna and flora

2.1 ARCTIC SPECIES

Arctic species are one of the most aneient groups of the Caspian Sea speeies (Fig. 2), represented by the sabellid polychaete Manayunkia caspia, the copepod Limnocalanus grimaldi, the isopod Saduria entomon, the amphipods Pseudalibrotus caspius, P. platy­ceras, Monoporeia affinis and Gammaracanthus loricatus, the mysids Mysis caspia, M microphthalma, M macrolepis and M amblyops, the white salmon Stenodus leucich­thys, the bulltrout Salmo trutta, and the seal Phoca caspia (Zenkevich 1963 and refer­ences therein). Recently tusks of a walrus were found on the bottom of the sea in the vicinity ofthe Absheron Peninsula. Probably, this inhabitant ofthe Arctic region used to live in the Caspian Sea (N. Vereschagin, pers. comm.). Also some plankton crustaceans (Cercopagidae) should probably belong to the northem invaders. According to regula­tory and molecular-biological studies of the genus Cercopagis they cannot be consid­ered as typical Caspian endemics (Richter et a1. 2001).

There are few hypotheses tending to explain how and when these organisms invaded the Caspian Sea. The fIrst of them (Ekman 1916; Sars 1927) stated that there was a direct contact between the Caspian Sea and the Arctic Ocean. At present, this hypothesis is outruled because of lack of evidence. Grimm & Kessler (eit. Zenkevich 1963) deemed that the Arctic imrnigrants arrived from the north via rivers. Today, this hypothesis is supported by suffIcient data. Guryanova & Pirojnikov (eit. Zenkevich 1963) assumed that immigrants originated in the Kara Sea. There are no direct confIrmations of this theory. Berg's (1928) hypothesis was based on the existence of an ancient lake, which stretched from the Baltic Sea up to Ladoga and Onega Lakes and further up to the White Lake and to the river Sheksna. This hypotheticallake ensured connection of the Caspian Sea with Arctic and Baltic waters and, consequently, penetration of Arctic immigrants, not directly from the Arctic Ocean, but from the Baltic and White Seas. Today, there is a lot of data supporting this hypothesis. Grosswald (1980) and Dawson (1992) presented the hypothesis that a superflood occurred during the late Valdai period (about 20,000 years ago). The level ofthe ancient Caspian rose by 2-3 m above the level ofthe ocean (Lamb 1977), and its waters run through the Azov-Black Sea basin. Waters of a Iarge ice lake that existed in the West Siberian Plain run into the Aral basin and from the Aral into the aneient Caspian.

354 N. V. Aladin, I. S. Plotnikov & A. A. Filippov

The Northern Caspian

Arclle

Autochthones

Middle and Southern Casplan

Alctlc Atl.nUc

Figure 2. Authochthonous, freshwater, Atlantic and Arctic elements in the northern, mid­die and southern Caspian Sea fauna.

Invaders in the Caspian Sea 355

2.2 FRESHW ATER ORGANISMS

The invasion of freshwater organisms (Fig. 2) into the Caspian Sea took place several times during its greatest freshening (see Chuykov 1994 for a comprehensive review). The gastropod molluscs are considered the most ancient freshwater elements. To certain degree this was facilitated by the nature ofthe salinity ofthe Caspian, essentially differ­ing from the oceanic water by its composition.

2.3 ATLANTIC-MEDITERRANEAN ELEMENTS

The fauna of Atlantic-Mediterranean origin (Fig. 2) is represented by Turbellaria (1 species) Coelenterata (1), Polychaeta (2), Copepoda (1), Cirripedia (2), Decapoda (3), Mollusca (3), Bryozoa (2), and 6 species of fish (Zenkevieh 1963). The first invaders penetrated during the Khvalyn period (approx. 50,000 years BP) in a natural way via the Kumo-Manycheskiy Strait connecting the Black and Caspian Seas. They included 7 species: the seagrass Zostera nana, the bryozoan Bowerbankia imbricata, the bivalve Cardium edule, the polychaete Fabricia sabella, and fish species (the silverside Ath­erina mochon pontica, the pipefish Syngnathus nigrolineatus, and the goby Pomato­schistus caucasicus).

3 Human-mediated unintentional introductions

3.1 EARL Y TRANSFERS

In the 20th century the number of introduced species from the Black Sea and the Medi­terranean suddenly increased. All the cases of introduction were related to anthropo­genie activity. The diatom algae Rhizosolenia calcar-avis and the bivalve Mytilaster lineatus were brought to the Caspian presumably by merchants, who transported their small wooden boats on carts from the Azov Sea. M lineatus was found for the first time in 1928. It is one ofthe most numerous benthic species ofthe Caspian Sea, but it is also known as an important fouling species. Diatom Rhizosolenia calcar-avis appeared in 1930. By 1936 it made up 2/3 ofthe total biomass ofphytoplankton.

3.2 THE VOLGA-DON CANAL - AN IMPORTANT INVASION CORRIDOR

The Volga-Don Canal was opened in 1952. Its length is 101 km, the highest water-Ievel is elevated by 88 m above the Volga level and by 44 m above Don level. The canal has 9 shipping locks at the Volga side and 4 locks at the Don side. It has also large reser­voirs along its course (Sokolov 1964). After opening the canal, a new group of species invaded the Caspian Sea. Most of them were carried from the Black Sea and the Sea of Azov by ships in ballast water or in biofouling assemblages (Karpevieh 1975). At least 10 species of algae penetrated into the Caspian, including the green algae Enteromorpha tubulosa and E. salina, the brown algae Ectocarpus confervoides v. jluviatilis, and En­tonema oligosporum, and the red algae Acrochaetium deviesii, Ceramium diaphanum, C. tenuissimum, and Polysiphonia variegata. Soon after its introduction C. diaphanum became a dominant species in the Northem Caspian.

Two species of bamacles, Balanus improvisus and B. eburneus, were brought in as vessel biofouling from the Black Sea and the Sea of Azov. B. improvisus was first de-

356 N. V. Aladin, I. S. Plotnikov & A. A. Filippov

tected in the Northern and Middle Caspian in 1955. Within a year, it spread all over the Caspian Sea. Now it is a dominant fouling organism on vessels and hydro-engineering structures. B. eburneus was found in the Caspian Sea in 1956. It is rarely found in foul­ing of vessels, since it cannot stand strong water currents (Sars 1927). The bryozoan Conopeum seurati, the hydroids Bougainvillia megas and Moerisia maeotica, the kamp­tozoan Barentia benedeni, the polychaete Ficopomatus enigmatica and the plankton cladoceran Pleopis polyphemoides penetrated in 1950s from the Black Sea and Sea of Azov. Most of these species live in shallow waters and occur in fouling of vessels, buoys, pipes, port structures, offshore oilrigs and piers.

The jellyfish Blackfordia virginica was first discovered in the Caspian Sea at the mouth ofthe river Kura in 1956. This invader originates from the north-eastern coast ofNorth America and came to the Caspian through the Sea of Azov. The North American mud crab Rhithropanopeus harrisii was found in the Northern Caspian in 1958. From the Northern Caspian, the crab spread with the aid of vessels and the cyclonic current along the western part of the Middle Caspian and all over the sea. In the 1970s the cladoceran Penilia avirostris was found in the Caspian Sea and in 1985 Podon intermedius ap­peared.

The eel Anguilla anguilla appeared in the waters of Azerbaijan in 1964. Some years later it was also found in the coastal waters from the Sarah Peninsula down to Iranian waters. Single eels used to be found in the basin of the Caspian Sea. According to Kessler (cit. Zenkevich 1963), they penetrated into the basins ofthe Black and Caspian Seas from the Baltic. The opening ofthe Volga-Baltic waterway and transplantation of larval eels (delivered from England and France) into the inland reservoirs of Russia, including basins along the Volga, facilitated its penetration into the Caspian. Eel is rather often caught as by-catch in different parts ofthe sea, which suggests that not only single fishes have penetrated the Caspian.

Draining of the Kara-Bogaz-Gol Bay facilitates the spread of halophilic cosmopolitan species. Not one of the above-mentioned species can be found in the hyperhaline Kara­Bogaz-Gol Bay. Only halophilous species inhabit this area. They represent a group of cosmopolitan forms originating in arid areas. All these halophilous organisms have a resting stage in their life cycle (delitescence eggs, spores, seeds and cysts) that can sur­vive drying, freezing and other unfavourable conditions (Makrushin 1985). Some cysts could remain viable for tens and hundreds of years. The resting stages are small in size and can be carried with the wind and migrating birds.

In the early 1980s adam was buHt in order to isolate the bay from the sea and to "im­prove" the water balance of the Caspian Sea. In 1900s the water discharge to the Kara­Bogaz-Gol Bay was restored. When the bay dried, resting phases of halophilic organ­isms remained on its exposed seabed and revived after the bay was refilled with salt water. The dry bay was a source of dust storms, which carried the cysts all over the world. This is the reason why many organisms that inhabit the Kara- Bogaz-Gol Bay are similar to the species from salt lakes of America, Europe, Asia, Africa and Australia.

Invaders in the Caspian Sea 357

3.3 MOST RECENT INVADER(S)

More species are currently invading the Caspian Sea, and will be registered in the ne ar­est future (Dumont 1995). In autumn of 1999 Aurelia aurita and the comb jelly Mne­miopsis leidyi were recorded on video film from the Caspian (Ivanov et al. 2000). No doubt, invaders will continue appearing in the Caspian unless a new balance between native species and invaders will become established. It is very difficult to predict when such a balance will be achieved, due to the current unstable environment ofthe Caspian Sea, because of climate changes, anthropogenie pollution and other environmental im­pacts. Until now changes in abiotic and biotic components of the ecosystems of the Caspian Sea has supported invaders.

Table 1. Recent invaders in the Caspian Sea. (B) benthos; (P) plankton; (Bf) biofouling; (P) parasite; (N) nekton; (N-B) nektobenthos; (SH) shipping; (H) with host; (A+) during acclimatization; (A) acclimatization; (Rw) by railway; (BI-Az) Black Sea - Sea of Azov; (Pac) Pacific; (Okh) Sea of Okhotsk; (NA) Northern America; (Med) Mediterranean; (Ind-Afrllndia-Africa. Species Ecol. group Origin Naturalization Donor area Vector Years Coelenterata B/ackfordia virginica BI NA + BI-Az Sh 1956 Bougainvillia megas BI NA + BI-Az Sh 1956 Moerisia maeotica BI BI + BI-Az Sh 1950s? Aurelia aurita* P BI ? BI-Az Sh 1999 Clenophora Mnemiopsis /eidyi P NA + BI-Az Sh 1999 Trematoda Apophallus mueh/ingi Pa BI + BI-Az H 1980-90s? P/agiorchis entamiatis Pa ? + ? H 1960s Rossicotrema donicum Pa BI + BI-Az H 1980-90s? Nico/a scriabini Pa BI + BI-Az H 1980-90s? Ancyrocepha/us vanbenedeni Pa BI + BI A+ 19305 W/assenkotrema /ongicollum Pa BI + BI A+ 19305 Saccocoe/ium obessum Pa BI + BI A+ 19305 Hap/osp/anchnus pachymosus Pa BI + BI A+ 19305 POlychaeta Nereis diversic%r B Bor? + Az A 1940 Ficopomatus enigmatica BI Pac? + BI-Az Sh 19505? Mollu5ca Mytilaster lineatus BI Med + BI Rw 19205 Dreissena bugensis BI Az-BI + BI-Az Sh 1994 Abra ovata B Med + Az A 19405 Monodacna c%rata B BI + Sh 19505 Lithog/yphus naticoides B Az-BI + BI-Az Sh 1971 Tenellia adspersa BI Med +(?) BI-Az Sh 1989 Cru5tacea (Cirripedia) Ba/anus improvisus BI NA + BI-Az Sh 1955 B. eburneus BI NA + BI-Az Sh 19505 Cru5tacea (Cladocera) Penilia avirostris P BI +(?) BI-Az Sh? ? P/eopis po/yphemoides P BI + BI-Az Sh 1957 Podon intermedius P Med + BI-Az Sh 1985 Cru5tacea (Copepoda) Acartia c/ausi P NA + BI-Az Sh 1981 Cru5tacea (Decapoda) Pa/aemon e/egans N-B Med + BI A+ 19305 P. adspersus N-B Med + BI A+ 19305 Rhithropanopeus harrisii B NA + BI-Az Sh 19505 Bryozoa

358 N. V. Aladin, I. S. Plotnikov & A. A. Filippov

Species Ecol. group Origin Naturalization Donor area Vector Years Conapeum seurati Bf Med + BI-Az Sh 1958 Kamptozoa Barentsia benedeni Bf Med + BI-Az Sh 1962 Pisces Pleuronectes flesus luscus N BI A 1902, 19305 Scomber scombrus N BI A 1902 Engraulis encrasichalus N BI A 1933-1934 Mullis barbatus N BI A 1933-1934 Rhombus maeoticus N BI A 1930 Mugil auratus N + BI A 1930-1934 M. saliens N + BI A 1930-1934 Ctenopharyngodon idella N + China A 1955-1956

1964-1977 Hypophthalmichtys molitrix N + China A 1964-1977 Aristichthys nobilis N + China A 1964-1977 Oncarhynchus keta N + Okh A 1962-1966 O. gorbuscha N Okh A 1964 O. mykiss N ? A 1975-1978 0. kisutch N ? A 1975-1978 Morone saxatilis N ? USA A 1972 Stenodus leucichthys nelma N Ob' A 1965 Mugil sa-iuy N BI A 1966,1979

4 Intentional introductions

In 1902 the first attempt to introduce non-native fish into the Caspian Sea was under­taken. Three species were transferred from the B1ack Sea: the mullets Mugil auratus and M saliens and the flounder Pleuronectes flesus luscus. This introduction was unsuc­cessful. A deliberate introduction of commercial and prey organisms exerted essential influence on the biodiversity ofthe Caspian. In the 1930s-1970s, at least nine species of fish were introduced into the Caspian Sea (Karpevich 1975). As part of an All-Union acclimatization programme, some invertebrates were also introduced in order to in­crease the food resources available for commercial fish.

The polychaete Nereis diversicolor was brought into the Caspian Sea from the Sea of Azov in 1939-1941. It has successfully naturalised and now occurs all over the Caspian, playing an important role in fish feeding. The bivalve Abra ovata was brought from the Azov-B1ack Sea into the Caspian in 1939-1940 and additionally in 1947-1948. By the end of 1959, A. ovata populated the western part of the Middle and Southern Caspian. The shrimps Palaemon elegans and P. adspersus were introduced from the Black Sea in 1931-1934 together with mullets. Later on these species have occupied the coastal zone of the Middle and Southern Caspian.

Two mullet species, Mugil saliens and M auratus, were introduced into the Caspian in 1930-1934 from the Black Sea. Both species are commercially valuable and they are widespread all over the Caspian, especially in the southeastern and southwestern parts. Two species of the mosquito fish, Gambusia affinis and G. holbrooki, were released into the Caspian basin to combat malaria, as a destroyer of larvae of malaria mosqui­toes. Nowadays it is found from Astara in the south up to Khacbmas in the northeast and is very abundant in low-lying waters of the Lenkoran natural area. Several other fish species were introduced in 1930s-1970s with various outcomes (Table 1).

Invaders in the Caspian Sea 359

4.1 IMPACT OF INTRODUCED SPECIES ON THE CASPIAN SEA ECOSYSTEM

The impact of introduced species on the biological diversity of the Caspian Sea is both chronic (Iong term) and acute (short-term). Acute impact was usually identified during the first years after the introduction of a new species, after which the effect weakens while impact on the biodiversity be comes chronic. For instance, in 1936 the biomass of the alga Rhizosolenia calcar-avis was about 65% ofthe total plankton biomass. Follow­ing the 'biological wave', the abundance ofthe species reduced. A short-term increase of abundance and its further reduction was recorded for the bivalve Mytilaster lineatus, and for two species of shrimps. Both chronic and acute impact can be of a positive or negative character. The introduction ofthe copepods Calanipeda aquaedulcis and Acar­tia clausi can be an example of a positive impact. They form a food base by plankton­feeding fish and thus increase the nutritional value of the Caspian zooplankton. The invasion of the comb jelly Mnemiopsis leidyi will probably have a negative impact on the biodiversity of the Caspian Sea (Ivanov et al. 2000). The species preys upon zoo­plankton and causes starvation for the plankton-feeding fish. According to Aladin & Plotnikov (2000) the ctenophore may cause complete loss of the Caspian population of sprat. A number of accidental introductions have appeared to be commercially useful. Many microscopic crustaceans increased the value of the Caspian plankton as a food base for fishes. A high number of accidental introductions did not have any significant impact on the biodiversity ofthe water body. However, some ofthem such as the bama­cles and the bivalve Mytilaster had a certain negative impact from man's point of view. The above-mentioned organisms cannot be used as food for fish because of their thick shells; they are typical representatives of non-food benthos. In addition, some intro­duced species can foul bottoms of vessels, port piles and offshore oilrigs. They hamper movement of the vessels and gradually corrode port and oil structures. The role of in­troduced species in the ecosystem of the Caspian and their impact on its biodiversity has been debated. There is no reason to dramatise the impact of them. They predominantly contribute to the Caspian rich biodiversity. However, there is no doubt that species, such as Mnemiopsis leidyi, needs to be managed. It is clear that the most ancient repre­sentatives of the Caspian flora and fauna should be protected against any negative im­pact, including the impact of newly introduced species. The Caspian indigenous flora and fauna are the main value of this continental water body. It is of high biological, ecological, genetic and commercial importance. It has been repeatedly specified (Dumont 1998; Zonn 2000) that biological resources of the Caspian are more valuable than its oil and gas resources.