Research Article |
Corresponding author: Ana A. Anđelković ( ana.andjelkovic21@gmail.com ) Academic editor: Ingo Kowarik
© 2022 Ana A. Anđelković, Danijela M. Pavlović, Dragana P. Marisavljević, Milica M. Živković, Maja Z. Novković, Slađana S. Popović, Dušanka Lj. Cvijanović, Snežana B. Radulović.
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:
Anđelković AA, Pavlović DM, Marisavljević DP, Živković MM, Novković MZ, Popović SS, Cvijanović DL, Radulović SB (2022) Plant invasions in riparian areas of the Middle Danube Basin in Serbia. NeoBiota 71: 23-48. https://doi.org/10.3897/neobiota.71.69716
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Riparian areas experience strong invasion pressures worldwide and represent important points of spread for invasive alien plants (IAPs) in the European mainland. The Danube Basin is a well-known point of high plant invasion levels. Given that the middle part of the Danube Basin is critically understudied and the general lack of data for Serbia, the study aimed to provide an insight into the spatial patterns of plant invasions in the riparian areas of Serbia (Middle Danube Basin area). A total of 250 field sites, distributed along 39 rivers (nine catchment areas) and six canal sections, were studied during a four-year period (2013–2016) for the presence and abundance of IAPs. At the landscape scale, we studied distribution patterns of IAPs, differences in invasion levels in different catchment areas and between rivers and canals. At the local scale, we investigated how the proximity to roads/railway lines, housing areas, different land-use types (primarily agriculture), and dominant vegetation on site related to invasion patterns. Of the 26 studied IAPs, those with a well-known weedy behavior, long history of cultivation and strong affinity for riparian areas prevailed in the study area. Riparian zones of the Danube catchment exhibited the highest invasion levels in terms of IAPs richness and abundance, followed by the catchment areas of the Timok, Sava and Zapadna Morava rivers. Surprisingly, the Danube-Tisa-Danube canal network had the lowest invasion level. At the local scale, agriculture in proximity of the field site and dominant vegetation on site were observed as significant predictors of the invasion level. On the other hand, proximity to roads/railway lines and housing areas was not related to the invasion level. Finally, our study provides the first systematic overview of IAPs’ distribution data for riparian areas of the Middle Danube Basin in Serbia, which could provide a basis for long-term monitoring of IAPs and development of future management plans.
Alien plants, Danube, Danube-Tisa-Danube hydro-system, invasion corridor, invasive plants, riparian zone, river, waterway
Estimates show that over 13,000 vascular plant species, approximately equaling the entire European native flora, have become naturalized outside of their native range (
Rivers and riparian areas are important hotspots of native species diversity (
For the European continent,
Consequently, the study was designed to assess plant invasions in riparian zones of the Middle Danube Basin in Serbia. We analyzed (i) general invasion patterns, (ii) distribution patterns of dominant IAPs, (iii) differences in invasion levels between river and canal sites, and (iv) how site-specific factors (proximity of roads/railway lines, housing areas, land use in the vicinity of the field site and dominant vegetation on site) relate to invasion patterns. Additionally, analyzed IAPs were grouped, based on their origin and life form, to test how specific groups of IAPs relate to altitude. Finally, distribution data on the 26 IAPs is provided.
Serbia lies in the central part of the Balkan peninsula, covering a territory of 88,361 km2. Its northern and southeastern parts are characterized by a continental climate, with cold winters and semi-arid summers, while its western parts experience a more humid, temperate climate. The eastern and central parts of Serbia are characterized by a semi-arid temperate-continental/sub-continental climate, with some transitional sub-Mediterranean elements (
The total length of all waterways in Serbia is 65,980 km, with a prevalence of small to medium rivers, not longer than 100 m. All rivers in Serbia belong to three main drainage basins. The Danube catchment area, belonging to the Black Sea drainage basin, covers 92.5% of the territory, containing also the longest rivers in Serbia: Danube, Sava, Tisa, Velika Morava, Timok, Mlava, and Pek, with many tributaries. The Adriatic Sea drainage basin occupies 5.4% of the territory, primarily consisting of the basin of the Beli Drim river, located mainly in the Metohija valley. The Aegean Sea drainage basin covers 2.2% of the total area of Serbia, with the Pčinja river being one of its three main rivers, located in the far southeastern part of the country (
The Danube-Tisa-Danube (DTD) canal system is the greatest hydrotechnical complex made in Europe (outside of Russia), built in the period from 1728 to 1957 (
Field research was carried out at a total of 250 field sites to cover all river catchments and the entire territory of Serbia (Fig.
Distribution of field sites included in the analysis within different catchment areas of Serbia. Original photos of three selected field sites a - canal section of the Danube-Tisa-Danube hydro-system, loc. Vlajkovac b - river Čemernica, Zapadna Morava catchment area, loc. Konjevići c - Pčinja river, Aegean Sea drainage basin, loc. PIO "Dolina Pčinje".
Field research was conducted during the peak of the vegetation season (July-September) over four consecutive years (2013–2016). The timing of field research was selected based on the period when the studied plant species are fully developed and in full bloom. Based on preliminary findings from these field studies, 26 IAPs which occurred in at least three of the 250 surveyed field sites were selected for the analysis. We did not include Portulaca oleracea L. in this analysis, due to its uncertain geographic origins (but see
Vegetation data was collected on 100 m long longitudinal transects, set up parallel to the watercourse (following
In order to test which site-specific conditions had a significant effect on the presence and abundance of the studied IAPs, a number of site-specific variables were tested against the total number and cover of IAPs per site. Data on the dominant vegetation type (broadleaf forest, tree plantation, shrub vegetation, herbaceous vegetation, bare land) and data on adjacent land use (housing areas, cropping land - field crops, pastures and meadows, primary natural habitat, industry) in the 500 m radius from the transect were recorded. These data were later verified, and amended if necessary, using original photographs from the field and Google Earth platform. Furthermore, distances to the nearest main road/railway track and housing area were measured, using the Google Earth platform.
The effects of dominant vegetation on the total number of analyzed IAPs and their total cover (of all target IAPs combined) were tested using one-way ANOVA, with dominant vegetation as a factor variable. To test for differences in invasion levels (expressed as the total number of IAPs recorded on site) between the catchment areas one-way ANOVA was also applied, with catchment area as a factor variable. Results were then compared and separated using Tukey’s honest significant difference test, with Levene’s test used to ascertain the homogeneity of variance.
To test whether invasion levels were greater in river vs. canal sites, the total number of IAPs and their total cover on site were compared using the Student’s t-test. The t-test was also used to compare invasion levels (expressed as the total number of IAPs recorded and their total cover) between field sites located in proximity (500 m radius) of a road/railway track, housing area and cropping land (field crops), and sites located at a distance over 500 m from these potential sources of propagules. Non-parametric Mann-Whitney U test was used to compare the total IAPs numbers in field sites located in urban zones vs. non-urban field sites.
Linear regression analysis was used to test for correlation between invasion level proxies (the total number of IAPs and their total cover) and altitude. Correlations between the total number of IAPs and their total cover and distances measured between the transect and the nearest road/railway track and housing area were also tested using linear regression analysis.
The database used for multivariate analysis consisted of 26 invasive alien taxa (Table
Number of records of the studied invasive plant taxa in different catchment areas in Serbia, with data pertaining to their life form and origin.
Taxon | code in the analyses | life form | origin | total number of records | number of records per catchment area | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Danube (S1) | Sava (S2) | Kolubara (S3) | Drina (S4) | Velika Morava (S5) | Zapadna Morava (S6) | Južna Morava (S7) | Aegean Sea (S8) | Timok (S9) | DTD system (K) | |||||
Abutilon theophrasti Medik. | ABUTH | T | As | 9 | 6 | - | - | - | - | - | 1 | - | - | 2 |
Acer negundo L. | ACRNE | P | NAm | 27 | 19 | 3 | - | - | 2 | 1 | 1 | - | 1 | - |
Ailanthus altissima (Mill.) Swingle | AILAL | P | As | 29 | 7 | 4 | - | - | - | 4 | 6 | - | 7 | 1 |
Amaranthus retroflexus L. | AMARE | T | NAm | 75 | 34 | 5 | 1 | 4 | 6 | 11 | 8 | - | 1 | 5 |
Ambrosia artemisiifolia L. | AMBEL | T | NAm | 85 | 29 | 10 | 12 | 6 | 2 | 8 | 4 | - | 1 | 13 |
Amorpha fruticosa L. | AMHFR | NP | NAm | 108 | 47 | 10 | 1 | 3 | 5 | 6 | 11 | 1 | 10 | 14 |
Asclepias syriaca L. | ASCSY | G | NAm | 6 | 2 | 1 | - | - | - | - | - | - | - | 3 |
Broussonetia papyrifera (L.) Vent. | BRNPA | P | As | 6 | 2 | 1 | - | - | 1 | - | - | - | - | 2 |
Datura stramonium L. | DATST | T | C+SAm | 14 | 8 | - | 2 | - | 1 | 1 | 1 | - | - | 1 |
Echinochloa crus-galli (L.) P. Beauv. | ECHCG | T | As | 99 | 42 | 7 | 9 | 9 | 5 | 14 | 6 | 2 | 5 | - |
Echinocystis lobata (Michx.) Torr. & A. Gray | ECNLO | T | NAm | 79 | 16 | 4 | 8 | 7 | 9 | 12 | 11 | - | 10 | 2 |
Eleusine indica (L.) Gaertn | T | mix | 4 | 3 | - | - | - | - | - | - | - | - | 1 | |
Erigeron annuus (L.) Pers. | ELEIN | T | NAm | 57 | 25 | 2 | 4 | 2 | 1 | 4 | 4 | - | 2 | 13 |
Erigeron canadensis L. | ERICA | T | NAm | 103 | 31 | 4 | 8 | 5 | 6 | 9 | 15 | 1 | 11 | 13 |
Fraxinus pennsylvanica Marshall | FRAPE | P | NAm | 19 | 1 | 3 | 7 | - | - | - | 6 | - | 2 | - |
Helianthus tuberosus L. | HELTU | G | NAm | 27 | - | 1 | 2 | 9 | - | 4 | 3 | 1 | 6 | 1 |
Parthenocissus quinquefolia (L.) Planch. | PARQU | L | NAm | 12 | 5 | 1 | - | - | 2 | - | - | - | 2 | 2 |
Paspalum distichum L. | PASDI | T | trop | 17 | 10 | 1 | - | 1 | - | 3 | - | - | 2 | - |
Phytolacca americana L. | PHYAM | G | NAm | 13 | 3 | - | 1 | - | - | 4 | 3 | - | 2 | - |
Reynoutria × bohemica J. Chrtek & A. Chrtkova | REYBO | H | As** | 12 | - | 3 | 1 | 4 | - | 4 | - | - | - | - |
Robinia pseudoacacia L. | ROBPS | P | NAm | 102 | 18 | 5 | 10 | 8 | 7 | 17 | 19 | 2 | 9 | 7 |
Solidago gigantea Aiton | SOLGI | H | NAm | 8 | 2 | - | - | - | - | - | - | - | - | 6 |
Sorghum halepense (L.) Pers. | SORHA | G | EuAs | 47 | 19 | 4 | 2 | 2 | 2 | 8 | 1 | - | - | 9 |
Symphyotrichum spp. | SYMSP | H | NAm | 45 | 10 | 2 | 6 | 3 | 6 | 1 | 10 | - | 2 | 5 |
Xanthium orientale subsp. italicum (Moretti) D. Löve | XANST | T | C+SAm | 142 | 43 | 11 | 13 | 9 | 10 | 18 | 21 | 2 | 11 | 4 |
Xanthium spinosum L. | XANSP | T | SAm | 8 | 2 | - | - | - | - | - | - | - | - | 6 |
Total number of IAPs in the catchment area | 1153 | 384 | 82 | 87 | 72 | 65 | 129 | 131 | 9 | 84 | 110 | |||
Total number of field sites in the catchment area | 250 | 74 | 17 | 17 | 18 | 16 | 25 | 34 | 2 | 14 | 33 | |||
Mean number of records per field site in the catchment area | 4.61 | 5.19 | 4.82 | 5.12 | 4.00 | 4.06 | 5.16 | 3.85 | 4.50 | 6.00 | 3.33 |
For further analysis, two groupings of taxa based on percentage covers were done using the “trait averages” option. Taxa were first grouped based on their origin (Table
Univariate analyses were done using STATISTICA 7.0 and CANOCO (ver. 5.0,
A total of 1153 records of the selected IAPs have been documented in riparian areas of the analyzed rivers (Table
Xanthium orientale subsp. italicum, Amorpha fruticosa, Robinia pseudoacacia and Echinochloa crus-galli occurrences in the studied sites of riparian areas of Serbia. Invasive species distribution points relate to the survey areas shown in Fig.
Erigeron canadensis, Amaranthus retroflexus, Ambrosia artemisiifolia and Abutilon theophrasti occurrences in the studied sites of riparian areas of Serbia. Invasive species distribution points relate to the survey areas shown in Fig.
When the number of invaded rivers is analyzed per taxon, R. pseudoacacia and X. orientale subsp. italicum stand out, being recorded along the course of 92.3% and 89.7% of rivers, respectively. They are closely followed by E. crus-galli and E. canadensis, both recorded along 71.8%, and A. fruticosa in the riparian areas of 64.1% rivers (data not shown).
With regards to their origin, IAPs originating from North America were most frequent in the field, with 766 records (66.4% of total IAPs records; see Suppl. material
The total number of IAPs per site was negatively correlated with altitude (r=-0.30, p < 0.001), as was their total cover (r=-0.19, p < 0.01). A generalized additive model revealed that altitude generally predicted individual IAPs cover on site (F = 7.1, p = 0.002). The abundance of R. pseudoacacia, Helianthus tuberosus and Reynoutria × bohemica was positively correlated with altitude, while the other IAPs’ cover exhibited a negative correlation with this parameter (Fig.
Response curves of the selected invasive alien plants in relation to altitude in the studied areas of Serbia. Names of taxa are abbreviated, see Table
Pie chart diagram (RDA) showing the association of selected invasive alien plants grouped by origin with field sites categorized by altitude (a = < 200 m a.s.l.; b = 200 – 500 m a.s.l.; c = 500 – 800 m a.s.l.). Names of groups are abbreviated, please refer to Table
Sites along rivers had significantly more IAPs than sites along canals (5.35±2.49 vs. 3.61±2.29, df = 248, p < 0.001; t-test). Similarly, the total cover (in %) of analyzed IAPs was significantly higher at river vs. canal sites (44.33±29.83 vs. 24.42±21.82, df = 248, t = 3.93, p < 0.001; t-test).
Catchment area had a highly significant effect on the total number of IAP records per field site (p < 0.001; See Suppl. material
Site-specific variables were differently related to invasion patterns in the study area. Sites in the proximity of roads or railways (< 500 m) had fewer IAP species, compared to the more distant sites (4.74±2.52 vs. 6.05±2.34, df = 248, t = 3.93, p < 0.001). Thus, an increase in distance from the road/railway track was positively correlated with IAPs number (r = 0.18, p < 0.001).
The proximity of housing areas did not have a significant effect on the total number or total cover of IAPs per site (See Suppl. material
Response curves of the selected individual invasive alien plants in relation to the distance to housing areas. Names of taxa are abbreviated, see Table
Sites located in proximity of agricultural land (< 500 m) had more IAP species, compared to the more distant sites (5.26±2.6 vs. 4.51±2.25, df = 248, t = 2.03, p < 0.05). On the other hand, contrary to our expectations, there was no significant difference (p > 0.05; Mann-Whitney U test) in the number and cover of IAPs per site between field sites located within an urban zone and those found outside of cities.
The total cover of studied IAPs per site was significantly different (p < 0.01) between sites with different vegetation types (See Suppl. material
This study provides the first systematic overview of plant invasion patterns and IAPs distribution data for riparian areas of the Middle Danube Basin in Serbia. General invasion patterns, differences among catchment areas, and among individual invasive species were detected. Additionally, we also show which site-specific variables were related to invasion patterns.
Results pertaining to the relevance of species’ origin and life form are consistent with those reported for other riparian systems (
The overall decrease in alien species richness with increasing altitudes is a well-known phenomenon, recorded worldwide (Pyšek et al. 2005;
This study has found significant differences in invasion levels between the studied catchment areas, highlighting the catchment areas of the Timok and Danube rivers as the most invaded overall. Such findings are consistent with other studies denoting the Danube as an important plant invasion corridor (
Surprisingly, results have shown that the canal network of the Danube-Tisa-Danube hydro-system is the least invaded of the analyzed catchment areas. Such invasion levels along the canals are contrary to general expectations, given that field sites along the canal network are under strong and constant anthropogenic pressure. Additionally, they are found within an entirely agricultural landscape of the Vojvodina Province and consequently experience seasonal nutrient-enrichment, due to N leaching from the surrounding agricultural fields (
The observed invasion tendencies on river vs. canal sites could potentially be explained by the management regime which is being undertaken by the stakeholders in charge of the DTD canal network upkeep. While the banks of the DTD canal system are under a regular management system (mowing), riverbanks are mostly free from this form of anthropogenic control and IAPs are therefore allowed to spread unchecked. Such a situation could suggest that traditional management regimes still being employed along the canal banks control the spread of IAPs along canals. Regardless, all management plans need to take into account those species where management activities such as mowing (R. × bohemica;
Our results on the most frequent and most abundant IAPs (Table
Amorpha fruticosa was recorded as the second most frequent IAP (Table
Finally, some of the most frequent IAPs in riparian areas (X. orientale subsp. italicum, E. canadensis, E. crus-galli, Amaranthus retroflexus, A. artemisiifolia) are also widely distributed in ruderal and agricultural areas of the region and spread intensively across the Balkans and SE Europe (
The rather constrained distribution of Asclepias syriaca in the riparian areas of Serbia was an unexpected result, given that previous research (
Local site conditions determine the susceptibility of a field site to invasion (
Agriculture, as land use type observed in the 500 m radius from the studied field site, was an important predictor of IAPs richness (See Suppl. material
Surprisingly, we did not detect a link between the proximity of roads/railway lines and the number of observed IAPs per site. The role of these transport corridors in the spread of invasive plants is generally well-known (
No effects were observed between the proximity of field sites to housing areas, or their position in urban areas, and the level of invasion. This was unexpected, given the importance of urbanization for plant invasions (
This study showed that dominant vegetation on site is a significant predictor of the total cover of studied IAPs. Riparian field sites dominated by shrub vegetation had the highest recorded cover of invasive plants, which aligns with other studies showing that riverine scrubs are characterized by the highest proportions of IAPs (
Consequently, we can surmize that agriculture and dominant vegetation on site override the importance of proximity of transport infrastructure and housing areas (as human-related factors sensu
Our study revealed differences in invasion levels between catchment areas of the Middle Danube Basin area. The Timok and Danube catchment areas were shown to support highest invasion levels. While some catchment areas (e.g. Sava and Zapadna Morava) also had high numbers of IAPs, other were less subjected to invasions. The results presented here have important practical implications and can support the development of future management plans for the control of IAPs in riparian areas of both rivers and canals in the region. Furthermore, we believe that our results, in addition to their local and regional value, will contribute to documenting the invasion trends of IAPs in riparian areas of the Danube Basin and this part of Europe. Finally, this snapshot study, with well-defined survey areas, could serve as a basis for long-term monitoring of IAPs, which is critically needed for supporting the prioritization of management and conservation actions (
The authors are grateful to two reviewers for their constructive comments and suggestions on earlier drafts of this manuscript. We are especially grateful to our editor, Ingo Kowarik, for all his help which significantly improved our manuscript from its original state. This research was conducted under the framework of the Project No. TR31018 of the Ministry of Education, Science and Technological Development of the Republic of Serbia. The authors are grateful to the Ministry for its ongoing financial support: Contract No. 451-03-9/2021-14/200010 to AAA, DMP and DPM, Contract No. 451-03-9/2021-14/200125 to DLjC, MZN and SBR, Contract No. 451-03-9/2021-14/200032 to MMŽ, and Contract No. 451-03-9/2021-14/200178 to SPP. The authors declare that no competing interests exist.
List of the studied rivers/canal sections and their catchment area affiliation (and code in the analysis)
Data type: List of rivers included in the filed word.
Explanation note: This file presents a comprehensive list of all the rivers which were included in the analysis. It is included as supplementary data as it provides additional information on the watercourses which were included in the analyses.
Geographical distribution data of the studied invasive alien speces
Data type: (measurement/occurrence/multimedia/etc.)
Explanation note: This file includes 26 tables containing geographical distribution data of the analyzed invasive alien plat taxa. In addition to latitude and londiude, data is also provided on the locality, watercourse along which data was recorded and the catchment area this watercourse belongs to.
Figure S3
Data type: Tiff file.
Explanation note: Origins of the analyzed invasive alien plants in the riparian areas of Serbia (expressed as the percent of records per each group).
Figure S4
Data type: Tiff file.
Explanation note: Biological spectrum of the analyzed invasive alien plants in the riparian areas of Serbia (expressed as the percent of records per each group).
Tables
Data type: Docx file.
Explanation note: Results of one-way ANOVA analyses, and subsequent Tukey’s HSD post hoc tests.
Table
Data type: Docx file.
Explanation note: Mean total numbers of invasive alien plants recorded per site and their total cover values (± SD) in field sites depending on their proximity to main road/railway track, housing and adjacent land use types (cropping land, field crops, pastures and meadows, primary natural habitat, industry).