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Scientific and Practical Center on Bioresources. National ... of alien species of invertebrates and fish into river ecosystems of Belarus have been analyzed.
Hydrobiological Journal, 2017, Vol. 53, No. 1

Alien Species of Invertebrates and Fish in River Ecosystems of Belarus: Distribution, Biological Contamination, and Impact† V. P. Semenchenko & V. K. Rizevskiy Scientific and Practical Center on Bioresources National Academy of Sciences of Belarus Minsk, Belarus

The concept of biological contamination of aquatic ecosystems and methods of its assessment are considered in the paper. Data on the distribution, main pathways and vectors of invasion, and also the influence of global factors on the processes of invasion are discussed. The effects registered as a result of invasion of alien species of invertebrates and fish into river ecosystems of Belarus have been analyzed. It has been shown that the main factors responsible for this process include hydrotechnical construction in Ukraine, navigation, and natural distribution of species. The examples of an adverse effect of invasive species on aboriginal species and communities are also given. KEY WORDS: alien species, invertebrates, fish, pathways and vectors of invasion, biological contamination, ecological influence

The problem of invasion of alien species of animals into aquatic ecosystems took on global features. It is accompanied by a set of adverse ecological, economical, and social consequences. Based on the conclusions of international experts, invasion of alien species is the second reason (after anthropogenic contamination of the environment) of dying away of aboriginal species and of the decrease in biodiversity [48]. Invasions are conditioned by different factors, including global climate changes [50, 54], the construction of various canals and reservoirs [19, 23, 35], and the increase in the intensity of navigation [5, 19, 28, 45], etc. A high frequency of successful invasions into freshwater ecosystems is conditioned by anthropogenic transformations of many water bodies and watercourses. In addition, it was favored by introduction of numerous alien species [21, 30, 47]. Unlike natural distribution of organisms, this process occurs rapidly [47]. †

Originally published in Gidrobiologicheskiy Zhurnal, 2016, Vol. 52, No. 5, pp. 28–44. 26

ISSN 0018-8166 ©

2017 Begell House, Inc.

Fig. 1: Distribution of alien species of aquatic invertebrates (above bar) and fish (below bar) in the basins of the Dnieper, Pripyat, and Neman rivers within the territory of Belarus.

It is evident that the intensity of invasion will increase [30]. This fact suggests that the process of invasion brings the threat to aboriginal species and communities and has a severe impact on ecology and economy. The literature on the distribution and influence of alien species on aboriginal communities and ecosystems is quite voluminous. This paper is dealt with some general problems on the pathways and vectors of invasion of aquatic animals into river ecosystems of Belarus, and also on the assessment of biological contamination. It should be noted that the vectors of fish invasion and its impact on aboriginal communities are better understood as compared to those of invertebrates. In addition, in aquatic ecosystems of Belarus the number of alien species of invertebrates is essentially higher than that of fish [47]. General characteristics of the alien aquatic fauna. At present 17 alien species of aquatic invertebrates and 13 species of fish are registered in river basins within the territory of Belarus. The introduced species, which do not reproduce under natural conditions of Belarus are absent in this list. The distribution of alien species in the basins of large rivers of Belarus, including the Dnieper, Pripyat, and Neman (Nemunas) rivers, is non-uniform, which is conditioned mainly by the presence of river ports (Figures 1 and 2). 27

Fig. 2: Total number of alien species of aquatic animals in the basins of large rivers of Belarus [44]. DB canal – Dnieper-Bug canal.

Fig. 3: Origin of alien species of aquatic animals in river ecosystems of Belarus.

The contribution of the species of the Ponto-Caspian complex to the total number of alien species accounts for 70% (Fig. 3). In Belarus, the increase in the number of alien species with time is almost exponential (Fig. 4). The main pathways and vectors of invasion into aquatic ecosystems of Belarus. The pathways of penetration of alien species into aquatic ecosystems of the basins of various rivers can significantly differ. The main reasons responsible for invasion into aquatic ecosystems of Belarus are as follows (Fig. 5): • Natural distribution of species from the places of their introduction favored by hydrotechnical construction (reservoirs, interbasin canals, melioration systems, etc.); 28

Fig. 4: Dynamics of the increase in the number of alien species of aquatic invertebrates and fish in river ecosystems of Belarus.

Fig. 5: Main factors responsible for the distribution of alien species of invertebrates and fish in the basins of the Dnieper and Pripyat rivers.

• Navigation; • Purposeful and non-purposeful introduction as a result of fishery; • Commerce in aquatic animals and their cultivation in aquaria. In the Pripyat and Dnieper rivers, the main factors include navigation and natural distribution of species inside basins. At the same time, the initial reason of penetration of alien species into the territory of Belarus was the construction of the cascade of reservoirs on the Dnieper River, in particular 29

of the Kiev Reservoir. At present, this water body is the main source of the alien fauna for the territory of Belarus. Some species income into the basin of the Neman River from the Kaunas Reservoir (Lithuania). Natural distribution as a result of hydrotechnical construction. Canals and their systems belonging to “invasive corridors” [9] are of considerable importance in interbasin distribution of alien species [35, 45]. The construction of the Dnieper-Bug canal was responsible for the penetration of the Ponto-Caspian fauna through the Pripyat River into the basin of the Visla River and into the Baltic Sea [22, 44]. This pathway known as the central invasive corridor is the main source of invertebrates and fish invasion into the territory of Belarus. The construction of the Minsk-Viliya water system resulted in the penetration of Neogobius fluviatilis Pallas into the Viliya River and into the territory of Lithuania. The same pattern is typical to the systems of canals connecting the Danube River with the basin of the Rhine River [51]. In addition, natural distribution of species is observed within the same basin. This is typical to fish and motile invertebrates. An example is the penetration of alien Ponto-Caspian species (Paramysis lacustris and Chelicorophium curvispinum) from the Kiev Reservoir (Ukraine) into the territory of Belarus (the Dnieper and Pripyat rivers) and from the Kaunas Reservoir (Lithuania) into the Neman River [42]. The distribution of alien species of fish in the Pripyat River essentially differs from that in the Dnieper River. Thus, in the Pripyat River among seven alien species of fish of the Ponto-Caspian origin five of them occur almost along the whole length of the river. In this case, in the upper sections of the Dnieper River their number is lower than that in its lower sections (Fig. 1). Other species of fish of the Ponto-Caspian origin (Benthophilus stellatus (Sauvage, 1874), Pungitius platygaster (Kessler, 1859), and species of the family Syngnathidae) were registered only in the lower section of the Dnieper River within the territory of Belarus. Navigation is the main reason of the distribution of many alien species [5, 19, 28, 45]. In this case, they can be transferred both with ballast waters and with the fouling of ships, which is typical, to a larger extent, to mollusks and Amphipoda [14]. Thus, in the Pripyat River within the territory of Belarus the largest number of alien species was found in river ports [46]. The distribution of Hypania invalida (Polychaeta) is also conditioned by hydrotechnical measurements in the ports. It is likely that a rapid distribution of Proterorhinus marmoratus in the upper reaches of the Pripyat River is also conditioned by navigation. For the most part, purposeful and non-purposeful introduction of various aquatic animals into water bodies and watercourses with the aim of increasing their productivity exerts an adverse ecological effect on the aboriginal fauna. Thus, in lakes and reservoirs of Belarus the introduced Cyprinus carpio is in the competition with aboriginal fish for trophic resources. The acclimatization of Carassius gibelio resulted in an essential decrease in the numbers of aboriginal Carassius carassius. In addition, it can result in their hybridization. It should be noted that Cyprinus carpio and Carassius gibelio income into all river basins of Belarus from the places of their initial introduction. An example is the introduction of Perccottus glenii. This species was introduced into the ponds located within the territory of Minsk 40 years ago. Now it is registered over the whole territory of Belarus (Fig. 6). Pseudorasbora parva penetrated into the Ptich River (the tributary of the Berezina 30

Fig. 6: Dynamics of the distribution of Perccottus glenii over water bodies and watercourses of Belarus (based on [24]).

River, the Pripyat River basin) as a result of the introduction of the Far East species of fish – Ctenopharyngodon idella and Hypophthalmichthys sp. Introduction is also the factor of non-purposeful influx of a set of species, which income into water bodies as a result of acclimatization. Thus, Physella integra (Gastropoda) was introduced into Lake Beloye used as the cooling pond of the thermal power station along with Macrobrachium nipponense [22]. According to [32], in Germany 80% of alien species were introduced accidentally as a result of acclimatization. Commerce in aquatic animals. Some species were distributed as a result of the commerce in exotic animals, or as a result of their cultivation in aquaria. Thus, the presence of Physella acuta and Amerius nebulosus within the territory of Belarus is conditioned by their cultivation in aquaria. It is likely that the distribution of Craspedacusta sowerbyi was conditioned by the cultivation of tropical aquatic plants in aquaria. Influence of global factors on invasive processes in aquatic ecosystems of Belarus. Global climate changes. Literature data [15, 17, 37, 54] suggest that invasive processes in aquatic ecosystems are favored by global climate changes. As a result of global heating, reservoirs become closely similar to estuarine ecosystems [4], which is favorable to the income of the brackish water fauna. The increase in water salinity in the Pripyat River almost by a factor of two registered for 20 recent years was responsible for naturalization of the Ponto-Caspian invertebrates [33]. Many alien species are characterized by a high rate of reproduction. Temperature increase will result in the increase in the number of their generations and in more intensive consumption of trophic resources [54]. Thus, global heating can result in the increase in the intensity of invasive processes. It is especially true of the thermophilous Ponto-Caspian fauna. Contamination and degradation of freshwater ecosystems are also among the factors responsible for rapid colonization of new habitats by alien species [23]. In particular, biocontamination in31

Fig. 7: Relationship between the values of biocontamination (ACI and RCI indices) and ecological water quality assessed in terms of the BMWP biotic index [7].

dex depends inversely on ecological water quality assessed in terms of the BMWP biotic index [7] (Fig. 7). The obtained data correlate to some extent with the concept of “free niches”, when aboriginal species give way to alien species as a result of the degradation of ecological conditions [49]. As it has been shown [30], successful invasions are favored by the degradation in the habitats of aboriginal communities. Thus, the sensitivity of aboriginal species of mollusks and Gammaridae to the influence of wave stirring caused by navigation is essentially higher than that in alien species [18]. Concept of biological contamination. The process of invasion can be characterized as biological contamination. Thus, its quantitative assessment is of considerable importance. Despite the difference between chemical and biological contamination, the theory of the assessment of its influence remains the same [16]. The concept “biological contamination” has two definitions: “biopollution” and “biocontamination” [16]. The term “biopollution” implies the influence of the introduced and invasive species resulting in essential degradation at the level of specimens, populations, and communities, including adverse economical consequences. The term “biocontamination” implies the penetration of species into ecosystems and communities without considerable effect, or when it is not determined. 32

It should be noted that the penetration of alien species into the community always results in its structural changes. Thus, from our point of view the difference between the terms “biocontamination” and “biopollution” is rather conventional. They reflect various stages of invasive process. For example, at the initial stages of invasion rather low numbers of alien species do not exert an adverse effect on the community. However, at a later time their increase can result in community degradation. Actually this process includes two stages: species penetration into a new community and its naturalization [10]. Methods of biological contamination assessment. At present, biological contamination of surface waters is assessed using two indices. Biopollution Index (BPI) was elaborated for assessing the degree of contamination of marine, brackish water, and freshwater ecosystems by invasive species [34]. This index makes it possible to assess the impact at the level of large ecosystems (bays, estuaries, and rivers). It is based on three variables: distribution, numbers, and the influence of alien species. However, its quantitative value is difficult to assess [29, 39, 52]. Site-specific biocontamination index (SBCI) was elaborated for assessing the degree of biological contamination of a certain habitat on the example of macrozoobenthos. It is based on two variables: numbers and alien species number [7]. In this case, two indices are calculated. The abundance contamination index (ACI) measures the community dominance by aliens, and is calculated as the proportion of specimens of alien species in a community. Ordinal richness contamination index (RCI) measures the impact of alien species on community structural organization, and is calculated as the proportion of alien orders within a community. With values of ACI and RCI, the SBCI is derived from matrix, as follows, and gives 5 classes (Table 1). The average values of the SBCI calculated for different sections of the Dnieper and Pripyat rivers in 2007–2011 based on [3, 43] are given in Table 2. In the middle reaches of the rivers, high values of SBCI are conditioned by the presence of large river ports. It should be noted that the RCI can be calculated for orders or families [7, 23, 25]. In rivers of Europe, close correlation between the occurring processes was established at the level of families [23, 25]. This phenomenon is accounted for by the fact that in performing monitoring based on various biotic indices (BMWP, BBI, IBGN, etc.) taxonomic composition is analyzed at the level of families. At the same time, at the initial stages of biological contamination taxonomic composition should be analyzed at the level of orders [8]. However, the values of the RCI calculated at the level of orders in some cases are responsible for underestimating the values of SBCI [25]. Taxonomic composition analysis at the level of orders characterized by specific peculiarities of food consumption is more reliable, because they can represent a new link of the trophic chain. Thus, Hypania invalida (Polychaeta) was found in macrozoobenthos of some sections of the Pripyat and Dnieper rivers. However, its invasion did not result in significant competition with aboriginal species of Chironomidae and Oligochaeta. At the same time, invasions of some species of the order Decapoda (Orconectes limosus, Eriocheir sinensis, and Rhithropanopeus harrisii) into freshwater ecosystems can result not only in changes in trophic link, but also in community degradation. Thus, the presence of Orconectes limosus in the basin of the Neman River resulted in a significant decrease in the numbers of aboriginal species of Decapoda, or, in some cases, in their total disappearance (the personal report of A.V. Alekhnovich). 33

Table 1 Assessment of the site-specific biocontamination index (SBCI) in terms of macrozoobenthos ACI RCI None

0.01–0.10

0.11–0.20

0.21–0.50

> 0.50

0.01–0.10

1

2

3

4

0.11–0.20

2

2

3

4

0.21–0.50

3

3

3

4

> 0.50

4

4

4

4

None

0

Note. 0 – no biocontamination, “high” ecological status; 1 – low biocontamination, “good” ecological status; 2 – moderate biocontamination, “moderate” ecological status; 3 – high biocontamination, “poor” ecological status; 4 – severe biocontamination, “bad” ecological status. Table 2 Average values of SBCI for different sections of the Dnieper and Pripyat rivers Rivers, sections

RCI

ACI

SBCI

Dnieper, upper section

0.18

0.02

2

Dnieper, middle section

0.10

0.63

4

Dnieper, lower section

0.14–0.27

0.05–0.25

3

Pripyat, upper section

0.06

0.01

1

Pripyat, middle section

0.06–0.23

0.25–0.61

4

Pripyat, lower section

0.16–0.27

0.05–0.25

3

Influence of alien species on aboriginal communities. Alien species can influence individual communities or ecosystems. Based on [12], the main of them are as follows: • changes or degradation in the biotic structure of the ecosystem; • influence on the normal vital activity of aboriginal species through the competition, amensalism, or decrease in the rate of reproduction; • increase in the rate of species dying away; • decrease in aquaculture productivity; • harmful effect upon humans, or upon surrounding them plants and animals. 34

Thus, the values of SBCI are indicative of transformations in the taxonomic composition and structure of communities. The risks conditioned by the penetration of alien species of fish into aquatic ecosystems of Belarus were analyzed using Fish Invasiveness Screening Kit (FISK) [27]. Its highest values were observed for Ameiurus nebulosus, Carassius gibelio, Neogobius melanostomus, Perccottus glenii, and Pseudorasbora parva. It should be noted that mass development of A. nebulosus is observed mainly in lakes, whereas P. glenii occurs mainly in ponds, where it is not consumed by predators. In the lakes with a predominance of A. nebulosus, the development of the aboriginal fish fauna is inhibited. In this case, the aboriginal Carassius carassius gives way to C. gibelio. In water bodies of the Northern America and Japan, alien species exert a more significant adverse effect as compared to that registered in Europe [41], which is primarily related to the peculiarities of the fauna of the regions. In the rivers of Belarus, the main alien species of invertebrates of the Ponto-Caspian origin include Amphipoda, which contributed significantly to the total numbers of macrozoobenthos. At different stations of the Dnieper and Pripyat rivers, their contribution can attain 15–20% [47] mainly at the expense of mass development of Dikerogammarus villosus and D. haemobaphes. A rapid distribution of D. villosus in these rivers resulted in the disappearance of the aboriginal Gammarus lacustris and also in a sharp decrease in the numbers of aboriginal species of Chironomidae and Oligochaeta. Based on original data, in the sections of the Dnieper River with high numbers of (250 specimens/m2) of D. villosus the numbers of “soft” macrozoobenthos decreased almost by a factor of two. The same effects conditioned by D. villosus invasion were observed in the reservoirs of Ukraine [2] and of the Western Europe [38]. In the Dnieper River basin, native species of Unionidae give way to Dreissena polymorpha [22]. Many alien invertebrates are capable of transmitting disease. For example, fish was infected with Rossicotrema donicum (Trematoda) as a result of penetration of Lithogliphus naticoides into Lake Lukomlskoye (Belarus) [26]. Alien Decapoda, especially Orconectes limosus, are also capable of transmitting disease. It should be noted that the influence of the alien Ponto-Caspian species of invertebrates on the aboriginal fauna is more distinct in the western part of Europe as compared to its eastern part. In the eastern part of Europe, the aboriginal freshwater fauna is more adapted to such influence [47]. The Eastern Europe is a source of the Ponto-Caspian species for its western part [13]. Invasive processes prediction. The prediction of possible invasions and their consequences is of considerable importance. The consequences of many invasions are difficult to predict [30]. It has been known that only 10% of alien species incoming into new areas of distribution are capable of invading new communities. Some rules for invasions of various fish species, which can be also used for aquatic invertebrates, are proposed by the authors (Table 3). It has been found [11] that successful invasions are most likely when native communities are disturbed and rich in trophic resources, which correlates well with rule 5 from Table 3. The obtained data on relationship between biocontamination index and ecological water quality also correlate with this rule. 35

Table 3 Rules for biological invasions into aquatic ecosystems during two major phases of invasive process (based on [31]) Penetration into the community

Naturalization in the community

1

Most invasions fail

Most successful invasions are accommodated without major community effects

2

All aquatic systems are invasible

Major community effects are most often observed where species richness is low

3

Species with a wide spectrum of nutrition are most likely to be successful in systems with low levels of human disturbance

Predators are most likely to alter invaded communities as compared to omnivores and detrivores

4

Any species with wide adaptive capabilities can invade new communities

Long-term success depends on a close physiological match between the invader and the system being invaded

5

Successful invasions are most likely when native assemblages are depleted or disrupted

Long-term success is most likely in aquatic systems significantly changed as a result of human activity

6

Invasibility of aquatic systems is related to interactions among environmental variability, predictability, and severity

Invasions are much more likely to extirpate native species in aquatic systems with either extremely high or extremely low variability or severity

At the same time, for aquatic invertebrates rule 1 on the results of integration of invasive species into a new community is not always true. Thus, in the basin of the Dnieper River a set of the Ponto-Caspian species does not exert an adverse effect on the aboriginal fauna [47]. Relationship between invasibility and the observed effects has been analyzed [40]. The term invasibility implies the rate of naturalization and distribution of species in the ecosystem. It has been found that invasibility and effects do not always correlate. For example, in different regions fresh waters were colonized by Craspedacusta sowerbyi. However, it did not exert an adverse effect on the ecosystem. The same is true of Proterorhinus marmoratus. For five years, almost all biotopes of the Pripyat River [45], the Volga River [50], rivers of Germany [53], and rivers of Czech Republic [36] were colonized by this species. However, it did not exert an adverse effect on these aquatic ecosystems. The reasons of the absence of relationship between invasibility and its adverse effect are not clearly understood. At the same time, relationship between invasibility and its adverse effect can be registered locally at the level of individual ecosystems and regions [40]. 36

New invasions prediction is based on the data of alien species monitoring [1]. This makes it possible to elaborate the decisions aimed at the prevention of new invasions, and also at the minimization of the risk of alien species distribution.

Conclusion Invasions of alien species into freshwater ecosystems represent irreversible processes, the intensity of which will increase with increasing the intensity of human economical activities. Thus, it is impossible to avoid new invasions [30]. However, data on the main vectors and factors responsible for invasive processes make it possible to assess possible consequences of new invasions. Data on the distribution of the alien fauna in watercourses of Belarus suggest that the main reasons of invasions include the construction of reservoirs on the Dnieper and Neman rivers, and also navigation. It has been found that the abundance of alien species depends inversely on ecological water quality. A set of alien species invaded the territory of Belarus exerts an adverse effect on its ecosystems. At present, biological influence of invasive species on aboriginal communities and ecosystems is not clearly understood [6]. Thus, the study of the influence of invasions in freshwater ecosystems and biotic and abiotic factors responsible for this process, and also their analysis and prediction, are of considerable importance [20, 36].

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