Corresponding author: Vladimir Pešić (
Academic editor: Fernando Jacinavicius
Water mites (
No ethical principles were violated when providing this study.
The authors declare no conflict of interests concerning this study.
Traditional morphology often underestimates the true diversity of water mites and, in recent years, it has been successfully replaced by an integrative approach that combines both morphological characteristics and molecular data (
Of the Balkan countries, Montenegro is one of the best studied from the taxonomic and faunistic point of view (
Currently, 201 species of water mites have been reported for Montenegro (
The aim of the study is to develop and evaluate the first library of barcodes for water mites from Montenegro, targeting a COI fragment of ~ 658 bp. Taking advantage of publicly available DNA barcode reference libraries, such as the BOLD and the use of the universal Barcode Index Number (BIN), allows us to assess the molecular diversity of water mite species inhabiting the territory of Montenegro, as well as to explore their distribution patterns in Europe. Moreover, this approach will allow us to also identify problematic species groups both for traditional taxonomy and for DNA barcoding.
Water mites were collected by hand netting, sorted live in the field and immediately preserved in 96% ethanol (EtOH) for the molecular analysis. Water mites were collected from 54 sampling sites in Montenegro (Fig.
Molecular analysis were conducted in the Canadian Centre for DNA Barcoding (Guelph, Ontario, Canada; (CCDB;
In CCDB, the chromatograms were assembled into consensus sequences for each specimen and uploaded to BOLD. The taxonomic account, voucher specimen ID, collecting locality and voucher depositor were incorporated into the system for further analysis. Water mite sequences, obtained during this study, were grouped in the “MNHYD” (DNA barcode reference library of Montenegrin water mites) dataset. Detailed voucher information, taxonomic classifications, photos, DNA barcode sequences, primer pairs used and trace files (including their quality) were uploaded to the dataset “MNHYD” on the Barcode of Life Data Systems (BOLD;
The translation of the
The reference library for the molecular identification of water mites sequenced in this study was analysed using the Barcode Index Number system (BIN) (
All obtained BINs were inspected for concordance using BOLD Workbench. The Refined Single Linkage (RESL) algorithm was used to assign water mite barcodes to Operational Taxonomic Units (OTUs).
Sequence comparisons were performed using MUSCLE alignment (
DNA barcodes of 233 specimens morphologically assigned to 86 species from 28 genera and 15 families of water mites from Montenegro were newly generated for this study. The specimens were collected through the “DNA-Eco” (DNA barcode reference library as a tool for sustainable management of freshwater ecosystems in the highly threatened Lake Skadar Basin) project. The current study develops the first COI barcode reference library of water mites for Montenegro with the focus on Skadar/Shkodra Lake catchment area.
Fragment lengths of the analysed DNA barcode fragments ranged from 201 to 658 (mean: 636.2) base pairs, including no stop codons, insertions or deletions. The DNA barcode region was characterised by a high AT-content: the mean sequence compositions were A = 30.82 ± 0.1252%, C = 20.39 ± 0.1222%, G = 14.91 ± 0.0709% and T = 33.88 ± 0.1253%. The obtained results are similar to those found in other arthropod studies (e.g.
The families
The mean intrageneric K2P distance was 20.2 ± 0.0% (range 6.09-42.37%). The mean intraspecific nucleotide K2P distances were 2.43 ± 0.01% (ranging from 0% to 24.16%). The summary statistics showing significant changes of average K2P distances within the different taxonomic levels are given in Table
The BIN and RESL (OTU) analyses assigned sequences to 98 BINs and 103 OTUs, respectively. Fifty BINs (159 records) were concordant (51%) and 48 BINs were represented by a single sequence (49%). At the time of publication of the dataset, fifty-five (56.1%) of these BINs (with 102 sequences) included sequences only from Montenegro, while the remaining BINs included sequences also from other countries.
Most of the morphologically-identified species show an intraspecific variation of less than 2%. However, the 14 taxa listed in Table
The NJ analyses, based on K2P distances, revealed non-overlapping clusters with bootstrap support values > 95% for 50 species (58%) with more than one analysed specimen indicating a high congruence between BINs affiliation and morphological species identification. Moreover, specimens showing high intraspecific distances are also clearly separated into different clades. A more detailed topology of all analysed specimens is presented in the supporting information (Suppl. material
This study provides COI barcodes for 233 specimens representing 86 morphologically identified species of water mites from Montenegro. These represent 42.8% of Montenegrin water mite fauna, based on
Of the 86 species recorded in this study, 79 species were previously reported for Montenegro. DNA barcoding confirmed the presence of four species new for Montenegro, i.e.
Moreover, species identification, based on molecular data conducted during this project, extended the list of Montenegrin water mites by description of several species new for science, i.e.
Our study confirmed efficiency of DNA barcoding as a tool for the identification of water mites. In particular, 72 of the 86 morphologically-identified species exactly matched the BINs defined from BOLD. This result coincides with high identification efficiency rates through the BOLD
Three species, i.e.
The sequences of
Taxonomic studies of the above species were outside the scope of this paper. Further studies with material from a wider geographical area, were needed to clarify taxonomy and elucidate the delimitation of the species in the above complexes. This process should be accompanied by sufficient barcode coverage to allow the detection of phylogeographic patterns and/or even the existence of possible overlooked cryptic species. The build-up of DNA barcode library for water mites of Montenegro represents a long-term task, aimed at improving molecular identification and inclusion of this group in environmental assessment programmes and, on the other hand, to stimulate further biodiversity research of this limnofaunistic group in Montenegro and the Balkans.
The authors are grateful to all those who helped during sample collections in Montenegro. This study is part of the “DNA-Eco” scientific project, supported by a grant of the Montenegrin Ministry of Science. The part of study was supported by Polish National Science Centre, Poland, grant no. 2017/27/N/NZ8/01568.
The authors declare no conflict of interests concerning this study.
Sampling sites from Montenegro. The green colour represents the Danube Basin (Black Sea) and the yellow colour represents the Adriatic Basin.
Details on barcoded specimens from Montenegro.
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Podgorica, Zeta River at Pričelje |
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Kolašin, Lalevića Dolovi, spring #1 |
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Kolašin, Lalevića Dolovi, spring #1 |
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Kolašin, Lalevića Dolovi, spring #1 |
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Bar, Poseljanski stream at Poseljani |
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Andrijevica, spring at Trešnjevik |
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Kolašin, Bistrica stream |
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Kolašin, Kolašinska rijeka stream |
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Kolašin, Kolašinska rijeka stream |
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Kolaši, Kolašinska rijeka stream |
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Kolašin, spring on road to Trešnjevik |
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Kolašin, spring on road to Trešnjevik |
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Kolašin, spring on road to Trešnjevik |
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Kolašin, Bistrica stream |
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Bijelo Polje, Lještanica stream |
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Bijelo Polje, Lještanica stream |
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Bijelo Polje, Lještanica stream |
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Bijelo Polje, Lještanica stream |
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Žabljak, Sedlo, spring Studenac |
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Bar, Međurječka rijeka stream |
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Bar, Međurječka rijeka stream |
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Bijelo Polje, Lještanica stream |
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Berane, spring nr Mon. Djurdjevi Stupovi |
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Mojkovac, Bistrica stream |
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Podgorica, Cijevna River at Dinoša |
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Bar, Medjurječka rijeka stream |
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Kolašin, Bistrica stream at Crkvine |
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Podgorica, Cijevna River at Dinoša |
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Kolašin, Bistrica stream at Crkvine |
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Danilovgrad, spring below the bridge |
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Nikšić, spring “Babino sicelo” |
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Bar, stream in Godinje Village |
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Bar, stream in Godinje Village |
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Bar, Rikavac stream above Old Bar |
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Bar, Rikavac stream above Old Bar |
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Bar, Rikavac stream above Old Bar |
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Bar, Rikavac stream above Old Bar |
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Bar, Medjurječka rijeka stream |
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Bar, Medjurječka rijeka stream |
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Danilovgrad, spring below the bridge |
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Danilovgrad, spring below the bridge |
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Danilovgrad, spring below the bridge |
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Kolašin, Kolašinska rijeka stream |
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Kolašin, Bistrica stream at Crkvine |
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Kolašin, Bistrica stream at Crkvine |
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Mojkovac, Bistrica stream |
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Mojkovac, Bistrica stream |
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Kolašin, Kolašinska rijeka stream |
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Tuzi, Vitoja, pool |
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Tuzi, Vitoja, pool |
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Tuzi, Vitoja, pool |
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Bar, Skadar Lake at Murići |
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Bar, Skadar Lake at Murići |
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Podgorica, Skadar Lake at Donja Plavnica |
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Podgorica, Gornja Plavnica, river |
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Bar, Medjurjecka rijeka stream |
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Danilovgrad, River Zeta near Slap |
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Bijelo Polje, Lještanica stream |
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Bijelo Polje, Lještanica stream |
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Berane, spring nr. Mon. Djurdjevi Stupovi |
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Kolašin, spring at Monastir Morača |
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Podgorica, Cijevna River at Dinoša |
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Cetinje, River Crnojevića |
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Podgorica, spring Mareza |
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Tuzi, Vitoja spring |
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Šavnik, spring of Bukovica stream |
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Šavnik, spring of Bukovica stream |
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Nikšić, spring Vukovo Vrelo |
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Žabljak, Sedlo, spring Studenac |
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Žabljak, Sedlo, spring Studenac |
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Ulcinj, Šasko Lake |
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Cetinje, Poseljanski stream, lower part |
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Bar, Skadar Lake at Murići |
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Bar, Skadar Lake at Murići |
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Podgorica, Mareza canal |
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Danilovgrad, spring Svinjiška vrela |
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Mojkovac, Bistrica stream |
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Mojkovac, Bistrica stream |
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Kolašin, Kolašinska rijeka stream |
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Žabljak, Ljutica stream |
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Bar, stream in Godinje Village |
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Bar, Rikavac stream above Old Bar |
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Danilovgrad, Zeta River at Spuž |
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Danilovgrad, Zeta River at Spuž |
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Berane, spring nr. Mon. Djurdjevi Stupovi |
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Budva, Lastva Grbaljska, stream |
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Šavnik, spring Kikov izvor near Boan |
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Žabljak, Sedlo, Studenac spring |
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Kolašin, Lalevića Dolovi, spring #1 |
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Nikšić, Lukavica Mt., spring Babino Sicelo |
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Nikšić, Lukavica Mt., spring Babino Sicelo |
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Nikšić, Lukavica Mt., spring Babino Sicelo |
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Žabljak, Mlinski potok stream |
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Kolašin, Biogradska River |
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Bijelo Polje, Lještanica stream |
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Bijelo Polje, Lještanica stream |
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Bijelo Polje, Lještanica stream |
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Kolašin, Biogradska River |
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Kolašin, Biogradska River |
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Mojkovac, Bistrica stream |
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Mojkovac, spring in Bistrica Village |
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Mojkovac, spring in Bistrica Village |
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Cetinje, spring “Smokov Vijenac” |
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Kolašin, Biogradska River |
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Podgorica, Cijevna River at Dinoša |
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Budva, Lastva Grbaljska, first order stream |
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Bar, stream in Godinje Village |
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Bar, Rikavac stream above Old Bar |
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Budva, Lastva Grbaljska, first order stream |
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Danilovgrad, spring below the bridge |
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Danilovgrad, spring below the bridge |
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Danilovgrad, spring below the bridge |
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Danilovgrad, Zeta River at Spuž |
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Podgorica, Morača River in Podgorica |
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Mojkovac, Bistrica stream |
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Kolašin, Biogradska rijeka stream |
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Podgorica, Cijevna River at Dinoša |
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Kolašin, Tara River near Mateševo |
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Bar, Međurječka rijeka stream |
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Kolašin, Bistrica stream at Crkvine |
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Kolašin, Bistrica stream at Crkvine |
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Bar, Orahovštica River |
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Bar, Orahovštica River |
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Kolašin, River Drcka near Mateševo |
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Bar, Rikavac stream above Old Bar |
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Bar, Rikavac stream above Old Bar |
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Kolašin, Bistrica stream at Crkvine |
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Kolašin, Bistrica stream at Crkvine |
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Kolašin, Kolašinska rijeka stream |
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Mojkovac, Bistrica stream |
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Kolašin, Bistrica stream at Crkvine |
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Bar, Međurječka rijeka stream |
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Bar, Međurječka rijeka stream |
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Kolašin, Kolašinska rijeka stream |
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Bar, Međurječka rijeka stream |
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Bar, Međurječka rijeka stream |
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Bar, Rikavac stream above Old Bar |
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Podgorica, Cijevna River at Dinoša |
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Bar, stream in Godinje Village |
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Bar, stream in Godinje Village |
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Tuzi, Vitoja, pools |
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Tuzi, Skadar Lake at Podhum |
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Podgorica, Cijevna River at Dinoša |
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Kolašin, Kolašinska rijeka stream |
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Mojkovac, Bistrica stream |
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Berane, spring nr. Mon. Djurdjevi Stupovi |
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Bar, Međurječka rijeka stream |
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Bar, Orahovštica stream |
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Podgorica, Pričelje, spring Studenac |
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Podgorica, Pričelje, spring Studenac |
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Mojkovac, Bistrica stream |
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Kolašin, Kolašinska rijeka stream |
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Budva, Lastva Grbaljska, first order stream |
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Danilovgrad, spring below the bridge |
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Danilovgrad, Zeta River at Spuž |
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Danilovgrad, spring below the bridge |
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Danilovgrad, Zeta River at Spuž |
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Bar, Orahovštica stream |
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Bar, Poseljani, Poseljanski stream |
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Podgorica, Mareza spring |
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Podgorica, Mareza spring |
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Žabljak, Sedlo, Studenac spring |
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Nikšić, Vidrovan, Vukovo Vrelo spring |
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Nikšić, Vidrovan, Vukovo Vrelo spring |
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Nikšić, spring in Miločani Village |
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Budva, spring Smokov Vijenac |
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Budva, spring Smokov Vijenac |
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Bar, Rikavac stream above Old Bar |
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Bar, Rikavac stream above Old Bar |
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Bar, Rikavac stream above Old Bar |
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Kolašin, spring nr. Monastir Morača |
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Kolašin, Kolašinska Rijeka stream |
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Podgorica, River Cijevna at Trgaja |
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Dnilovgrad, River Zeta near Slap |
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Danilovgrad, River Zeta near Slap |
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Podgorica, Mareza canal |
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Podgorica, Mareza canal |
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Kolašin, Crkvine, Bistrica stream |
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Bar, Poseljanski stream at Poseljani |
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Bar, Poseljanski stream at Poseljani |
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Žabljak, Mlinski potok stream |
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Kolašin, Tara River near Mateševo |
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Podgorica, Mareza canal |
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Tuzi, Vitoja, pool |
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Tuzi, Vitoja, pool |
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Bar, Poseljani, Poseljanski stream |
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Tuzi, Skadar Lake at Podhum |
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Bar, Medjurječka rijeka stream |
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Bar, Medjurječka rijeka stream |
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Bar, Medjurječka rijeka stream |
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Bar, Medjurječka rijeka stream |
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Šavnik, spring Kikov izvor near Boan |
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Kolašin, Lalevića Dolovi, spring #1 |
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Kolašin, Lalevića Dolovi, spring #1 |
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Kolašin, Lalevića Dolovi, spring #1 |
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Danilovgrad, River Zeta at Spuž |
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Tuzi, Vitoja, pool |
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Tuzi, Vitoja, pool |
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Tuzi, Vitoja, pool |
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Ulcinj, Šasko Lake |
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Ulcinj, Šasko Lake |
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Ulcinj, Šasko Lake |
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Tuzi, Vitoja, pool |
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Ulcinj, Šasko Lake |
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Cetinje, River Cnojevica ( |
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Danilovgrad, Moromiš pond |
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Danilovgrad, Moromiš pond |
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Danilovgrad, Moromiš pond |
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Danilovgrad, Moromiš pond |
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Danilovgrad, Moromiš pond |
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Danilovgrad, Moromiš pond |
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Šavnik, spring of Bukovica stream, pool |
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Nikšić, Vukovo Vrelo spring, pool |
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Nikšić, Vukovo Vrelo spring, pool |
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Tuzi, Vitoja, pool |
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Danilovgrad, Moromiš pond |
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Danilovgrad, Moromiš pond |
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Podgorica, Mareza canal |
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Bar, Medjurječka rijeka stream |
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Cetinje, Poseljanski stream |
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Podgorica, Cijevna River at Dinoša |
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Danilovgrad, Zeta River at Spuž |
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Danilovgrad, Zeta River at Spuž |
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Danilovgrad, Zeta River at Vranjske Njive |
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Danilovgrad, Spuž, spring near Zeta River |
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Bar, Skadar Lake at Murići |
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Bar, Skadar Lake at Murići |
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Bar, Skadar Lake at Murići |
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Podgorica, Mareza canal |
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Šavnik, Tušina River at Boan |
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Šavnik, Tušina River at Boan |
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Podgorica, Mareza canal |
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Nikšić, Lukavica Mt., pools |
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Summary table of K2P genetic distances within the different taxonomic levels derived from 233 analysed water mite specimens from Montenegro. The list of studied species is provided in Table 1. Deletion Method: Pairwise Deletion. Alignment: BOLD Aligner (Amino Acid based HMM).
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Within Species | 200 | 53 | 391 | 0.00 | 2.43 | 24.16 | 0.01 |
Within Genus | 207 | 14 | 2291 | 6.09 | 20.20 | 42.37 | 0.00 |
Within Family | 168 | 7 | 1054 | 16.17 | 37.14 | 63.16 | 0.01 |
Species with intraspecific (ISD) maximum pairwise distances > 2.2% (p-dist.). Divergence values were calculated for all studied sequences, using the Nearest Neighbour Summary, implemented in the Barcode Gap Analysis tool provided by the Barcode of Life Data System (BOLD). BINs are based on the barcode analysis from 15 November 2021. Country codes (alpha-2 code): BG = Bulgaria, CH = Switzerland, DE = Germany, ES = Spain, FR = France, GB = United Kingdom, GL = Greenland, IT = Italy, NO = Norway, NL = Netherlands, ME = Montenegro, MK = North Macedonia, PL = Poland, RO = Romania, RS = Serbia, RU = Russia, SK = Slovakia.
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BOLD:ACR9598 | 2 | 0.8 | 0.8 | ME, NL |
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12.52 |
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20 | 0.64 | 1.36 | NL, BG, ME, MK, IT, PL, SK |
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2.88 | |
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BOLD:AEI925 | 3 | 0.64 | 0.96 | ME |
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12.02 | |
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1 | N/A | N/A | ME |
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2.78 |
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18 | 0.18 | 0.34 | NL, PL, ME |
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2.78 | |
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1 | N/A | N/A | ME |
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6.96 | |
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3 | 1.27 | 1.6 | ME, MK |
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2.76 |
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2 | 0.16 | 0.16 | ME |
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2.76 | |
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133 | 0.81 | 2.37 | NL, FR, ME, DE, GB, BG, IT, PL, SK, ES, CH |
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3.89 |
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12 | 0.14 | 0.85 | ME |
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3.89 | |
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3 | 0.32 | 0.48 | ME, MK |
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2.72 |
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28 | 0.55 | 3.12 | NO, DE, ME |
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7.53 | |
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11 | 1.68 | 3.47 | NL, DE, NO, MK, ME, RU |
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8.7 |
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1 | N/A | N/A | ME |
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8.7 | |
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1 | N/A | N/A | ME, RO |
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4.83 |
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9 | 0.29 | 0.97 | NO, IT, ME |
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9.83 | |
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2 | 0.16 | 0.16 | ME |
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1.44 |
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2 | 0.64 | 0.64 | ME, SR |
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1.44 | |
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8 | 1.46 | 2.25 | ME, MK |
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6.57 |
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4 | 1.42 | 2.09 | ME |
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6.25 | |
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2 | 0.32 | 0.32 | ME |
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2.17 |
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4 | 0.82 | 1.34 | RS, ME, RO |
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2.17 | |
11. |
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1 | N/A | N/A | ME |
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4.81 |
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1 | N/A | N/A | ME |
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4.81 | |
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41 | 0.59 | 3.05 | NO, NL, GL, DE, ME, RS |
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13.3 |
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2 | 0 | 0 | ME |
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13.3 | |
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2 | 1.2 | 1.2 | NO, ME |
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16.18 |
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2 | 1.03 | 1.03 | DE, ME |
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14.61 | |
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3 | 0.59 | 0.7 | ME |
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17.02 |
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7 | 0.09 | 0.32 | NO, NL, ME |
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16.03 |
Molecular distances
Molecular distances
Molecular distances, based on the Kimura 2-parameter model of the analysed specimens of water mites from Montenegro. BINs are based on the barcode analysis from 15 November 2021.
File: oo_613357.xlsx
Compact Neighbour-Joining tree
Neighbour-joining tree
Compact Neighbour-Joining tree of all analysed water mite species based on Kimura 2-parameter distances. The tree was edited in MEGA7 (Kumar et al. 2016). Specimens are classified using ID numbers from BOLD and species name. BINs are based on the barcode analysis from 15 November 2021. Numbers next to nodes represent non-parametric bootstrap values (1,000 replicates, in %). The analyses involved all 233 COI nucleotide sequences.
File: oo_613358.pdf