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Article

First Record of the Alien Tintinnid Ciliate Rhizodomus tagatzi Strelkow and Wirketis 1950 in the Adriatic Sea

by
Jakica Njire
1,
Natalia Bojanić
2,*,
Davor Lučić
1 and
Ivana Violić
3
1
Institute for Marine and Coastal Research, University of Dubrovnik, Kneza Damjana Jude 12, 20000 Dubrovnik, Croatia
2
Institute of Oceanography and Fisheries, Šetalište Ivana Meštrovića 63, 21000 Split, Croatia
3
Department of Applied Ecology, University of Dubrovnik, Ćira Carića 4, 20000 Dubrovnik, Croatia
*
Author to whom correspondence should be addressed.
Water 2023, 15(10), 1821; https://doi.org/10.3390/w15101821
Submission received: 16 April 2023 / Revised: 3 May 2023 / Accepted: 8 May 2023 / Published: 10 May 2023
(This article belongs to the Special Issue The Study of Plankton in the Mediterranean Sea)
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Abstract

:
The tintinnid ciliate Rhizodomus tagatzi has spread rapidly in recent decades in neritic areas of the Mediterranean and adjacent seas, where it is classified as a non-indigenous species. The present study documents the first finding of the species in the Adriatic Sea, in the transitional waters of the Neretva River estuary. Zooplankton material was collected with 5 L Niskin bottles in three layers (1, 5 and 7 m) at two stations, at the mouth of the Neretva River and 16 km upstream, in the period from May 2022 to January 2023. In addition to the morphological characteristics of R. tagatzi, we discuss the state and variability of the populations based on the abundance of the species and the influence of abiotic environmental factors (temperature and salinity) and possible pathways of entry into the Adriatic Sea. The maximum abundance of R. tagatzi in the Neretva River estuary of ~2 × 103 cells L−1 is among the highest in the Mediterranean Sea, and the species has a significant contribution to the tintinnid community (>80%), indicating successful establishment of the population in the estuary and intense influence on ecosystem functioning until the strong river flow completely displaces the wedge from the seabed. Statistical methods confirm the differences between stations in the total abundance of tintinnids and differences in their vertical distribution at the upstream station.

1. Introduction

Tintinnid ciliates are a common, occasionally abundant and important component of planktonic food webs. They represent a monophyletic branch of the subclass Choreotrichia consisting exclusively of loricate forms, but also suggest paraphyly of certain genera [1,2]. The use of molecular methods in taxonomic research allows for more reliable species identification, but is still rare in this group of organisms [1,3]. Tintinnid loricae exhibit significant intraspecific polymorphism, but their morphology, i.e., differences in size, overall shape, ornamentation, fine surface structures and the presence or absence of agglutinated particles, remains the most important feature for their taxonomy.
According to the available literature, Rhizodomus tagatzi is distributed only in the Northern Hemisphere in tropical to temperate latitudes [4]. It was probably first described by Busch in 1925 as a form of Tintinnopsis karajensis in the coastal waters of Indonesia [5]. It was later recorded under the name Rhizodomus tagatzi in the Pacific coastal waters of Russia [6] and Japanese coastal waters [7], from where it spread to the Gulf of Mexico, the Caribbean Sea [8,9] and the Arabian Gulf [10] under the name Tintinnopsis corniger. In the 1980s, the species was found in the coastal waters of the western Mediterranean, where it was described as the new species Tintinnopsis nudicauda [11] and T. corniger [12]. Subsequently, specimens were determined in other Mediterranean regions: T. corniger in the central Mediterranean [13], in the eastern Mediterranean [14,15] and in the Marmara Sea [16], as T. nudicauda in the eastern Mediterranean [17] and as Rhizodomus tagatzi in the Black Sea [18]. According to the European Alien Species Information Network (EASIN) [19,20] tintinnid Rhizodomus tagatzi Strelkow and Wirketis 1950 is classified as an alien species introduced into the eastern Mediterranean Sea in 2007 [15].
This paper reports the first record of Rhizodomus tagatzi in the Adriatic Sea from plankton samples collected during the monitoring program in the Neretva River estuary in the southern part of the Adriatic Sea. The paper focuses simultaneously on the morphology of Rhizodomus tagatzi, the status of its population in the estuary and its relationships with thermohaline features of the environment, taking into account the temporal variability of all parameters. Considering that EASIN classifies the species as alien [20], the origin of this species in the Adriatic Sea is also discussed.

2. Materials and Methods

2.1. Study Area

The Neretva is the largest river on the eastern coast of the Adriatic Sea, surrounded by karst hills to the north, east and south and the Adriatic Sea to the west. The river flows through Bosnia and Herzegovina (193 km) and Croatia (22 km). In the lower alluvial valley in Croatia, the Neretva divides into several river courses and forms a delta with an area of about 280 km2. The delta has been reduced by extensive land reclamation projects, and the marshes, lagoons and lakes that once characterised this plain have been largely reduced and transformed into one of the most productive agricultural areas in Croatia. In addition, the estuary and adjacent areas have been intensively exploited for various economic purposes, including transportation, fishing and more recently, tourism and recreation. The lower Neretva region consists of five ornithological, ichthyological and landscape protected areas with a total area of 1624 ha.
The Neretva River estuary is a salt-coast type, where the inflow of river water is much greater than that of sea water, and vertical mixing is limited to a thin transitional boundary between the freshwater at the surface and the salt water below [21]. The influence of the inertial effect of the sea is particularly strong when the inflows of the Neretva are low, and is observed up to above Metković, 23 km from the mouth (Figure 1). According to the author, the water regime of the Neretva River is characterised by high winter water levels (November and December and sometimes until April) and low summer water levels (June to October). The average annual flow of the Neretva in Metković is 355 m3 s−1, with a minimum of 32 m3 s−1 and a maximum of over 2400 m3 s−1 [22]. The dynamics of seawater intrusion is influenced by the tidal fluctuations of the Adriatic Sea and the upstream inflows, which depend mainly on the operation of hydroelectric power plants. The salt wedge reaches Metković at discharges of 180 m3 s−1, while no seawater can enter the riverbed at discharges higher than 500 m3 s−1 [23]. Seawater intrusion can threaten ecosystem function and affect the quality of freshwater for agriculture or water supply. Therefore, sea level rise has been identified as one of the major threats to such low-lying areas [24].

2.2. Field Sampling and Laboratory Processing

Samples were collected monthly or sometimes more frequently from May 2022 to January 2023 by a small fishing boat at two stations in the Neretva River estuary (Figure 1). Station S1 is located at the mouth of the river near the port of Ploče and station S2 is 16 km upstream from it in the main stream. The depth of both stations is 8.0 m. Zooplankton were sampled at three depths of 1 m, 5 m, and near the bottom (~7 m) using 5 L Niskin bottles. Samples were preserved in a 2.5% formaldehyde–seawater solution previously buffered with CaCO3. Preparation of samples for microscopic analysis has been described in detail in [25]. Since the cells were not visible, we counted all loricae. Counting and taxonomic identification were performed using an inverted microscope (Olympus IMT-2) at 100× and 400× magnification. The entire bottom of the sedimentation chamber was examined, and abundance was expressed as the number of cells per litre (cells L−1). To determine the morphometric characteristics of Rhizodomus tagatzi, 56 specimens were measured microscopically at 200× and 400× magnification using a calibrated ocular micrometre.
Vertical temperature and conductivity profiles were measured with a mobile probe SEBA Hidrometrie KLL-Q-2 with an accuracy of >±0.01 °C and ±0.02, respectively. Thermohaline properties were determined in parallel with the collection of zooplankton material at the same oceanographic levels.

2.3. Data Analysis

The Mann–Whitney and Kruskal–Wallis nonparametric statistical tests were used to detect differences among stations and sampling depths in total tintinnid abundance (Addinsoft 2023, XLSTAT statistical and data analysis solution. New York, NY, USA. https://www.xlstat.com). Similarity patterns between stations and sampling depths were described using non-metric multidimensional scaling (MDS) and hierarchical clustering (HC) methods [26]. The distance between the extracted factor station/depth was calculated using Bray–Curtis similarity. Clustering was performed using the group average method, with the “similarity profile” permutation test (SIMPROF) applied to test the significance of the internal structure within the constructed cluster. An MDS plot was created to illustrate the similarity, with the overlapping clusters coming from a SIMPROF cluster dendrogram. These statistical analyses were performed using PRIMER 7 software (version 7.1.21 of PRIMER-E Ltd., Plymouth, UK) [26].

3. Results

Taxonomic classification of species Rhizodomus tagatzi Strelkow and Wirketis, 1950 according to World Ciliophora Database [27]:
Class Oligotrichea
Subclass Oligotrichia
Order Choreotrichida
Suborder Tintinnina
Family Tintinnida incertae sedis

3.1. Morphological Features of Rhizodomus tagatzi

The lorica of R. tagatzi is 149.1–217.6 μm long overall in specimens preserved in formaldehyde and consists of a cylindrical bowl that gradually narrows toward the aboral end and terminates in a branched aboral horn (Table 1 and Figure 2A). The walls of the cylindrical part of the bowl appear rigid; they are flat and covered with coarse material that makes them opaque, and at the aboral end, the bowl tapers to a horn-like projection. Due to the agglutination of the lorica, it is not possible to detect the presence of spiral turns. The mouth opening is complete, rough and 28.7–36.1 μm wide. The aboral end is 34.3–56.5 μm long and consists of a large, rather flat, pointed horn surrounded by one to five smaller, single-pointed appendages. The length of these lateral buds is quite small compared to the main horn (Figure 2B,C). Only sometimes (in less than 5% of the measurements) were two main horns observed. In contrast to the rest of the lorica, the aboral end has a hyaline structure with a fine reticulation.

3.2. Distribution Pattern of Rhizodomus tagatzi and Environmental Settings in the Neretva River Estuary

At upstream station S2, the species occurs from early July to early November, with most specimens occurring in the 5 and 7 m layers in a temperature and salinity range of 21.01–24.37 °C and 30.88–38.36, respectively (Figure 3, Figure 4 and Figure 5). The highest abundance, 1958 cells L−1, was recorded on 1 July, at 5 m depth at 22.28 °C and 30.88. In the same period, very low abundances of the species were recorded at the mouth of the Neretva River, station S1 (less than 5 cells L−1). Except for on 1 July, they were not found at a depth of 7 m, and the highest abundance was only 22 cells L−1 (5 m), at a temperature of 23.85 °C and salinity of 37.35. On this basis, we estimate the limits of hydrographic parameters for Rhizodomus tagatzi in the Neretva estuary to be a temperature of 21.01–25.51 °C and salinity of 30.88–38.71. However, a few specimens were also found at lower temperature (min. 14.94 °C) and salinity values (1.39–6.90), but due to the way the plankton samples were collected and processed, we cannot determine with certainty whether the specimens were alive.
During the study period, Rhizodomus tagatzi contributed an average percentage of 8.68 ± 20.96% on S1 and 11.19 ± 24.91% on S2 to the total tintinnid abundance. This species dominated the community at both stations in early July (Figure S1). At the upstream station (S2), an average of 83.32 ± 16.96% and a maximum of 96.83% were recorded at 5 m depth, and a very high value of 55.68% was also recorded at 5 m depth on 21 July. In contrast, at the station in the Neretva estuary (S1), these values were lower, with an average of 71.56 ± 11.46% and a maximum of 78.58% at 5 m depth on 1 July. A relatively high community percentage of 35.71% was measured at 5 m depth in early November. Statistical analysis revealed significant differences between stations in total abundance of tintinnids (U = 1029.5, p = 0.045), while differences in vertical distribution were significant only at station S1 in the surface layer compared to deeper layers (K = 15.864, p = 0.001). A list of tintinnid taxa detected in the Neretva River estuary during this study can be found in Table S1.
To investigate the degree of similarity of the tintinnid community in the Neretva River estuary, the total abundance of these organisms was subjected to hierarchical clustering and MDS ordination (Figure 6). According to the SIMPROF test, two clusters were statistically significant (indicated by dashed lines) at a significance level of p = 0.004: (I) the cluster comprising the sampling layers of 5 and 7 m depth at the upstream station S2, where the highest values of total abundance of tintinnids as well as R. tagatzi were detected, and (II) the cluster comprising all other samples. Although the surface layer at both stations (as two branches) is separated from the deeper layers at the confluence station (S1), the differences are not statistically significant.

4. Discussion

The tintinnid Rhizodomus tagatzi is common in ecosystems with high trophic levels and stable water column, such as the Thau Lagoon [12] and the lagoon of Urbino in the northern Mediterranean [11], the Damietta Harbour in Egypt [14], the coast of Hurghada in the Red Sea [28], Lake Faro in Sicily (central Mediterranean) [4], northern Lebanon in the eastern Mediterranean [29], Izmir Bay in the Aegean Sea [15], the Gulf of Gemlik in the Sea of Marmara [16], and Sevastopol Bay in the Black Sea [18,30]. For a more detailed overview of the geographic distribution of R. tagatzi outside the Mediterranean Sea, the reader can refer to the work of Dolan and Pierce [31] and Saccà and Giufrè [4].
In general, data on the status of plankton communities in the Neretva River estuary are still sparse and mostly limited to the lowest part of the estuary [32,33,34,35]. According to Article 2 of the Water Framework Directive (WFD 2000/60/EC), this area is classified as “transitional waters”, the main characteristics of which is the occurrence of pronounced vertical stratification of the water column in terms of salinity, nutrient concentration, oxygen content, and plankton community composition. The occurrence of stratification is caused by a relatively low amplitude of ocean changes, the energy of which is insufficient to cause significant vertical mixing of the water column [36]. The sea penetrates upstream along the Neretva riverbed into a clearly separated bottom layer of saline water upstream to behind Metković [23]. The thickness of the upper freshwater layer is variable and depends primarily on the flow of the river, the characteristics of the riverbed, and synoptic conditions.
In addition, water quality is classified as mesotrophic due to extensive anthropogenic activities in the lower estuary and its surroundings [34]. Long-term phytoplankton surveys in the area of the adjacent Mali Ston Bay have confirmed that the nanoplankton component of the phytoplankton is equally represented as the microphytoplankton in all seasons [37]. Size fractions of nano- and picoplankton are considered a suitable food source for tintinnids [38,39,40,41]. Under such environmental conditions, tintinnids can develop high population densities. Some species can rapidly adapt to a new habitat, reproduce, and reach much higher densities than in their original habitats. This phenomenon has already been observed in the oceanic species Xystonella lohmanni and Eutintinnus tubulosus in the Krka River estuary (middle Adriatic Sea) [42] and in Amphorides laackmanni in the northern part of the Adriatic Sea [43].
The high abundances (~2 × 103 cells L−1) of R. tagatzi that we found at the 16 km upstream station (S2) of the Neretva estuary in layers more than 5 m deep were due to the entry of a seawater wedge into the riverbed itself. Especially in summer, when the species was most abundant, the salt wedge penetrates up to 25 km from the mouth due to the lower flow of the river [23]. The significantly higher population densities at the upstream station (S2) compared to the estuary (S1) indicate favourable environmental conditions. Indeed, the sharp interface between layers, which in the estuary is a halocline and often a thermocline [23], is also associated with the nutricline, which creates suitable conditions for the development of phytoplankton and microbial communities, as well as microzooplankton as their primary consumers [41,44,45,46]. Depending on physical conditions such as wind-driven turbulent mixing, plankton organisms can also be transported out of the pycnocline into frontal areas and even cause a surface bloom [47]. In our study, the lowest abundance of tintinnids was found in the surface layer, indicating the lack of intense vertical mixing of the layers.
From what is known so far, the species has been observed in land-sea transition zones (estuaries, lagoons, coastal lakes) and in the neritic marine environment offshore of estuaries. It appears to tolerate a relatively wide range of salinity (16–37) and prefers relatively warmer water conditions (18–29 °C) [4]. Therefore, it was detected in samples only during the summer–autumn period of the year, with a maximum in summer, which is consistent with our results. Table 1 provides a summary overview of the abundance of the species and the temperature and salinity data in which it was detected. The preference of tintinnids for high temperatures appears to be common in many nearshore and estuarine marine waters, which may be related to better growth at higher temperatures and chlorophyll a concentrations [14]. The abundance of R. tagatzi in the Neretva River estuary is among the highest recorded in the Mediterranean and surrounding seas (Table 1). Higher values were found only in Uranouchi Inlet in Japan in summer 1997 (5 cells mL−1) [48] and in Lake Faro in July 2002 (4.5 × 103 cells L−1) [13]. The formation of dense populations and their dominance in the tintinnid community may have a strong impact on ecosystem functioning. Future research must therefore address the composition and quantity of the entire plankton community.
Table
Table 1. Abundance and environmental data for Rhizodomus tagatzi, Tintinnopsis corniger or Tintinnopsis nudicauda in the Mediterranean Sea and adjacent seas. (The bold values for temperature and salinity indicate the environmental conditions under which the highest abundance was recorded).
Table 1. Abundance and environmental data for Rhizodomus tagatzi, Tintinnopsis corniger or Tintinnopsis nudicauda in the Mediterranean Sea and adjacent seas. (The bold values for temperature and salinity indicate the environmental conditions under which the highest abundance was recorded).
Study AreaTem./Sal.Abundance/BiomassReference
Thau Lagoon, northern Mediterranean SeaWarmer waters with high salinity
11.8–23.2 °C/31.5–37.9		June 1994
25,215 µg m−3		[12] 2
Lake Faro, NE corner of Sicily, Italy (central Mediterranean Sea)12.5–29.3 °C/34.1–37.0
19.0 °C and 36.4		July–September 2022
4.52 × 103 cells L−1 (July 2002)		[4,13] 1,2
Damietta Harbour, Egypt (Eastern Mediterranean Sea)27–33 °CJuly 2003
Max. total TIN abundance
73.5 × 103 cells m−3
(no data for T. corniger)		[14] 2
Northern Lebanese coastal waters (Eastern Mediterranean Sea)No dataJuly–October
September 2006 and 2014
(7 cells L−1)
August 2010		[17] 3
Novorossiysk Harbour and Gelendzhik Bay, North-eastern Black Sea26–28 °C5 × 104 cells m−3
(August-September 2015)		[49] 1
Sevastopol Bay, Black SeaSummer: 18.2–28.0 °C (23.6 ± 1.7 °C)/15.5–18.0 (17.6 ± 0.2)
Autumn: 5.0–20.9 °C (14.1 ± 3.0 °C)/17.2–17.88 (17.63 ± 0.11)		summer–autumn
(summer 2010: 45% of total TIN abundance)
Mean 1: 12,819 cells m−3
1.01 × 105 cells m−3
(summer)		[18] 1
Marmara Sea, Gulf of Gamlik, Turkish coastal waters18–28 °C/16–18
18 °C/16
19 °C and 18		August–October 2010
850 cells L−1
(October)		[16] 2
Al-Max Bay, Alexandria, Egypt~22 °C/~24Autumn 2014
16,902 ± 6453 cells m−3		[50] 3
Neretva River estuary, Adriatic Sea21.01–25.51 °C/30.88–38.71
22.28 °C and 30.88		July–November 2022
1958 cells L−1 (1 July 2022)		This paper 1
1, Rhizodomus tagatzi; 2, Tintinnopsis corniger; 3, Tintinnopsis nudicauda.
A relatively small number of publications address the measurement of lorica (Table 2), and a small number of these studies are supplemented with descriptions of lorica and/or environmental parameters. The agglutinated lorica in the upper, more or less cylindrical part, with a hyaline caudal extension, resembled those of specimens of R. tagatzi from the Black Sea [49], T. nudicauda found in the Urbino Lagoon in Corsica [11] and in Lebanese coastal waters [17], and T. corniger found on the Red Sea coast near Hurghada [28] and in Izmir Bay in the coastal waters of Turkey [15]. On the other hand, differences in the appearance of the main horn and lateral branches, as well as in the agglutination of the lorica, were observed most frequently. In contrast to the specimens from the Neretva River estuary, the aboral horns are much more robust in R. tagatzi from Peter Great Bay in Russia [6], Jiaozhou Bay in China [51], and Sevastopol Bay [18], and in T. corniger from the Gulf of Gemlik in Turkish coastal waters [16]. A considerably longer caudal horn (more than one-third of the total lorica length) was found in T. corniger from the Strait of Hormoz and waters of the United Arab Emirates [10], while a completely hyaline lorica was found in R. tagatzi from Lake Faro in Sicily [52].
The intense shipping traffic that characterises the Adriatic Sea favours the expanding speed of marine organisms. Ballast water has been a vector for tintinnid transport for many years, and it may no longer be possible to determine the original distribution of many tintinnid species [53]. Ballast water has been used in maritime transport for more than a hundred years, so it is reasonable to assume that some tintinnid species, like other planktonic organisms, have successfully established populations in new locations. Although it cannot be said with certainty that every occurrence of a new species is related to ballast water, it is very likely that ballast water, which is regularly discharged in the port of Ploče during the loading of ships, served as a transmission vector for this neritic tintinnid species. The non-indigenous copepod species Pseudodiaptomus marinus [54] and a very high proportion of non-indigenous macrozoobenthic species have already been found in this port [55]. Interestingly, P. marinus was also found upstream from the port of Ploče (S2 station in our study), confirming seawater intrusion into the upper reaches of the river [56]. According to the available data, a total of 1.035 × 106 m3 of ballast water was discharged into the Port of Ploče since 2013, with the largest amount in 2021 [57]. More than 90% of the ballast discharged into this port originated from the Mediterranean Sea (70% from the Adriatic Sea). The presence of R. tagatzi in ballast water tanks [15,49,53] suggests that transport by ballast water is the likely mechanism for the spread of this species in the Adriatic. The formation of cysts is an additional advantage for the spread of this genus [58,59]. In addition to transmission through ballast water, transfer through aquaculture has also been mentioned as one of the introduction or dispersal routes for this tintinnid species [4]. According to the authors, transfer of juvenile mussels from natural spawning areas to nurseries (mussel farms) is a common practice. However, since mussel farming in Mali Ston Bay (Figure 1) has been carried out in a traditional way with autochthonous juveniles since the 16th century [60], we can consider this method of introduction of R. tagatzi into the Adriatic Sea as unlikely.
One of the problems in the identification of non-indigenous species (NIS) species is the insufficient number of studies. R. tagatzi is a relatively large tintinnid with a very peculiar morphology, so it is difficult to assume that it was not noticed in previous studies. Extensive surveys of zooplankton at the terminals used for cargo loading in the twelve Adriatic ports were conducted in 2013–2016 as part of the BALMAS project (www.balmas.eu), but the finding of this species was not reported. However, the zooplankton survey focused on mesozooplankton [61], while microzooplankton was surveyed only in four Croatian ports (Pula, Rijeka, Šibenik and Split) [62]. As a semi-enclosed sea with limited water exchange with other seas, the Adriatic Sea is highly susceptible to any form of pollution, introduction of non-indigenous species, and thus to any hazards arising from the discharge of ballast water. It is unclear what impact introduced tintinnids may have on the local food web.
There is a possibility that many introduced species will not have a significant impact at the point of introduction. However, even if an introduced organism does not cause an obvious ecological problem, it may displace native species and eventually lead to a decline in biodiversity. These introductions are expected to increase in the future. Therefore, it is of interest to monitor endangered areas to assess ecological status and identify introductions and their impact on the native community. Thus, this study could be a good basis for further research and contribute to a better understanding of the functioning of pelagic ecosystems, especially in ecologically sensitive ecosystems.

5. Conclusions

The paper documents the first occurrence of the alien tintinnid ciliate Rhizodomus tagatzi in the Adriatic Sea, in the habitat of the transitional waters of the Neretva River estuary.
The results confirm that the species occurs in the warm season (20.01–25.51 °C) and tolerates a wide range of salinity (30.88–38.71). The maximum abundance of ~2 × 103 L−1 cells is among the highest in the Mediterranean and surrounding seas and is related to the intrusion of a seawater wedge into the riverbed itself. The formation of dense populations and their dominance in the tintinnid community may have a strong impact on ecosystem functioning.
According to our study, it is very likely that ballast water is the main transmission vector for this neritic tintinnid species in the Adriatic Sea. Although this species is not currently an obvious ecological problem in the estuary, it may displace native species and reduce biodiversity. Therefore, this study could be a good basis for further research and contribute to a better understanding of the functioning of pelagic ecosystems, especially in ecologically sensitive environments.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/w15101821/s1, Figure S1: Relative abundance of Rhizodomus tagatzi in tintinnid community at two stations and three sampling depths in the Neretva River estuary from May 2022 to January 2023; Table S1: List of the tintinnid taxa identified at two stations in the Neretva River estuary in the period from May 2022 to January 2023 (+, present; blank, absent).

Author Contributions

Conceptualization, N.B. and D.L.; methodology, J.N. and N.B.; formal analysis, N.B.; investigation, J.N., D.L. and I.V.; resources, J.N. and D.L.; data curation, J.N.; writing—original draft preparation, N.B. and J.N.; writing—review and editing, N.B., I.V. and D.L.; visualization, N.B. and I.V.; supervision, D.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

The data supporting the findings of this research are available upon reasonable request from the first author.

Acknowledgments

We thank the fishermen and residents of the Neretva estuary, especially Mile Marević for his active support during the fieldwork. We are very grateful to the reviewers who contributed to the improvement of this manuscript with their comments, valuable advice, and useful suggestions. We also thank our colleague Jasna Arapov from the Institute of Oceanography and Fisheries (Split, Croatia) who helped us with the preparation and photographing of R. tagatzi with the scanning electron microscope.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Study area with the sampling stations in the Neretva River estuary (Southern Adriatic Sea) (S1, 43°1′10.0″ N 17°26′36.0″ E and S2, 43°01′4.65″ N 17°33′57.7″ E).
Figure 1. Study area with the sampling stations in the Neretva River estuary (Southern Adriatic Sea) (S1, 43°1′10.0″ N 17°26′36.0″ E and S2, 43°01′4.65″ N 17°33′57.7″ E).
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Figure 2. Photomicrographs of Rhizodomus tagatzi from the Adriatic Sea: (A) the overall lorica morphology of a specimen fixed in formaldehyde solution (scale = 50 µm), (B) aboral horn with (C) lateral buds imaged with a scanning electron microscope (SEM). [Photos by J. Njire (A) and J. Arapov and N. Bojanić (B,C)].
Figure 2. Photomicrographs of Rhizodomus tagatzi from the Adriatic Sea: (A) the overall lorica morphology of a specimen fixed in formaldehyde solution (scale = 50 µm), (B) aboral horn with (C) lateral buds imaged with a scanning electron microscope (SEM). [Photos by J. Njire (A) and J. Arapov and N. Bojanić (B,C)].
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Figure 3. Temporal and vertical variability of Rhizodomus tagatzi and other tintinnids at two stations in the Neretva River estuary from May 2022 to January 2023.
Figure 3. Temporal and vertical variability of Rhizodomus tagatzi and other tintinnids at two stations in the Neretva River estuary from May 2022 to January 2023.
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Figure 4. Scatterplot of Rhizodomus tagatzi abundances as a function of thermohaline water properties at two stations (S1 and S2) and three layers (1, 5 and 7 m depth) in the Neretva River estuary.
Figure 4. Scatterplot of Rhizodomus tagatzi abundances as a function of thermohaline water properties at two stations (S1 and S2) and three layers (1, 5 and 7 m depth) in the Neretva River estuary.
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Figure 5. Vertical temperature and salinity profiles at two stations (S1 and S2) in the Neretva River estuary from May 2022 to January 2023.
Figure 5. Vertical temperature and salinity profiles at two stations (S1 and S2) in the Neretva River estuary from May 2022 to January 2023.
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Figure 6. Non-metric multidimensional scaling (MDS) ordination of two stations (S1 and S2) and three sampling depths (1, 5 and 7 m) based on Bray–Curtis similarities from untransformed abundance data of Rhizodomus tagatzi and other tintinnids. Statistically significant separations are indicated by the dashed line at a similarity level of 6.97, Π = 9.63, and p = 0.0039. Superimposed bubbles indicate relative abundance of R. tagatzi at sampling stations and depths. (Stress = 0.01).
Figure 6. Non-metric multidimensional scaling (MDS) ordination of two stations (S1 and S2) and three sampling depths (1, 5 and 7 m) based on Bray–Curtis similarities from untransformed abundance data of Rhizodomus tagatzi and other tintinnids. Statistically significant separations are indicated by the dashed line at a similarity level of 6.97, Π = 9.63, and p = 0.0039. Superimposed bubbles indicate relative abundance of R. tagatzi at sampling stations and depths. (Stress = 0.01).
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Table
Table 2. Morphological characteristics and localities for the species Rhizodomus tagatzi, Tintinnopsis corniger or Tintinnopsis nudicauda. (The number in parentheses indicates the mean with standard deviation).
Table 2. Morphological characteristics and localities for the species Rhizodomus tagatzi, Tintinnopsis corniger or Tintinnopsis nudicauda. (The number in parentheses indicates the mean with standard deviation).
Study AreaTotal Lorica Length [µm]OLD [µm]Horn Length [µm]Reference
Peter the Great Bay, Russia (subpolar sector of the Japan Sea)168.3–244.8 (213.65 ± 1.44)30.6–35.7 (30.6)40.8–91.8 (70.25 ± 0.93)[6] 1
Strait of Hormoz and the United Arab Emirates waters166–20029–31>1/3 total length[10] 2
Urbino Lagoon (Corsica, Western Mediterranean Sea170–19030–35No data[11] 3
Lebanese coastal waters (Eastern Mediterranean Sea)130–19027–2844–46[17] 3
Marmara Sea, Gulf of Gamlik, Turkish coastal waters165–170 (167 ± 1.9)30–33 (31 ± 1.1)40–45
(43 ± 2)		[16] 2
Lake Faro, NE corner of Sicily (central Mediterranean Sea)133–250 (178)29–35 (32)
external		35–60 (50)[52] 1
Izmir Bay, Turkish coastal water18533Up to 40[15] 2
Sevastopol Bay, Black Sea133–20530–4044–46[18] 1
Adriatic Sea, Neretva River estuary149.1–217.6
(175.3 ± 19.7)		28.7–36.1
(32.1 ± 1.6)		34.3–56.5
(44.7 ± 6.0)		This paper 1
1, Rhizodomus tagatzi; 2, Tintinnopsis corniger; 3, Tintinnopsis nudicauda.
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Njire, J.; Bojanić, N.; Lučić, D.; Violić, I. First Record of the Alien Tintinnid Ciliate Rhizodomus tagatzi Strelkow and Wirketis 1950 in the Adriatic Sea. Water 2023, 15, 1821. https://doi.org/10.3390/w15101821

AMA Style

Njire J, Bojanić N, Lučić D, Violić I. First Record of the Alien Tintinnid Ciliate Rhizodomus tagatzi Strelkow and Wirketis 1950 in the Adriatic Sea. Water. 2023; 15(10):1821. https://doi.org/10.3390/w15101821

Chicago/Turabian Style

Njire, Jakica, Natalia Bojanić, Davor Lučić, and Ivana Violić. 2023. "First Record of the Alien Tintinnid Ciliate Rhizodomus tagatzi Strelkow and Wirketis 1950 in the Adriatic Sea" Water 15, no. 10: 1821. https://doi.org/10.3390/w15101821

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