New record of the planktonic copepod Oithona davisae Ferrari and Orsi in the Black Sea with notes on the identity of Oithona brevicornis

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1 Aquatic Invasions (2012) Volume 7, Issue 3: doi: The Author(s). Journal compilation 2012 REABIC Open Access Short Communication New record of the planktonic copepod Oithona davisae Ferrari and Orsi in the Black Sea with notes on the identity of Oithona brevicornis Alexandra Temnykh 1 * and Shuhei Nishida 2 1 Institute of Biology of the Southern Seas, 2, Nakhimov Ave., Sevastopol 99011, Ukraine 2 Atmosphere and Ocean Research Institute, University of Tokyo, Kashiwanoha, Kashiwa , Japan atemnykh@yandex.ua (AT), nishida@aori.u-tokyo.ac.jp (SN) *Corresponding author Received: 1 December 2011 / Accepted: 10 February 2012 / Published online: 27 February 2012 Abstract Specimens of small (< 1 mm) cyclopoid copepods of the genus Oithona were collected from Sevastopol Bay and an offshore area of the Black Sea. On the basis of a combination of characteristics such as those in the maxillule and the genital double-somite, the specimens were identified as O. davisae Ferrari and Orsi, The identity of O. brevicornis that was reported in the Black Sea and the possible origin of O. davisae in the Black Sea are discussed. Key words: Oithona davisae, species identification, ballast water, synanthropic introduction Introduction Reports since 2001 outline the occurrence of the cyclopoid copepod Oithona brevicornis Giesbrecht, 1891 (see also Giesbrecht 1893 ["1892"]), in the Black Sea (Zagorodnyaya 2002; Altukhov and Gubanova 2006; Gubanova and Altukhov 2007; Selifonova et al. 2008; Selifonova 2009). The identification was based on the examination of a few morphological characters, such as the shape of the head (rounded anteriorly) and rostrum (sharply pointed) and the numbers of s on segments 1 3 of legs 1 4 (with the formula of 1, 1, 3; 1, 1, 3; 1, 1, 3; 1, 1, 2) in the female (Zagorodnyaya 2002; Gubanova and Altukhov 2007). However, according to our recent examination of copepod specimens from the Black Sea, there is another species of Oithona that is similar to O. brevicornis with respect to the above features, but shows marked differences in some other characters. This further led us to suspect that the cyclopoid species recently recorded as new to the Black Sea may not be O. brevicornis, or include one or more species that resemble O. brevicornis. Here we describe the characteristics of the present specimens and compare them with those of O. brevicornis and other related species, and identify the species with notes on their distributions. Possible causes for the introduction of the species into the Black Sea are also discussed. Materials and methods Plankton samples were collected by verticallystratified tows of a Juday net (mouth area, 0.1 m 2 ; mesh size, 115 µm) from depth layers of , 65 40, 40 25, 25 10, and 10 0 m in an offshore area of the Black Sea (around N, E; depth, m) on November Samples were also collected by vertical tows of the same net (but with mesh size, 85 µm) from 5 m depth to the surface in Sevastopol Bay ( N, E; depth, 14 m) on 18 November Immediately after collection the samples were fixed and preserved in 4% formaldehyde/seawater solution and buffered with sodium tetraborate. Temperature and salinity of the sampling sites were measured with a hydrobiophysical complex SALPA (Vasilenko et al. 1997). In the laboratory, small adult females (< 1 mm) Oithona copepods that had a rounded anterior margin of the prosome and a sharply pointed rostrum were sorted from each sample. These specimens were put in a drop 425

2 A. Temnykh and S. Nishida Figure 1. Photographs of Oithona davisae collected from the Black Sea in the present study. A, rostrum, lateral view; B, mandible, focusing on setae on the endopod (arrows); C, maxillule, focusing on long distal-most (arrow) on the first inner lobe and the single seta (arrowhead) on the endopod; D, genital-and next somite, lateral view, showing absence of hair-rows on the dorsal surfaces (arrows). of 10% glycerine/distilled water on a depression slide, and total length measured from the anterior end of the prosome to the posterior end of the caudal ramus, excluding caudal setae, with a calibrated ocular micrometer, under a compound microscope. For detailed examination, appendages including the mandible, maxillule, and swimming legs, were dissected from the body trunk and examined at a magnification of 1000 with a 10 eyepiece and an oil-immersion objective lens ( 100); the Humes and Gooding's (1964) method was applied. Results The water column at the sampling site in Sevastopol Bay was vertically mixed with temperature and salinity of ca.16.5 С and 18 psu, respectively. In the offshore water the upper m was well mixed with temperature and salinity of ca.16.5 С and 17.5 psu. A marked thermocline existed in the m layer, where the temperature decreased with depth to 9 С and salinity increased to 18.3 psu. The targeted Oithona specimens were found in the samples from Sevastopol Bay and from the upper 65 m of the offshore area, but they were not recorded in samples from m. The following characteristics were common to all the present specimens: total length ranged from 0.50 to 0.59 mm (n=20); anterior margin of prosome was rounded in lateral view and ventrally terminated in a sharply pointed rostrum (Figure 1A; see also Figure 2H); the endopod of the mandible bore 4 setae (Figure 1B, arrows; see also Figure 2I); the distal on the first inner lobe of the maxillule was very long, ca. 2.5 times as long as the next (Figure 1C, arrow; see also Figure 2J, arrow); the endopod of

3 Oithona in Black Sea Figure 2. Character comparison between Oithona brevicornis (A-D), O. aruensis (E-G), and O. davisae (H-K). A, E, H: rostrum. B, F, I: mandible. C, G, J: maxillule; indicating distal-most (thin arrow) of first inner lobe, endopod (arrowhead), seta on second inner lobe (dotted arrow; absent in J) and seta on second basal segment (thick arrow; absent in J). D: genital double-somite and next somite, lateral view; indicating rows of hairs (arrows) in O. brevicornis. K: genital double-somite, lateral view. After Nishida (1985: A-D), Nishida and Ferrari (1983: E-G) and Ferrari and Orsi (1984: H-K). Not to scale. 427

4 A. Temnykh and S. Nishida Table 1. Comparison of characteristics in adult females among four species and the present specimens of Oithona. Species Oithona brevicornis Oithona wellershausi Oithona aruensis Oithona davisae Present specimens Total length (mm) Rostrum Number of setae on endopod of maxillule curved and sharply pointed curved and sharply pointed curved and sharply pointed curved and sharply pointed curved and sharply pointed Distal-most on first inner lobe of maxillule shorter than next > 2 times as long as next ca. 3 times as long as next ca. 2.5 times as long as next ca. 2.5 times as long as next Number of seta on second inner lobe of maxillule Number of seta on second basal segment of maxillule Hair-rows on dorsolateral surface of genital double-somite and next somite present absent absent absent absent Geographic distribution Indo-West Pacific Pearl River estuary (China) Indo-West Pacific East Asia, California, Chile, Mediterranean Black Sea Fine-scale distribution outer part of enclosed bays not available estuaries and inner part of enclosed bays estuaries and inner part of enclosed bays Sevastopol Bay and offshore water References Nishida et al. (1977), Ferrari (1981: as O. spinulosa), Nishida and Ferrari (1983), Nishida (1985) Ferrari (1981) Nishida and Ferrari (1983), Nishida (1985) Nishida et al. (1977), Ferrari and Orsi (1984), Nishida (1985), Hirakawa (1988), Saiz et al. (2003) This study the maxillule bore only one seta (Figure 1C, arrowhead; see also Figure 2J, arrowhead); there were no setae on the second inner lobe and the second basal segment of the maxillule (see Figure 2J, dotted- and thick arrows); the exopod segments 1 3 of legs 1 4 bore 1, 1, 3; 1, 1, 3; 1, 1, 3; 1, 1, 2 lateral s; there were no hair rows on the dorsolateral surface of the genital double-somite and/or the next somite (Figure 1D, arrows). The mean total length of the specimens from the Sevastopol Bay [0.568±0.018 mm (mean ±SD), n=10] was slightly larger than that of the offshore specimens (0.533±0.029 mm, n=10) (t-test, p<0.01), while there were no marked differences in other characters between the specimens from the two localities. Table 1 compares the characteristics of the present specimens with those of the four Oithona species, namely O. brevicornis (Figure 2A D; Nishida 1985), O. wellershausi Ferrari, 1981, O. aruensis Früchtl, 1923 (Figure 2E G; Nishida and Ferrari 1983) and O. davisae Ferrari and Orsi, 1984 (Figure 2H K). Characteristics such as body form (oval prosome with sharply pointed rostrum) and swimming legs (number of exopod s on legs 1 4: 1, 1, 3; 1, 1, 3; 1, 1, 3; 1, 1, 2) are similar. In all the characteristics listed in Table 1, the present specimens correspond with O. davisae, but not with the other species. Oithona brevicornis differs from the other species in that the distal-most on the first inner lobe of the maxillule is much shorter than 428

5 Oithona in Black Sea the next (much longer than the next in the other species: Figure 2C, G, J, thin arrows) and rows of fine hairs are present on the posterior dorsolateral surface of the genital double-somite and the anterior dorsolateral surface of the next somite (such rows are absent in the other species: Figure 2D, K, arrows). Oithona davisae differs from O. aruensis and O. wellershausi in having only one seta on the endopod [three setae in O. aruensis (Figure 2G, J, arrowheads) and O. wellershausi (figure not shown)] and lack of a seta on the second basal segment of maxillule [one seta present in O. aruensis (Figure 2G, J, thick arrows) and O. wellershausi (figure not shown)]. Oithona davisae also lacks a seta on the second inner lobe of maxillule while it is present in O. brevicornis and O. aruensis (Figure 2C, G, J, dotted arrows). From these observations we conclude that the present Oithona specimens are O. davisae. Discussion Oithona davisae has been reported from the coastal waters of Japan (e.g. Nishida et al. 1977, as O. brevicornis f. minor ; Nishida and Ferrari 1983, as O. aruensis ; Nishida 1985; Ohtsuka et al. 2008) and Korea (Lee et al. 2001; Orui- Sakaguchi et al. 2011), with its occurrences also being reported from California, the type locality (Ferrari and Orsi 1984), Chile (Hirakawa 1988), and the northwestern Mediterranean (Nishida s unpublished observation cited by Saiz et al. 2003). Kasyan (2010) reported the occurrence of O. davisae in the ballast water of ships that arrived at Vladivostok from Chinese coasts. With these records, it is widely accepted that O. davisae is originally endemic to the temperate coastal waters of East Asia and its occurrence in other remote regions are due to synanthropic introduction, mainly in ship s ballast waters, as proposed by Ferrari and Orsi (1984), Nishida (1985), and Hirakawa (1988) (e.g. Carlton 1987; Hooff and Bollens 2004; Cordell et al. 2008). In Puget Sound, US, O. davisae was found to be one of the most common and abundant nonindigenous organisms found in ships from both foreign and domestic ballast discharges (Cordell et al. 2009; Lawrence and Cordell 2010). In contrast, O. brevicornis and O. aruensis are distributed widely in the subtropical-tropical coastal waters of the Indo-Pacific (Giesbrecht 1891; Früchtl 1923; Wellershaus 1969; Nishida 1985), while the geographic distribution of O. wellershausi is still unknown except for the type locality (Pearl River estuary, China: Ferrari 1981). Records of the occurrence of O. brevicornis in the Mediterranean (e.g. Pesta 1920; Vaisierre and Seguin 1980; Shuvalov 1980) should be considered with caution, since these records are not accompanied with any descriptions of features that distinguish O. brevicornis from other related species (Nishida 1985). A revision of actual species should be carried out in the Mediterranean. There is also evidence that shows O. aruensis is an estuarine species while O. brevicornis is more stenohaline and distributed in more saline waters than the former, although their distributions may partially overlap (Table 1; Nishida 1985; Chew and Chong 2011). The water temperature and salinity at the collection sites (16 17 С, psu) and their yearly fluctuation in the surface waters of the Black Sea (6 25 С, psu: e.g. Ovsyaniy et al. 2000; Repetin et al. 2003; Ivanov et al. 2006; Kondrat yev 2010) are consistent with those in the temperate embaymental waters where O. davisae has been recorded (rather than in tropical-subtropical waters). In the Black Sea the occurrence of O. brevicornis has been reported mostly from near-shore waters, such as Sevastopol Bay (Zagorodnyaya 2002; Gubanova and Altukhov 2007) and Novorossiysk and Tuapse Ports (Selifonova 2009). Selifonova et al. (2008) reported the occurrence of O. brevicornis from open waters of the western Black Sea, but did not indicate exact localities nor abundance. Temnykh et al. (in press) observed, for the first time, high abundances (> 9000 ind. m -3 ) of O. brevicornis in an offshore area in the Black Sea off the Crimean Peninsula (depth: ca m). However, the specimens identified as O. brevicornis were re-examined and proved to be O. davisae. It is unknown whether the significant size difference in the specimens (collected during this research) between the two collection sites represents infraspecific variation due to different environmental conditions during development, or distinct populations with genetic differences; this invites a further study applying molecular genetics. In summary, this research and previous records strongly suggest that O. brevicornis that has been reported to be recently introduced into the Black Sea is indeed O. davisae. The true absence of the species before 2001 should be confirmed on the basis of a retrospective analysis 429

6 A. Temnykh and S. Nishida of samples covering areas of the Black Sea from bays to offshore waters. If we assume the absence of O. davisae from the original Black Sea fauna, the following hypotheses may be proposed for the introduction of O. davisae from the coastal waters of East Asia: (1) direct introduction from East Asia in ships ballast waters (as in the cases of, e.g. the veined Rapa whelk Rapana venosa, the shrimp Palaemon macrodactylus and the blood cockle Anadara inaequivalvis: Skolka and Preda 2010) ; (2) secondary introduction of the Mediterranean populations, which were introduced and settled in some regions of the Mediterranean (such as those in Barcelona, Saiz et al. 2003), either by the copepods dispersal along coastal waters through the Turkish Straits System, which act as a strong barrier for many species (Oguz and Öztürk 2011) (e.g. the pelagic copepod Acartia tonsa: Kovalev et al. 1998; see also Oguz and Öztürk 2011 for examples from other animals), or in ships ballast waters (see Selifonova 2011 for copepod examples). However, the possibility cannot be ruled out that O. brevicornis and O. aruensis (or one of them) may have also been introduced into the Black Sea, if we consider the wide distribution of these species in the coastal waters of the Indo-Pacific region and the potential for their introduction in ships ballast waters from the countries where these species are distributed and where the ports of origin may be located. For a better understanding of the current status of the Oithona species in the Black Sea and the history of their introduction, it is necessary to re-examine the samples previously collected from the Black Sea, directly examine the copepod species in ballast waters of ships arriving at ports in the Black Sea, and inquire into the historical records of the ships origins and destinations, on the basis of precise species identifications. Acknowledgements The authors would like to express their sincere gratitude to Dr. Yuri N. Tokarev, Dr. Victor V. Melnikov and Dr. Julia A. Zagorodnyaya for providing the information on temperature and salinity, and for their help in sampling and other field activities. Special thanks are due to Dr. Frank D. Ferrari and two anonymous reviewers for their invaluable advice on the manuscript and Dr. Monica Sullivan for editing the English text. Publication of this paper was supported by the EC 7th Framework Programme through the envirogrids project (Grant Agreement No ). References Atukhov DA, Gubanova AD (2006) Oithona brevicornis Giesbrecht in the Sevastopol Bay in October, 2005-March, Morskoy Ekologicheskiy Zhurnal (Marine Ecology Journal) 5: 32 Carlton JT (1987) Patterns of transoceanic marine biological invasions in the Pacific Ocean. Bulletin of Marine Science 41: Chew LL, Chong VC (2011) Copepod community structure and abundance in a tropical mangrove estuary, with comparisons to coastal waters. 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