• Sonuç bulunamadı

First distribution record of the invasive copepod Oithona davisae Ferrari and Orsi, 1984, in the coastal waters of the Aegean Sea

N/A
N/A
Protected

Academic year: 2021

Share "First distribution record of the invasive copepod Oithona davisae Ferrari and Orsi, 1984, in the coastal waters of the Aegean Sea"

Copied!
9
0
0

Yükleniyor.... (view fulltext now)

Tam metin

(1)

Marine Ecology. 2019;40:e12548. wileyonlinelibrary.com/journal/maec  

|

  1 of 9 https://doi.org/10.1111/maec.12548

© 2019 Blackwell Verlag GmbH

1 | INTRODUCTION

The Mediterranean Sea is a hotspot heavily exposed to nonin‐ digenous invasion (Rilov & Galil, 2009). Particularly, the eastern Mediterranean Sea is sensitive to invasion due to its geographic po‐ sition between Ponto‐Caspian and Indopacific areas, the latter via the Red Sea, where maritime traffic is crowded through the straits of Gibraltar, Dardanelles and the Suez Canal, and where mariculture treatments are existent (Galil & Zenetos, 2002; Zenetos et al., 2011). A total of 821 alien species were introduced to the Mediterranean Sea, and majority of them have been established in the Mediterranean ecosystems (Zenetos et al., 2017). Among the 50 alien zooplankton species that were recorded in the Mediterranean Sea, only 12 co‐ pepod species were established in this region (Zenetos et al., 2005). In recent years, the number of introduced alien copepod species in‐ creased, and there have been new additions day by day (Olazabal & Tirelli, 2011; Ounissi, Laskri, & Khelifi‐Touhami, 2016; Terbıyık Kurt,

2018; Zagami, Costanzo, & Crescenti, 2005; Zenetos et al., 2012). According to a recent study, 18 alien Copepoda species were found in the Mediterranean coast of Turkey; six of them were reported in the coast of the Aegean Sea (Bakir et al., 2014).

Small marine pelagic copepods are the most abundant meta‐ zoans on Earth (Turner, 2004). Specifically, oithonids are among the most abundant copepod species. Their worldwide distribu‐ tion extends from the polar region to the equator, oligotrophic to eutrophic waters, and open seas to coastal waters (Gonzalez & Smetacek, 1994; Paffenhofer, 1993). The small invasive cope‐ pod Oithona davisae Ferrari & Orsi, 1984, prefers neritic waters (Uchima, 1988), and the species is highly abundant in coastal and estuarine regions (Hirota, 1990; Nishida, 1985). This species was first described in the Sacramento–San Joaquin Estuary (Ferrari & Orsi, 1984), and since its discovery, it has been reported in dif‐ ferent parts of the world (Razouls et al., 2015–2019). The species has also been considered native to the coastal waters of East Asia, Received: 19 October 2018 

|

  Revised: 24 April 2019 

|

  Accepted: 13 May 2019

DOI: 10.1111/maec.12548

S H O R T C O M M U N I C A T I O N

First distribution record of the invasive copepod Oithona

davisae Ferrari and Orsi, 1984, in the coastal waters of the

Aegean Sea

Tuba Terbıyık Kurt

1

 | Şengul Beşiktepe

2

1Department of Marine Biology, Faculty of Fisheries, Çukurova University, Adana, Turkey

2The Institute of Marine Sciences and Technology, Dokuz Eylul University, İzmir, Turkey

Correspondence

Tuba Terbıyık Kurt, Department of Marine Biology, Faculty of Fisheries, Çukurova University, Adana, Turkey.

Emails: tterbiyik@cu.edu.tr and tubaterbiyik@gmail.com Funding information

Ministry of Environment and Urbanization/ General Directorate of EIA, Grant/Award Number: ctue.17.2113; Izmir Metropolitan Municipality General Directorate of Water and Sewage Administration, Grant/Award Number: DBTE‐199, 2015

Abstract

The occurrence of the invasive nonindigenous copepod Oithona davisae Ferrari and Orsi, 1984, is reported for the first time in the Aegean Sea. The data we collected in August 2017 from 14 stations along the Turkish coast of the Aegean Sea reveal the spatial distribution of O. davisae between the openning of the Dardanelles Strait in the north and the Izmir Bay in the south. The O. davisae individuals, in seven meso‐ zooplankton samples collected from a single station, were consistently found in the inner part of the Izmir Bay from April 2015‐October 2016. The abundance of female

O. davisae ranged from 4 ind./m3 in April 2015 to 31,524 ind./m3 in July 2016 and

contributed to the total oithonid female population by 10.8% in April 2015 and 92.8% in September 2016. Our results show that this species is well established in the inner part of Izmir Bay and that it has become a permanent component of the copepod community in the area.

K E Y W O R D S

(2)

particularly around Japan (Nishida, 1985) and China (Razouls et al., 2015–2019), and most abundant in eutrophic areas like Tokyo Bay (Nagasawa & Marumo, 1984), Hiroshima Bay (Uye, Ayaki, & Onbe, 1992) and Ariake Bay (Hirota, 1990). The species has also been found to be invasive along the San Francisco coasts (Ferrari & Orsi, 1984), in the Barcelona port (Saiz, Calbet, & Broglio, 2003), in the Wadden Sea (North Sea; Cornils & Wend‐Heckmann, 2015) and in the Black Sea (Altukhov, Gubanova, & Mukhanov, 2014). Zagorodnyaya (2002) reported this species in the Black Sea after continuously observing it in several areas (Gubanova & Altukhov, 2007; Mihneva & Stefanova, 2013; Temnykh & Nishida, 2012; Üstün & Terbıyık Kurt, 2016; Yıldız, Feyzioğlu, & Beşiktepe, 2017). Few specimens of O. davisae were observed in 2008 in Marmara Sea (Kurt, 2016), and a high abundance of the species was re‐ ported in September 2014 in Büyükçekmece Bay of the Marmara Sea (Doğan & İşinibilir Okyar, 2016). This species was recognized in 2000 in the Barcelona Port (Razouls et al., 2015–2019; Saiz et al., 2003) in the western Mediterranean Sea, and it was recently reported in Lakes Faro and Ganzirri in the central Mediterranean Sea (Zagami et al., 2018) and in the Venice Port in the eastern Mediterranean Sea (Vidjak et al., 2018).

This study reports the first record of O. davisae in the Aegean Sea, describes its expansion along the Turkish coast of the Aegean Sea as well as its seasonal variation in the inner part of the Izmir Bay, compares its relative abundance with that of the indigenous Oithona

nana and discusses the possible mechanisms behind their introduc‐

tion in the study area.

2 | MATERIALS AND METHODS

2.1 | Study area

The Aegean Sea is a distinct sub‐basin at the eastern Mediterranean Sea, connected through the Cretan Straits with the Ionian and Levantine Seas in the south and through the Dardanelles Strait with the Marmara Sea in the north. Although the Aegean Sea has a lot of bays and capes, its eastern part has a narrow continental shelf, and it is rugged in terms of bottom structure. Its hydrographical charac‐ teristics are influenced by the water masses coming from the Black Sea in the northwest and the Levantine Sea in the southwest and by the atmospheric forcing, which leads to the formation of new water masses and the driving of circulation (Beşiktepe, 2015). The Aegean Sea exhibits an oligotrophic character, which varies horizon‐ tally with the nutrient concentrations and biological resources that are higher in the north–northwest Aegean Sea than in the south– southeast Aegean Sea (Stergiou, Christou, Georgopoulos, Zenetos, & Souvermezoglou, 1997). Moreover, the surface outflow of water from the Black Sea to the northeast Aegean Sea is enriched with dis‐ solved organic carbon and dissolved organic nitrogen (Lykousis et al., 2002; Polat & Tugrul, 1996).

Positioned in the central Aegean Sea, Izmir Bay has three dis‐ tinctive parts in terms of their physical characteristics: outer, middle and inner. Its depth decreases gradually from the outer bay (80 m)

to the inner bay (10 m). Maximum temperature values and strong thermal stratification have been observed during summer. Water column is almost homogenous because of the surface cooling and vertical mixing induced by the winds during winter. The freshwater input during winter and spring, and evaporation during summer af‐ fect the seasonal variation in surface salinity (Eronat & Sayin, 2014; Sayın, 2003). The low salinities were observed around freshwater in‐ puts such as the Gediz, Melez, Ilıca, Narlı, Bornova, Bostanlı, Manda and Poligon Rivers in the Izmir Bay (Akinci, Guven, & Ugurlu, 2013; Özkan, Büyükışık, & Sunlu, 2013). A significant amount of freshwater discharge in the form of wastewater is the main cause of low salin‐ ity both in summer and winter in the inner İzmir Bay (Küçüksezgin, Kontas, Altay, Uluturhan, & Darilmaz, 2006). Heavy urbanization, in‐ dustrial development and maritime traffic resulted in the increased pollution of the bay (Gürü, Beyazıt, & Öksüz, 2006; Küçüksezgin et al., 2006; Lemenkova, 2016). Izmir Bay exhibits a pronounced trophic gradient which is eutrophic in the inner part and oligotrophic in the outer part, where the bay merges with the Aegean Sea. The high lev‐ els of discharge of organic and inorganic nutrients through the rivers, streams, local coastal and diffusive sources result in the eutrophica‐ tion of the inner bay (Kontaş, Kucuksezgin, Altay, & Uluturhan, 2004; Küçüksezgin et al., 2006; Kükrer & Büyükişik, 2013). Therefore,

(3)

plankton composition and diversity notably differ in the inner and the outer bay. Although mesozooplankton studies have been carried out intensively in Izmir Bay, published data are very limited and are presented only as the presence or absence of species. Aker (2015) reported that Acartia clausi and O. nana dominated the copepod community in the inner bay during winter and spring, whereas the

Paracartia grani and Centropages kroyeri dominated in summer and au‐

tumn. Another calanoid copepod, Paracalanus parvus, was observed in all seasons in the inner bay (Sunlu et al., 2005). The oithonids common in the middle and outer parts of the bay are Oithona similis, Oithona se‐

tigera and Oithona plumifera (Besiktepe, unpublished data). Copepod

richness increases from the inner to the outer part of the bay. Among the Corycaeidae, C. brehmi was the only species observed in the inner bay, whereas Corycaeus clausi, Corycaeus limbatus, Corycaeus typicus,

Corycaeus furcifer, Corycaeus giesbrechti and Farranula rostrata were

reported in the outer bay (Sever & Mavili, 2002).

2.2 | Mesozooplankton sampling

Zooplankton was collected during the routine mesozooplankton sur‐ vey cruises. Two different data sets were used to show the seasonal variation and spatial distribution of O. davisae. With the first data set, we examined the seasonal variation of the species by reanalysing the zooplankton samples collected from a single station (stA) in the inner Izmir Bay (Figure 1) from April 2015‐October 2016 (Table 1).

With the second data set, we determined the spatial distribution of the species in the Aegean Sea through the samples obtained during an oceanographic cruise from 19 to 25 August 2017. The mesozoo‐ plankton samples for the second data set were collected from 14 stations along the Turkish coast of the Aegean Sea, located from the Enez coast in the north to the Gökova Bay in the south (Figure 1). In both of the data sets, the zooplankton samples were vertically col‐ lected with WP2 net (mouth diameter: 57 cm; mesh size: 200 µm) in the epipelagic layer (200 m) of the sea. The vertical tows were made 3–4 m above the bottom to the surface in stations located in the continental shelf area (<200 m; Table 1). Except in the shal‐ low stations (<20 m), the zooplankton samples were collected from two distinct layers: above thermocline (AT) and below thermocline (BT), to cover the thermal stratification of the sea. After their col‐ lection, the samples were preserved in 4% borax‐buffered for‐ maldehyde. The subsamples for first data set were collected using wide‐bore plastic pipettes. Depending on the zooplankton density, 250–950 individuals were counted and identified at the species or taxon level. Duplicate subsampling was done whenever the number of individuals collected was less than 100. Filtered volume of the net was determined using flowmeter during the sampling period. The sea surface salinity and temperature were measured using SBE 37‐SM MicroCAT. Stereo microscopes (ZEISS Discovery V12) and light microscopes (ZEISS Primovert) were used for the taxonomic identification of the samples. The subsamples for the second data

Station No Data set Sampling date Locations Total depth (m) Sampling layer (m) Longitude (E) Latitude (N) A First 29.04.2015 27.1358 38.4500 10 0–6 A First 15.09.2015 27.1358 38.4500 10 0–6 A First 12.11.2015 27.1358 38.4500 10 0–6 A First 03.02.2016 27.1358 38.4500 10 0–6 A First 10.03.2016 27.1358 38.4500 10 0–6 A First 21.07.2016 27.1358 38.4500 10 0–6 A First 26.10.2016 27.1358 38.4500 10 0–6 B1 Second 19.08.2017 26.0238 40.7053 17) 0–13.5 B2 Second 18.08.2017 26.8000 40.6050 44 0–10; 11–44 B3 Second 19.08.2017 26.1503 39.9540 18 0–16 B4 Second 19.08.2017 25.9950 39.4132 308 0–10; 14–246 B5 Second 20.08.2017 26.4808 39.4040 99 0–10; 10–95 B6 Second 21.08.2017 26.9513 38.8213 20 0–15 B7 Second 21.08.2017 27.0567 38.4307 12 0–7 B8 Second 22.08.2017 26.3190 38.7638 223 0–10; 11–216 B9 Second 22.08.2017 26.4391 38.4215 65 0–16; 17–65 B10 Second 22.08.2017 26.3308 38.0855 366 0–10; 10–210.5 B11 Second 23.08.2017 27.2557 37.9440 40 0–10; 10–36 B12 Second 23.08.2017 27.2027 37.4200 32 0–10; 10–28 B13 Second 24.08.2017 27.4881 37.2417 37 0–10; 10–32 B14 Second 25.08.2017 28.1527 37.0022 67 0–10; 10–62

TA B L E 1   Sampling information for

(4)

set were obtained using Folsom Splitter. Two aliqouts were counted and examined under Olympus SZX16 and Leica CME. The number of counted individuals was determined based on the zooplankton den‐ sity of the samples. Approximately 500 mesozooplankton individu‐ als were counted in high‐density samples. The species description by Temnykh and Nishida (2012) was used to identify O. davisae in both data sets, but only the females of O. davisae and O. nana could be identified. Copepod abundance was calculated as ind. (individuals)/ m3 in both data sets.

3 | RESULTS

3.1 | Seasonal variation in the inner İzmir Bay

The seasonal variation in the sea surface temperature and salinity at station stA in the inner Izmir Bay is illustrated in Figure 2. The sur‐ face temperature ranged from 11.4°C in February to 26.9°C in July. The highest salinity (39.7 ppt) was observed in July and October, and the lowest (37.4 ppt) was in March because of high freshwater input.

Two oithonid species, O. davisae and O. nana, were observed in the area. The relative contribution of the cyclopoids to the cope‐ pod abundance ranged from 36% in March to 100% in April. The maximum abundance of cyclopoids (44,410 ind./m3) was observed

in July, corresponding to 99% of the total copepod abundance (Figure 3). The abundance of oithonid copepods varied from 45 ind./ m3 in April 2015 to 8,867 ind./m3 in July 2016. Their contribution

to the oithonids ranged from 1% in September 2015 to 55% in April 2015. The total oithonid male abundance ranged from 49 ind./m3 in

March 2016 to 943 ind./m3 in July 2016. They were not observed in

the April and November 2015 samples, and their maximum contri‐ bution to the total oithonids was ≤10% (Figure 3). Only the female individuals were identified to the species level. Moreover, due to the low contribution of the oithonid males, only the seasonal cycle of the females could be characterized through their abundance. The abundance of the female O. davisae ranged from 4 ind./m3 in April

2015 to 31,524 ind./m3 in July 2016 (Figure 3). High abundance

values were observed during the summer months (September, July) and in the winter (February). This species contributed approximately 11% to the total oithonid females in April 2015, and their contribu‐ tion in the subsequent sampling periods was higher, exceeding 90% in summer and early autumn (Figure 3). The abundance of O. nana females with similar niche characteristics (Altukhov et al., 2014; Zagami et al., 2018) ranged from 20 to 3,076 ind./m3. In general,

the ratio of female O. davisae to female O. nana was quite high, >10 in warmer periods (Table 2). In spring (April, March), O. nana had higher abundance values than O. davisae (Table 2).

F I G U R E 2   Temperature and salinity

values in the sampling periods in inner İzmir Bay (st.A) 36 36.5 37 37.5 38 38.5 39 39.5 40 0 5 10 15 20 25 30

Apr. 15 Sep. 15 Nov. 15 Feb. 16 Mar. 16 Jul. 16 Oct. 16

Station A

T emperature Salinity

ppt C

o

F I G U R E 3   (a) Seasonal variations in

oithonids, other copepod abundance. (b) Proportion of Oithona davisae (♀),Oithona

nana (♀), Oithona copepodit and Oithona

(5)

3.2 | Spatial distribution in the Aegean Sea

The coast of the Turkish Aegean Sea was surveyed to determine the spatial distribution of O. davisae (Figure 1). The species was observed in the four stations: stB3, stB7, stB8 and stB9 (Figure 1 and Figure 4) but not in the southern stations (stB10 to stB14). Samples were col‐ lected from both layers, AT and BT, but O. davisae was observed only in the AT layer. The abundance of O. davisae females ranged from 0.24 ind./m3 (stB3) to 121 ind./m3 (stB7; Figure 4) in August 2017 in

the AT layer. The contribution of this species to the oithonid female population was higher in the inner İzmir Bay (98.2% in stB7) and the Karaburun coast (61.5% in stB8) than other stations (Figure 5). In the rest of the stations, the contribution was below 9.5% (Figure 4).

O. nana was observed in most of the stations both in the AT and BT

layers. The contribution of O. nana was generally low (at most 38.5% in the Karaburun coast; Figure 5), and the abundance of this species varied from 0.29 ind./m3 (st1) to 25 ind./m3 (st13) in the AT layer

(Figure 4).

4 | DISCUSSION

So far, 15 oithonid species were reported in the Aegean Sea (Razouls et al., 2015–2019). Among these species, only eight were observed in the Turkish coast of this basin (Bakir et al., 2014; Ministry of Environment & Urbanization, TUBITAK‐MRC, 2018; Sever, 2009).

O. davisae is becoming a permanent member of the copepod com‐

munities in the Turkish coast of the Black and Marmara Seas, but in this study, we also observed the species in the in the coastal waters of the Aegean Sea, where the total number of the oithonid species (n = 9) has increased.

The spatial distribution of O. davisae was restricted between the opening of the Dardanelles Strait in the north and the İzmir Bay in the south in the Aegean coast of Turkey. The presence of O. davisae near the opening of the Dardanelles Strait suggests that it may have passed through the Black Sea surface flow from Marmara to the Aegean Sea. Indeed, the northern Aegean Sea is affected by surface current coming from the Black Sea through the Turkish Strait System (Tuğrul, Beşiktepe, & Salihoglu, 2002). However, the presence of the

international harbour in the Izmir Bay suggests that the individuals may have been transported by ballast waters from different regions and may have dispersed from the bay to the adjacent stations such as the Karaburun and Ildır coasts. In many studies, it is emphasized that the main route of this species is ballast waters (Cordell, Bollens, Draheim, & Systema, 2008; Cornils & Wend‐Heckmann, 2015; Vidjak et al., 2018; Yıldız et al., 2017). The invasive O. davisae has successfully settled in transitional ecosystems, such as Lakes Faro and Ganziri and the Golden Horn Estuary (Isinibilir, Svetlichny, & Hubareva, 2016; Zagami et al., 2018), and has dominated zooplank‐ ton communities with their increasing numbers in certain periods (Zagami et al., 2018).

The abundance of O. davisae was high in the summer months (September, July) and in February in the inner Izmir Bay. This spe‐ cies is thermophilic (Svetlichny et al., 2016); they are generally most abundant during the warmer periods and least abundant during win‐ ter and early spring in their habitats (Altukhov et al., 2014; Mihneva & Stefanova, 2013; Seregin & Popova, 2016; Üstün & Terbıyık Kurt, 2016; Uye & Sano, 1998; Yıldız et al., 2017; Zagami et al., 2018). However, in the south of San Francisco Bay, O. davisae was most abundant only during autumn particularly in October and November (Ambler, Cloern, & Hutchinson, 1985). In the Fukuyoma Harbour, the abundance of this species was lowest from March to April. Their abundance increased only after this period peaking by mid‐ June and decreased thereafter until late winter (Uye & Sano, 1995). Variations in the population density of O. davisae showed clear sea‐ sonal cycle in the Sevastopol Bay, where the total abundance of the species was proportionally low within the middle spring and late summer; it increased until late autumn and dramatically decreased until mid‐February to March after the previous period (Svetlichny, Hubareva, & Işinibilir, 2018). The highest abundance of O. davi‐

sae in many regions of the Black Sea was reported during summer

until autumn (Altukhov et al., 2014; Gubanova & Altukhov, 2007; Mihneva & Stefanova, 2013; Üstün & Terbıyık Kurt, 2016; Yıldız et al., 2017). Its highest abundance occurred in late spring to early sum‐ mer in Lakes Faro and Ganzirri (Zagami et al., 2018). O. davisae has become a component of the copepod communities in the Wadden Sea (Cornils & Wend‐Heckmann, 2015), and the temperature of the study area where the species was found has dropped to −1.8°C (Cornils & Wend‐Heckmann, 2015). Although O. davisae is a ther‐ mophilic species, their females have a unique adaptive strategy to deal with cold waters (Svetlichny et al., 2016). Doğan and İşinibilir Okyar (2016), using 200 µm net, reported the highest abundance of O. davisae in August (1,175 ind./m3) and September 2014 (1,999

ind./m3) in the Büyükçekmece Bay of the Marmara Sea. The abun‐

dance values of O. davisae obtained in the present study cannot be compared directly with those in the literature because of the larger mesh size of the zooplankton net that we used. It is not suitable for small species and, hence, may underestimate the count. However, the data from this study provide an idea of the spatial distribution and the relative seasonal variation of the species within the mesozo‐ oplankton communities. Because of the similar mesh size used, we attemped to compare the abundance of O. davisae in the Izmir Bay

TA B L E 2   Seasonal variations of the ratio of female abundance

values of Oithona davisae to Oithona nana and percentage of

Oithona davisae in total copepods in the İzmir inner Bay

Sampling

date O. davisae/O. nana

Percentage of O. davisae female in total copepod (%)

Apr−2015 0.1 5.0 Sep−2015 11.5 53.6 Nov−2015 7.0 26.2 Feb−2016 7.2 42.2 Mar−2016 0.7 13.8 July−2016 10.2 70.3 Oct−2016 10 40.2

(6)

with that in the Büyükçekmece Bay (Doğan & İşinibilir Okyar, 2016). The relative abundance in the Izmir Bay was much higher than that in the Büyükçekmece Bay. Trophic status and components of the bays can affect the abundance. The effects of abundance, food types and predators on the seasonal succession and distribution of O. davisae in different habitats have been discussed in literature (Svetlichny et al., 2018; Uye & Sano, 1995).

The high feeding threshold of this species supports its acclima‐ tization in different habitats such as inshore waters, bays and es‐ tuaries with high food concentrations (Almeda, Augustin, Alcaraz, Calbet, & Saiz, 2010; Uye & Sano, 1995; Zagami et al., 2018). Zagami et al. (2018) stated that O. davisae abundance increased rapidly when the abundance of small‐sized flagellates was high in the Lakes Faro and Ganzirri. O. davisae feed on flagellates and ciliates (Saiz, Griffell, Calbet, & Isari, 2014), and recently, it was shown that they were se‐ lectively feeding on cryptophytes in the Black Sea (Khanaychenko,

Mukhanov, Aganesova, Besiktepe, & Gavrilova, 2018). The inner part of the İzmir Bay is eutrophic (Kontaş et al., 2004; Küçüksezgin, 2011), able to supply available and saturated food systems for

O. davisae. Furthermore, some diatom species were dominant in

early winter in the inner İzmir Bay, and after the diatom bloom, the abundance of dinoflagellates peaked in late spring and late sum‐ mer based on microzooplankton data (Gençay & Büyükışık, 2004). Apart from the abundance of O. davisae in stB7 in the inner İzmir Bay, the species was also relatively more abundant in stB9 than in the other two stations (stB8 and stB3) in August 2017. StB9 is lo‐ cated in a small inlet (Ildır), most probably under the effect of inor‐ ganic and organic discharges from local settlements. While we do not have any nutrient or phytoplankton data from the stations for robust comparison, station stB9 seems more productive than the adjacent stations. Morever, predators also play an important role in the seasonal and spatial distribution of the species. The decrease in

F I G U R E 4   Spatial abundance

distribution of female Oithona davisae and

Oithona nana in AT layer in Turkish coast

of Aegean Sea

F I G U R E 5   Proportional contribution

of Oithona davisae, Oithona nana, Oithona male, Oithona copepodites and other female oithonids in Aegean Sea

0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100% B1 B2 B3 B4 B5 B6 B7 B8 B9 B10 B11 B12 B13 B14

(7)

O. davisae abundance in midsummer in the Fukuyama Harbour and

in September and October in the Sevastopol Bay was attributed to predation by jellyfish (Svetlichny et al., 2016; Uye & Sano, 1995).

Despite the large number of the nonindigenous species identi‐ fied from marine and estuarine habitats, the potential consequences of their presence in their new habitats are not yet well known. Even though we used large mesh size, the existence and high relative abun‐ dance of O. davisae in the Aegean Sea, as indicated in this study, raise some critical issues such as the consequences of its presence espe‐ cially on its congener, O. nana, and more generally its trophic impact on other zooplankton species. A detailed zooplankton monitoring pro‐ gramme with suitable sampling mesh size needs to be carried out for better understanding of the spatial and seasonal distribution of O. da‐

visae and of the impacts of the species on the zooplankton communi‐

ties in the Aegean Sea.

ACKNOWLEDGEMENTS

We are grateful to Erdem Sayın for providing temperature data, Gökhan KAMAN for helping to sampling and to the crew of R/V K. Piri Reis and R/V TÜBİTAK MAM Marmara Research Vessel for technical assistance during cruises. This work has been funded by “Integrated Marine Pollution Monitoring 2017‐2019 Programme” carried out by Ministry of Environment and Urbanization/ General Directorate of EIA, Permit and Inspection/Department of Laboratory, Measurement and coordinated by TUBITAK‐MRC ECPI, and Izmir Metropolitan Municipality General Directorate of Water and Sewage Administration through DBTE‐199, 2015 project.

ORCID

Tuba Terbıyık Kurt https://orcid.org/0000‐0002‐2937‐6816 Şengul Beşiktepe https://orcid.org/0000‐0003‐4372‐7106

REFERENCES

Aker, H. V. (2015). Zooplankton of the Aegean Sea. In T. Katağan, A. Tokaç, Ş. Beşiktepe, & B. Öztürk (Eds.), The Aegean sea marine biodi‐ versity, fisheries, conservation and governance (pp. 176–187). Istanbul, Turkey: TUDAV.

Akinci, G., Guven, D. E., & Ugurlu, S. K. (2013). Assessing pollution in Izmir Bay from rivers in western Turkey: Heavy metals. Environmental Science: Processes & Impacts, 15(12), 2252–2262.

Almeda, R., Augustin, C. B., Alcaraz, M., Calbet, A., & Saiz, E. (2010). Feeding rates and gross growth efficiencies of larval developmen‐ tal stages of Oithona davisae (Copepoda, Cyclopoida. Journal of Experimental Marine Biology and Ecology, 387, 24–35. https ://doi. org/10.1016/j.jembe.2010.03.002

Altukhov, D. A., Gubanova, A. D., & Mukhanov, V. S. (2014). New invasive copepod Oithona davisae Ferrari and Orsi, 1984: Seasonal dynamics in Sevastopol Bay and expansion along the Black Sea coasts. Marine Ecology, 35, 28–34. https ://doi.org/10.1111/maec.12168

Ambler, J. W., Cloern, J. E., & Hutchinson, A.( 1985). Seasonal cycles of zooplankton from San Francisco bay. In J. E. Cloern, & F. H. Nichols(Eds.), Temporal dynamics of an estuary: San Francisco bay.

Developments in hydrobiology, (Vol. 30, pp. 177 – 197). Dordrecht, Netherlands: Springer.

Bakir, A. K., Katağan, T., Aker, H. V., Özcan, T., Sezgin, M., Ateş, A. S., … Kirkim, F. (2014). The marine arthropods of Turkey. Turkish Journal of Zoology, 38, 765–831. https ://doi.org/10.3906/zoo‐1405‐48 Beşiktepe, Ş. (2015). Physical oceanography of the Aegean sea: A review.

In T. Katağan, A. Tokaç, Ş. Beşiktepe, & B. Öztürk (Eds.), The Aegean Sea marine biodiversity, fisheries, conservation and governance (pp. 27– 39). Istanbul, Turkey: TUDAV.

Cordell, J. R., Bollens, S. M., Draheim, R., & Systema, M. (2008). Asian co‐ pepods on the move: Recent invasions in the Columbia– Snake River system, USA. ICES Journal of Marine Sciences, 65, 753–758. https :// doi.org/10.1093/icesj ms/fsm195

Cornils, A., & Wend‐Heckmann, B. (2015). First report of the plank‐ tonic copepod Oithona davisae in the northern Wadden Sea (North Sea): Evidence for recent invasion? Helgoland Marine Research, 69, 243–248.

Doğan, G., & İşinibilir Okyar, M. (2016). First report of a new invasive spe‐ cies Oithona davisae Ferrari and Orsi, 1984 (Copepoda: Cyclopoida) in the Sea of Marmara. Turkish Journal of Fisheries and Aquatic Sciences, 16, 469–473.

Eronat, C., & Sayin, E. (2014). Temporal evolution of the water character‐ istics in the bays along the eastern coast of the Aegean Sea: Saros, İzmir, and Gökova bays. Turkish Journal of Earth Sciences, 23, 53–66. https ://doi.org/10.3906/yer‐1307‐4

Ferrari, F. D., & Orsi, J. (1984). Oithona davisae, new species, and Limnooithona sinensis (Burckhardt, 1912) (Copepoda: Cyclopoida: Oithonidae) from the Sacramento‐San Joaquin estuary. California. Journal of Crustacean Biology, 4, 106–126.

Galil, B. S., & Zenetos, A.( 2002). A sea change—exotics in the Eastern Mediterranean Sea. In E. Leppäkoski, S. Gollasch, & S. Olenin(Eds.), Invasive aquatic species of Europe. Distribution, impacts and manage‐ ment(pp. 325 – 336). Dordrecht, Netherlands: Springer.

Gençay, H. A., & Büyükışık, B. (2004). Effects of sewage outfall on Phytoplankton community structure in Izmir Bay (Aegean Sea). Ege University Journal of Fisheries & Aquatic Sciences, 21, 107–111. Gonzalez, H. E., & Smetacek, V. (1994). The possible role of the cyclo‐

poid copepod Oithona in retarding vertical flux of zooplankton faecal material. Marine Ecology Progress Series, 113, 233–246. https ://doi. org/10.3354/meps1 13233

Gubanova, A., & Altukhov, D. (2007). Establishment of Oithona brevicor‐ nis Giesbrecht, 1892 (Copepoda: Cyclopoida) in the Black Sea. Aquatic Invasions, 4, 407–410. https ://doi.org/10.3391/ai.2007.2.4.10 Gürü, M., Beyazıt, T., & Öksüz, I. (2006). Evaluation of Izmir bay's pol‐

lution, sources and abatement techniques. Journal of International Environmental Application & Science., 1, 120–124.

Hirota, R. (1990). Microdistribution of the marine copepod Oithona da‐ visae in the shallow waters of Ariake‐kai mud flats, Japan. Marine Biology, 105, 307–312. https ://doi.org/10.1007/BF013 44300 Isinibilir, M., Svetlichny, L. S., & Hubareva, E. S. (2016). Small oithonid co‐

pepods in the northeastern Marmara Sea. Rapports Et procès‐verbaux Des Réunions Commission Internationale Pour L'exploration Scientifique De La Mer Méditerranée, 41, 483.

Khanaychenko, A., Mukhanov, V., Aganesova, L., Besiktepe, S., & Gavrilova, N. (2018). Grazing and feeding selectivity of Oithona davi‐ sae in the Black Sea: Importance of Cryptophytes. Turkish Journal of Fisheries and Aquatic Sciences, 18, 937–949.

Kontaş, A., Kucuksezgin, F., Altay, O., & Uluturhan, E. (2004). Monitoring of eutrophication and nutrient limitation in the Izmir Bay (Turkey) before and after wastewater treatment plant. Environment International, 29, 1057–1062. https ://doi.org/10.1016/ S0160‐4120(03)00098‐9

Küçüksezgin, F. (2011). The water quality of Izmir Bay: A case study. Reviews of Environmental Contamination and Toxicology, 211, 1–24.

(8)

Küçüksezgin, F., Kontas, A., Altay, O., Uluturhan, E., & Darilmaz, E. (2006). Assessment of marine pollution in Izmir Bay: Nutrient, heavy metal and hydrocarbon concentration. Environment International, 32, 41–51.

Kükrer, S., & Büyükişik, H. B. (2013). Size‐fractionated phytoplankton and nutrient dynamics in the inner part of İzmir Bay, eastern Aegean Sea. Turkish Journal of Botany, 37, 177–187.

Kurt, T. (2016). Regional changes in mesozooplankton assemblages in Northeastern Mediterranean, Turkish Straits system and the Black Sea. (Doctoral Dissertation), Çukurova University.

Lemenkova, P. (2016). Industrial water discharge into the Izmir Bay: Environmental threats to the local ecosystems. Nauka. Nauchno‐ proizvodstvenniy Zhurnal, 4, 8–12.

Lykousis, V., Chronis, G., Tselepides, A., Price, N. B., Theocharis, A., Siokou‐Frangou, I., … Voutsinou‐Taliadouri, F. (2002). Major outputs of the recent multidisciplinary biogeochemical researches under‐ taken in the Aegean Sea. Journal of Marine Systems, 33–34, 313–334. https ://doi.org/10.1016/S0924‐7963(02)00064‐7

Mihneva, V., & Stefanova, K. (2013). The non‐native copepod Oithona da‐ visae (Ferrari FD and Orsi, 1984) in the Western Black Sea: Seasonal and annual abundance variability. Bioinvasions Records, 2, 119–124. https ://doi.org/10.3391/bir.2013.2.2.04

Ministry of Environment and Urbanization, TUBITAK‐MRC (2018). Integrated marine pollution monitoring 2017–2019 programme: 2017 Aegean Sea report. Kocaeli, Turkey: TÜBİTAK‐MRC Press.

Nagasawa, S., & Marumo, R. (1984). The zooplankton community and its abundance in Tokyo Bay. La Mer, 22, 277–286.

Nishida, S. (1985). Taxonomy and distribution of the family Oithonidae (Copepoda, Cyclopoida) in the Pacific and Indian Oceans. Bulletin of the Ocean Research Institute. University of Tokyo, 20, l–167.

Olazabal, A., & Tirelli, V. (2011). First record of the egg‐carrying calanoid co‐ pepod Pseudodiaptomus marinus in the Adriatic Sea. Marine Biodiversity Records, 4, 1–4. https ://doi.org/10.1017/S1755 26721 1000935 Ounissi, M., Laskri, H., & Khelifi‐Touhami, M. (2016). Net‐zooplankton

abundance and biomass from Annaba Bay (SW Mediterranean Sea) under estuarine influences. Mediterranean Marine Sciences, 17, 519– 532. https ://doi.org/10.12681/ mms.1474

Özkan, E. Y., Büyükışık, B., & Sunlu, U. (2013). Nutrient fluxes and their dynamics in the Inner Izmir Bay sediments (Eastern Aegean Sea). In F. S. G. Einschlag (Ed.), Waste water‐treatment technologies and recent analytical developments (pp. 173–187). London, UK: IntechOpen. Paffenhofer, G. A. (1993). On the ecology of marine cyclopoid cope‐

pods (Crustacea, Copepoda). Journal of Plankton Research, 15, 37–55. https ://doi.org/10.1093/plank t/15.1.37

Polat, C., & Tugrul, S. (1996). Chemical exchange between the Mediterranean and the Black Sea via the Turkish straits. Dynamics of Mediterranean Straits and Channels. CIESM Science Series no. 2 (17) (pp. 167–186). Monaco: Bulletin de l'Institut océanographique de Monaco. Razouls, C., de Bovée, F., Kouwenberg, J., & Desreumaux, N. (2015–

2019). Diversity and geographic distribution of marine planktonic cope‐ pods. Sorbonne Université, CNRS. http://copep odes.obs‐banyu ls.fr/en Rilov, G., & Galil, B. (2009). Marine bioinvasions in the Mediterranean

Sea–history, distribution and ecology. In G. Rilov, & J. A. Crooks (Eds.), Biological invasions in marine ecosystems (pp. 549–575). Berlin, Germany: Springer.

Saiz, E., Calbet, A., & Broglio, E. (2003). Effects of small‐scale turbu‐ lence on copepods: The case of Oithona davisae. Limnology and Oceanography, 48, 1304–1311.

Saiz, E., Griffell, K., Calbet, A., & Isari, S. (2014). Feeding rates and prey: Predator size ratios of the nauplii and adult females of the marine cyclopoid copepod Oithona davisae. Limnology and Oceanography, 59, 2077–2088.

Sayın, E. (2003). Physical features of the Izmir Bay. Continental Shelf Research, 23, 957–970. https ://doi.org/10.1016/S0278‐ 4343(03)00083‐9

Seregin, S. A., & Popova, E. V. (2016). Long‐term dynamics of the copepod invader Oithona davisae in coastal waters of the Black Sea. Russian Journal of Biological Invasions, 7, 374–382. https ://doi.org/10.1134/ S2075 11171 604007X

Sever, T. M. (2009). Pelagic Copepoda fauna of the Aegean Sea and the distribution of the common species. Ege University Journal of Fisheries & Aquatic Sciences, 26, 203–209. (in Turkish).

Sever, T. M., & Mavili, S. (2002). First observations on the distribution of Corycaeidae (Copepoda) in Izmir Bay (Aegean Sea). Ege University Journal of Fisheries & Aquatic Sciences, 19(1–2), 227–232. (in Turkish). Stergiou, K. I., Christou, E. D., Georgopoulos, D., Zenetos, A., &

Souvermezoglou, E. (1997). The Hellenic Seas: Physics, chemis‐ try, biology and fisheries. Oceanography and Marine Biology, 35, 413–538.

Sunlu, U., Büyükışık, H. B., Koray, T., von Brökel, K., Sunlu, F. S., Sever, T. M., … Orçun, E. (2005). Effect of wastewater treatment plant on the lower trophic levels in Izmir Bay. TUBITAK‐ÇAYDAG, 102Y116, 253 pp. (in Turkish).

Svetlichny, L., Hubareva, E., & Işinibilir, M. (2018). Population dynamics of the copepod invader Oithona davisae in the Black Sea. Turkish Journal of Zoology, 42, 684–693. https ://doi.org/10.3906/zoo‐1804‐48 Svetlichny, L., Hubareva, E., Khanaychenko, A., Gubanova, A., Altukhov,

D., & Besiktepe, S. (2016). Adaptive strategy of Thermophilic Oithona davisae in the Cold Black Sea Environment. Turkish Journal of Fisheries Aquatic Sciences, 16, 77–90.

Temnykh, A., & Nishida, S. (2012). New record of the planktonic cope‐ pod Oithona davisae Ferrari and Orsi in the Black Sea with notes on the identity of" Oithona brevicornis". Aquatic Invasions, 7, 425–431. https ://doi.org/10.3391/ai.2012.7.3.013

Terbıyık Kurt, T. (2018). Contribution and acclimatization of the swarming tropical copepod Dioithona oculata (Farran, 1913) in Mediterranean coastal ecosystem. Turkish Journal of Zoology, 42, 567–577.

Tuğrul, S., Beşiktepe, S. T., & Salihoglu, I. (2002). Nutrient exchange fluxes between the Aegean and Black Seas through the Marmara Sea. Mediterranean Marine Science, 3, 33–42. https ://doi.org/10.12681/ mms.256

Turner, J. T. (2004). The importance of small planktonic copepods and their roles in pelagic marine food webs. Zoological Studies, 43, 255–266.

Uchima, M. (1988). Gut content analysis of neritic copepods Acartia omorii and Oithona davisae by a new method. Marine Ecology Progress Series, 48, 93–97. https ://doi.org/10.3354/meps0 48093

Üstün, F., & Terbıyık Kurt, T. (2016). First Report of the Occurrence of Oithona davisae Ferrari FD & Orsi, 1984 (Copepoda: Oithonidae) in the Southern Black Sea, Turkey. Turkish Journal of Fisheries Aquatic Sciences, 16, 413–420.

Uye, S., Ayaki, Y., & Onbe, T. (1992). Seasonal geographical distribution of zooplankton in Hiroshima Bay and its adjacent waters, the Inland Sea of Japan. Journal of the Faculty of Applied Biological Science, Hiroshima University, 31, 99–119.

Uye, S., & Sano, K. (1995). Seasonal reproductive biology of the small cyclopoid copepod Oithona davisae in a temperate eutrophic inlet. Marine Ecology Progress Series, 118, 121–128. https ://doi. org/10.3354/meps1 18121

Uye, S., & Sano, K. (1998). Seasonal variations in biomass, growth rate and production rate of the small cyclopoid copepod Oithona davisae in a temperate eutrophic inlet. Marine Ecology Progress Series, 163, 37–44. https ://doi.org/10.3354/meps1 63037

Vidjak, O., Bojanić, N., de Olazabal, A., Benzi, M., Brautović, I., Camatti, E., … Tirelli, V. (2018). Zooplankton in Adriatic port en‐ vironments: Indigenous communities and non‐indigenous spe‐ cies. Marine Pollution Bulletin, https ://doi.org/10.1016/j.marpo lbul.2018.06.055

Yıldız, İ., Feyzioğlu, A. M., & Beşiktepe, S. (2017). First observation and seasonal dynamics of the new invasive planktonic copepod

(9)

Oithona davisae Ferrari and Orsi, 1984 along the southern Black Sea (Anatolian Coast). Journal of Natural History, 51, 127–139.

Zagami, G., Brugnano, C., Granata, A., Guglielmo, L., Minutoli, R., & Aloise, A. (2018). Biogeographical distribution and ecology of the planktonic copepod Oithona davisae: Rapid invasion in Lakes Faro and Ganzirri (Central Mediterranean Sea). In M. Uteri (Ed.), Trends in Copepod Studies ‐ Distribution, Biology and Ecology (pp. 59–82). New York, NY: Nova Science Publishers.

Zagami, G., Costanzo, G., & Crescenti, N. (2005). First record in Mediterranean Sea and redescription of the bentho‐planktonic calanoid copepod species Pseudocyclops xiphophorus Wells, 1967. Journal of Marine Systems, 55, 67–76. https ://doi.org/10.1016/j.jmars ys.2004.07.018

Zagorodnyaya, Y. A. (2002). Oithona brevicornis in Sevastopol Bay: Is it a single event or a new invader in the Black Sea fauna? Ecologiya Morya, 61, 43. (in Russian).

Zenetos, A., Çinar, M. E., Crocetta, F., Golani, D., Rosso, A., Servello, G., … Verlaque, M. (2017). Uncertainties and validation of alien species catalogues: The Mediterranean as an example. Estuarine, Coastal and Shelf Science, 191, 171–187. https ://doi.org/10.1016/j. ecss.2017.03.031

Zenetos, A., Çinar, M. E., Pancucci‐Papadopoulou, M. A., Harmelin, J. G., Furnari, G., Andaloro, F., … Zibrowius, H. (2005). Annotated list of marine alien species in the Mediterranean with records of the worst

invasive species. Meditterranean Marine Sciences, 6, 63–118. https :// doi.org/10.12681/ mms.186

Zenetos, A., Katsanevakis, S., Poursanidis, D., Crocetta, F., Damalas, D., Apostolopoulos, G., … Malaquias, M. (2011). Marine alien species in Greek seas: Additions and amendments by 2010. Meditterranean Marine Sciences, 12, 95–120. https ://doi.org/10.12681/ mms.55 Zenetos, Α., Gofas, S., Morri, C., Rosso, A., Violanti, D., García Raso, J.

E., … Verlaque, M. (2012). Alien species in the Mediterranean Sea by 2012. A contribution to the application of European Union's marine strategy framework directive (MSFD). Part 2. Introduction trends and pathways. Meditterranean Marine Sciences, 13, 328–352. https :// doi.org/10.12681/ mms.327

How to cite this article: Terbıyık‐Kurt T, Beşiktepe Ş. First

distribution record of the invasive copepod Oithona davisae Ferrari and Orsi, 1984, in the coastal waters of the Aegean Sea.

Mar Ecol. 2019;40:e12548. https ://doi.org/10.1111/ maec.12548

Referanslar

Benzer Belgeler

1000 kişi başına düşen hastane sayısı (kamu+özel), kamu hastane sayısı, özel hastane sayısı, hastane yatak sayısı (kamu+özel), kamu hastane yatak sayısı, özel

Gram negatif periodontal patojen Actinobacillus actinomycetecomitans tarafından üretilen Dispersin B'nin bazı stafilokok türlerinde biyofilm oluşumu için önemli

Aşağıda künyeleri verilen makalelerde Yavuz ORUÇ’un ORCİD numarası yazar tarafından sehven yanlış verilmiş olup ORCİD numarasının 0000-0002-3321-3665 olması

The purpose of this study was to investigate to what extent explicit instruction of vocabulary in collocations, using different techniques, develops awareness in students

EFFECTS OF FEEDING SYSTEM ON RATES OF FEEDING AND WELFARE BEHAVIOURS BY KARAYAKA MALE LAMBS WITH DIFFERENT BIRTH WEIGHT - Arda Yıldırım, Nuh Ocak, Zafer Ulutaş,.. Muhammet

Şimdi, pek sevdiği ve harab hayatım, kıyılarında sürükliyerek bitirdiği Bü- yükadanm münzevî bir köşesinde din - lenen Ahmed Refiği rahmet ve hürmet­

Elde edilen bu formüllere göre boru bağlantı elemanları için en iyi sonucu 420x500' lük derece.. sisteminin

From the Department of Radiology, University of Iowa Hospital and Clinics, Iowa City, Iowa (S.G.K.); Departments of Anesthesiology and Reanimation (L.D., Z.T.S., H.S.D.K.,