Environmental determinants of water mite (Acari: Hydrachnidia) distribution in the ancient Lake Skadar system

JGLR-01487; No. of pages: 9; 4C: Journal of Great Lakes Research xxx (xxxx) xxx

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Environmental determinants of water mite (Acari: Hydrachnidia) distribution in the ancient Lake Skadar system Andrzej Zawal a,⁎, Aleksandra Bańkowska a, Grzegorz Michoński a, Michał Grabowski b, Agnieszka Szlauer-Łukaszewska a, Tomasz Czernicki a, Edyta Stępień c, Mateusz Płóciennik b, Vladimir Pešić d a Department of Invertebrate Zoology and Limnology, Institute for Research on Biodiversity, Faculty of Biology, Center of Molecular Biology and Biotechnology, University of Szczecin, Wąska 13, 71–415 Szczecin, Poland b Department of Invertebrate Zoology and Hydrobiology, University of Łódź, Poland c Department of Plant Taxonomy and Phytogeography, Institute for Research on Biodiversity, Faculty of Biology, University of Szczecin, Wąska 13, 71-415 Szczecin, Poland d Department of Biology, University of Montenegro, Cetinjski put b.b., 81000 Podgorica, Montenegro

a r t i c l e

i n f o

Article history: Received 24 September 2018 14 April 2019 Accepted 7 May 2019 Available online xxxx Communicated by Christian Albrecht Keywords: Water mites Mesotrophic lake Mediterranean lake Littoral zone Sublacustrine springs

a b s t r a c t In comparison to Central Europe, the knowledge about water mites inhabiting the natural lakes of southern Europe is scarce. This is a first study focusing on the water mite species composition and zonation in a large Mediterranean lake, i.e. ancient Lake Skadar basin, and identifying the role of physical and chemical water parameters in their distribution. The Hydrachnidia community of Lake Skadar is composed of 53 species. The most diverse water mite assemblages were found in the littoral zone and in the sublacustrine springs. Our study revealed that water mites were most abundant in the deeper, open part of Lake Skadar. Typically sublacustrine species dominated in all zones and habitats of Lake Skadar. The rheobiontic and rheophilic species also had a substantial share, mainly in sublacustrine springs, but also in the open lake area. The unique feature of the Lake Skadar water mite community was an absence of many species typical for the vernal astatic waters and for the shallow phytolittoral zone, even if such habitats were present. We conclude that the structure of the water mite communities in Lake Skadar are associated with particular zones (sublacustrine springs, littoral, open lake area) of the lake and with local environmental conditions, predominantly temperature. © 2019 Published by Elsevier B.V. on behalf of International Association for Great Lakes Research.

Introduction Water mites are the most diverse group of arachnids occurring in lentic and lotic aquatic ecosystems (Davids et al., 2007). They are important component of macroinvertebrate assemblages and can be reliable bioindicators for monitoring pollution and anthropogenic influences (Goldschmidt, 2016). Despite the fact that Hydrachnidia reach the highest diversity in the Mediterranean region, the studies upon their distribution and ecology in the Mediterranean lakes are very scarce. There are mostly taxonomic and faunistic data (Pešić, 2002, 2003; Baker et al., 2008), while the distribution and abundance of water mite assemblages in lakes have rarely been studied (Rieradevall and Gil, 1993). Most of the lakes studied for water mites are situated in Central Europe (Davids et al., 2007). These studies showed that water mites are most abundant in the littoral zone, while in the pelagic zone they are present only sporadically (Davids et al., 2007). The highest numbers of species are found in vegetation zone with a difference between water ⁎ Corresponding author. E-mail address: [email protected] (A. Zawal).

mite communities associated with emerged and submerged vegetation (Pieczyński, 1959, 1960; Kowalik, 1977; Zawal, 1992, 2008a; Stryjecki et al., 2016, 2017; Zawal et al., 2017, 2018). Many ecological studies identify vegetation, trophy of the water and water temperature as significant factors affecting the abundance of water mites (Kowalik, 1973, 1984; Meyer and Schwoerbel, 1981; Bagge, 1989; Rieradevall and Gil, 1993). Lake Skadar is a shallow lacustrine ecosystem located in the outer part of the Dinaric Alps, in the western Balkans. The local climate is typically Mediterranean with hot and dry summers as well as mild and wet winters, with temperature never, or extremely rarely, falling below 0 °C. It is the largest lake on the Balkan Peninsula with a surface area fluctuating seasonally between 353 and 500 km2 (Pešić et al., 2018a). Recent studies have shown that the present lake itself is very young and formed not earlier than 1200 years before present (Mazzini et al., 2015). However, the Skadar basin with its system of sublacustrine springs is ancient and dates back at least to the Pliocene (Grabowski et al., 2018). The first paper on water mite fauna of the Lake Skadar basin was published at the beginning of the 20th century by Thon (1903). Since then, water mites of Lake Skadar have been sporadically studied (Pešić, 2002; Smit and Pešić, 2004).

https://doi.org/10.1016/j.jglr.2019.06.002 0380-1330/© 2019 Published by Elsevier B.V. on behalf of International Association for Great Lakes Research.

Please cite this article as: A. Zawal, A. Bańkowska, G. Michoński, et al., Environmental determinants of water mite (Acari: Hydrachnidia) distribution in the ancient Lake Skad..., Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2019.06.002

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Recently, Pešić et al. (2018a) published numerous new faunistic records from Lake Skadar, based on materials collected by the Andrzej Zawal and his team during their scientific expeditions to Montenegro in 2014 and in 2015. An overview of the water mite richness and endemism in the Skadar Lake basin, including the history of research, was provided by Zawal and Pešić (2018). However, knowledge of the ecology and distribution of water mites in Lake Skadar is still limited. Bańkowska et al. (2016) studied the reproduction of selected species from this lake, but the spatial and temporal variability of water mite community structure in relation to environmental conditions has not been studied. Our study is the first attempt to identify the main drivers defining the distribution of the water mite fauna in a large and shallow Mediterranean lake. Thus, the aims of our study are: 1) to verify whether different zones of Lake Skadar are inhabited by distinct water mite assemblages, 2) to identify which, if any, environmental parameters determine the composition and distribution of water mite assemblages.

were also made for additional categories for plant cover-abundance scales: 1 (b5%), 2, (5–10%), 3 (11–25%), 4 (25–50%), 5 (50–75%), and 6 (75–100%). The substrates were split into organic, fragmented sludge – mud; and inorganic – all the others. Inorganic substrates were categorized depending on the grain size: sand b2 mm, gravel – 2–20 mm, stones – 21–100 mm, rocks N100 mm.

Water physical-chemical parameters Physical-chemical parameters of water were measured for each lake zone (Table 3). The water physical-chemical parameters were measured in situ during macroinvertebrate sampling. Temperature, pH, electrical conductivity and dissolved oxygen content were measured with an Elmetron CX401 multiparametric sampling probe; BOD5 by Winkler's method; and P-PO4, N-NO3, N-NH4 with a Slandi LF205 photometer.

Study area Statistical analysis The study focused on the Skadar/Shkodra Lake itself and on a large flooded area along its northwestern shoreline (hereafter “lake and floodplain area”). The latter consists of a part (10268 ha) that is constantly flooded and a part (2042 ha) subjected to seasonal floods (Knežević and Todorovic, 2004). For the purpose of the further analyses, the study area was partitioned as follows: a) mouths of inflowing rivers; b) sublacustrine springs; c) littoral and open lake area. Almost the entire bottom of the lake is in the photic zone, meaning there is no typical profundal zone. However, in the photic areas we distinguish: a) the typical shallow littoral (0.3–1.5 m depth) with mosaic bottom (rocks, stones, sand) and macrophytes; b) the open deeper part of the lake (open lake area) (2–6 m) with muddy bottom, almost devoid of vascular plants. Material and methods Water mite sampling method The samples were collected in May (N = 22), July (N = 40) and September (N = 30) of 2014. Samples from the depth down to 1.5 m were collected using a hydro-biological sampler (hand-net) with a triangular hoop: side length 30 cm, mesh size 200 μm, applying the semi-quantitative approach described by Gerecke et al. (1998). The sampling method involved 40 sweeps performed directly above the bottom surface over an area of about 2 m2, at each site. Samples from greater depths were collected using a dredge with a triangular hoop: side length 30 cm, mesh size 200 μm. The dredge was dragged across a length of about 100 m, which covered an area comparable to that sampled with the hand-net. Additionally, light-traps (Zawal, 2018) were used for collecting water mites at the depths from 1.5 to 20 m depth (the latter in sublacustrine springs). The light-traps were used only to get an overview of the full species diversity and the data obtained this way were not included in the statistical analyses. Water mites were determined to species level using the keys by Davids et al. (2007), Zawal (2008b), Di Sabatino et al. (2010) and Gerecke et al. (2016). Environmental parameters The depth was measured by “Raymarine e7 Hybrid Touch” depth sounder. Parameter “plants” means degree of bottom coverage by water plants referred to the Braun-Blanquet methods modified by Stępień et al. (2019). The parameters are: mud, sand, gravel, stones, rocks were estimated as a share in the whole substratum also by the Braun-Blanquet (1964) methods modified by Stępień et al. (2019), where the sum of all substrates had to amount 100%. The records

Samples were grouped according to zone from which they were collected (open lake area N = 32, river mouth N = 4, littoral N = 23, sublacustrine springs N = 33) and according to months (May N = 22, July N = 40, September N = 30) in order to estimate the diversity/species richness patterns. The diversity indices (S – number of species, N – number of total specimens, d – Margalef Index, J′ – Pielou Index, H′ (loge) – Shannon Index, 1-Lambda′ – Simpson Index, ES(n) – rarefaction) were calculated using PRIMER 6 software (Clarke and Gorlay, 2006). The rarefaction index ES(n) (Zar, 1984), was derived for n = 170 (specimens/zone) and n = 1067 (specimens/month). The oneway ANOSIM (Analysis of Similarity) using Bray-Curtis Index for two factors – ‘zone’ and ‘month of sampling’ was conducted using PRIMER 6 software (Clarke and Gorley, 2006). Multivariate ordination analyses were used to determine the environmental parameters responsible for the distribution of water mite species in the Skadar Lake (Canoco for Windows 4.5 package). The Detrended Correspondence Analysis (DCA) (Hill and Gauch, 1980; ter Braak and Prentice, 1988) was used to assess the length of the biotic data gradient with detrending by segments. As it was long (19.97 SD units and 3.27 SD units for the first and second DCA axes respectively), the Canonical Correspondence Analysis (CCA) (ter Braak, 1986; ter Braak and Verdonschot, 1995) was applied to identify environmental factors that significantly influence biota distribution. Three separate CCAs were applied, each one for different scale environmental factors: zones of lake (macrohabitats) – binominal scale (1 – yes, 0 – no), sampling mesohabitats: depth – uniform scale; participation of substrates – interval scale (1 – b5%, 2–5–10%, 3–11–25%, 4–25–50%, 5–50–75%, and 6–75–100%), and water hydrochemical parameters – uniform scale. The significance of the effect of the respective environmental variables on species composition was determined using stepwise variable selection (p ≤ 0.05). The Monte Carlo test with 499 unrestricted permutations under full model was conducted in order to pinpoint the significant variables. One-way ANOVA was used, based on the log-transformed dataset, to verify the statistical significance of differences between water mite abundances in particular zones and months (Jayaraman, 1999). These analyses were performed using the Statistica 13 PL package (StatSoft Inc., 2015). Water mites were categorized into several synecological groups: a) lacustrine species – typical for lakes; b) species of small water bodies – typical for ponds and other small, permanent reservoirs; c) species characteristic for astatic waters – typical for spring, periodic reservoirs; d) rheobiontic and rheophilic species – typical for lotic waters; e) crenobionts and crenophilous species – typical for springs; f) tyrphobionts and tyrphophilous species – typical for peatbogs (Davids et al., 2007).

Please cite this article as: A. Zawal, A. Bańkowska, G. Michoński, et al., Environmental determinants of water mite (Acari: Hydrachnidia) distribution in the ancient Lake Skad..., Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2019.06.002

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Results Altogether, 4606 individuals (1953 females, 1952 males, 696 deutonymphs and 5 larvae) belonging to 42 species of water mites were collected from 45 localities (Table 1, Fig. 1). The number of individuals per sample ranged from 1 to 514 (in average 50 ind./sample). The species Unionicola aculeata was an eudominant – contributing 43.4% of the total number of collected individuals. Four species (Hygrobates longipalpis, Lebertia porosa, H. nigromaculatus, H. fluviatilis) were dominants, while each of the remaining species was represented by b1% of individuals (Table 1). Together, the eudominant and dominant species accounted to 74.2% of the collected material. The highest frequency was observed for Unionicola aculeata (44.8% of samples), followed by U. minor (18.8%), Lebertia porosa, L.

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longiseta and Hygrobates fluviatilis (17.7%), Hexaxonopsis serrata and Oxus strigatus (15.6%) (Table 1). Typically lacustrine taxa formed the most species-rich synecological group in the water mite fauna of the Skadar Lake, including 21 species and contributing 75% of the collected material. Rheobionts and rheophiles, with 11 species, contributed 23% of the total collected material. The share of water mites characteristic for small water bodies, with seven species, was markedly lower (2%). The least numerous were tyrphophiles and crenophiles, each with two species only. Lacustrine species dominated in the littoral zone, with 11 species accounting to 53% of the whole material. The share of rheobionts and rheophiles, represented by six species, was also substantial (42%). The lacustrine species dominated also in the open part of the lake, with 11 species, accounting to almost 100% of the whole material. In the mouths of the

Table 1 List and abundance of water mite species collected in four different zones of Lake Skadar: F – females, M – males, De – deutonyphs, L – larvae, Do – dominance, Fq – frequency, lit. – littoral, o.l.a. – open lake area, r.m. – river's mouth, spr. – sublacustrine springs, n.o. – numbers. Species

F

M

De

Lebertia ineaqualis (Koch, 1837) Lebertia longiseta (Bader, 1955) Lebertia porosa Thor, 1900 Lebertia sp. Oxus angustipositus K. Viets, 1908 Oxus longisetus (Berlese, 1885) Oxus ovalis (Müller, 1776) Oxus setosus (Müller, 1776) Oxus sp. Sperchon clupeifer (Piersig, 1896) Teutonia cometes (Koch, 1837) Monatractides stadleri (Walter, 1924) Torrenticola amplexa (Koenike, 1908) Brachypoda versicolor (Müller, 1776) Hexaxonopsis romijni (K. Viets, 1923) Hexaxonopsis serrata (Walter, 1928) Atractides nodipalpis Thor, 1899 Hygrobates fluviatilis (Ström, 1768) Hygrobates longipalpis (Hermann, 1804) Hygrobates nigromaculatus Lebert, 1879 Hygrobates setosus Besseling, 1942 Hygrobates sp. Limnesia undulata (Müller, 1776) Limnesia undulatoides Davids, 1997 Limnesia sp. Forelia liliacea (Müller, 1776) Forelia variegator (Koch, 1837) Forelia sp. Piona coccinea (Koch, 1836) Piona disparilis (Koenike, 1895) Piona imminuta (Piersig, 1897) Piona pusilla (Neuman, 1875) Piona rotundoides (Thor, 1897) Piona stjoerdalensis (Thor, 1897) Piona sp. Pionopsis lutescens (Hermann, 1804) Neumania deltoides (Piersig, 1894) Neumania limosa (Koch, 1836) Neumania sp. Unionicola crassipes (Müller, 1776) Unionicola gracilipalpis (K. Viets, 1908) Unionicola minor (Soar, 1900) Unionicola aculeata (Koenike, 1890) Unionicola sp. Arrenurus albator (Müller, 1776) Arrenurus buccinator (Müller, 1776) Arrenurus conicus Piersig, 1894 Arrenurus cylindratus Piersig, 1894 Arrenurus stjordalensis Thor, 1899 Arrenurus sp. Mideopsis roztoczensis Biesiadka & Kowalik, 1979 larvae Total

24 54 144

34 38 163

121 14 83 7

2 2 9 4

L

1

2 13 1

1 3 1 1 15 56 45 1 113 239 121 1

114 169 99 11

14

2 5

1

6 20 53

2 1 39 23 109 6

36 1

18

1 2

2 10 3 2 14 1

7

1 31 1

7 1

1 48 1 2 3 2 4

14 2 1 1

54 1 88 831

4 117 1015

23 153 26

1 1 1 1 4 1 1 1953

3

1952

696

4 5

Total

Do (%)

Fq (%)

179 106 391 7 2 4 22 4 1 1 4 1 1 21 78 99 1 266 431 329 12 6 2 19 1 102 2 2 6 14 7 2 21 1 14 3 39 2 1 58 1 228 1999 26 1 1 1 1 4 4 1 4 4606

3.9 2.3 8.5 0.2 0.04 0.09 0.5 0.09 0.02 0.02 0.09 0.02 0.02 0.5 1.7 2.1 0.02 5.8 9.4 7.1 0.3 0.1 0.04 0.4 0.02 2.2 0.04 0.04 0.1 0.3 0.2 0.04 0.5 0.02 0.3 0.07 0.8 0.04 0.02 1.3 0.02 5.0 43.4 0.6 0.02 0.02 0.02 0.02 0.09 0.09 0.02 0.09

4.2 17.7 17.7 3.1 1.0 2.1 8.3 1.0 1.0 1.0 3.1 1.0 1.0 8.3 6.3 15.6 1.0 17.7 9.4 8.3 2.1 1.0 1.0 3.1 1.0 8.3 1.0 1.0 3.1 1.0 2.1 1.0 2.1 1.0 4.2 1.0 4.2 2.1 1.0 9.4 1.0 18.8 44.8 3.1 1.0 1.0 1.0 1.0 3.1 1.0 1.0 2.1

lit. (N = 23)

o.l.a. (N = 32)

r.m. (N = 4)

spr. (N = 33)

n.o.

(%)

n.o.

n.o.

(%)

n.o.

(%)

163 35 93

16.7 3.6 9.5 0.0 0.0 0.1 1.1 0.0 0.0 0.0 0.4 0.1 0.1 1.7 8.0 4.0 0.0 3.5 24.3 0.0 0.0 0.0 0.2 1.6 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.2 0.0 0.0 0.2 0.0 2.6 0.1 0.1 4.7 0.1 13.2 0.2 0.0 0.0 0.0 0.0 0.0 0.0 0.4 0.0 0.0

0.0 4.7 0.0 0.0 0.0 0.0 0.6 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.6 0.0 0.0 0.0 0.0 0.0 1.2 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.6 0.0 0.6 0.0 8.8 81.8 0.0 0.0 0.0 0.0 0.0 0.6 0.0 0.0 0.0

16 63 298 6 2 3 8 4 1 1

0.9 3.5 16.7 0.3 0.1 0.2 0.4 0.2 0.1 0.1 0.0 0.0 0.0 0.1 0.0 2.6 0.1 13.0 10.9 18.4 0.7 0.3 0.0 0.0 0.0 5.7 0.1 0.1 0.2 0.8 0.0 0.0 0.1 0.1 0.6 0.2 0.8 0.0 0.0 0.5 0.0 0.2 18.8 1.5 0.0 0.1 0.1 0.1 0.2 0.0 0.1 0.1

1 11

4 1 1 17 78 39 34 237

2 16 1

2

2 25 1 1 46 1 129 2

4

976

1

2

3 13

2

1

3 7 20 1

2 81 1523 1

2 1675

(%) 0.0 0.0 0.0 0.1 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.2 0.0 0.8 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.2 0.0 0.4 0.0 1.2 0.0 0.1 0.0 0.0 0.0 0.0 0.1 0.0 4.8 90.9 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.1

8

1

1

2

1 1 15 139

1

170

1 47 1 231 194 327 12 6

102 2 2 3 14

1 1 11 3 14

9 3 335 26 1 1 1 3 1 2 1782

Please cite this article as: A. Zawal, A. Bańkowska, G. Michoński, et al., Environmental determinants of water mite (Acari: Hydrachnidia) distribution in the ancient Lake Skad..., Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2019.06.002

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Fig. 1. Map of the investigated area with sampling localities.

inflowing rivers, the typically lacustrine species were represented by seven species (94% of the total material collected in this zone). Only two species of rheobionts and rheophiles (5% of the total number of individuals) were collected in this zone. In sublacustrine springs, the lacustrine species dominated with 16 species and 63% of total material collected in this habitat, followed by the 8 species of rheobionts and reophiles (36% of the material). The species characteristic for a small water bodies were least represented in sublacustrine springs, both in term of diversity (4 species) and the percentage (1%) of the collected material. Twenty three species with 979 individuals were collected in the littoral, while 13 species with 1675 individuals were collected in the open, deeper part of the lake. The average number of individuals per sample was higher in the open part of the lake (52.3 ind./sample) than in the littoral zone (40.8 ind./sample). On the other hand, the average number of species was higher in the littoral (2.5 species/sample) than in the open part of the lake (2.1 species/sample). A total of 1796 individuals belonging to 32 species was collected from sublacustrine springs, with the average of 51.3 individuals and 2.8 species per sample, respectively. Only 170 individuals belonging to 10 species were collected from the mouths of inflowing rivers, with the average of 42.5 individuals and 3.5 species per sample, respectively (Tables 1 and 2). The abundance of water mites differed significantly between zones (ANOVA: F3, 84 = 6.01, P b 0.009). The ANOSIM conducted for ‘zone’ factor indicated that the pairs springs-littoral, springs-open lake area and littoral-open lake area differed significantly. In contrary, the following pairs: springs-mouths of rivers, littoral-mouths of rivers and open lake area-mouths of rivers did not differ significantly (p 0.05). The global significance level of sample statistic was 0.1%, and the number of possible permutations was at

least 14,950. The R statistics was high for littoral-open lake area (0.454) and for springs-open lake area (0.290), equalling globally to 0.261. The other pairs revealed low R statistics (springs-littoral 0.117; springs-mouths of rivers −0.054; littoral-mouths of rivers −0.015, and open lake area-mouths of rivers 0.155). The Global R value for ‘zone’ factor/matrix and the R value obtained by permutation of the similarity matrix are shown in Electronic Supplementary Material (ESM) (Fig. S1). The number of permuted statistics greater than or equal to Global R was 0. The ANOSIM conducted for the ‘zone’ factor showed that Hydrachnidia communities differed significantly between open lake area and the littoral zone (including sub-lacustrine springs), while the river mouths communities were partially similar for the all lake area, being especially common in the coastal zone. The highest number of species was found in sublacustrine springs, next in littoral, open lake and river mouths, while the highest

Table 2 Richness, abundance and diversity of water mite assemblages in four different zones of the Skadar Lake: (S - number of species, N - number of total specimens, M - average number of specimens, d - Margalef Index, J′ - Pielou Index, H′(loge) - Shannon Index, 1-Lambda′ Simpson Index, ES(n) - rarefaction). Habitat

S

N

M

d

J′

ES (170)

H′ (loge)

1-Lambda ′

Littoral River mouth Open lake area Sublacustrine springs

24 10 13 32

985 170 1671 1715

40.8 42.5 52.3 51.3

3.34 1.75 1.62 4.16

0.74 0.33 0.17 0.64

16.29 10.00 6.25 15.99

2.35 0.76 0.44 2.23

0.87 0.32 0.17 0.86

Please cite this article as: A. Zawal, A. Bańkowska, G. Michoński, et al., Environmental determinants of water mite (Acari: Hydrachnidia) distribution in the ancient Lake Skad..., Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2019.06.002

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Table 3 Values of some physical-chemical parameters recorded in four different zones of the Skadar Lake: min, max (median).

Temperature (°C) pH Conductivity (μS cm−1) Ammonium (mg L−1) Nitrates (mg L−1) Phosphates (mg L−1) Water hardness (mg L−1) BOD5 (mg L−1)

Littoral (N = 23)

Open area lake (N = 32)

Sublacustrine springs (N = 33)

River mouth (N = 4)

24–32 (26.5) 6.9–9.1 (7.75) 202–348 (256.4) 0.05–0.55 (0.195) 0.1–0.18 (0.107) 0.01–0.87 (0.291) 4.0–8.72 (5.780) 1.68–7.86 (4.281)

9–28 (20.1) 6.9–8.6 (8.06) 205–334 (242.7) 0.05–0.61 (0.106) 0.1–0.21 (0.111) 0.01–0.708 (0.109) 4.0–10.28 (5.951) 1.05–8.40 (3.624)

7–29 (18.8) 6.8–8.1 (7.88) 205–400 (276.2) 0.05–0.863 (0.237) 0.1–0.23 (0.109) 0.01–0.75 (0.091) 1.3–12.14 (7.347) 0.22–7.63 (2.607)

17–29 (24.5) 7.1–8.4 (7.71) 102–274 (174.2) 0.05–0.30 (0.155) 0.1 0.1 1.6–5.45 (2.917) 2.78–4.42 (3.437)

abundance was observed in sublacustrine springs, open lake, littoral and river mouths. The diversity and species richness (Pielou Index, Shannon-Wiener Index, Simpson Index, rarefaction) was highest in littoral, next in the sublacustrine springs, river mouths and open lake macrohabitats (Table 2). The dominant water mite species in the open part of the lake was Unionicola aculaeata, while Hygrobates longipalpis, Lebertia ineaqualis, Unionicola minor and L. porosa dominated in the littoral zone. The dominants in the sublacustrine springs were: U. aculeata, Hygrobates nigromaculatus, Lebertia porosa, H. fluviatilis and H. longipalpis, while in the mouths of inflowing rivers, the water mite assemblages were dominated by Unionicola aculeata (Table 1). The CCA obtained for macrohabitat zonation indicated that presence of shallow littoral and sublacustrine springs significantly determined Hydrachnidia communities, whereas open lake area zone and river estuaries did not have characteristic groups of taxa. The first canonical axis explained 6.1%, and 2nd axis explained 5.6% of species data variance. Simultaneously, they explained respectively 52% and 47.6% of species-environment relation variance. The environmental variables used in this ordination explained 11.72% of the total variability of occurrence of the species - littoral 5.57% and sublacustrine springs 6.06%. Presence of sublacustrine springs was negatively correlated, whereas presence of river estuaries and presence of open lake area zone positively with the first canonical axis. Presence of littoral zone was correlated positively with second canonical axis. Water mites grouped in three clusters (Fig. 2). Group 1 included the species associated with the littoral macrohabitat type(s). Group 2 included the species associated with sublacustrine springs, while the group 3 included species living outside sublacustrine springs and thus associated with more open lake area and mouths of inflowing rivers. The results of CCA analysis performed to identify the relationship between the occurrence of water mites and the mesohabitat quality (plants coverage, stones, rocks, depth, sand, mud, gravel) showed that the first four factors were significant. The first canonical axis explained 6.8%, and 2nd axis 4.3% of species data variance. Simultaneously they explained respectively 33% and 20.6% of species-environment relation variance. The environmental variables used in this ordination explained 20.68% of the total variability of occurrence of the species, presence of aquatic plants 5.08%, stones 4.69%, lake depth 3.81% and rocks 3.22%. Presence of stones and plants on the bottom was positively correlated whereas presence of mud negatively with the axis 1. All the other factors were not correlated with the first two canonical axes. The results of CCA analysis performed to reveal the relationships between abundance of water mites and substrate parameters showed presence of three species groups. The first and second group, including

the highest number of species, were typical for periphyton and perilithon mesohabitats. They appeared on aquatic plants and stones. The second group aggregated only two species Hygrobates longipalpis and Lebertia inaequalis. The third group, including mostly the typical lacustrine species avoided such types of habitats (Fig. 3). The analysis of the vertical distribution of water mites revealed that most species occurred in the deeper littoral and on the depths of 6, 10 and 20 m (Fig. 4). In terms of abundance, the highest average number of individuals was found at the depth of 4 m. In the sublacustrine springs, the highest average numbers of species were found at the depths of 2, 3 and 6 m, consecutively. In contrast, the highest numbers of individuals were observed at the depths of 2 and 4 m, consecutively. In contrary, the highest average numbers of species and individuals in the mouths of inflowing rivers were found on the depth of only 1 m (Fig. 5). Generally, species occurrences and abundances in particular depths were extremely variable between samples (Figs. 4 and 5). The results of CCA analysis performed to identify the relationship between the occurrence of water mites and the hydrochemical parameters, showed that only PO4, temperature, BOD5 and NO3 content had significantly impact. The first canonical axis explained 6.0%, and 2nd axis 5.7% of species data variance. Simultaneously they explained respectively 26.8% and 25% of species-environment relation variance. The environmental variables used in this ordination explained 22.51% of the total variability of occurrence of the species, P-PO4 5.28%, temperature 4.69%, BOD5 3.62% and N-NO3 content 2.44%. Conductivity, water temperature and pH are correlated positively whereas oxygen content correlated negatively with the canonical axis 1. Content of N-NH4 and

Table 4 Richness, abundance and diversity of water mite assemblages in the Skadar Lake during the three sampling periods: (S - number of species, N - number of total specimens, M - average number of specimens, d - Margalef Index, J′ - Pielou Index, H′(loge) - Shannon Index, 1-Lambda′ - Simpson Index, ES(n) - rarefaction). Months

S

N

M

d

J'

ES(1067)

H′(loge)

1-Lambda′

May July September

25 26 24

1067 2319 1155

17.4 20.3 13.1

3.44 3.23 3.26

0.58 0.48 0.60

25.00 21.46 23.61

1.88 1.56 1.91

0.77 0.62 0.76

Fig. 2. CCA analysis of water mite occurrence in particular zones of Skadar Lake: 1–3 groups of water mites associated with particular lake zones.

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permutations was very high, the R statistics were low, and globally equalled 0.066 (September–May 0.130; September–July 0.024; May– July 0.097). The Global R value for ‘month’ factor/matrix (dotted black line in ESM Fig. S1) and the R value obtained by permutation of the similarity matrix overlain. The number of permuted statistics greater than or equal to Global R was 5. The ANOSIM conducted for the ‘month' factor revealed that Hydrachnidia communities in Skadar Lake did not change distinctly during the sampling season. The species most abundant in May were Hygrobates longipalpis, Lebertia ineaqualis, and L. porosa, while Hygrobates nigromaculatus, Unionicola aculeata dominated in July. The abundance of some species was lower in September. Four species (Hygrobates longipalpis, Lebertia ineaqualis, L. porosa and Unionicola crassipes) occurred predominantly in May; while five species (Hygrobates nigromaculatus, H. fluviatilis, Unionicola aculeata, Forelia liliacea and Hexaxonopsis romijni) were reported from July. Lebertia porosa and Unionicola minor were characterized by a similar number of individuals in May and in September (Fig. 7). Discussion Richness of water mite fauna in Lake Skadar

Fig. 3. CCA analysis of water mite occurrence according to environmental parameters: 1–3 groups of water mites associated with particular parameters.

P-PO4 in the water were correlated positively with axis 2. Content of NNO3 and BOD5 were not correlated with the first two axes. Almost the same numbers of species and average number of individuals were collected in each month (May N = 22, July N = 40, September N = 30) (Table 4). The Simpson Index, Margalef Index and rarefaction values were highest in May, next in September and July; however the Pielou and Shannon-Wiener indices were highest in September, next in May and July (Table 4). The abundance of water mites did not differ significantly between particular months (ANOVA: F2, 85 = 0.37, P = 0.69). The ANOSIM conducted for ‘month' factor indicated that the pairs September–May and July–May differed significantly, but the pair September–July did not differ (p N 0.05). Whereas global significance level of sample statistic was 0.6%, and the number of possible

Summarising the data from our study and from the literature, a total of 53 Hydrachnidia species have been reported so far from Lake Skadar and from the associated water bodies (Pešić et al., 2018a; Zawal and Pešić, 2018). Our study confirmed presence of 42 species in Lake Skadar and in its flooding zone. Nine species known from the literature (i.e. Hydrochoreutes krameri, Tiphys torris, N. vernalis, N. papillosa, Forelia cetrata, Arrenurus claviger, A. cuspidifer, A. maculator, A. sinuator) were not found during the present study. Fifty three species is still a small number of water mite species for such a big lake as Lake Skadar (Zawal and Pešić, 2018). In Central Europe, lakes of similar size contain much higher diversity of water mites (Cichocka and Biesiadka, 1994; Biesiadka, 2003); even the smaller oligotrophic lakes or the water bodies belonging to different trophic levels (hypertrophic or dystrophic) have often a similar number of species (Pieczyński, 1960; Bagge, 1989; Zawal, 1992, 2007; Cichocka and Biesiadka, 1994; Davids et al., 1994; Biesiadka and Cichocka, 1997; Kłosowska et al., 2013). Also the abundance of water mites in Lake Skadar, calculated as the average number of individuals per sample, was very low. Usually the abundance of water mites in lakes is higher, reaching even 2000 specimens (Pieczyński, 1959, 1960; Smith et al., 2010). Our study revealed that the richest water mite assemblage in Lake Skadar occurred at the depth between 4 and 6 m. For comparison, in a lake in Finland, Bagge (1983, 1989) found 70% of the total number of species at the depth down to 1.5 m, while Viets (1924, 1930) collected water mites even down to 30 m in lakes of northern Germany. Synecological analysis of the water mite community of Lake Skadar revealed that the lacustrine and rheophilous species groups were most abundant, consecutively. The high share of lacustrine species is not unusual but a large proportion of rheophilous species in water mite assemblage of this shallow lake is surprising. In most European lakes, rheophilous species poorly contribute to water mite assemblages (Zawal, 1992, 2007, 2010; Dąbkowski et al., 2007; Kłosowska et al., 2013; Zawal et al., 2017). There are two possible reasons that explains such a higher share of rheophilous species in Lake Skadar community. First, many of rheophilous species can be associated with sublacustrine springs. Second, some rheophilous species, such as Lebetia porosa, L. ineaqualis and L. longiseta, may occur more frequently in South European lakes than in the northern part of the continent (Pešić, 2002, 2003; Baker et al., 2008; Zawal and Pešić, 2018). Spatial pattern of water mite assemblage of Lake Skadar

Fig. 4. Average number of water mite species in the Skadar Lake depth profile.

Our study revealed that water mites were most abundant (as the average number of specimens per sample) in the deeper, open part of Lake

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A. Zawal et al. / Journal of Great Lakes Research xxx (xxxx) xxx

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Fig. 5. Average abundance of water mite assemblages in the Skadar Lake depth profile: A – lake with floodplain area, B – lake reservoir, C – sublacustrine springs, D – river mouths.

Skadar, followed by sublacustrine springs, littoral zone and the mouths of inflowing rivers. The observed results are in strong opposition to the situation in Central European lakes, where water mites inhabit mainly littoral (Pieczyński, 1959, 1960; 1989; Zawal, 1992, 2007; Cichocka and Biesiadka, 1994; Davids et al., 1994; Biesiadka and Cichocka, 1997; Kłosowska et al., 2013; Zawal et al., 2013a, 2013b; Stryjecki et al., 2017). On the other hand, the most diverse water mite assemblage in Lake Skadar was found in littoral zone, followed by sublacustrine springs, river mouths, and the open lake (Table 2). In Central European lakes, the water mite assemblages associated with littoral zone are mainly represented by the species characteristic for the small water bodies (Pieczyński, 1960; Bagge, 1989; Zawal, 1992, 2007; Cichocka and Biesiadka, 1994; Davids et al., 1994; Biesiadka and Cichocka, 1997; Kłosowska et al., 2013; Zawal et al., 2013a; Stryjecki et al., 2017). In Lake Skadar, the littoral zone was inhabited by typically lacustrine (Hygrobates longipalpis, Unionicola minor, U. crassipes, Hexaxonopsis serrata) and rheophilous species (Lebertia ineaqualis, L. porosa, L. longiseta, Hexaxonopsis romijni, Hygrobates fluviatilis). The deeper, open part of the lake was inhabited only by typically lacustrine species (Unionicola aculeata, U. minor, Hexaxonopsis serrata). The unique feature of Lake Skadar was an absence of numerous water mites characteristic for vernal astatic waters and for the shallow phytolittoral zone. It is an unusual situation as Lake Skadar is characterized by a vast phytolittoral and astatic zones. The astatic zone of Lake Skadar was almost without any water mites, while in the phytolittoral zone mites were present in very low numbers or, in many sampled localities, they were completely absent. Zawal and Pešić (2018) assumed that this is a result of the predation pressure posed by the fry and fingerlings of many commercial fish species living in Lake Skadar as well as by the two alien invasive species, mosquito fish (Gambusia affinis) and the topmouth gudgeon (Pseudorasbora parva), that are very abundant in the seasonally inundated area and in the phytolittoral zone of Lake Skadar. The impact of these two fish species on macroinvertebrate fauna abundance is generally estimated to be very high (e.g. Merkley et al., 2015). The diversity and abundance of water mite assemblage in the shallow littoral zone of sublacustrine springs was higher than in the shallow

littoral zone of the other parts of the lake. Sublacustrine springs are generally characterized by much lower temperatures in comparison to the rest of the lake, especially from spring to autumn. Also the populations of Gambusia affinis and Pseudorasbora parva are much less abundant there (Zawal and Pešić, 2018). Proper thermal conditions are essential for the distribution and metabolism of the generally warm water G. affinis (Craig et al., 2019). In higher temperatures, this fish has a significant impact on many macroinvertebrates, including water mites (Preston et al., 2017). It is likely these factors can overcome any other environmental variables and become the main agent shaping water mite assemblages (Zawal and Pešić, 2018). An increase of the water temperature causes the oxygen content dropdown, while most of the water mites require relatively high oxygen contents and relatively low water temperatures (Davids et al., 2007). The analysis of the community structure of water mite assemblage of Skadar Lake showed dominance of two species only (Unionicola aculeata, Lebertia porosa). According to the Thienemann's rule, such situation is characteristic of degraded lakes with a limited number of habitats (Lampert and Sommer, 2007). Obviously, Lake Skadar is not degraded, and such results together with a relative poverty of habitats are rather an effect of the shallowness and very short history of the present lake. Based on the macroinvertebrate communities, two zones, the littoral and open lake, can be distinguished within Lake Skadar (Pešić et al., 2018c). The types, the number of available habitats and water temperature mainly determines the species richness of water mite assemblage in the littoral zone. Generally, the eudominant and dominant species in Lake Skadar were represented by eurythermic species, characteristics usually occurring in lakes and slow-flowing rivers (i.e. Hygrobates longipalpis, H. nigromaculatus, Lebertia porosa). The superdominant (Unionicola aculeata) in the open lake zone, probably like other unionicolids, preys on zooplankton (Proctor and Pritchard, 1990). The species with highest frequency were associated with open lake (Unionicola aculeata), they were also eurythermic rheophilous species (Lebertia porosa, Lebertia longiseta, Hygrobates fluviatilis), species connected with phytolithoral (Unionicola minor, U. crassipes, Oxus ovalis, Brachypoda versicolor, Hexaxonopsis serrata, Hygrobates nigromaculatus), and species associated with mineral bottom deposits (H. longipalpis).

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A. Zawal et al. / Journal of Great Lakes Research xxx (xxxx) xxx

Phenology of water mite assembaleges Numerous studies revealed that water mite assemblages of Central European lakes are characterized by two peaks of abundance, in spring and late summer, or by one peak in the summer (e.g. Pieczyński, 1959; Kowalik, 1973, 1977; Biesiadka, 1972; Zawal, 1992, 2007; Zawal et al., 2013a; Kłosowska et al., 2013). Two peaks of abundance appear in lakes with large shallow phytolittoral zones (Biesiadka, 1972; Cichocka, 1998). The water mite community of such lakes is dominated by species characteristic for astatic waters (Parathyas and Hydryphantes) or for small water bodies and for lake phytolittoral zone (Hydrodroma, Limnesia, Piona, Neumania, Arrenurus and others) (Cichocka, 1998; Gerecke et al., 2016). On the other hand, one peak of abundance of water mite assemblage is characteristic for lakes lacking a vast phytolittoral zone, with typically lacustrine species dominating in their community structure (Rieradevall and Gil, 1993; Biesiadka and Cichocka, 1997; Zawal, 2007). The duration of our study period was too short to assess reliably the seasonal differences, and we could not detect any significant differences in the seasonal abundance of water mites in Lake Skadar. However, we found some differences in the community composition between the studied months (Fig. 7). Interestingly, we found that species such as Hygrobates longipalpis, Lebertia ineaqualis, L. porosa and Unionicola crassipes, that in Central Europe occur during summer (Kłosowka et al., 2013; Gerecke et al., 2016), in Lake Skadar showed up mainly in spring. Phenology of these species in the Mediterranean region was not studied before; but, possibly, it depends on a number of agents including their hosts' phenology and some environmental factors.

Relationships between water mite occurrence and environmental parameters Several studies stressed importance of vegetation for the distribution of water mites (Pieczyński, 1959, 1960; Biesiadka, 1972, 2003; Stryjecki et al., 2017). Most of the water mites in our study, including both the lacustrine and rheophilous species, were associated with aquatic plants (Fig. 5). In sublacustrine springs, the water mites were found predominantly also among plants. The typically lacustrine species like Unionicola aculeata were associated with greater depths, while Lebertia ineaqualis and Hygrobates longipalis (species occurring both in lakes and slow-flowing rivers) were associated with stones both in the littoral and in sublacustrine springs (Figs. 4 and 5).

Fig. 7. Phenology of particular species of water mites in Skadar Lake.

The occurrence pattern in case of most water mites in Lake Skadar suggested their preference for low temperature (Fig. 6). Such species were associated mainly with sublacustrine springs. The second group of species consisted of water mites whose occurrence correlated with a higher trophy (indicated by a high value of P-PO4) and included species found in littoral or in the open lake area. The third group included species with apparent preferences to higher temperatures. These species occurred in the open lake area. In summary, the results of our study revealed that assemblages of water mites in Lake Skadar may be defined by particular lake zones (sublacustrine springs, littoral, open lake area); however, the zones differed only by temperatures and not by their trophic level. As a result of the increasing eutrophication process, the trophic level of Lake Skadar has changed from oligotrophic in the 1970s to mesotrophic in recent years (Pešić et al., 2018b). Presence of particular water mite species was correlated to specific conditions that exists in specific habitat and/ or zone. The correlation between presence of Hexaxonopsis romijni and level of P-PO4 indicated that this species was more typical for the littoral environment of higher trophy. On the other hand, the occurrence of typical lacustrine Unionicola aculeata correlated negatively with presence of plants. Given the global changes and ongoing climatic changes and increased demand for water, Lake Skadar (Pešić et al., 2018d), as many other shallow Mediterranean lakes, is seriously threatened and further conservation strategies are required. The further monitoring should include water mites, having in the mind a high taxonomic diversity of this group and sensitivity of their different synecological groups to detect changes in its environmental compartment in a highly sensitive ecosystem of a shallow Mediterranean lakes. Supplementary data to this article can be found online at https://doi. org/10.1016/j.jglr.2019.06.002. Acknowledgements The study was supported by the statutory funds of the University of Szczecin. Participation of Michal Grabowski in the fieldwork was supported by the statutory funds of the University of Lodz and by the Polish Ministry of Science and Education, grant number N N303 579439. The author expresses sincerely gratitude to anonymous referees for reviewing the manuscript and helping to improve the text and the language. References

Fig. 6. CCA analysis of water mite occurrence according to physical-chemical parameters: 1–3 groups of water mites associated with particular parameters.

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Please cite this article as: A. Zawal, A. Bańkowska, G. Michoński, et al., Environmental determinants of water mite (Acari: Hydrachnidia) distribution in the ancient Lake Skad..., Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2019.06.002