Establishment of Oithona brevicornis Giesbrecht , 1892 ( Copepoda : Cyclopoida ) in the Black Sea

Long-term, regular studies of coastal plankton communities were resumed in 2002, based on bi-weekly plankton casts at three stations located within and adjacent to Sevastopol Bay, Crimea, northern Black Sea. In October 2005 two adult females of Oithona brevicornis were initially discovered in a sample taken during a routine plankton survey. Within one month after this discovery O. brevicornis began to appear in the samples regularly. In November 2005 the total abundance of O. brevicornis exceeded 1000 ind./m in the central part of the Bay. From April 2006, O. brevicornis disappeared completely from net catches and was absent until July 2006 when this species reappeared. The peak abundance of this species – 42667 ind./m – was recorded at the central station within the Bay at the end of October 2006. The possible route of invasion and the seasonal dynamics of this new copepod species in the Black Sea coastal region are discussed.


Introduction
Sevastopol Bay in southwestern Crimea, Ukraine is about 7000 m long and 850 m wide, with an average depth of 12 m.It receives freshwater input from the Chernaya River.Oithona brevicornis Giesbrecht, 1892 (Figure 1) is widespread in the tropical and temperate Pacific, Indian and Atlantic oceans (Shuvalov, 1980;Razouls et al., 2005Razouls et al., -2007)), where it can be abundant in shallow coastal waters.
This euryhaline marine copepod is common in estuarine and brackish waters and may occur in low salinity (10-13‰) waters (Deevey, 1948).O. brevicornis had not previously been reported from the Black Sea and Sea of Azov.So, special attention was paid to the study of the ecology of O. brevicornis in a new habitat for this species.

Materials and Methods
Samples of zooplankton were collected during 2005-2006 from two stations located in Sevastopol Bay and one station located outside (Figure 2).
Samples were typically collected by vertical hauls through the whole water column (from bottom to the sea surface) using a Juday plankton net (mouth area 0.1 m 2 and mesh size 150 µm).Samples were taken in the morning usually biweekly and were fixed with 4% formaldehyde solution and subsampled.Zooplankton counts were made under a MBS-9 stereomicroscope in Bogorov counting chamber.Copepods of all developmental stages (I-VI copepodite stages) were identified to species using the taxonomic keys of Shuvalov (1980).Abundance was calculated per cubic meter.Appendages were dissected under a stereomicroscope and mounted in microscope slides for detailed examination.

Results
Only two of 44 species of the genus Oithona Bair, 1843, presently known in the World Ocean (Razouls et al. 2005(Razouls et al. -2007)), were native in the Black Sea: Oithona nana Giesbrecht, 1892 and O. similis Claus, 1866.Detailed descriptions of the species belonging to Oithona were given by Shuvalov (1980) and by Nishida (1985).Specieslevel identification is rendered more difficult by the small size of these copepods.Fortunately, the two native Black sea species of Oithona and invader O. brevicornis differ markedly in the shape of the head and rostrum (Figure 3).
A brief comparison of the head and rostrum of these three Oithona species is given below: -O. nana: head narrow, truncate anteriorly in dorsal view; rostrum blunt and not visible dorsally.
-O. brevicornis: head rounded anteriorly in dorsal view; frontal margin produced ventrally into sharply pointed, slightly curved rostrum, readily visible in lateral view.
-O. similis: head anteriorly abruptly blunt or slightly rounded; rostrum ventrally directed, sharply pointed and not visible dorsally.
In Sevastopol Bay the body lengths of these three species varied as follows: -O. nana: female 0.5 -0.53 mm; male 0.48 -0.51 mm.
Oithona similis is a cosmopolitan species widespread in the World Ocean.According to Shuvalov (1980), in the tropical zones these copepods occur mostly in areas influenced by coldwater currents.In the Black Sea O. similis represents the coldwater copepod complex (Greze 1971).
Krichagin (1873) was the first to find O. nana in the Black Sea and he described it as O. minuta Krichagin, 1873.Later, Giesbrecht (1892), unacquainted with Krichagin's paper, described the same copepod as O. nana.These two species are synonyms (Karavaev 1895), but O. minuta T. Scott, 1894 is a separate species.O. nana is a eurythermic species that is widespread in the World Ocean (Nishida 1985, Razouls et al. 2005-2007).Until the late 20th century it was among the most abundant copepods in the neritic zone of the Black Sea (Greze 1971).Since the 1990s, O. nana has not been found there (Gubanova et al. 2002).
Throughout the period of study the abundance of O. brevicornis gradually increased in the central locations compared to the mouth of the Bay.At the station outside the Bay (in more than 40 m water depth), the abundance of O. brevicornis was considerably less than inside the Bay, over the entire period of study.

Discussion
As other recent pelagic invaders -the copepod Acartia tonsa Dana, 1849, ctenophores Mnemiopsis leidyi A. Agassiz, 1865 and Beroe ovata Bruguiere, 1789 (Pereladov 1983, Belmonte et al. 1994, Konsulov and Kamburska 1998, Gubanova 2000) -O.brevicornis was most probably brought into Sevastopol Bay in the ballast water of a ship.Accessibility or low resilience of the native zooplankton community to O. brevicornis invasion was possibly preconditioned by earlier invasions of the predatory ctenophores M. leidyi and B. ovata.The unexpected, but highly destructive invasion of M. leidyi into the Black Sea in the early 1980s extremely increased grazing pressure on plankton in the late 1980s -early 1990s, especially during summer and autumn (Gubanova et al. 2002).As a result, some indigenous species, including O. nana with its peak abundance during autumn, disappeared completely from the community.The abundance of other species dropped drastically at the same time.In the late 1990s, due to the accidental invasion of the comb-jelly predator B. ovata, consuming M. leidyi, its mass development time decreased considerably and reduced the grazing pressure on the plankton during summer and autumn (Gubanova 2003).Therefore, we infer that the establishment success of O. brevicornis is due to the loss of O. nana, an ecologically closely similar and closely related species that vanished from plankton, and to the reduced predation impact of M. leidyi upon copepods that reproduce in autumn.
Based on the 20-year (1976-1996) study completed in the Sevastopol Bay, it was hypothesized (Gubanova et al. 2002) that the unstable state of zooplankton community during 1989-1990s might force further changes in the copepod population structure and species composition.Our investigation confirms this prediction.

Conclusions
The establishment of the copepod O. brevicornis in the Black Sea is reported.Most probably, this copepod, formerly unknown in the Black Sea, was transported to this region in the ballast waters of a ship.In the Black Sea O. brevicornis occupies coastal areas.The peak abundance of O. brevicornis in Sevastopol Bay was registered in October 2006.Most likely, O. brevicornis will be the dominant copepod species in the Sevastopol Bay in autumn.In the middle of the Bay this species dominated in copepod community from mid-September to mid-December 2006, whereas at the mouth of the bay -only from mid-September to late October 2006.

Figure 1 .Figure 2 .Figure 3 .
Figure 1.O. brevicornis Giesbrecht 1892: A. female, dorsal view; B. male, dorsal view (from sample taken in the central part of Sevastopol Bay in October 2006) but this discovery appeared to represent an isolated record.New specimens were found in Sevastopol Bay only four years later: two adult females of O. brevicornis were found at stations 2 and 3 (one at each station) in October 2005.Two months later, at the end of December 2005 more than 2000 ind/m 3 of O. brevicornis in the central and coastal areas of the Bay were found (Figure4).

Figure 4 .
Figure 4. Seasonal variation in O. brevicornis abundance at two stations in Sevastopol Bay: 1 -central part of Bay; 2mouth of Bay

Figure 5 .
Figure 5. Seasonal changes of contribution (%) of O. brevicornis to total copepod abundance at two stations in Sevastopol Bay: grey bars: station 2; black bars: station 3 (no data for 29 September 2006)