Research Article |
Corresponding author: Ivan Špelić ( ispelic@agr.hr ) Academic editor: Ali Serhan Tarkan
© 2022 Ana Marić, Ivan Špelić, Tena Radočaj, Zoran Vidović, Tamara Kanjuh, Lorenzo Vilizzi, Marina Piria, Vera Nikolić, Dubravka Škraba Jurlina, Danilo Mrdak, Predrag Simonović.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Marić A, Špelić I, Radočaj T, Vidović Z, Kanjuh T, Vilizzi L, Piria M, Nikolić V, Škraba Jurlina D, Mrdak D, Simonović P (2022) Changing climate may mitigate the invasiveness risk of non-native salmonids in the Danube and Adriatic basins of the Balkan Peninsula (south-eastern Europe). In: Giannetto D, Piria M, Tarkan AS, Zięba G (Eds) Recent advancements in the risk screening of freshwater and terrestrial non-native species. NeoBiota 76: 135-161. https://doi.org/10.3897/neobiota.76.82964
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Salmonids are an extensively hatchery-reared group of fishes that have been introduced worldwide mainly for their high commercial and recreational value. The Balkan Peninsula (south-eastern Europe) is characterised by an outstanding salmonid diversity that has become threatened by the introduction of non-native salmonids whose potential risk of invasiveness in the region remains unknown and especially so under predicted climate change conditions. In this study, 13 extant and four horizon non-native salmonid species were screened for their risk of invasiveness in the Danube and Adriatic basins of four Balkan countries. Overall, six (35%) of the screened species were ranked as carrying a high risk of invasiveness under current climate conditions, whereas under predicted conditions of global warming, this number decreased to three (17%). Under current climate conditions, the very high risk (‘top invasive’) species were rainbow trout Oncorhynchus mykiss and brown trout Salmo trutta (sensu stricto), whereas under predicted climate change, this was true only of O. mykiss. A high risk was also attributed to horizon vendace Coregonus albula and lake charr Salvelinus namaycush, and to extant Atlantic salmon Salmo salar and brook trout Salvelinus fontinalis, whose risk of invasiveness, except for S. fontinalis, decreased to medium. For the other eleven medium-risk species, the risk score decreased under predicted climate change, but still remained medium. The outcomes of this study reveal that global warming will influence salmonids and that only species with wider temperature tolerance, such as O. mykiss will likely prevail. It is anticipated that the present results may contribute to the implementation of appropriate management plans to prevent the introduction and translocation of non-native salmonids across the Balkan Peninsula. Additionally, adequate measures should be developed for aquaculture facilities to prevent escapees of non-native salmonids with a high risk of invasiveness, especially into recipient areas of high conservation value.
AS-ISK, extant, fish, horizon, invasive, risk screening
Following the exponential increase in recent years in the number of introduced species worldwide (
Amongst freshwater fishes, salmonids are one of the most widely introduced groups (
Located in south-eastern Europe, the Balkan Peninsula was a glacial refugium for a large number of endemic species (
The exact period of first introduction, re-introduction and translocation of salmonids in the Balkan Peninsula remains unknown, though in the past century these activities have intensified considerably as a result of re-stocking for recreational fishing (
Previous risk screenings have been carried out for salmonid species partly covering the Danube and Adriatic basins of the Balkan Peninsula (
To fill the above knowledge gap, the aims of this study were to: (i) identify the translocated and introduced salmonid species of the Danube and Adriatic basins of the Balkan Peninsula; (ii) identify by horizon scanning which non-native salmonid species might enter the Balkan Peninsula in the (near) future from neighbouring countries; and (iii) evaluate the risk of invasiveness of both the identified extant and horizon salmonids under current and future (predicted) climate conditions for the risk assessment area. Given their extensive use in aquaculture, regular monitoring of the invasiveness of non-native salmonids is crucial to achieve better management of the native freshwater biota of the Balkan Peninsula with the aim of improving appropriate conservation measures.
The risk assessment area includes the Danube and Adriatic basins of Bosnia and Herzegovina, Croatia, Montenegro and Serbia (including Kosovo) (Fig.
Map of the risk assessment area (Danube and Adriatic Basins of Bosnia and Herzegovina, Croatia, Montenegro and Serbia with Kosovo) and neighbouring countries for evaluating the potential invasiveness of non-native salmonids.
The Danube Basin includes large lowland rivers, amongst which the most important, besides the River Danube, are the River Sava (Bosnia and Herzegovina, Croatia, Serbia) and the River Tisa (Serbia). The largest river of the Adriatic Basin is the River Neretva (Bosnia and Herzegovina, Croatia). Several other large rivers are present, though the main characteristic of the Adriatic Basin’s hydrology is the presence of numerous karst-sinking rivers, springs and perennial streams (
The Balkan Peninsula is characterised by a remarkable diversity of native salmonids, especially in the countries of Bosnia and Herzegovina (
In total, 17 salmonid species were included as part of the risk screening (Table
Extant and horizon non-native salmonids evaluated for their potential risk of invasiveness in the Danube and Adriatic Basins of Bosnia and Herzegovina, Croatia, Montenegro and Serbia (including Kosovo) – the risk assessment area. The criteria for selection of species are: 1 = Native species translocated from the Danube Basin to the Adriatic Basin; 2 = Native species translocated outside their native range but within the Danube Basin; 3 = Native species translocated outside their native range, but within the Adriatic Basin; 4 = Native species translocated from the Aegean Basin to the Danube Basin; 5 = Non-native species already present and naturalised/acclimatised in one or more drainage basins; 6 = Horizon species, i.e. not yet reported but likely to enter the risk assessment area in the near future. For extant species, details about the native distribution area are provided including the location and year of introduction. For all species, the a priori categorisation outcome into Non-invasive and Invasive is provided, based on a multi-tiered protocol (after
Taxon name | Common name | Criterion | Distribution area | A priori categorisation | |||||||
---|---|---|---|---|---|---|---|---|---|---|---|
Native | Introduced | Year | FishBase | GISD | CABI | IESNA | GScholar | Outcome | |||
Extant | |||||||||||
Coregonus lavaretus | European whitefish | 5 | Northern Europe | Plitvice lakes, Peruča Reservoir, River Cetina | 1937 | N | – | – | – | N | Non-invasive |
Coregonus peled | peled | 5 | Northern Europe | Plitvice Lakes, Peruča reservoir, River Cetina | 1937 | – | – | – | – | N | Non-invasive |
Hucho hucho | huchen | 2 | Europe | Rivers Đetinja, Jerma, Nišava, Mlava, Moravica | 2001 | N | – | – | – | N | Non-invasive |
Oncorhynchus mykiss | rainbow trout | 5 | North America | Vlasina Reservoir | 1792 | Y | Y | Y | Y | n.a. | Invasive |
Salmo labrax | Black Sea salmon | 1 | Eurasia | Rivers Gacka, Vrijeka | 1948 | N | – | – | – | N | Non-invasive |
Salmo letnica | Ohrid trout | 5 | Europe, Lake Ohrid | Vlasina Reservoir | 1950 | N | n.e. | – | – | N | Invasive |
Salmo macedonicus | Macedonian trout | 4 | Central Europe | River Jerma | 2000 | N | – | – | – | N | Non-invasive |
Salmo obtusirostris | soft-muzzled trout | 3 | Europe, Adriatic Basin | River Žrnovnica | 1970s | N | – | – | – | N | Non-invasive |
Salmo salar | Atlantic salmon | 5,6 | Northern Europe | Krka Estuary, rivers Sava and Drava | 1980 | N | N | Y | – | n.a. | Invasive |
Salmo trutta (sensu stricto) | brown trout | 5 | Western Europe | Rivers Gacka, Gradac, Vratna | 1970 | Y | Y | Y | Y | n.a. | Invasive |
Salvelinus alpinus | Arctic charr | 5 | Northern Europe | Plitvice lakes, River Neretva, Peruča accumulation, Lake Kokin Brod | 1963 | N | – | – | – | N | Non-invasive |
Salvelinus fontinalis | brook trout | 5 | North America | Plitvice lakes, River Neretva, Peruča accumulation, Lake Kokin Brod | 1960 | Y | Y | Y | – | n.a. | Invasive |
Thymallus thymallus | grayling | 1 | Eastern Europe | Rivers Cetina, Gacka, Istria, Neretva, Rude | 1960 | N | – | – | – | N | Non-invasive |
Horizon | |||||||||||
Coregonus albula | vendace | 6 | – | – | – | N | Y | – | – | n.a. | Invasive |
Oncorhynchus tshawytscha | chinook salmon | 5 | – | – | – | – | N | – | – | N | Non-invasive |
Salvelinus namaycush | lake charr | 6 | – | – | – | N | Y | Y | – | n.a. | Invasive |
Salvelinus umbla | Alpine charr | 6 | – | – | – | N | – | – | – | N | Non-invasive |
Risk screening was undertaken using the Aquatic Species Invasiveness Screening Kit (AS-ISK:
To achieve a valid screening, the assessor must provide for each question a response, a level of confidence for the response (see below) and a justification based on literature sources. The outcomes are a BRA score and a (composite) BRA+CCA score, which is obtained after adding or subtracting up to 12 points to the BRA score or leaving it unchanged in case of a CCA score equal to 0. Scores < 1 suggest that the species poses a ‘low risk’ to become invasive in the risk assessment area, whereas scores ≥ 1 indicate a ‘medium risk’ or a ‘high risk’. The threshold (Thr) value to distinguish between medium-risk (BRA and BRA+CCA score < Thr) and high-risk (BRA and BRA+CCA score ≥ Thr) species for the risk assessment area is obtained by ‘calibration’ based on the Receiver Operating Characteristic (ROC) curve analysis (see
For the ROC curve analysis to be implemented, the species selected for screening must be categorised a priori as ‘non-invasive’ or ‘invasive’ using literature sources. The a priori categorisation of species was implemented as per
CF = ∑(CLQi)/(4 × 55) (i = 1, …, 55)
where CLQi is the CL for Qi, 4 is the maximum achievable value for confidence (i.e. very high: see above) and 55 is the total number of questions comprising the AS-ISK questionnaire (
Implementation of the ROC curve analysis followed the protocol described in
Across all four assessors (Fig.
Box-and-whisker plots showing the Aquatic Species Invasiveness Screening Kit (AS-ISK) outcome scores (Basic Risk Assessment, BRA: light grey; BRA + Climate Change Assessment, BRA+CCA: dark grey) for the four assessors (AM = Ana Marić; IŠ = Ivan Špelić; TK = Tamara Kanjuh; TR = Tena Radočaj) screening the non-native salmonids for the risk assessment area (see Fig.
There were differences in AUCs between AM and TK (P < 0.01), whose AUC had a much lower value (i.e. 0.6143, hence below acceptable discriminatory power) compared to the AUCs from AM, IŠ and TR (i.e. 0.9143, 0.8000 and 0.8786, respectively, hence with excellent to outstanding discriminatory power). As a result, the BRA score outcomes from TK were removed from subsequent analyses and the threshold value was computed, based on the mean BRA scores from AM, IŠ and TR. The ROC curve resulted in an AUC of 0.9286 (0.7810–1.0000 95% CI), which indicated outstanding discriminatory power. Youden’s J provided the threshold of 19.25, which was used for calibration of the risk outcomes. Accordingly, based on the BRA scores, the threshold allowed the distinction of medium-risk species with scores within the interval [1, 19.25 [from high-risk species with scores within [19.25, 68]; based on the BRA+CCA scores, the threshold allowed the distinction of medium-risk species with scores within the interval [1, 19.25 [from high-risk species with scores within [19.25, 80]. Low-risk species had BRA scores within [−20, 1 [and BRA+CCA scores within [−32, 1 [(see Table
Permutational ANOVA results for the Aquatic Species Invasiveness Screening Kit (AS-ISK) outcome scores and for the confidence factor (CF) of the non-native salmonids screened for the risk assessment area. Component = BRA, BRA+CCA (see Table
Source of variation | df | MS | F #/t | P# |
---|---|---|---|---|
Scores | ||||
Component | 1 | 6.431 | 7.177 | 0.009 |
Assessor | 3 | 4.578 | 5.109 | 0.002 |
AM vs. IŠ | 1 | – | 3.402 | < 0.001 |
AM vs. TK | 1 | – | 3.228 | 0.003 |
AM vs. TR | 1 | – | 2.522 | 0.014 |
IŠ vs. TK | 1 | – | 0.343 | 0.734 |
IŠ vs. TR | 1 | – | 0.717 | 0.476 |
TK vs. TR | 1 | – | 0.928 | 0.352 |
Component × Assessor | 3 | 0.045 | 0.050 | 0.984 |
Residual | 128 | 0.896 | ||
CF | ||||
Component | 1 | 10.540 | 24.515 | < 0.001 |
Assessor | 2 | 23.664 | 55.040 | < 0.001 |
AM vs. IŠ | 1 | – | 5.058 | < 0.001 |
AM vs. TR | 1 | – | 10.111 | < 0.001 |
IŠ vs. TR | 1 | – | 5.604 | < 0.001 |
Component × Assessor | 2 | 0.929 | 2.162 | 0.123 |
Residual | 96 | 0.430 |
The highest-scoring species (BRA and BRA+CCA scores > 30, taken as an ad hoc ‘very high risk’ threshold) were Oncorhynchus mykiss and Salmo trutta for both the BRA and BRA+CCA and Oncorhynchus mykiss only for the CCA. The CCA resulted in a slight increase in the BRA score for only one species (Oncorhynchus mykiss), in no change for another species (Salmo macedonicus) and in a decrease for the remaining 15 species (Table
The mean CFTotal was 0.707 ± 0.017 SE, the mean CFBRA 0.720 ± 0.018 and the mean CFCCA 0.593 ± 0.020. Across the three assessors (i.e. AM, IŠ and TR), the mean CFBRA was significantly higher than the mean CFCCA and the overall CF (i.e. for the BRA and CCA) for assessor AM (0.792 ± 0.112) was significantly higher than that for assessors IŠ (0.663 ± 0.135) and TR (0.515 ± 0.147), which also differed significantly. However, there was no interaction term, indicating that CFBRA and CFCCA did not differ between each other depending on the assessor (Table
Risk outcomes for the non-native salmonids screened with AS-ISK for the risk assessment area. For each species, the following information is provided: a priori categorisation of invasiveness (N = non-invasive; Y = invasive: see Table
Taxon name | A priori | BRA | BRA+CCA | Delta | CF | ||||||
---|---|---|---|---|---|---|---|---|---|---|---|
Score | Outcome | Class | Score | Outcome | Class | Total | BRA | CCA | |||
Coregonus albula | Y | 19.3 | H | TP | 10.0 | M | – | −9.3 | 0.64 | 0.64 | 0.58 |
Coregonus lavaretus | N | 18.7 | M | – | 14.0 | M | – | −4.7 | 0.74 | 0.77 | 0.54 |
Coregonus peled | N | 14.5 | M | – | 10.5 | M | – | −4.0 | 0.73 | 0.75 | 0.57 |
Hucho hucho | N | 10.0 | M | – | 0.0 | L | TN | −10.0 | 0.75 | 0.76 | 0.61 |
Oncorhynchus mykiss | Y | 33.7 | VH | TP | 42.3 | VH | TP | 8.7 | 0.86 | 0.88 | 0.72 |
Oncorhynchus tshawytscha | N | 17.5 | M | – | 13.5 | M | – | −4.0 | 0.70 | 0.70 | 0.68 |
Salmo labrax | N | 19.2 | M | – | 15.2 | M | – | −4.0 | 0.70 | 0.71 | 0.64 |
Salmo letnica | Y | 15.8 | M | – | 11.2 | M | – | −4.7 | 0.64 | 0.65 | 0.60 |
Salmo macedonicus | N | 18.3 | M | – | 17.0 | M | – | −1.3 | 0.57 | 0.58 | 0.44 |
Salmo obtusirostris | N | 8.0 | M | – | 2.0 | M | – | −6.0 | 0.72 | 0.72 | 0.75 |
Salmo salar | Y | 22.2 | H | TP | 17.5 | M | – | −4.7 | 0.65 | 0.68 | 0.44 |
Salmo trutta | Y | 32.8 | VH | TP | 26.8 | H | TP | −6.0 | 0.76 | 0.78 | 0.58 |
Salvelinus alpinus | N | 19.2 | M | – | 13.2 | M | – | −6.0 | 0.72 | 0.73 | 0.61 |
Salvelinus fontinalis | Y | 29.8 | H | TP | 24.5 | H | TP | −5.3 | 0.76 | 0.79 | 0.53 |
Salvelinus namaycush | Y | 24.5 | H | TP | 15.8 | M | – | −8.7 | 0.66 | 0.67 | 0.57 |
Salvelinus umbla | N | 9.8 | M | – | 3.8 | M | – | −6.0 | 0.63 | 0.63 | 0.63 |
Thymallus thymallus | N | 14.8 | M | – | 8.8 | M | – | −6.0 | 0.80 | 0.82 | 0.58 |
In this study, the risk of invasiveness of 17 salmonids was determined with a very high level of accuracy (cf. discriminatory power), based on independent assessors. According to the threshold value of 19.25, based on the BRA, only six (35%) species were classified as carrying a high risk of invasiveness for the risk assessment area, whereas based on the BRA+CCA, this number decreased to three (17%). A similar decrease in score for salmonids under predicted climate change scenarios has been observed for Croatia and Slovenia (
Of the screened species, seven were found to pose a high to very high risk of invasiveness for the RA area under current climate conditions (BRA). However, after accounting for predicted climate change conditions (CCA), for four of these species, the risk of invasiveness decreased from high to medium (Table
Oncorhynchus mykiss is a top predator whose negative effects in its introduced range resulting from its carnivorous diet have been documented worldwide (
Salmo trutta (sensu stricto) is one of the most attractive recreational salmonids in the risk assessment area that, however, poses a major threat to the native salmonids because of genetic contamination. Introgression of alien Atlantic haplotypes into the indigenous Salmo labrax and Salmo obtusirostris gene pool has already been documented (
Salvelinus fontinalis is a valuable species for angling both in the risk assessment area and worldwide (
The three a priori invasive species Coregonus albula, Salmo salar and Salvelinus namaycush gained a high risk of invasiveness under current climate conditions (cf. BRA) whereas under the BRA+CCA, their risk became medium. Coregonus albula and Salmo salar are characterised by behavioural and developmental plasticity, which makes them capable to react and potentially adapt to variation in environmental conditions. However, there are limitations to these capacities, especially over short periods of time (
Salmo letnica was the only a priori invasive species found to carry a medium risk of invasiveness likely due to its low dispersal mechanism traits, but also to the scarce data available to answer the AS-ISK questions about ‘undesirable traits’ (see
As cold-water species, salmonids are likely to be strongly affected by climate change. An increase in temperature and a decrease in precipitation can directly influence water levels in rivers and lakes (e.g.
The most suitable streams for salmonid farming in the risk assessment area are in Montenegro, western Croatia and Bosnia-Herzegovina because of the presence of extensive areas with higher altitudes and boreal climate conditions. Interestingly, all salmonid farming in the risk assessment area and surrounding countries (i.e. Albania, Bulgaria, North Macedonia) is based on non-native species with Oncorhynchus mykiss being predominant (
Overall, it is advised that non-native species introductions should be brought to a minimum or avoided altogether and that every introduction of a new species should be conducted only after a full risk assessment (e.g.
In the countries of the risk assessment area, freshwater fishing is regulated by different fisheries acts. For example, in Serbia, stocking is limited by law to native species only (
Possibly the most challenging (and still unrecognised) problem for the Balkan Peninsula is the legal stocking of salmonid streams with Salmo trutta (sensu stricto), which poses a threat to native genetic integrity (
Control and containment of introduced salmonids, once established, is the only advisable approach, since eradication is virtually impossible in river systems and large lakes (
Special thanks to Linda Zanella for providing constructive comments on an earlier draft of the manuscript. This research was supported by the Croatian Science Foundation (grant IP-2016-06-2563 “Climate change and invasive species – assessing effects on the biodiversity of native freshwater crayfish and salmonids and their conservation”), by the Croatia-Serbia bilateral programme 2019–2021 and by the Ministry of Education, Science and Technological Development of the Republic of Serbia (grant 451-03-9/2021-14/200178).
Combined AS-ISK report including the 68 screenings for the 17 salmonid species screened for the Danube and Adriatic basins of Bosnia and Herzegovina, Croatia, Montenegro and Serbia (including Kosovo)
Data type: pdf file
Explanation note: Combined AS-ISK report including the 68 screenings for the 17 salmonid species screened for the Danube and Adriatic basins of Bosnia and Herzegovina, Croatia, Montenegro and Serbia (including Kosovo).