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Article

Invasive Alien Species of Benthic Macroinvertebrates and Fish in the Bulgarian Sector of the Danube River—Results of the Joint Danube Survey 4 (JDS4)

by
Teodora Trichkova
1,*,
Milcho Todorov
1,
Marian Kenderov
2,
Zdravko Hubenov
3,
Ivan Botev
1,
Tihomir Stefanov
3,
Dilian Georgiev
4 and
Pavel Jurajda
5
1
Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences (IBER-BAS), 1 Tsar Osvoboditel Blvd., 1000 Sofia, Bulgaria
2
Biological Faculty, Sofia University ‘St. Kliment Ohridski’, 8 Dragan Tsankov Blvd., 1164 Sofia, Bulgaria
3
National Museum of Natural History, Bulgarian Academy of Sciences, 1 Tsar Osvoboditel Blvd., 1000 Sofia, Bulgaria
4
Biological Faculty, Plovdiv University ‘Paisii Hilendarski’, 2 Todor Samohodov Street, 4000 Plovdiv, Bulgaria
5
Institute of Vertebrate Biology, Czech Academy of Sciences, Květná 8, 603 65 Brno, Czech Republic
*
Author to whom correspondence should be addressed.
Water 2022, 14(15), 2299; https://doi.org/10.3390/w14152299
Submission received: 23 June 2022 / Revised: 17 July 2022 / Accepted: 18 July 2022 / Published: 24 July 2022
(This article belongs to the Special Issue Biological Invasions in Changing Aquatic Ecosystems: Future Perspectives)
Browse Figure
Versions Notes

Abstract

:
The aim of this study was to assess the status of aquatic invasive alien species (IAS) in the shoreline zone of the Bulgarian sector of the Danube River, Danube tributaries, and adjacent standing water bodies in the frame of the Joint Danube Survey 4 (JDS4). Seven benthic macroinvertebrates and seven fish IAS were identified. The crayfish Faxonius limosus was frequently found and abundant in the tributaries. The mussels Corbicula fluminea, Dreissena rostriformis bugensis, and Sinanodonta woodiana dominated in the Danube River and the middle and lower reaches of the tributaries, while the fish Carassius gibelio, Perccottus glenii, and Lepomis gibbosus were most abundant in the standing water bodies. The integrated biocontamination estimated by taxonomic groups (crayfish, molluscs, and fish), sampling methods, and type of water bodies ranged from moderate in the shoreline zone of the Danube River, through moderate to high in the canals and lakes, to severe in the Danube tributaries and the reservoirs. The results demonstrate the importance of IAS in the assessment of the ecological status/potential of the water bodies in the DRB. The comprehensive evaluation of the aquatic IAS pressure will provide valuable information and support for the implementation of the national and EU IAS and water policies in the DRB.

1. Introduction

The multiple usages of the Danube River have put immense pressure on this valuable resource, facilitated by climate change over the past years. This has resulted in the degradation of water quality, hydro-morphological changes, and loss of biodiversity and ecosystem functions and services in the Danube River Basin (DRB) [1,2,3,4,5,6]. The Danube River and its floodplain have also been considered an important part of the South-European Aquatic Invasion Corridor, which links the Black Sea Basin with the North Sea Basin via the Danube–Main–Rhine Canal, and part of the European invasion network [7]. Invasive alien species (IAS) are recognized as one of the main threats to aquatic biodiversity in the DRB [8,9] and a major issue to be addressed by the Danube River Basin Management Plan [10,11].
The International Commission for the Protection of the Danube River (ICPDR) supports and coordinates the implementation of the EU Water Framework Directive 2000/60/EC (WFD) [12] at a regional level in the DRB. The aim of WFD is to establish a framework for the protection and enhancement of the status of inland surface waters (rivers and lakes) and to ensure sustainable use of water resources. It also aims to ensure that all EU Member States achieve ‘good status/potential’ in all water bodies. Joint Danube Surveys (JDSs) [5,6] have been conducted every sixth year since 2001 and coordinated by ICPDR in order to produce comparable data on water quality and to harmonize water monitoring practices and procedures at the regional level in accordance with the WFD. Considering the importance of IAS in terms of the implementation of WFD, a specific IAS program has been developed and implemented during JDS4 (2019) at the national level [13,14]. Furthermore, the ICPDR has prepared a guidance document on IAS relevant to the DRB, including a list of IAS of concern to the DRB and tools for risk assessment and evaluation of impact [15]. In the frame of the IAS JDS4 Program, the experts from participating countries had a possibility to sample additional sites and use additional methods in order to improve and increase the efficiency of the applied monitoring procedures and analyses [13,14].
At the EU level, the Regulation (EU) No. 1143/2014 of the European Parliament and of the Council of 22 October 2014 on the prevention and management of the introduction and spread of invasive alien species has been in force since 2015 [16]. A list of the IAS of Union concern was adopted and is being updated regularly by the European Commission (EC), together with the scientific community and the competent authorities of the Member States [17,18,19]. Currently, the list contains 66 IAS of Union concern, of which there are 36 plants, 8 invertebrates, and 21 vertebrate species. At the national level, a list of priority alien species to Bulgaria has been developed during the ESENIAS-TOOLS project [20,21]. The list has 122 species: 40 plants, 20 fungi, and 62 animals (12 marine, 28 freshwater, and 22 terrestrial species).
There are different metrics, tools, and schemes developed with the aim to screen, assess, compare, and eventually predict the risk of invasiveness and the magnitude of the impact posed by the IAS [22,23,24,25,26]. A series of screening tools have been developed, tested, and calibrated in order to assist in the identification and assessment of risks associated with aquatic IAS and to provide support to decision makers involved in the aquatic IAS management [27]. Based on the Weed Risk Assessment (WRA) [28], the Fish Invasiveness Screening Kit (FISK) was created [29] and further adopted to other taxonomic and ecological groups: the Freshwater Invertebrate Invasiveness Scoring Kit (FI-ISK), the Marine Invertebrate ISK (MI-ISK), the Marine Fish ISK (MFISK), and the Amphibian ISK (Amph-ISK) [27,30]. Finally, the Aquatic Species Invasiveness Screening Kit (AS-ISK) combined the five taxon-specific toolkits for amphibians and freshwater and marine fish and invertebrates [27]. A conceptual risk assessment toolkit (RAT) for IAS introductions via European inland waterways was established, with specific protocols that focus on the development of environmental indicators within the socioeconomic context of the driving forces–pressures–state–impact–response (DPSIR) framework [7]. The FISK and FI-ISK screening tools, as well as the RAT risk assessment tool, were followed as approaches to develop the IAS risk assessment procedure for the DRB (IAS–RAP–Danube) [15]. Three indexes to assess the IAS pressure that can be fitted within the existing schemes for water quality assessment were proposed for data analysis during JDS4–SBC/IBC (for macroinvertebrates and fish), and BPL and BAI indexes (for all biological quality elements) [13,14]. The site-specific biocontamination index (SBCI)/integrated biocontamination index (IBCI) includes abundance and richness calculations and allows for the estimation of biocontamination at specific study sites and integrated assessments of ecosystems or other assessment units [7,31]. The biological pollution level (BPL) index classifies the impact of alien species on native species, communities, habitats, and ecosystem functioning [32]. It requires more detailed information about the alien species, together with its exact measurable impact on different spatial and temporal scales—information that is sometimes not available. The bioinvasion assessment index (BAI) considers both abundance and characteristics of each particular taxon [15].
The aim of this study was to assess the status (based on qualitative and quantitative parameters) of aquatic IAS in the shoreline zone of the Bulgarian sector of the Danube River, Danube tributaries, and adjacent standing water bodies in the frame of the Joint Danube Survey 4 (JDS4). The implementation of this task included the following objectives:
  • Monitoring of benthic macroinvertebrate IAS, with a focus on crayfish and molluscs of concern to EU, DRB, and Bulgaria;
  • Monitoring of fish IAS of concern to EU, DRB, and Bulgaria;
  • Assessment of IAS pressure in the water bodies studied.
The results will provide baseline data for comparison with other Danube River sectors and countries and for future IAS monitoring programs. The results will also help to improve further monitoring efforts and methods at a large river basin scale in Europe.

2. Materials and Methods

2.1. Study Period

The field surveys were conducted in the period July–October 2019 (Supplementary Table S1).

2.2. Study Sites

A total of 82 sites along the entire Bulgarian sector of the Danube River were visited and sampled (Figure 1 and Supplementary Table S1):
  • 38 sites in the Danube River;
  • 28 sites in the Danube tributaries, including the Yantra River Basin (with a catchment area of over 4000 m2);
  • 9 sites in the Danube River adjacent canals and lakes;
  • 7 sites in reservoirs in the DRB.

2.3. Target Species

The monitoring focused on species that are alien to Bulgaria, particularly IAS of Union concern [15], IAS of concern to the DRB [15], and priority species to Bulgaria [20,21]. The study did not consider translocated species. The target taxonomic groups were crayfish, molluscs and fish. These groups contain the highest percentage of alien species and are easily identified to a species level. The alien benthic macroinvertebrate species belonging to other taxonomic groups were also registered but not included in the analyses of IAS pressure.

2.4. Collection and Processing of Samples

The samples of animals were collected and processed according to the standard procedure for IAS monitoring during JDS4 [13,14,15] and methods developed and tested in the frames of the projects ESENIAS-TOOLS [20] and IBBIS [33].
The benthic invertebrates were sampled by using the following methods:
  • Triangular dredge net (33/33 cm) towed from the shore (up to 2 m depth);
  • Rectangular dredge net (50/20 cm) towed from the shore or a boat (from 2 to 4.5 m depth);
  • Dip net and sieves;
  • LiNi traps for the collection of crayfish.
The fish were caught by using the following methods:
  • Beach seine nets–with a length of 7 m and a mesh size diameter of 5 mm (for the Danube River) and a length of 5 m and a mesh size of 4 mm (for inland water bodies);
  • Dip net–with a diameter of the opening of 60 cm and a mesh size of 4 mm;
  • LiNi traps;
  • Gill nets.
Some of the collected animals were determined and counted in the field and released back into the water. The rest of the samples were fixed in alcohol and processed under laboratory conditions. The crayfish, molluscs, and fish were determined to the species level, while the other benthic invertebrate taxa were determined to the lowest possible taxonomic level.

2.5. Analysis of Data

The data were analyzed by types of water body and by taxonomic groups.
The frequency of occurrence (dF, %) was determined in all analyzed groups. The relative abundance (RA, %) was calculated for benthic macroinvertebrates, while the relative abundance and catch-per-unit effort (CPUE—number of individuals per 100 m of shoreline) were calculated for fish [34].
The level of biocontamination of sampling sites was assessed based on the site-specific biocontamination index (SBCI) derived from the two metrics: (1) abundance contamination index (ACI), which is the ratio between number of specimens of alien species and total number of specimens in the sample; and (2) ordinal richness contamination index (RCI), which is the ratio between total number of alien species and total number of identified species [7,13,14,15,31]. With values of ACI and RCI, SBCI was derived from a matrix which has five index classes: 0 (no biocontamination), 1 (low biocontamination), 2 (moderate biocontamination), 3 (high biocontamination), and 4 (severe biocontamination) [7,31]. The integrated biocontamination index (IBCI) for each type of water body was calculated by averaging the ACI and RCI of all studied sites and ranking IBCI on mean values according to the same matrix [7,31]. The IBCI for each sampling site was obtained as a median of SBCI for different taxonomic groups (crayfish, molluscs, and fish) and sampling methods. The ecological status of the studied water bodies was evaluated based on the level of biocontamination [7,31]. When IBCI for a water body had an intermediate value, the worse ecological status was accepted.
As mentioned above, the biocontamination index was assessed separately for each taxonomic group and for each sampling method. Regarding the studied sites in the Danube River, the index was assessed based on the data of crayfish, molluscs at different depths (up to 2 m and between 2 and 4.5 m), and fish sampled by beach seine and gill nets (Supplementary Table S4). Then the IBCI was calculated for each site and for each taxonomic group. A similar approach was applied to other sites depending on the relevant taxonomic groups and sampling methods. The biocontamination index of the studied sites in the Danube tributaries was assessed separately based on data on crayfish, molluscs, and fish (Supplementary Table S7). Regarding the standing water bodies, the biocontamination index of different sites was assessed based on data on molluscs (Gastropoda) and fish for canals and lakes (Supplementary Table S10); and on data on crayfish, molluscs (Bivalvia), and fish for reservoirs (Supplementary Table S12).
The taxonomy of benthic invertebrates is according to References [35,36], and the taxonomy of fish is according to References [37,38,39].

3. Results

A total of 97 samples of benthic macroinvertebrates (11,426 specimens) and 64 samples of fish (7473 specimens) were collected and processed. We identified 60 taxa of benthic macroinvertebrates and 45 fish species. Of them, 14 species (7 macroinvertebrates and 7 fish) are invasive alien species, including 4 IAS of Union concern, 14 IAS of DRB concern, and 13 species of priority to Bulgaria (Table 1). Six IAS originate from North America, seven IAS originate from Asia, and one (Dreissena rostriformis bugensis) is of Ponto–Caspian origin but considered alien to the DRB.

3.1. Danube River

The benthic macroinvertebrate animals recorded in the Bulgarian sector of the Danube River included 2 crayfish species; 23 mollusc species (15 Gastropoda and 8 Bivalvia) (Table 2 and Supplementary Table S2); and representatives of Bryozoa, Turbelaria, Amphipoda, Trichoptera, Diptera, etc. Of them, seven species were alien to Bulgaria and the Danube River: Pectinatella magnifica, Girardia tigrina, Faxonius limosus, Physella acuta, Sinanodonta woodiana, D. rostriformis bugensis, and Corbicula fluminea.
A total of 35 fish species were recorded in the Danube River, one of them caught by fishermen (Ctenopharyngodon idella) (Table 2 and Table S3). Two of these species (Pseudorasbora parva and Lepomis gibbosus) are IAS of Union concern, DRB concern and priority to Bulgaria, while three of the species (Carassius gibelio, Ctenopharyngodon idella, and Hypophthalmichthys molitrix) are IAS of DRB concern and priority to Bulgaria. Among all fish IAS, most frequently found was C. gibelio.
The integrated biocontamination index of different sites ranged from ‘no biocontamination’ to ‘severe biocontamination’ (Supplementary Table S4). At seven sites, there were no IAS found, and correspondingly, their ecological status was assessed as ‘high’. At seven sites, the biocontamination was low, which corresponded to ‘good’ ecological status. At 12 sites, the biocontamination was moderate and they were assessed of ‘moderate’ ecological status related to IAS. At three sites, the biocontamination was high (‘poor’ ecological status), while at six sites, it was severe (‘bad’ ecological status) (Supplementary Table S4). Regarding distribution of sites along the Bulgarian sector of the Danube River, the sites with high and severe biocontamination were located in the middle section from Dolni Tsibar Village to Marten Village (downstream of Ruse Town). The upstream sites (from Vrav Village to Lom Town) were characterized with ‘no biocontamination’ to ‘moderate biocontamination’, with the exception that the site at the Vidin canal, where the biocontamination was higher, while the sites downstream of Marten had low to moderate biocontamination.
Among different taxonomic groups, the integrated biocontamination was the highest (4) related to molluscs at depths above 2 m. In the rest of the groups, the integrated biocontamination was from low to moderate (1–2). The integrated biocontamination index for the entire Bulgarian sector also showed moderate biocontamination, corresponding to ‘moderate’ ecological status (Table 3 and Supplementary Table S4).

3.2. Danube Tributaries

In the Danube tributaries, two species of crayfish and 10 molluscs (4 Gastropoda and 6 Bivalvia) were found (Table 2 and Table S5), as well as representatives of Oligochaeta, Odonata, Ephemeroptera, Heteroptera, Coleoptera, etc. Of them four species were alien to Bulgaria and the DRB: F. limosus, P. acuta, S. woodiana and C. fluminea.
A total of 29 fish species were found in the tributaries, of which three IAS–C. gibelio, P. parva and L. gibbosus. Among IAS most frequently found was C. gibelio, which was also one of the most abundant species (Supplementary Table S6).
At seven sites, there were no IAS recorded, and correspondingly, their ecological status was assessed as ‘high’. Those were sites located in the middle reaches of the tributaries in Northwest Bulgaria and at tributaries in the Yantra River Basin. At five sites, the biocontamination was moderate, and accordingly, the ecological status was assessed as ‘moderate’. Those were also mostly sites located in the upper reaches of the Yantra River Basin. At the rest 13 sites, the integrated biocontamination was estimated from high to severe, and the ecological status was rated from ‘poor’ to ‘bad’. Those were the sites in the lower and lowermost reaches of the Danube tributaries (Supplementary Table S7).
The integrated biocontamination by taxonomic groups was assessed as severe (4) related to crayfish and molluscs, and moderate (2) related to fish. Based on these results, the integrated biocontamination level of all Danube tributaries was assessed as severe, which showed ‘bad’ ecological status based on IAS (Table 3 and Supplementary Table S7).

3.3. Lakes and Canals

In the studied standing water bodies adjacent to the Danube River (lakes and canals), seven species of molluscs (Gastropoda) were found (Table 2 and Supplementary Table S8), as well as representatives of Turbelaria, Hirudinea, Isopoda, Odonata, Ephemeroptera, Heteroptera, Coleoptera, and Diptera. Two of the species were alien to Bulgaria and the DRB–Girardia tigrina and P. acuta. Girardia tigrina had high relative abundance in Malak Preslavets Lake (Supplementary Table S8).
Regarding fish, 19 species were recorded, of which five IAS: C. gibelio, P. parva, Ameiurus melas, L. gibbosus, and Perccottus glenii (Table 2 and Supplementary Table S9). Carassius gibelio and P. glenii occurred most frequently at the studied sites, while C. gibelio had the highest relative abundance (Supplementary Table S9).
At one of the sites (Canal at Dobri Dol Village), there was no IAS recorded. At four sites, the IBCI was from low to moderate; at one site, it was high; and at two sites, it was severe.
Regarding taxonomic groups, the integrated biocontamination level was low related to gastropods—the alien P. acuta was recorded only at one site. However, in relation to fish, the integrated biocontamination level was severe. Based on these data, the IBCI of all standing water bodies adjacent to the Danube River showed moderate-to-high biocontamination (Table 3 and Supplementary Table S10).

3.4. Reservoirs

Two native crayfish species, namely Astacus astacus and Astacus leptodactylus, and two species of the genus Dreissena, namely the native D. polymorpha and the alien D. rostriformis bugensis, were recorded in the studied reservoirs. In Ogosta Reservoir, where both Dreissena species occurred, the relative abundance of D. rostriformis bugensis was much higher (84%) than that of D. polymorpha.
In the reservoirs, nine fish species were recorded, of which three were IAS, namely C. gibelio, A. melas and L. gibbosus. Lepomis gibbosus occurred most frequently and ranked second in abundance after the native goby Neogobius fluviatilis (Table 2 and Supplementary Table S11).
At two of the sites, the integrated biocontamination was from low to moderate; at one site, it was from high to severe; and at two sites, it was severe. Regarding taxonomic groups, there was no biocontamination related to crayfish, while the biocontamination was severe related to molluscs and fish. The IBCI for all reservoirs and groups also showed severe biocontamination (Table 3 and Supplementary Table S12).
The integrated biocontamination by type of water bodies and by different taxonomic groups and methods of sampling at all studied sites in Bulgaria during JDS4 ranged from moderate in the shoreline zone of the Danube River, to moderate to high in the canals and lakes adjacent to the Danube River, and to severe in the Danube tributaries and studied reservoirs (Table 3).

4. Discussion

A total of 14 species (7 benthic macroinvertebrates and 7 fish species) were identified as IAS of concern to EU and DRB, and priority to Bulgaria, out of 60 taxa of benthic macroinvertebrate animals and 45 fish species recorded in the shoreline zone of the Bulgarian sector of the Danube River, the Danube tributaries, and the adjacent standing water bodies during JDS4. These numbers account for up to 12% of all benthic macroinvertebrate taxa and 16% of all fish species recorded in Bulgaria during the present study. For comparison, the number of IAS for the whole Danube River Basin during JDS4 was 35 benthic macroinvertebrates and 17 fish species [9]. However, of them, 21 benthic macroinvertebrates and 5 fish species are of Ponto–Caspian origin and considered native to the Lower Danube, including the Bulgarian sector.
Two crayfish species were recorded in the Danube River and the tributaries—the native Pontastacus leptodactylus and the alien F. limosus (Table 2). In the Danube River, F. limosus was found at only one site, and its relative abundance was close to that of P. leptodactylus. However, in the tributaries, the frequency of occurrence and relative abundance of F. limosus was almost two times higher than that of P. leptodactylus. In Bulgaria, F. limosus was first reported in 2015 from three tributaries of the Danube River, in the northwestern part of the country [40]. It was assumed that the species has been introduced through natural dispersal downstream from the Serbian and Romanian sectors, where it was reported earlier [41,42,43]. Our results confirm the occurrence of the species at those sites, and we also report it from the Danube River at an open canal in Vidin Town (786 rkm). This crayfish species seems to further continue its spread downstream, as its most recent records are from the Danube River at Skomen Island (760 rkm), where an abundant population was observed on 24 September 2021 [44].
Regarding molluscs, an overall decrease in the former abundance of C. fluminea was reported in some Danube River sections during JDS4 compared to previous JDSs [9]. In the Bulgarian section, at depths of up to 2 m, although with lower values than gastropods, C. fluminea had the highest frequency and relative abundance compared to all other mussels; meanwhile, at depths of 2–4.5 m, this species had the highest frequency (found at 10 of 11 studied sites) and relative abundance (76.46%) compared to all molluscs (Supplementary Table S2). In addition, unusual massive mortality of this species was observed, especially in July 2019. Large amounts of soft tissues of C. fluminea were flowing in the water, while numerous shells and dying individuals were stranded within shallow disconnected pools. This could be owing to abrupt changes in water level in combination with other factors. The water level was low during all sampling period, decreasing in July and August to average values around 100 cm at Novo Selo Village (834 rkm) and Ruse Town (495 rkm), and reaching the lowest values in October: −6 cm in Ruse, and an average of 40 cm in Novo Selo [45]. Extreme abiotic conditions, including both drought and flooding, as well as high and low temperatures, are recognized as the primary drivers of mass mortality events in invasive freshwater bivalves [46,47]. Large-scale mortality of invasive bivalves, including C. fluminea, caused by drought conditions, has already been reported in the Danube River [48]. Another reason for mass die-offs of C. fluminea could be food limitations under unfavorable water temperatures. Impressive summer mortalities of C. fluminea reported from the rivers Rhine, Saône, and Meuse/Maas have been associated with food limitation during heatwaves [49,50,51]. In July and August, the average water temperature in the Danube River littoral during our survey was 27.8 °C. The concentration of dissolved oxygen ranged from 5.6 to 14.6 mg/L, and the oxygen saturation ranged from 70 to 194%.
In the Danube tributaries, C. fluminea occurred most frequently among all molluscs, followed by S. woodiana. Corbicula fluminea also showed the highest relative abundance (70.66%) (Supplementary Table S5). The two mussel IAS of Asian origin have similar patterns of introduction and spread to the Bulgarian waters. The first specimens of C. fluminea were reported in 2001 from three different sites in the Danube River (807, 597, and 395 rkms) [52,53,54]. In the following years, this species has established itself in the entire Bulgarian sector, where it reached densities of up to 16,560 ind./m2. The species extended its range rapidly upstream of the Danube tributaries and also established in standing water bodies (reservoirs and sand-pit lakes), reaching altitudes of up to 525 m a.s.l. [53,54]. Sinanodonta woodiana was reported at first from the Danube River sector between 655 and 498 rkms in 2005 [55] and spread subsequently along the entire Bulgarian sector and upstream of the tributaries [53]. The results of the present study showed extension in the range of the two mussels in Bulgaria. Compared to previously published data [54,55], C. fluminea is reported from new rivers (Topolovets, Voinishka, and Lom), and new upstream localities of the Yantra River (at Ledenik Village) and its tributaries the Rositsa River (at Resen Village), and Stara Reka River (at Gorski Dolen Trambesh Village) (Figure 1 and Table 2). Sinanodonta woodiana is newly reported from the Archar and Lom rivers and new upstream localities of the Yantra River (at Dolna Oryahovitsa Town) and its tributary the Stara Reka River (at Gorski Dolen Trambesh Village) (Figure 1, Table 2). Another mussel IAS which showed comparatively high relative abundance in the Danube River was D. rostriformis bugensis (Supplementary Table S2). In the Danube River, this species had a lower frequency of occurrence than the native D. polymorpha, and its abundance was higher only at higher depths. However, in Ogosta Reservoir, where both Dreissena species occurred, the relative abundance of D. rostriformis bugensis was much higher than that of D. polymorpha (84% vs. 16%, respectively). The first records of D. rostriformis bugensis from the Danube River and Ogosta Reservoir were from 2005 [56,57]. Pectinatella magnifica was recorded at two sites during the present survey, which are the first records of this species in the Bulgarian shoreline zone of the Danube River [58]. Based on the earlier records from the Serbian–Romanian sector during JDS3 [59] and from the Ukrainian part of the Danube Delta Biosphere Reserve [60], it was assumed that the species had already been present in the Bulgarian sector, but in low abundance and size of colonies [58].
The results of the present survey showed a comparatively low abundance of fish IAS in the Danube River (Supplementary Table S3). C. gibelio occurred most frequently, at 37.04%. These results do not differ considerably from an earlier study (2005/2006) of the ichthyofauna in the shoreline zone of the Danube River in Bulgaria, using two methods, beach seine and electrofishing [34]. The recorded fish IAS (C. gibelio, P. parva, G. holbrooki, L. gibbosus, and P. glenii) had comparatively low frequency of occurrence and abundance. More recent (2015 and 2016) fish monitoring in the Bulgarian Danube River sector by six sampling methods reports that C. gibelio had a relative abundance of 1.64% among all fish [61]. Among other IAS detected (C. idella, H. molitrix, P. parva, L. gibbosus, and P. glenii), P. parva was most abundant, followed by L. gibbosus. The JDS4 assessment of fish data for the entire Danube River showed that the alien Hypophthalmichthys sp. and C. gibelio were among the 20 most abundant species, ranking seventh and eighth, respectively [62]. In the present study, Hypophthalmichthys molitrix was detected in the gill net catches, although in low relative abundance (Supplementary Table S3). However, according to local fishermen, this species has been regularly found in the catches recently. In the Danube tributaries, C. gibelio was most frequently found among the IAS and is one of the species with the highest abundance (Supplementary Table S6).
The highest percentage of fish IAS was recorded in the standing water bodies—canals, lakes, and reservoirs adjacent to the Danube River. Most frequently found and most abundant in these water bodies were C. gibelio, P. glenii, and L. gibbosus. Pseudorasbora parva and A. melas were also detected in standing waters but of lower frequency and abundance (Supplementary Tables S9 and S11). Similar to the invasion pattern of the macroinvertebrate IAS discussed above, the introduction of fish IAS to Bulgaria has been associated with the Danube River. Lepomis gibbosus was first recorded in 1920 in Svishtov Marsh along the Danube River, and, since then, it has spread to all river basins in Bulgaria [63]. The occurrence of C. gibelio in the Bulgarian sector of the Danube River was reported for the first time in the 1940s [64]. The genetic diversity based on allozyme analyses of 10 populations of C. gibelio indicated a gene flow from the DRB to the water bodies of the Aegean Sea and the Black Sea basins in Bulgaria [65]. The first records of P. parva in Bulgaria were reported in 1975 from Mechka fishponds along the Danube River near Ruse [66], and in 1976 from Malak Preslavets Marsh and the Danube River near Krivina Village [67]. From the Danube River and adjacent ponds and marshes, the species spread rapidly to the inland water bodies of Bulgaria [68,69]. Perccottus glenii and A. melas are comparatively recent invaders whose distribution is still confined to the DRB [70,71]. In Bulgaria, Perccottus glenii was reported first in 2005 from the Danube River in the region of Vidin [34,72], while A. melas was found in Srebarna Lake in 2013 [70].
Shipping and inland canals, as well as aquaculture, pet/aquarium trade, and stocking activities, are identified as the major pathways of introduction of freshwater IAS in Europe [73]. The same pathways are valid for the Danube River and DRB in Bulgaria. Most of the benthic macroinvertebrates and fish have probably been introduced and spread in the Bulgarian sector of the Danube River through secondary natural dispersal from neighboring countries in both directions, downstream and upstream. This can happen with passive transport of statoblasts (P. magnifica) [58], or planktonic larvae of bivalves (C. fluminea and D. rostriformis bugensis) [54,56]; by parasitic larvae–glochidia, using different fish hosts [55]; or by active movement (crayfish and fish) [40,72]. The introduction and spread of IAS to the Bulgarian Danube River section may be additionally facilitated by international shipping, boating, aquaculture, and fishing activities; for example, P. parva was considered to be introduced along with the introduction of herbivorous Asian carps (Hypophthalmichthys molitrix, H. nobilis, and C. idella) to Mechka fishponds or other fish farms along the Danube River located upstream [66,67]. When established in the Bulgarian sector of the Danube River and adjacent canal systems and lakes, the species further spread to inland waters, using various pathways, as passive or active movement upstream of the tributaries (C. fluminea, A. woodiana, and F. limosus) [40,53,54], spring high waters, and flooding (P. glenii) [72], or associated with human activities. The following were identified as potential dispersal mechanisms of Dreissena sp. in the reservoirs of Northwestern Bulgaria: the direct waterway connection with the Danube River, as well as transport of larvae and adult individuals with fishing equipment, boats, and fish stocking material from the Danube River, fish farms nearby, and other infested reservoirs [57,74]. Activities such as sand and gravel extraction and transportation, aquaculture, fishing and use of live bait, and recreational activities have most likely facilitated the introduction of aquatic IAS in the river system and standing water bodies in the region [54,57,65,69,71,74].
The JDS4 has confirmed the results of previous JDSs and concluded that DRB is under considerable influence of biological invasions [9]. It highlights that the number of identified alien species has increased since 2007. The level of biocontamination of the Danube River was estimated as moderate to high, with higher levels for the Upper (high to severe biocontamination) and Middle Danube (moderate to high biocontamination), in comparison to the Lower Danube (low biocontamination). The reduced pressure by IAS in the Lower Danube River is explained by the fact that Ponto–Caspian species are considered native in this section [9]. Our assessment of the integrated biocontamination index for the Bulgarian sector of the Lower Danube showed a higher level of IAS impact—moderate biocontamination, indicating ‘moderate’ ecological status. This difference could be due to some of/combination of the following factors: (i) much higher number of additional sites sampled (totally 38 compared to 3 JDS4 sites for benthic macroinvertebrates and 6 for fish as biological quality elements in Bulgaria); (ii) sampling only in the shoreline zone (up to 4.5 m for benthic macroinvertebrates and 7 m for fish); and (iii) using additional methods as dredges and a dip net for benthic macroinvertebrates and beach seine net, dip, and gill nets for fish. Our assessment also revealed moderate-to-high biocontamination in the canals and lakes adjacent to the Danube River, severe (‘bad’ ecological status) in the Danube tributaries, and severe biocontamination in the studied reservoirs. A previous assessment of 12 reservoirs in the DRB, Northwestern Bulgaria, based only on metrics of benthic macroinvertebrates, including IBCI, classified the ecological potential of the reservoirs in the range from ‘Good’ to ‘Bad’, with most of them being ‘Moderate’ [75]. The established aquatic IAS in the surveyed region may have environmental and/or socioeconomic impact manifested by various mechanisms, such as competition, predation, transfer of parasites, biofouling, etc., and magnitude [24,25,26]. For example, changes in water physical and chemical parameters (water column transparency, oxygen concentration, pH, nutrients, etc.) and alteration of trophic structure as a result of Dreissena sp. filtration activities are reported in the Ogosta Reservoir and other infested reservoirs in the DRB [76,77,78,79,80,81]. The presence of D. rostriformis bugensis and D. polymorpha in the Ogosta Reservoir has caused direct and/or indirect effects on size structure and quantitative parameters of bacterioplankton [79,82]. Dreissena infestation in reservoirs and lakes in the DRB has been reported to also influence the dominant structure and quantitative composition of phytoplankton and zooplankton [79,80,83,84,85], as well as the benthic macroinvertebrate and fish communities [75,77]. Damages on irrigation and fish cage facilities due to Dreissena biofouling have been documented in Ogosta and other reservoirs in the region [57]. Clogging of fishing nets by P. magnifica was reported by fishermen in the Danube River [58]. New alien fish parasites have been introduced with fish IAS: L. gibbosus in Ogosta and Kula reservoirs [86] and A. melas in Srebarna Lake [87] that may have a potential adverse impact on native ichthyofauna. The recently introduced crayfish IAS F. limosus is expected to have a negative impact on native crayfish populations in Bulgaria through the competition for resources and as a vector of the crayfish plague Aphanomyces astaci [88,89]. In the Romanian sector of the Danube River, the introduction of F. limosus has already caused a dramatic decrease in abundance and replacement of 70–90% of the P. leptodactylus population by F. limosus. The presence of A. astaci DNA is detected in at least 32% of the invasive and 41% of the native crayfish coexisting in the Danube River [88]. More studies need to be conducted to further evaluate the potential impact of benthic macroinvertebrate and fish IAS in the DRB in Bulgaria.

5. Conclusions

During the present study, the integrated biocontamination estimated by taxonomic groups (crayfish, molluscs, and fish), sampling methods, and type of water bodies ranged from moderate, indicating ‘moderate’ ecological status, in the shoreline zone of the Danube River; from moderate to high in the canals and lakes adjacent to the Danube River; to severe (‘bad’ ecological status) in the Danube tributaries; and severe in the studied reservoirs. These results clearly demonstrate the importance of IAS in the assessment of the ecological status/potential of the water bodies in the DRB. They also highlight the necessity of extending the sampling area by covering the Danube River, as well as selected Danube tributaries and adjacent standing water bodies and wetlands. Many IAS, which have been introduced through the Danube River by natural dispersal across borders, have found suitable habitats and established abundant populations in the tributaries (crayfish and mussels) or adjacent standing water bodies (fish). The impact of IAS on these water bodies, most of which are habitats of rare and threatened species, is expected to be much higher compared to the Danube River. They also may facilitate the spread of IAS into the inland waters of Bulgaria, e.g., by passive or active dispersal upstream of the tributaries and/or by human activities (sand and gravel extraction, aquaculture, fishing, recreation, etc.). For future IAS monitoring programs, we can further recommend the adaption and application of additional/new methods of sampling, which may be more efficient for IAS early detection related to particular groups of species and habitats. The comprehensive assessment of the aquatic IAS pressure will provide valuable information and support for the implementation of the national and EU IAS and water policies in the DRB.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/w14152299/s1. Table S1: Study sites with indicated geographic coordinates and the Danube River kilometres (rkm), sorted by dates and types of water body. The sites visited more than once have the same number with the number of visits in brackets. Table S2. Benthic macroinvertebrates: crayfish and molluscs (Gastropoda and Bivalvia) recorded in the Bulgarian sector of the Danube River during JDS4 (2019). dF (%)—frequency of occurrence; RA (%)—relative abundance. Table S3. Fish species recorded in the Bulgarian sector of the Danube River during JDS4 (2019). dF (%)—frequency of occurrence; RA (%)—relative abundance; CPUE—catch-per-unit effort 100 m beach seining. Table S4. Biocantamination and ecological status of studied sites in the Bulgarian sector of the Danube River during JDS4 (2019). SBCI—site-specific biocontamination index; IBCI—integrated biocontamination index of particular site or taxonomic group of animals according to the sampling method [1;2]; N/A—not assessed. Table S5. Benthic macroinvertebrates: crayfish and molluscs recorded in the Danube tributaries during JDS4. dF (%)—frequency of occurrence; RA (%)—relative abundance. Table S6. Fish species recorded in the Danube tributaries during JDS4. dF (%)—frequency of occurrence; RA (%)—relative abundance; CPUE—catch-per-unit effort 100 m dip net. Table S7. Biocantamination and ecological status of studied sites in the Danube tributaries during JDS4. SBCI—site-specific biocontamination index; IBCI—integrated biocontamination index of particular site or taxonomic group of animals; N/A—not assessed. Table S8. Benthic macroinvertebrates (Gastropoda) recorded in the standing water bodies (lakes and canals) adjacent to the Danube River during JDS4. dF (%)—frequency of occurrence; RA (%)—relative abundance. Table S9. Fish species recorded in the standing water bodies (lakes and canals) adjacent to the Danube River during JDS4. dF (%)—frequency of occurrence; RA (%)—relative abundance. Table S10. Biocantamination of studied sites in the standing water bodies (lakes and canals) adjacent to the Danube River during JDS4 (2019). SBCI—site-specific biocontamination index; IBCI—integrated biocontamination index of particular site or taxonomic group of animals. Table S11. Fish species recorded in the studied reservoirs in the Danube River Basin during JDS4 (2019). dF (%)—frequency of occurrence; RA (%)—relative abundance. Table S12. Biocantamination of studied reservoirs in the Danube River Basin during JDS4 (2019). SBCI—site-specific biocontamination index; IBCI—integrated biocontamination index of particular site or taxonomic group of animals; N/A—not assessed.

Author Contributions

Conceptualization, T.T. and M.T.; Methodology, T.T., M.T. and P.J.; Formal Analysis, T.T., M.T., I.B., Z.H. and P.J.; Investigation, T.T., M.T., M.K., Z.H., I.B., T.S., D.G. and P.J.; Writing—Original Draft Preparation, T.T.; Writing—Review and Editing, all authors. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by the Enterprise for Management of Environmental Protection Activities in Bulgaria; the Ministry of Environment and Water, Contract No. 13063/03.07.2019; and Alien CSI Cost Action CA17122, co-funded by the National Science Fund of Bulgaria, Project KP-06-COST-13/06.08.2019. T.T., M.T., T.S., and P.J. were additionally supported by the Ministry of Education and Science of Bulgaria (Agreement No. DO-230/06-12-2018) and through Bilateral grant agreement between the Bulgarian Academy of Sciences and Czech Academy of Sciences. The publication of this paper was funded by the National Science Fund of Bulgaria, Project KP-06-COST-13/06.08.2019.

Institutional Review Board Statement

The research projects of IBER-BAS, under which the present study was conducted, were approved by the Scientific Council and included in the scientific plan of IBER-BAS according to the following protocols: No. 55/20.11.2018, 5/17.05.2019, 6/14.06.20019, 8/20.09.2019 and 9/18.10.2019.

Data Availability Statement

All data generated or analysed during this study are included in this published article and the Supplementary Materials.

Acknowledgments

We acknowledge the support and coordination of the Executive Environment Agency (ExEA), Bulgaria; the International Commission for the Protection of the Danube River (ICPDR); and the Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences (IBER-BAS). We are grateful to Mina Asenova from ExEA, Momir Paunović from ICPDR, and Luchezar Pehlivanov from IBER-BAS for their assistance and support. We express our gratitude to the following institutions and persons for their collaboration: Executive Agency of Fishery and Aquaculture (EAFA), Vidin; Regional Inspectorate of Environment and Water (RIEW), Montana; RIEW, Ruse; Milen Metodiev from EAFA, Vidin; Anelia Nikolova from RIEW, Ruse; Lyubomir Kenderov from the Biological Faculty of Sofia University (BF-SU); and Vladimir Vladimirov from IBER-BAS. We also thank Mario Vichev, Georgi Angelov, Lyubomir Krasimirov, and Yordan Yordanov for the help during the field survey.

Conflicts of Interest

The authors declare that they have no known conflict of interests or personal relationships that could have appeared to influence the work reported in this paper.

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Water 14 02299 g001 550
Figure 1. Map of the study area and sites (indicated with red dots) in the Danube River Basin (Bulgaria) during JDS4 (2019). For numbers of sampling sites, please see Supplementary Table S1.
Figure 1. Map of the study area and sites (indicated with red dots) in the Danube River Basin (Bulgaria) during JDS4 (2019). For numbers of sampling sites, please see Supplementary Table S1.
Water 14 02299 g001
Table
Table 1. List of invasive alien species (IAS) of benthic macroinvertebrates and fish recorded in the Bulgarian sector of the Danube River and adjacent water bodies during JDS4 (2019). X—indicates the status of the species according to the following categories: invasive alien species (IAS) of Union concern, IAS of Danube River Basin (DRB) concern and priority species to Bulgaria.
Table 1. List of invasive alien species (IAS) of benthic macroinvertebrates and fish recorded in the Bulgarian sector of the Danube River and adjacent water bodies during JDS4 (2019). X—indicates the status of the species according to the following categories: invasive alien species (IAS) of Union concern, IAS of Danube River Basin (DRB) concern and priority species to Bulgaria.
No.TaxonNative RangeIAS of Union ConcernIAS of DRB ConcernPriority Species to Bulgaria
Bryozoa
Pectinatellidae
1Pectinatella magnifica (Leidy, 1851)North America XX
Turbelaria
Dugesiidae
2Girardia tigrina (Girard, 1850)North America X
Decapoda
Cambaridae
3Faxonius limosus (Rafinesque, 1817)North AmericaXXX
Gastropoda
Physidae
4Physella acuta (Draparnaud, 1805)North America XX
Bivalvia
Unionidae
5Sinanodonta woodiana (I. Lea, 1834)Asia XX
Dreissenidae
6Dreissena rostriformis bugensis (Andrusov, 1897)Ponto–Caspian species XX
Cyrenidae
7Corbicula fluminea (O.F. Müller, 1774)Asia XX
Actinopterygii
Cyprinidae
8Carassius gibelio (Bloch, 1782)Asia X
9Ctenopharyngodon idella (Valenciennes, 1844)Asia X
10Hypophthalmichthys molitrix (Valenciennes, 1844)Asia XX
11Pseudorasbora parva (Temminck and Schlegel, 1846)AsiaXXX
Ictaluridae
12Ameiurus melas (Rafinesque, 1820)North America XX
Centrarchidae
13Lepomis gibbosus (Linnaeus, 1758)North America XX
Odontobutidae
14Perccottus glenii Dybowski, 1877AsiaXXX
Table
Table 2. List of all species of benthic macroinvertebrates (crayfish and molluscs) and fish recorded in the Bulgarian sector of the Danube River and adjacent water bodies during JDS4 (2019). X—indicates the presence of the species in the corresponding type of water body monitored (Danube River, Danube tributaries, lakes and canals, and reservoirs). For quantitative parameters, see Supplementary Materials Tables S2, S3, S5, S6, S8, S9 and S11.
Table 2. List of all species of benthic macroinvertebrates (crayfish and molluscs) and fish recorded in the Bulgarian sector of the Danube River and adjacent water bodies during JDS4 (2019). X—indicates the presence of the species in the corresponding type of water body monitored (Danube River, Danube tributaries, lakes and canals, and reservoirs). For quantitative parameters, see Supplementary Materials Tables S2, S3, S5, S6, S8, S9 and S11.
TaxonDanube RiverDanube TributariesLakes and CanalsReservoirs
Decapoda
Astacus astacus (Linnaeus, 1758) X
Pontastacus leptodactylus (Eschscholtz, 1823)XX X
Faxonius limosus (Rafinesque, 1817)XX
Gastropoda
Theodoxus danubialis (Pfeiffer, 1828)X
Theodoxus fluviatilis (Linnaeus, 1758)X
Theodoxus transversalis (Pfeiffer, 1828)X
Viviparus acerosus (Bourguignat, 1862)X
Viviparus contectus (Millet, 1813) X
Viviparus sphaeridius (Bourguignat, 1880)X
Viviparus viviparus (Linnaeus, 1758)X
Esperiana esperi (Férussac, 1823)X
Microcolpia daudebartii (Prevost, 1821)X
Holandriana holandrii (C. Pfeiffer, 1828)X
Bithynia danubialis (Glöer & Georgiev, 2012)X
Bithynia tentaculata (Linnaeus, 1758)X
Lithoglyphus naticoides (C. Pfeiffer, 1828)XX
Lymnaea stagnalis (Linnaeus, 1758) X
Radix auricularia (Linnaeus, 1758)XX
Physa fontinalis (Linnaeus, 1758) XX
Physella acuta (Draparnaud, 1805)XXX
Gyraulus laevis (Alder, 1838) X
Planorbarius corneus (Linnaeus, 1758)X X
Planorbis planorbis (Linnaeus, 1758) X
Bivalvia
Anodonta anatina (Linnaeus, 1758) X
Pseudanodonta complanata (Rossmässler, 1835)X
Sinanodonta woodiana (I. Lea, 1834)XX
Unio crassus Philipsson, 1788XX
Unio pictorum (Linnaeus, 1758)XX
Unio tumidus Philipsson, 1788X
Dreissena rostriformis bugensis Andrusov, 1897X X
Dreissena polymorpha (Pallas, 1771)XX X
Corbicula fluminea (O. F. Müller, 1774)XX
Cyprinidae
Abramis brama (Linnaeus, 1758)XX
Alburnoides bipunctatus (Bloch, 1782) X
Alburnus alburnus (Linnaeus, 1758)XXX
Ballerus ballerus (Linnaeus, 1758)X
Ballerus sapa (Pallas, 1814)X
Barbus barbus (Linnaeus, 1758)XX
Barbus petenyi (Heckel, 1852) X
Blicca bjoerkna (Linnaeus, 1758)XXX
Carassius gibelio (Bloch, 1782)XXXX
Chondrostoma nasus (Linnaeus, 1758)XXX
Ctenopharyngodon idella (Valenciennes, 1844)X
Cyprinus carpio Linnaeus, 1758XX
Gobio gobio (Linnaeus, 1758) sensu lato X
Hypophthalmichthys molitrix (Valenciennes, 1844)X
Leucaspius delineatus (Heckel, 1843)XXX
Leuciscus aspius (Linnaeus, 1758)XX
Leuciscus idus (Linnaeus, 1758)XX
Pelecus cultratus (Linnaeus, 1758)X
Pseudorasbora parva (Temminck & Schlegel, 1842)XXX
Rhodeus amarus (Bloch, 1782)XXX
Romanogobio vladikovii (Fang, 1943)X
Rutilus rutilus (Linnaeus, 1758)XXX
Scardinius erythrophthalmus (Linnaeus, 1758)X X
Squalius cephalus (Linnaeus, 1758)XXXX
Vimba vimba (Linnaeus, 1758)XX
Cobitidae
Barbatula barbatula (Linnaeus, 1758) X
Cobitis elongatoides (Băcescu & Maier, 1969)XXXX
Cobitis strumicae (Karaman, 1955)XX
Misgurnus fossilis (Linnaeus, 1758) X
Sabanejewia balcanica (Karaman, 1922) X
Ictaluridae
Ameiurus melas (Rafinesque, 1820) XX
Siluridae
Silurus glanis Linnaeus, 1758X X
Esocidae
Esox lucius Linnaeus, 1758X
Gasterosteidae
Pungitius platygaster (Kessler, 1859) X
Syngnathidae
Syngnathus abaster Risso, 1826X X
Centrarchidae
Lepomis gibbosus (Linnaeus, 1758)XXXX
Percidae
Perca fluviatilis Linnaeus, 1758XX X
Sander lucioperca (Linnaeus, 1758)X
Odontobutidae
Perccottus glenii Dybowski, 1877 X
Gobiidae
Babka gymnotrachelus (Kessler, 1857)XX
Neogobius fluviatilis (Pallas, 1811)XXXX
Neogobius melanostomus (Pallas, 1814)XX
Ponticola kessleri (Günther, 1861)XX
Proterorhinus semilunaris (Heckel, 1837)XXXX
Table
Table 3. Biocontamination of studied sites in Bulgaria during JDS4 (2019). IBCI–integrated biocontamination index.
Table 3. Biocontamination of studied sites in Bulgaria during JDS4 (2019). IBCI–integrated biocontamination index.
SitesIBCI Crayfish
(Nets)		IBCI Crayfish
(Dip Net 100 m)		IBCI
Molluscs (Dredging up to 2 m)		IBCI
Molluscs (Dredging 2–4.5 m)		IBCI
Molluscs
(Dredging 10 m2)		IBCI
Fish
(Beach Seine 100 m)		IBCI
Fish
(Dip Net 100 m)		IBCI
Fish
(Gill Nets)		IBCI
Danube River (39 sites)1 24 1 22
Danube tributaries (28 sites) 4 4 2 4
Lakes and canals (9 sites) 1 4 2/3
Reservoirs (7 sites) 4 4 4
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Trichkova, T.; Todorov, M.; Kenderov, M.; Hubenov, Z.; Botev, I.; Stefanov, T.; Georgiev, D.; Jurajda, P. Invasive Alien Species of Benthic Macroinvertebrates and Fish in the Bulgarian Sector of the Danube River—Results of the Joint Danube Survey 4 (JDS4). Water 2022, 14, 2299. https://doi.org/10.3390/w14152299

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Trichkova T, Todorov M, Kenderov M, Hubenov Z, Botev I, Stefanov T, Georgiev D, Jurajda P. Invasive Alien Species of Benthic Macroinvertebrates and Fish in the Bulgarian Sector of the Danube River—Results of the Joint Danube Survey 4 (JDS4). Water. 2022; 14(15):2299. https://doi.org/10.3390/w14152299

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Trichkova, Teodora, Milcho Todorov, Marian Kenderov, Zdravko Hubenov, Ivan Botev, Tihomir Stefanov, Dilian Georgiev, and Pavel Jurajda. 2022. "Invasive Alien Species of Benthic Macroinvertebrates and Fish in the Bulgarian Sector of the Danube River—Results of the Joint Danube Survey 4 (JDS4)" Water 14, no. 15: 2299. https://doi.org/10.3390/w14152299

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