Marine Biological Invasions in Waters of the Port of ... - Springer Link

ISSN 1063-0740, Russian Journal of Marine Biology, 2009, Vol. 35, No. 3, pp. 242–249. © Pleiades Publishing, Ltd., 2009. Original Russian Text © Zh.P. Selifonova, 2009, published in Biologiya Morya.

ECOLOGY

Marine Biological Invasions in Waters of the Port of Novorossiysk in the Black Sea Zh. P. Selifonova Murmansk Marine Biological Institute, Kola Science Center Russian Academy of Sciences, Murmansk, 183010 Russia e-mail: [email protected] Received January 29, 2009

Abstract—The results of the monitoring of ballast waters of commercial vessels and research on the ecosystem biodiversity of the Novorossiysk Port are reported. Data on structure of immigrant fauna, its abundance, survival and origin of species were obtained. It has been established that the risk of introduction of Mediterranean species into the Novorossiysk Bay is the most probable. The basic “risk groups” are copepods and polychaetes. It has been hypothesized, that ship ballast water can become a primary factor of the “mediterranization” of the copepod fauna (Copepoda) in the northeast of the Black Sea. During the period of research in the Novorossiysk Bay, 36 species of Mediterranean copepods were recorded. A massive number of the cyclopoid copepod Oithona brevicornis Giesbr., 1891, a new species for the Black Sea, was recorded in samples collected in the autumn of 2005 and 2006. The status of the invader was attributed to the polychaete of the Streblospio genus. The necessity of ship ballast water control in Russia and the development of methodology, methods, and regulations for the prevention of the intrusion of pathogenic and potentially dangerous organisms by marine traffic were corroborated. Key words: ballast waters, holoplankton, meroplankton, invasions, biological control, ecosystem of the Novorossiysk Port, Black Sea. DOI: 10.1134/S1063074009030080

In recent years, the basic source of anthropogenic sea invasions has been the transportation of alien organisms with ship ballast water. Holoplankton animals and meroplankton larvae of bottom invertebrates have the greatest chances for expansion, not as individuals, but whole communities and, it is possible to state that even entire ecosystems are transported with ship ballast water. A meaningful example of the destructive effects of invader species on marine ecosystems is the invasion and naturalization of the ctenophore Mnemiopsis leidyi from waters of the Northwest Atlantic to the Black Sea [3–5]. The problem of biological invasions with sea traffic as a source of ecological danger for the water resources of Russia began to develop and be intensively discussed rather recently [5, 15]. An important step made in that direction was the implementation of regular investigation of ship ballast waters and their control in Novorossiysk Port [9, 10]. The Novorossiysk Port is the largest transportation node in the south of Russia, settled in the northeast of the Black Sea. The carrying capacity of the port is more than 5000 ships and 100 million tons of cargo each year (80% of this is oil and oil products). These ships in handling cargo dump more than 50 million tons of water from the segregated ballast tanks in the bay. Generalized data on the problem of marine bioinvasion in the Novorossiysk Port are unavailable in the literature. Meanwhile, such information is extremely necessary for understanding of the

degree of study of invader species in the territorial waters of the Black Sea and for the development of national and international measures directed at the improvement of the quality of the marine environment and fisheries resources. MATERIAL AND METHODS In 2004–2005 hydrochemical and hydrobiological monthly investigations of the ballast waters of commercial vessels (sea water salinity, holoplankton, and meroplankton) were undertaken in the Port of Novorossiysk for the first time in Russia, at the Murmansk Marine Biological Institute of the Kola Science Center of the RAS,. Vessels that loaded oil products in the Sheskharis and Pyataya Pristan Harbor were chosen as objects of research (Fig. 1). The assays of ballast water were sampled from the water surface. The salinity of water was measured using Mor’s argentometric method with an error not exceeding 0.02% (GOST 27384-87). The zooplankton samples were concentrated from ballast tanks by filtration of 80–100 liters of water through gauze with a mesh size of 100 µm. In total, 145 samples were collected. 2004–2007, ecosystem investigations of biodiversity were carried at permanent stations in the Novorossiysk Bay (Fig. 1): phytoplankton, nanoplankton, microplankton, holoplankton, meroplankton, ich-

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MARINE BIOLOGICAL INVASIONS IN WATERS OF THE PORT OF NOVOROSSIYSK

O i Py l ha at rb ay or a

sR

Easte regionrn

me

tral Cengion re

ern est n W egio r

Tse

243

ive

r

Oil harbor Sheskharis 5 10

20 20

2004–2007 2005 2006–2007

20

Fig. 1. The scheme of the Novorossiysk Bay and sampling stations.

thyoplankton, macrozoobenthos and macrophytobenthos were studied. In total, 1063 samples were taken. The complete list of flora and fauna included 417 taxa (nano- and microplankton, 30; phytoplankton, 109; mesoplankton, 73; meroplankton, 57; ichthyoplankton, 27; macrozoobenthos, 35; macrophytobenthos, 86). RESULTS AND DISCUSSION In March–April of 2004, the zooplankton in ship ballast water consisted of 31 holoplankton taxa and 15 taxa of meroplanktona [6] (Tables 1, 2). In the ballast water of the tankers Adriatiki, Fedor, and Prosky organisms unusual for the Black Sea (14 taxa), including the copepods Calanopia elliptica, Clausocalanus arcuicornis, Corycaeus furcifer, Ctenocalanus vanus, Oithona decipiens, O. brevicornis, Oncaea mediterranea, O. media, Paracalanus nanus and Temora longicornis were found. The zooplankton density varied from 1.3 up to 60000 ind./m3. The greatest number of zooplankton was revealed in the ballast water of the Prosky, and 74% were copepods of the Acartiidae fam-

ily. Species of Black Sea alien origin prevailed among them. A high density of Oithona nana (10000 ind./m3), which dominated among Black Sea copepods up to the middle of 1980s, was recorded in the samples. During a bloom in the density of the predatory invader ctenophore Mnemiopsis leidyi, the density of O. nana was abruptly reduced, and now its occurrence in the basin is rare [7, 17]. In the ship’s ballast water meroplankton, the larvae of Black Sea alien polychaetes (3500 ind./m3) and bivalves (1000 ind./m3), mostly species of the Microspio and Pygospio genera with unusual morphologies, holoplankton polychaetes and bivalve larvae belonging to the Cardiidae family, prevailed. It is known that meroplankton in such numbers were registered in the most polluted coastal areas of the seas [26]. The warm-water holoplankton species, Penilia avirostris, Centropages kroyeri and C. ponticus, uncharacteristic in the studied season, were recorded in the ballast water of the Adriatiki. The overwhelming portion of the fauna revealed in the ballast water of the Fedor was Synchaeta rotifers (4400 ind./m3) and copepods of the Acartiidae family (2700 ind./m3). In the population

Table 1. Some parameters of the water ballast delivered into the Novorossiysk Port March–April of 2004 Tanker’s Name

Sample date

Temperature, °C

Salinity, ‰

Volume, thousands m3

Adriatiki Fedor Aegean Pride Sea Falcon II Prosky

04.03.04 11.03.04 16.04.04 23.04.04 27.04.04

7 7 10 11 11

25.91 22.47 18.19 17.74 23.00

7.3 27.0 36.5 27.3 18.6

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Country, donor port Greece, Agios Theodori Italy, Trieste France; Fos-sur-Mer Bulgaria, Burgas Greece, Saloniki

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Table 2. Taxonomic structure and density of zooplankton (ind/m3) in ballast water of tankers that arrived into the Novorossiysk Port March–April of 2004 Taxon DINOPHYTA Noctiluca scintillans (Macartney) Kof et Swezy, 1921 INFUSORIA Favella ehrenberii var. helgolandica (Clap., Lach.) Tintinnopsis sp. ROTATORIA Synchaeta sp. POLYCHAETA (meroplankton) Nereis sp. Spionidae gen. sp. Microspio sp. Microspio mecznikowianus (Clap, 1868) Pygospio sp. Polydora cornuta Bocs., 1802 Magelona sp. Typhloscolecidae gen. sp. CLADOCERA Penilia avirostris Dana, 1849 Pleopis polyphemoides (Leuck., 1859) COPEPODA Acartia clausi Giesbr., 1889 A. margalefi Alcaraz, 1976 A. discaudata mediterranea Steuer, 1929 Acartia sp. 1 Acartia sp. 2 Calanus euxinus (Hulsemann, 1991) Calanopia elliptica (Dana, 1849) Centropages ponticus Karav., 1894 C. kröyeri Giesbr., 1892 Clausocalanus arcuicornis (Dana, 1849) Corycaeus furcifer Claus, 1863 Ctenocalanus vanus Giesbr., 1888 Labidocera brunescens Czern., 1868 Oithona nana Giesbr., 1892 O. decipiens Farran, 1913 O. similis Claus, 1866 O. brevicornis Giesbr., 1891 Oncaea mediterranea (Claus, 1863) O. media Giesbr., 1891 Paracalanus parvus (Claus, 1863) P. nanus Sars, 1907 Pontella mediterranea (Claus, 1863) Pseudocalanus elongatus (Boeck, 1864) Temora longicornis Müller, 1792 Nauplii of Copepoda HARPACTICOIDA CIRRIPEDIA (meroplankton) Amphibalanus improvisus Darwin, 1854 Chthamalus fragilis (Darwin, 1854) DECAPODA (meroplankton) Pilumnus hirtellus (L., 1755) Pontophilus trispinosus Hailston, 1835 ISOPODA BIVALVIA (meroplankton) Mytilus galloprovincialis Lam., 1819 Cardiidae gen. spp. GASTROPODA (meroplankton)

Adriatiki

Fedor

–

–

– –

– –

–

4400

– – – – – – –

– – – – – – –

20 20

– –

990 – – – – – – 30 30 20 10 – – – 20

– – – 80 –

2480 – – – 240 10 – 60 – 160 – 40 10 50 10 50 10 10 10 100 20 – 340 120 740 –

Aegean Pride

Sea Falcon II

70

160

1600

– 800

7450 –

28000 –

400

3200

– – – – – – –

– – – 600 – – –

– –

–

– –

10000 10 10 10 35000 – 30 60 – 10 – – – 9800 – – –

20480 – – – – 10 – – – – – – – – – – –

10010 – – – – – – – – – – – – – – 3000 –

10 –

– 80

– –

– – – – 190

10 – – 90 800

– 200 – 1400 3400

– –

– –

220 100

110 –

600 –

– – 10

10 – –

– 10

– – –

– – –

– 70 20

– 10 –

30 1000 20

– – –

2400 – –

– – 10

Prosky

– 100 200 1000 – 1000 200 50 1000

–


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Fig. 2. Euphausiid Larvae in the furcilia stage from ballast water of the Huntestern tanker.

Fig. 3. The General appearance of the Streblospio sp. polychaete.

structure of Acartia, copepodit and nauplial stages were recorded concurrently with mature individuals. Neritic plankton of the Black Sea (tintinnid infusorians, Synchaeta rotifers, meroplankton, small copepods of the Harpacticoida order and Acartia clausi) were present in significant number in the ballast water of the tankers Sea Falcon II and Aegean Pride, one of which departed from a Bulgarian port. Thus, our data supported the idea that the water intake into ship ballast tanks in most instances was carried out in the corresponding port areas. The water salinity in the ballast tanks of tankers varied from 17.7 up to 25.9‰. The water salinity was 17– 18‰ in the Black Sea and 30–35‰ in the Mediterranean [18, 19]. Thus, the salinity of the ballast water corresponded to that of Black Sea water (17.74−18.19‰) only in two tankers, the Aegean Pride and Sea Falcon II. Hence, it follows that the crews of some commercial vessels broke the International Convention [11] and forged the records on ballast water replacement in ship’s logs. Sustainable organisms of holo- and meroplankton alien to the Black Sea were revealed in ship ballast waters in 2004–2005. The finding of larvae of euphausiids in the caliptopis II and furcilia I stages was of greater interest (Fig. 2). The euphausiids are stenobiont organisms requiring an extremely exact environment, and that made their culturing practically impossible in vitro [28]. The ballast tanks of the Huntestern tanker were filled with water in the Limassol Port (Cyprus) on September 24th, 2004 when the ship was 5 days underway. The detection of live euphausiid larvae in ballast waters of that vessel demonstrated their ability to survive for rather a long time in ship tanks. Organisms are in their habitual environment, not only during transportation, but also after the dumping of ballast waters into the recipient water basin, as the water masses retained their parameters for some time. The comparative analysis of ship ballast water and biodiversity in the Novorossiysk Bay revealed key “risk groups” of invaders in the northeastern Black Sea. First

of all, these are Copepoda and Polychaeta. We recorded, for example, that the Prosky tanker dumped more than 85 million meroplankton at one time in the bay. The larvae of Black Sea alien polychaetes of the Spionidae family occurred repeatedly in ship ballast water. The density of the Streblospio sp. polychaetes revealed in the mouth of Tsemes River (Fig. 3) was 980 ind./m2 in 2001, and reached 9000 ind./m2 in 2007 [12]. A total of four species of this genus inhabit the World Ocean, and only Streblospio shrubsolii was recorded in the Black Sea (and some lakes at the Bulgarian coast). Species of the Streblospio genus dominate in eutrophied brackish water, survive in the organic enrichment of bottoms, and are often used as pollution markers. In the Novorossiysk Port the biocenosis of Streblospio sp. was located in the Tsemes estuary (depth 8–10 m, water salinity 12.9‰). This small worm, up to 10 mm in size, occupied the upper layer of silt substrate, with a smell of hydrogen sulfide. Deposits in the Tsemes estuary with a 11.6 cm3/kg methane content are highly toxic, this is an indirect indication of anaerobic processes and of an extremely unfavorable ecological situation [8]. The edaphic environment and hydrochemical regime in the Novorossiysk Port, apparently are favorable for the adaptation of larvae of the Streblospio sp. to a new environment and for development of a maternal bottom population.


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According to Aleksandrov [1], riverine estuaries and deltas are the most vulnerable locations in the Black Sea from the point of view of the invasion of new species. Ecosystem biodiversity and stability decreased there under the effect of pollution, and new ecological niches filled with invaders arose. The risk of invasion of species from the Mediterranean Sea (from which 62% of the ship ballast water comes) is the most probable in the Novorossiysk Bay (Fig. 4). In Novorossiysk, autumn blooms (up to 1600 ind./m3) of the copepod Oithona brevicornis, a new species of Black Sea fauna, inhabiting the coastal waters of tropical and temperate latitudes of the Mediterranean Sea in particular, may No. 3

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SELIFONOVA Atlantic Ocean, 0.5% North Europe, 1.5% Mediterranean Sea, 62%

Red Sea, South-East Asia, Indo-Pacific, 2% Black Sea, 34%

Fig. 4. The origin of the ballast water dumped by ships in the Novorossiysk Port (2004–2005).

0.2 mm Fig. 5. Oithona brevicornis from the samples taken in the Novorossiysk Bay.

North-eastern part, 29%

Northwestern part, 28% Crimea, 7%

Near-Bosporus region, 36% Fig. 6. The ratio of Mediterranean copepod species in various areas of the Black Sea, % from the total number of copepod species (after: [3, 17, 23; 24]).

serve as an illustrative example of such invasion [21]. The first burst of density of that species was registered in Novorossiysk in 2003 (Yu.A. Zagorodnyaya, pers. comm.); unfortunately, the data on their abundance and size–sexual structure is unavailable. In 2004, the present author found few mature individuals of O. brevicornis in the Port of Novorossiysk during the summer and autumn seasons. In October of 2005, the density of that species had increased up to 1600 ind./m3 and reached 500 and 1400 ind./m3, respectively in October and November of 2006 [12]. The length of O. brevicornis was 0.5–0.6 mm and 0.45 mm, for females and males respectively. The sexual structure of the copepod population varied those years. In October of 2005, females prevailed in the population; 50% of them had egg pouches. In October–November of 2006, 80–90% of the population were nonbearing females and copepodits in older stages; males and females with egg pouches occurred in small numbers (Fig. 5). In 2005 and 2006, the number of O. brevicornis increased by the end of autumn, in February–May the considered species did not occur. In September samples of 2007, only a few mature individuals of O. brevicornis, were revealed, and in October–December that species was not found in the plankton. The peculiarities of the dynamics of population development and the domination of copepodits in older stages and of females with significantly developed ovaries enabled us to assume that O. brevicornis forms a temporary population able to reproduce in the Novorossiysk Port. In the opinion of Beklemishev [2], the temporary or periodically arising dependent populations consisting of individuals that moved from independent populations of species in biotopes where conditions were favorable for species existence do not survive; upon the termination of the favorable period the individuals die. In the Novorossiysk Bay the distribution of O. brevicornis was confined to the locations of the dumping of ship ballast waters (the port and oil harbor Sheskharis), which corroborated its allochtonous origin. The literature [23] and our data demonstrated an increase of O. brevicornis during the autumn period in the ports of Sevastopol, Novorossiysk and Tuapse, which speaks for its ability to survive during a rather long time in the port areas. In turn, that allowed us to hypothesize that O. brevicornis can form an independent population in the Black Sea waters. We are reminded that 36 species of Mediterranean copepods were revealed in the Novorossiysk Bay for 2004–2005 [17] (Table 3). It is quite probable that many of the specified species are a casual find (were brought with ship ballast water). The total number of Mediterranean Copepoda found in the Black Sea has reached 100 taxa (Selifonova, Shmelev, unpublished data). About 30% of the finds fall on the northeast of the Black Sea (Fig. 6). Numerous finds of Mediterranean copepods in the west of the Black Sea are related to inflow through the Bosporus with water exchange [24]. However, water exchange is not only means of invasion


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Table 3. The list of Mediterranean species of Copepoda revealed in the Novorossiysk Bay 2004–2005 Genus (family): species Acartia (Acartiidae): A. josephinae Crisafi, 1974; A. negligens Dana, 1849. Calocalanus (Paracalanidae): C. pavoninus Farran, 1936. Centropages (Centropagidae): C. kröyeri Giesbr., 1892; C. violaceus (Claus, 1863). Clausocalanus (Clausocalanidae): C. furcatus (Brady, 1883). Corycaeus (Corycaeidae): C. furcifer Claus, 1863. Corycella (Corycaeidae): C. rostrata Claus, 1863. Euterpina (Tachydiidae): E. acutifrons (Dana, 1847). Microsetella (Ectinosomatidae): M. rosea Dana, 1847. Oithona (Oithonidae): O. brevicornis Giesbr., 1891; O. decipiens Farran, 1913; O. plumifera Baird, 1843; O. simplex Farran, 1913. Oncaea (Oncaeidae): O. clevei Fruchtl, 1923; O. conifera Giesbr., 1891; O. dentipes Giesbr., 1891; O. mediterranea (Claus, 1863); O. media Giesbr., 1891; O. minuta Giesbr., 1892; O. subtilis Giesbr., 1892; O. venusta Philippi, 1843; O. venusta venella Farran, 1929; O. vodjanitskii Shmel., Delalo, 1965; O. zernovi Shmel., 1966; Oncaea sp. Paracalanus (Paracalanidae): P. aculeatus Giesbr., 1888; P. indicus Wolfenden, 1905; P. denudatus Swell, 1929; P. nanus Sars, 1907; P. pygmaeus Claus, 1863. Paroithona (Oithonidae): Paroithona sp. Parvocalanus (Paracalanidae): P. crassirostris (Dahl, 1894). Pleuromamma (Phaennidae): P. gracilis (Claus, 1863). Saphirella (Clausidiidae): Saphirella sp. Temora (Temoridae): T. stylifera (Dana, 1849).

As a result of the monthly monitoring of ship ballast waters (March 2004–October of 2005), the first steps for the systematic study of alien species in the Novorossiysk Port were performed and a provisional technique for the monitoring of ship ballast waters was developed. The method included the investigation of ship ballast waters (determination of the salinity and density of the sea water) and ecosystem monitoring of the bay area (study of the plankton, benthos, and ichthyofauna), with subsequent assessment of the risk of invasive species [9, 10]. The chosen technique, along with hardening of the policies of the port authorities has led to an increase in the number of ships, which have taken measures on water ballast management. In 2004, the ship ballast water was completely replaced in more than 70% of all tankers, and in 2005 the number of such vessels reached 90% (Fig. 7). We remember that RUSSIAN JOURNAL OF MARINE BIOLOGY

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replacement of water ballast is obligatory in the Black Sea, if the ballast was taken outside of that region [11]. CONCLUSIONS Analysis of the obtained data enabled us to ascertain that the ballast water of commercial ships is the main source of ecological danger to the inland and territorial sea waters of Russia. Sampling and analysis of ballast water assays is one of the methods enabling the control of the occurrence of potentially dangerous organisms in the environment with the dumping of water ballast, and to assess the efficiency of actions on the management of these waters. The revelation of polychaetes of the Stre100 Ratio, %

of alien fauna into the basin. The significant number of Mediterranean species at ship routes and in the areas of large seaports of the Crimea and Caucasus are most likely possible to explain by their transfer with the ballast waters of commercial ships to these regions [12, 17, 20, 23, 27]. It is especially worth noting the species regularly occurring in plankton in the areas of the Ports of Sevastopol, Novorossiysk and Tuapse. These are Centropages kroyeri, Paracalanus indicus, P. aculeatus, O. brevicornis, O. decipiens, Oncaea media, O. mediterranea and O. venella. Biological invasion with ship traffic undoubtedly enhances the “mediterranization” of the Black Sea fauna, which can entail a change of the historically developed native faunistic complex.

80 60 40 20 0

III

V IV

VII IX XI III V VII IX VI VIII X II IV VI VIII X 2005 2004 Month

Fig. 7. The percentage of tankers that arrived in the Novorossiysk Port in 2004–2005 for loading, without replacement or with partial replacement of ballast waters (designated by black color). No. 3

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blospio genus in the Novorossiysk Port demonstrated the possibility of anthropogenic introduction of bottom fauna into the Black Sea basin. The invasion of Mediterranean species is the most probable risk; the key “risk groups” of such bioinvasion are copepods and polychaetes. In the Novorossiysk bay 36 species of Mediterranean copepods were recorded; the cyclopoid copepod Oithona brevicornis new to the Black Sea was revealed in mass quantity. Thus ship ballast waters can become a primary factor of the “mediterranization” of the fauna of copepods (Copepoda) in the northeast of the Black Sea. It is necessary to develop scientifically proven and obligatory techniques for ship ballast water control in the ports of Russia as soon as possible. This, in particular, would allow reconciliation of the issues of the International Convention for the Control and Management of Ship Ballast Waters and Sediments with the existing national sea and coastal management systems.

7.

8.

9.

10. 11.

ACKNOWLEDGMENTS This work was performed within the framework of the Program of Basic Research of the Department of Earth Science entitled The Environmental Status and Forecasting of Its Dynamics due to the Effects of Rapid Global Regional Natural and Social and Economic Changes, for 2009–2011 and the Ecological Invasions of Alien Organisms into the Barents and Black Seas, Development of Monitoring Technology, and the Ecosystem Modeling Projects, as well as the Forecasting During Investigation of Natural Resources under Conditions of an Arid Climate, Project 5.9.

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