Hydrobiologia (2018) 819:197–215 https://doi.org/10.1007/s10750-018-3637-5 PRIMARY R ESEARCH P APER Spatial patterns of diatom diversity and community structure in ancient Lake Ohrid . . . Aleksandra Cvetkoska Aleksandar Pavlov Elena Jovanovska . . . . Slavica Toﬁlovska Saul Blanco Luc Ector Friederike Wagner-Cremer Zlatko Levkov Received: 17 November 2017 / Revised: 24 April 2018 / Accepted: 30 April 2018 / Published online: 14 May 2018 The Author(s) 2018 Abstract The extraordinary diversity in long-lived zones: littoral and sublittoral. The latter one is being lakes is largely driven by distinct eco-evolutionary characterized with higher endemic diversity. The a processes. With their unique biota and numerous and b diatom diversity and community distribution in endemic taxa, these lakes are key settings for funda- the northern and eastern part of the lake are inﬂuenced mental studies related to ecology, diversity, and by the presence of vertical (bathymetrical) and evolution. Here, we test how the environment shapes horizontal barriers. The zonation of the diatom diatom diversity and community patterns over space in communities appears driven by two large-scale fac- ancient Lake Ohrid. By applying Bray–Curtis simi- tors: (i) water depth, and (ii) water chemistry, primar- larity analyses of diatom community data, including ily, the concentration of total phosphorus, nitrogen widespread and endemic taxa, we identiﬁed two major ammonia, and conductivity. Both drivers appear to equally inﬂuence diatom diversity and community patterns. We present initial data on diatom–environ- Handling editor: Judit Padisa ´k ment relations, where the results support earlier ecological studies emphasizing the relevance of A. Cvetkoska (&) A. Pavlov S. Toﬁlovska ongoing human-induced eutrophication in the north- Z. Levkov Institute of Biology, University Ss Cyril and Methodius, ern lake area. This study provides background infor- Skopje, Macedonia mation on the role of the environment in structuring e-mail: email@example.com contemporary diatom diversity. However, future A. Cvetkoska F. Wagner-Cremer research needs to focus on the biotic component Palaeoecology, Department of Physical Geography, including species competition in order to reveal the Utrecht University, Utrecht, The Netherlands mechanisms driving spatial community dynamics in Lake Ohrid. E. Jovanovska Department of Animal Ecology and Systematics, Justus Liebig University, Giessen, Germany Keywords Lake Ohrid Diatoms Diversity Spatial community patterns Environmental drivers S. Blanco The Institute of the Environment, University of Leon, La Serna, Leo ´ n, Spain L. Ector Environmental Research and Innovation Department (ERIN), Luxembourg Institute of Science and Technology (LIST), Belvaux, Luxembourg 123 198 Hydrobiologia (2018) 819:197–215 Introduction speciation due to the presence of physical barriers in the lake (Schreiber et al., 2011; Hauffe et al., 2016). The biological diversity across Earth is characterized While much effort has been devoted to understand by a heterogeneous spatial distribution, which is the drivers of present-day diversity and community shaped by the complex interplay of ecological and patterns of the main invertebrate groups in Lake evolutionary processes. In terms of biodiversity at Ohrid, relevant studies addressing these questions in species level, ancient lakes are considered as diversity the contemporary algal groups are still missing. The ‘‘hot-spots’’ (Rossiter & Kawanabe, 2000). Their intensive ecological studies, arising from the increas- prolonged isolation from other ecosystems resulted ing concerns about habitat modiﬁcation and human in extraordinary biodiversity and high numbers of impact on Lake Ohrid, are mostly focused on the endemic lineages (Brooks, 1950; Martens, 1997; overall planktonic communities, their seasonal suc- Cristescu et al., 2010). Revealing the geographical cession and response to increased nutrient input in the and environmental factors that inﬂuence the evolu- lake (Kozarov, 1960, 1974; Allen & Ocevski, 1976; tionary and assembly processes that regulate this Mitic, 1985, 1992). Diatoms (Bacillariophyta), single- unique diversity is of a recent fundamental research celled siliceous protists, as the most species rich algal interest. Moreover, global change during the 21st group in the lake have the potential for testing the role century and beyond is highlighted as a potential cause of the abiotic and biotic factors in structuring for increased extinction risks for a broad variety of communities over spatial scales. The groups’ species organisms in many ecosystems, including ancient richness, endemicity and relictness are well studied lakes (IPCC, 2014). Several studies already provide and available through the intensive ﬂoristic and evidence for the negative effects of global change and taxonomic diatom research of the lake (Fott, anthropogenic pressure over the biodiversity in 1933, 1935; Hustedt, 1945; Jurilj, 1948, 1954; Levkov ancient lakes Tanganyika (Cocquyt, 2000), Ohrid et al., 2007a; Levkov, 2009; Levkov & Williams, (Matzinger et al., 2007) and Baikal (Moore et al., 2011, 2012; Cvetkoska et al., 2012, 2014; Jovanovska 2009). et al., 2013; Pavlov & Levkov, 2013). However, the Lake Ohrid, located at the Balkan Peninsula on the environmental determinants of diversity and commu- border between Macedonia and Albania, is the oldest nity patterns in planktonic and benthic diatoms still lake in Europe and well recognized for its unique remain largely unknown. Hence, we here aim to biodiversity. Recent age assessments place the onset determine which environmental factors inﬂuence the of the lake formation between 1.9 and 1.3 million present-day spatial structure of the diatom communi- years before present (Lindhorst et al., 2015; Wagner ties in Lake Ohrid. We speciﬁcally targeted the et al., 2017). Biological investigations available so far objectives of this study to (i) identify potential spatial describe more than 300 endemic eukaryotic species in subdivision of the diatom communities; (ii) recognize Lake Ohrid (Fo ¨ ller et al., 2015). Taking its small distributional trends of the endemic diversity; (iii) surface area of 358 km into account, Lake Ohrid may infer the relative quantitative importance of water therefore have the highest endemicity index of all depth and water chemistry in structuring spatial lakes worldwide (Albrecht & Wilke, 2008). The community patterns; and (iv) provide implications of question, which mechanisms drive this extraordinary the observed patterns and their environmental drivers biological diversity, endemism and community struc- for the diatom ecology and paleoecology in Lake turing, has attracted many scientists ever since the Ohrid. landmark publication of Stankovic ´ (1960). Earlier hypotheses, mainly based on observational evidence, emphasized the presence of bathymetric and horizon- Methods tal barriers in the lake as primary driver for the geographic modes of speciation (Stankovic ´, 1960; Sampling site Radoman, 1985; Albrecht & Wilke, 2008). More recent studies applying speciation models on the 0 0 Lake Ohrid (4101 N, 2043 E, 693 m a.s.l., Figure 1) gastropods also reveal the importance of ecological is calcium bicarbonate dominated and characterized by a mean water depth of 155 m up to maximum 123 Hydrobiologia (2018) 819:197–215 199 Fig. 1 Location of Lake Ohrid at the Balkan Peninsula (right corner). Topographic and bathymetric map of Lake Ohrid showing the sampling locations at each transect: Kalishta, Struga, Sateska, Ohrid, Peshtani and St. Naum 293 m (Lindhorst et al., 2015). Its hydrological temperature is 26C during summer, and - 1C 3 -1 balance is regulated via 37.3 m s inﬂow of during winter, while the average annual precipitation -1 which * 25% origins from direct precipita- is * 750 mm year . The lake is oligotrophic and tion, * 25% from river input and * 50% from the phosphorus limited (Allen & Ocevski, 1977); how- karst aquifers. Outﬂow is regulated through the river ever, recent studies showed that the mean total -3 Crni Drim (* 60%) and evaporation (* 40%; phosphorus concentration has risen to 4.5 mg P m Matzinger et al., 2006). The average surrounding air 123 200 Hydrobiologia (2018) 819:197–215 as result of the global warming and local anthro- connected to a LI-250A Light Meter. The diffuse pogenic impact (Matzinger et al., 2006, 2007). attenuation coefﬁcients (K ) of the downward PAR were calculated following Zhang et al. (2006). The Sampling and analytical work samples for the analyses of the water chemistry were also collected with 1L Ruttner sampler. The concen- Sampling was conducted in November 2009 in six trations of nitrate nitrogen (NO -N), total phosphorus 2- shoreline transects (Fig. 1) at 5–10 m distance inter- (TP), sulphate (SO ), silica (SiO ), cobalt (Co), 4 2 vals, starting from 0.5 to 50 m water depth. The aluminium (Al), barium (Ba), iron (Fe), magnesium transect names are referring to the nearest landmarks (Mg), calcium (Ca), potassium (K) and sodium (Na) or settlements (Table 1). The depth of the lake at every were measured according to APHA (1998). The sampling point was measured with a mini echo- concentration of ammonia nitrogen (NH -N) was sounder device SM-5 Depthmate Portable Sounder . determined by the Spectrophotometric method in Two types of samples were collected at each point: a accordance with NEN 6472 (1983). diatom sample, taken from the lake sediment surface, and a water sample from * 50 cm above the sedi- Statistical analyses ment surface, used for physical and chemical analyses. The diatom surface sediments were taken with a The Shannon Index (H) was calculated for each Van Veen Grab Sampler. Each sample was acid- sampling point, as a measure for the a diversity taking cleaned with potassium permanganate (KMnO ) and the species richness and species’ relative abundances hydrochloric acid (HCl) to oxidize organics and into account. Spatial variations in community struc- remove the carbonates (Cvetkoska et al., 2014). ture among the different transects were explored by Permanent microscope slides were prepared using calculating the Whittaker Index of b diversity (Whit- Naprax and analysed under oil immersion at 1500x taker, 1960, 1972; Anderson et al., 2011). To test for magniﬁcation with Nikon Eclipse E-80 microscope, possible subdivision of the diatom communities along equipped with Nikon Coolpix P600 digital camera. To the sampling locations, we applied the unweighted analyse the diatom communities, at least 400 valves pair group method with arithmetic mean (UPGMA) were counted per slide, using the standard transect- clustering based on Bray–Curtis similarity measure. In based method (Battarbee, 1986). The only exception the next step, widespread taxa were removed from the was Sa 1 (Sateska, 0.5 m water depth) where only 100 analyses and Bray–Curtis similarity was calculated valves were counted due to the low diatom concen- with endemic taxa percentages only, to assess poten- trations. Diatom taxa were identiﬁed using standard tial subdivisions among the endemic diversity over the literature (Krammer & Lange-Bertalot, sampled area. Criteria and species classiﬁcation into 1986, 1997, 2000, 2004) and the dedicated Ohrid widespread and endemic followed Levkov & Wil- and Prespa taxonomic work of Levkov et al. liams (2012). (2007a, b), Levkov (2009), Jovanovska et al. (2013) To determine which individual species contributed and Cvetkoska et al. (2014). All diatom samples and most to the differences between the samples, we used microscope slides are stored at the Macedonian the species contribution to similarity method (SIM- National Diatom Collection (MKNDC) at the Faculty PER), which measures the percentage contribution of of Natural Sciences in Skopje, Macedonia. each species to average dissimilarity between groups Water temperature (T, C), electric conductivity (Clarke & Ainsworth, 1993). (Cond.) and pH were measured in situ with Hanna The combined effect of the different environmental HI98129 Combo tester. Additional physical and parameters on the variation in species composition chemical characteristics (Table 1) of the bottom water among the sites was modelled with redundancy layer were measured in laboratory on samples col- analyses, RDA (Rao, 1964; Legendre & Legendre, lected with a 1L Ruttner sampler. The underwater 1998; Legendre & Anderson, 1999). The linear Photosynthetic Photon Flux Density (PPFD) as a response in the species dataset, as suggested by the measure of the Photosynthetically Active Radiation low gradient lengths (Standard deviation = 2.1), jus- (PAR, 400–700 nm) was measured with a LI-192 tiﬁes the selection of RDA as the most appropriate cosine corrected Underwater Quantum Sensor technique. Diatom abundances were square-root 123 Hydrobiologia (2018) 819:197–215 201 Table 1 List of sampling locations at Lake Ohrid and explanatory variables measurements used for the ordination analysis Sampling site Depth Sediment pH T(C) PAR N0 -N NH -N TP Mg Cond. DO 3 3 (m) type (mean) (mg/L) (mg/L) (mg/L) (mg/L) (lS/cm) (mg/I) Kalishta 0.5 Sand 8.46 12.4 424.900 0.042 0.00318 0.083 9.095 265 9.7 (Ka) l Ka 2 1 Sand 8.35 12.4 309.700 0.058 0.00079 0.075 8.999 284 8.9 Ka 3 5 Chara spp. 8.17 12.2 185.825 0.348 - 0.00239 0.187 9.508 224 9.8 Ka 4 10 Mud/Chara 8.32 12 144.553 0.042 - 0. 0.131 9.098 228 7.6 spp. 00211 Ka 5 15 Mud/ 8.30 11.1 124.901 0.042 - 0.00051 0.082 8.751 240 6.8 Dreissena spp. Ka 6 20 Mud 8.23 12.4 132.675 0.038 - 0.00131 0.134 8.897 222 7.5 Ka 7 25 Mud 8.24 11.4 / 0.054 - 0.00211 0.221 8.928 238 7.7 Ka 8 30 Mud 8.20 11.1 / 0.058 / 0.244 8.899 222 6.2 Ka 9 40 Mud 8.18 11.1 / 0.095 / 0.214 9.103 217 6.6 Ka 10 50 Mud 8.10 11.1 212.124 0.078 0.00608 0.132 9.610 229 6.6 Struga (St) 1 0.5 Mud/sand 8.17 11.4 / 0.042 0.00252 0.084 9.275 212 8.1 St 2 1 Mud 8.20 11.3 291.180 0.033 0.00050 0.088 9.196 207 7.5 St 3 5 Mud/Chara 8.18 11.7 228.138 0.038 0.00098 0.081 9.343 208 6.7 spp. St 4 10 Mud/Chara 8.16 12.8 0.038 0.00069 0.076 9.158 214 7.8 spp. St 5 15 Mud/sand 8.23 12.8 244.834 0.046 0.00098 0.145 9.232 213 8.4 St 6 20 Mud/ 8.16 11.8 / 0.070 0.00050 0.207 9.333 214 7.7 Dreissena spp. St 7 25 Mud 8.17 11.7 0.107 0.00245 0.168 9.540 216 7.8 St 8 30 Mud 8.12 11.4 216.218 0.058 / 0.093 9.330 214 8 St 9 40 Mud 8.14 11.1 / 0.066 0.00049 0.110 9.148 222 8.3 St 10 50 Mud 8.00 10.1 309.231 0.091 0.00290 0.243 9.235 221 7.7 River Sateska 0.5 Sand 7.90 9.1 106.655 0.311 0.01017 0.243 9.627 254 7.8 (Sa) 1 Sa 2 1 Sand pebbles 8.10 10.5 / 0.054 0.01319 0.209 9.369 240 9.2 SB 3 5 Mud 8.17 11.4 79.212 0.033 0.00049 0.094 9.287 212 6.4 Sa 4 10 Mud/ 8.27 11.6 0.029 - 0.00029 0.068 9.352 210 6.7 Dreissena spp. Sa 5 15 Mud/ 8.17 11.5 46.074 0.062 0.00301 0.178 9.408 209 7.4 Dreissena spp. Sa 6 20 Mud/ 8.36 11.2 / 0.021 - 0.00059 0.098 9.251 213 6.6 Dreissena spp. Sa 7 25 Mud/ 8.30 11.1 15.836 0.046 0.00271 0.139 9.397 218 7.4 Dreissena spp. Sa 8 30 Mud/ 8.50 11.1 / 0.033 - 0.00089 0.143 9.510 211 7.9 Dreissena spp. Sa 9 40 Mud 8.30 9.3 // / / / 216 6.2 123 202 Hydrobiologia (2018) 819:197–215 Table 1 continued Sampling site Depth Sediment pH T(C) PAR N0 -N NH -N TP Mg Cond. DO 3 3 (m) type (mean) (mg/L) (mg/L) (mg/L) (mg/L) (lS/cm) (mg/I) Sa 10 50 Mud 7.90 7.7 / 0.111 0.00094 0.019 9.356 221 6.4 City of Ohrid 0.5 Sand 7.14 8.8 130.815 0.033 - 0.00121 0.020 9.131 212 5 (Oh) l Oh 2 1 Sand 7.11 9.8 137.033 0.029 - 0.00121 0.045 8.922 207 5.3 Oh 3 5 Mud/sand/ 7.18 10.3 142.288 0.025 - 0.00111 0.053 9.051 210 5.7 Chara spp. Oh 4 10 Sand/Chara 7.02 10.7 / 0.033 - 0.00081 0.032 8.772 260 5.7 spp. Oh 5 15 Mud/ 7.13 10.5 148.126 0.029 - 0.00151 0.031 8.998 207 5.8 Dreissena spp. Oh 6 20 Mud/ 7.10 11.4 / 0.033 - 0.00181 0.021 8.908 212 7 Dreissena spp. Oh 7 25 Mud 7.00 10.9 165.829 0.062 - 0.00091 0.050 8.908 210 5.1 Oh 8 30 Mud/ 6.80 10.2 / 0.050 - 0.00131 0.045 8.613 216 5.2 Dreissena spp. Oh 9 40 Mud/sand 6.87 9.6 141.374 0.070 - 0.00111 0.051 8.972 216 6 Oh 10 50 Sand/mud 6.82 9.8 / 0.062 - 0.00194 0.056 9.047 220 6.4 Peshtani (Pe) 0.5 Sand 7.80 12.4 866.500 0.033 0.00887 0.034 9.122 213 7.9 Pe 2 1 Sand 8.74 12.7 761.233 0.029 0.00548 0.041 8.912 213 8.4 Pe 3 5 Sand/Chara 8.71 14.8 324.765 0.033 0.00588 0.053 9.038 212 9 spp. Pe 4 10 Sand/Chara 8.73 13 / 0.029 0.00698 0.011 8.867 210 9.3 spp. Pe 5 15 Mud/ 8.73 13 / 0.042 0.00548 0.072 8.750 217 9.9 Dreissena spp. Pe 6 20 Mud/ 8.74 13 254.756 0.029 0.00907 0.021 8.655 216 10.5 Dreissena spp. Pe 7 25 Sand 8.74 13 / 0.029 0.00548 0.014 8.879 214 5 Pe 8 30 Sand 8.65 12.7 409.244 0.050 0.00872 0.021 9.049 224 10 Pe 9 40 Sand/ 8.69 13.4 / / // / 214 4 Dreissena spp. Pe 10 50 Sand 8.45 12.2 439.414 // / / 228 5.7 St. Naum 0.5 Sand 8.71 13.6 489.250 0.062 0.00558 0.016 8.695 229 7.7 (sN) 1 sN 2 1 Sand 8.69 13.1 377.500 0.058 0.00508 0.028 8.532 223 7 sN 3 5 Sand 8.51 12.9 230.830 0.156 0.00548 0.048 8.359 235 7.3 sN 4 10 Sand/ 8.63 12.6 / 0.091 0.00518 0.030 8.558 220 7.4 Dreissena spp. sN 5 15 Sand/ 8.56 12.5 190.062 0.131 0.00568 0.018 8.264 228 6.8 Dreissena spp. 123 Hydrobiologia (2018) 819:197–215 203 Table 1 continued Sampling site Depth Sediment pH T(C) PAR N0 -N NH -N TP Mg Cond. DO 3 3 (m) type (mean) (mg/L) (mg/L) (mg/L) (mg/L) (lS/cm) (mg/I) sN 6 20 Mud/ 8.60 11.6 / 0.115 0.00538 0.021 8.395 221 6 Dreissena spp sN 7 25 Sand/ 8.68 12.5 / 0.050 0.00508 0.036 8.818 226 6.9 Dreissena spp. sN 8 30 Mud/ 8.69 11.7 / 0.058 0.00684 0.062 8.640 219 6.5 Dreissena spp. sN 9 40 Mud 8.66 11.8 84.320 0.042 0.00528 0.028 8.928 216 6.1 sN 10 50 Mud 8.57 10.7 / 0.058 0.00478 0.015 8.988 218 5.5 The italicized numbers represent minima and maxima values transformed and centred, as this transformation tries Redundancy analyses and Var-Part were performed rather to stabilize variances, and down-weight rare in Canoco v.5.0 (ter Braak & Smilauer, 2012), while taxa to avoid overemphasizing their effects over the the Bray–Curtis similarity analyses, the UPGMA results (Legendre & Legendre, 1998). The validity of clustering, the diversity indices and SIMPER analysis the model was tested with linear transects permutation were implemented in the statistical package PAST test with 999 permutations. The explanatory power of (Hammer et al., 2001). each environmental predictor was determined with an interactive forward selection and optimal ﬁt was achieved after 14 predictors were taken into account Results (Table 3). The conditional effects of the explanatory variables Diatom diversity and community patterns were further tested with variation partitioning (Bor- card et al., 1992;Smilauer & Leps ˇ, 2014) between two A total of 290 diatom taxa including morphological groups of explanatory variables, water chemistry (TP, varieties were identiﬁed in the samples. Dominant in NH -N and Cond.) and water depth. Groups were most of the samples are Amphora indistincta Levkov, predetermined based on the forward selection results, Pantocsekiella ocellata complex (Pantocsek) Kiss & ´ ´ only variables with P \ 0.01 were chosen for the Acs, Pantocsekiella minuscula (Jurilj) Kiss & Acs, analysis. Encyonopsis microcephala (Grunow) Krammer, To analyse the response of the diatom a diversity Pseudostaurosira brevistriata (Grunow) Williams & (Shannon’s diversity index) to abiotic factors, we Round and Staurosirella pinnata (Ehrenberg) Wil- implemented a Generalized Linear Model (GLM) liams & Round. In terms of endemic species rich- ANCOVA model using transect and sediment type as ness, * 33% taxa are endemic, as compared to the categorical predictors, and environmental variables total number of identiﬁed taxa. (Table 1) as continuous predictors. To avoid collinear- Lowest AIC values were obtained for a GLM model ity, variables with VIF values above 10 were excluded. using an inverse Gaussian error distribution and a Environmental variables were selected based on a power (squared) link function. The model incorporates ‘best subsets’ routine. To compare the performance of only four variables with no signiﬁcant interactions: the different models generated, we used Akaike’s depth (P \ 0.001), sulphates (P B 0.05), transect (P Information Criterion (AIC). Computations were B 0.01) and sediment type (P B .01) (Fig. 2a–d). performed with Statistica V. 10.0 (StatSoft, 2011). There is a clear, monotonic tendency of H to decrease 123 204 Hydrobiologia (2018) 819:197–215 Fig. 2 A–D Shannon’s index plotted against the environmental predictors selected by the GLM ANCOVA model with increasing depth, irrespective of other factors. observed in Sateska and on mud/sand samples, This structural parameter varied also largely depend- respectively. ing on transect sampled and sediment typology but did The a diversity shows overall minimum and not depend signiﬁcantly on any other limnological or maximum values in the transect at city of Ohrid (code: physiographical variable. The variability of this met- Oh), H = 1.82, at Oh 10 and H = 3.44 at Oh 3. min max ric, as measured in terms of standard errors (Fig. 2c– Generally, the Struga (code: St) transect has the d), shows also a great dependence on transect location highest average diversity H = 3.13, while the Sateska and sediment type, the largest variances being transect (code: Sa) displays the lowest average of 123 Hydrobiologia (2018) 819:197–215 205 H = 2.64. However, an overall trend of bipartite supporting delineation of two major groups, littoral variation in diversity is notable at each transect and sub-littoral, at a similarity threshold value, (Figs. 2, 3a) for its littoral [0–10(15) m] and sub- S = 0.45. Each group consists of two sub-groups, at littoral zone [10(15)–50 m]. In the littoral zone, the S = 0.48 and 0.55, respectively (Fig. 4a), and hence diversity increases towards ca. 5 m water depth, and we here deﬁne four diatom assemblage zones in Lake subsequently decreases to its minima around 10(15) m Ohrid, excluding the sample from Sa (0.5 m) as most water depth. Similarly, in the sub-littoral zone, distinct: diversity values increase between 10(15) and 25(30) (i) north-eastern (NE) and eastern (E) littoral, m and successively decline after 30 m water depth. including samples from 0.5 to 15 m water The b diversity values (Fig. 3b) show lowest values depth collected from the St, Sa, Oh, Peshtani (1.67) at the St transect, whereas Kalishta (code: Ka) (code: Pe) and St. Naum (code: sN) transects; displays the highest value (2.3) of all transects. (ii) north-western to eastern (NW-E) littoral The Bray–Curtis similarity analysis of the wide- (samples between 0.5–10 m at Ka; at 5 and spread and endemic taxa shows diatom assemblages 15 m from St; and 1–5 m from Sa); cluster by depth as well as transect location, thus Fig. 3 Bathymetric map of Lake Ohrid displaying the a (A) and b (B) diversity and their values 123 206 Hydrobiologia (2018) 819:197–215 Fig. 4 a Bray–Curtis similarity analysis of the diatom communities in Lake Ohrid. b Bray–Curtis similarity analysis of the endemic diatom communities (iii) NW sub-littoral (10–50 m, Ka, St and Sa); The SIMPER analysis shows that * 70% of the and. cumulative dissimilarity between the Bray–Curtis (iv) NE sub-littoral (10–50 m, Sa, Oh, Pe and groups is owed to 13 taxa (Table 2). Among them, sN). Amphora pediculus (Ku ¨ tzing) Grunow, Staurosirella sp. and P. brevistriata dominate the littoral zone, The Bray–Curtis similarity applied to the endemic while the P. ocellata complex and P. minuscula communities (Fig. 4b) delineates ﬁve zones at dominate the sub-littoral, all together already con- S = 0.2: (i) samples mainly from the lake littoral tributing with * 50% to the cumulative group (1–15 m); (ii) samples from the sub-littoral dissimilarity. (15–50 m); (iii) samples from Pe 0.5 m, sN 0.5 m, sN 1 m; (iv) Sa 0.5 m, Oh 0.5 m; and (v) samples from Environmental variables the NE littoral of Ka, St and Oh (Ka 10 m, St 5 m, Oh 10 m, St 10 m, Ka 5 m) which has lowest similarity The environmental parameters used in the ordination, index as compared to the other locations. The number their measurements and marked minimum and max- of endemic taxa per water depth for each transect is imum values are presented in Table 1. The four RDA shown in Fig. 5. 123 Hydrobiologia (2018) 819:197–215 207 Fig. 5 Endemic richness at each sampling location. The sample collected at 0.5 m water depth at the Sa transect has been removed from the diagram due to possible bias resulting from the low diatom counts Axes together explain 52% of the total variation in the NW sub-littoral align along the TP and Magnesium diatom data, of which 26.1% are explained by Axis 1 (Mg) gradient, while water depth and sediment type and 15.3% by Axis 2. The explanatory variables appear as major drivers of the variation observed in the account for 71.6% of the explained variation in the NE sub-littoral diatom zone (Fig. 6a). diatom data. The inﬂation factors of all variables were Variation in the group of centric species, such as lower than the critical heuristic value of 10, indicating Pantocsekiella ocellata (5–10 lm, 3 ocelli), P. minus- that they are not correlated. The only exceptions were cula and Cyclotella fottii Hustedt appear to be driven downward PAR intensity at the bottom (Ed ), by the depth and sediment type at each sampling bottom which showed high positive correlation of r = 0.9 to location. However, the P. ocellata morphodemes with PAR, and dissolved oxygen (DO) with a r = 0.7 to T more than three ocelli and above 10 microns seem to (C), and these two parameters were removed from the rather be related to the TP and Mg concentrations. The analysis. The interactive forward selection by using inﬂuence of the explanatory variables on the diatom unrestricted permutation test showed that only four taxa is visualized in Fig. 6b and conforms the variables have signiﬁcant (P \ 0.01) explanatory SIMPER analyses (Table 2). Species abundances in power, together accounting for 43% of the total the NE littoral zone, like Staurosirella spp., Amphora explained variation in the diatom data (Table 3). The pediculus, Karayevia clevei (Grunow) Round and RDA results indicate that large proportion of variation Placoneis pseudanglica (Lange-Bertalot) Cox are in the diatom data is driven by the water depth. mostly driven by NH -N, PAR, T and pH, while the The NE littoral diatom zone appears related to a species abundances in NW littoral and sub-littoral combination of several water chemistry parameters, zones, like Staurosirella pinnata, A. indistincta, NH -N, PAR, T (C), pH and Cond., while the Navicula cryptotenella Lange-Bertalot, P. ocellata variation in the NW littoral zone can be mostly ([ 10 lm, 5 ocelli), P. ocellata ([ 10 lm, 3 ocelli), P. explained by Cond., NO -N and TP. Samples from the ocellata (5–10 lm, [ 3 ocelli) are explained by 123 208 Hydrobiologia (2018) 819:197–215 Table 2 Results from the SIMPER analysis showing the cumulative percentage (Cum. %) and the mean abundance of average dissimilarity between the groups as delineated by the taxa in the groups (NE, E littoral, NW-E littoral, NW sub- Bray–Curtis similarity analysis, percentage contribution (Con- littoral and NE sublittoral). Only taxa with [ 1% contribution trib. %) of the species to the average community dissimilarity, are shown Taxon Average Contrib. Cum. NE, E NW-E NW sub- NE sub- dissimilarity % % littoral littoral littoral littoral Pantocsekiella ocellata (5–10 lm, 8.5 13.5 13.5 4.5 6.5 18.2 30.7 3 ocelli) Pantocsekiella minuscula 4.8 7.7 21.2 2.2 1.2 3.1 16.5 Pantocsekiella ocellata (\ 5 lm, 3 3.9 6.2 27.4 1.8 4.8 14.4 8.4 ocelli) Amphora pediculus 3.5 5.5 38.9 12.8 5.2 1.6 3.5 Staurosirella spp. 2.8 4.5 48.4 8.6 3.1 1.4 5.3 Pseudostaurosira brevistriata 2.5 3.9 52.2 5.7 3.0 5.6 3.3 Encyonopsis microcephala 2.0 3.2 55.5 1.5 9.2 3.1 1.0 Staurosirella pinnata 1.7 2.6 58.1 1.7 4.9 4.6 0.9 Amphora sp. 1.7 2.6 60.7 5.3 0.06 0.2 1.8 Amphora indistincta 1.3 2.0 62.8 3.0 4.3 1.5 1.0 Gomphonema sp. 0.9 1.4 64.2 1.5 3.5 0.9 0.9 Cocconeis placentula 0.8 1.3 65.5 0.6 3.9 0.3 0.5 Planothidium frequentissimum 0.7 1.2 66.7 2.6 0.8 0.3 0.4 Pantocsekiella ocellata 0.7 1.0 67.7 0.1 0.6 2.1 0.8 (5–10 lm, [3 ocelli) Table 3 Results from the Variable unit Explains % Contribution % pseudo-F P interactive forward selection of the explanatory Depth m 19.9 27.8 6.7 0.002 variables used in the RDA TP mg/L 12.5 17.5 4.8 0.002 ordination NH -N mg/L 5.4 7.5 2.2 0.004 Conductivity lS/cm 4.7 6.5 1.9 0.01 PAR lmol/s/m 3.1 4.4 1.4 0.148 mean Mg mg/L 3.1 4.3 1.3 0.148 pH 2.7 3.8 1.2 0.242 2- SO mg/L 2.5 3.4 1.1 0.358 T C 2.5 3.5 1.1 0.31 NO -N mg/L 2.6 3.6 1.1 0.318 Sediment type 2.2 3.1 1.0 0.488 Al mg/L 2.1 2.9 0.9 0.504 Si mg/L 1.7 2.3 0.7 0.694 K mg/L 1.3 1.8 0.6 0.868 conductivity, NO -N and TP. The species from the NE predictors explain similar proportion of the variance, sub-littoral zone are correlated to water depth and while the shared fraction is very small (Fig. 7). sediment type (Fig. 6b). The total variance partition- ing shows that the environmental and the spatial 123 Hydrobiologia (2018) 819:197–215 209 Fig. 6 a Axis 1 versus Axis 2 sample scores from the RDA squares), NW sub-littoral (pink triangles) and NE sub-littoral analysis. The symbols conform to the Bray–Curtis similarity (green circles); and b Axis 1 versus Axis 2 species scores from groups: NE and E littoral (red triangles), NW-E littoral (yellow the RDA analysis Fig. 7 Results from the variation partitioning between the explanatory variables with P \ 0.01 Discussion Diatom diversity and community patterns The results show distinct spatial patterns of the diatom Diatom species richness in Lake Ohrid was estimated diversity and community structure within the Mace- to 789 taxa, 117 of which were considered endemic for donian side of Lake Ohrid, driven by a combination of the lake (Levkov & Williams, 2012). These numbers water depth and water chemistry. have certainly increased due to the revisions of several diatom genera and new species descriptions, resulting from the intensive taxonomic and palaeoecological research on the lake over the past few years. In this 123 210 Hydrobiologia (2018) 819:197–215 study, we identiﬁed 210 widespread and 80 endemic the NW-E gradient indeed, probably associated to the diatom taxa. complex sedimentary characteristics in the basin. The results yielded distinct vertical and horizontal Similarly, to Lake Ohrid, the benthic diatom commu- patterns in diatom diversity and community structure nity from the neighbouring Lake Prespa showed that reﬂected in (i) changes in relative abundances of the different species dominated in the littoral zone of the widespread taxa along the depth gradients; (ii) pres- eastern and western parts of the lake, related to ence of different widespread taxa in the NW and NE-E differences in geology and sediment structure (Levkov part; and (iii) presence of different rare and endemic et al., 2007b). taxa at different depths and sampling locations. Concerning the endemic diatom taxa, earlier stud- The presence of vertical and horizontal patterns of ies (Levkov et al., 2007a; Levkov & Williams, 2012) distribution and speciation due to differences in noticed several spatial levels of their distribution in the substrate, sedimentation, vegetation, physical and whole watershed area, including Lake Prespa where chemical characteristics, was already recognized taxa are (i) restricted to only one of the lakes, (ii) within the invertebrate groups in Lake Ohrid (Stan- common to both lakes and iii) restricted to the spring kovic ´, 1960; Radoman,1985; Albrecht & Wilke, 2008: area and/or Lake Ohrid. Our results show that some see Figs. 9, 10). Our results indicate that vertical endemic taxa, like Amphora ohridana Levkov, (bathymetrical) and horizontal zonation can be applied Caloneis acuta Levkov, Sellaphora krsticii Levkov, Nakov & Metzeltin appeared to have limited distri- to the diatom communities in Lake Ohrid. Bathymet- rically, there are four sub-zones (a) upper littoral bution in the littoral zone, while others, such as (0.5–5 m); local variations in diversity, but generally Caloneis biconstrictoides Levkov, Cymbopleura jur- increasing up to highest values around 5 m water iljii Levkov & Metzeltin and Sellaphora macedonica depth; (b) lower littoral [5–10(15) m, or the ‘‘Chara Levkov & Metzeltin were restricted to the sublittoral belt’’]; markedly sharp decline in diatom diversity; zone of the lake. The comparison of the number of (c) upper sub-littoral [10(15)–30 m, the ‘‘Dreissena endemic taxa per water depth (Fig. 5) yielded that in belt’’]; increase in the diatom diversity; and d) lower general the endemicity is higher in the sublittoral sub-littoral (30–50 m); successive decline in diversity zones, similarly as observed for the gastropod com- to lowest values at the transition towards the profundal munities (Hauffe et al., 2011). An exception is the zone. The horizontal zone can be divided in three sub- shallow littoral zone (0.5–1 m depth) of Peshtani and zones (a) NW, Kalishta zone; the most distinct St. Naum, where the endemic taxa comprised up to community, supported by the highest b diversity; 25% of their diatom community. Overall, the results (b) NE, Struga and Sateska zone; b diversity reﬂects from this study covering Lake Ohrid only, imply that high community turnover between each site; and (c) E, the presence of horizontal and vertical barriers might Ohrid, Peshtani, and St. Naum zone, less pronounced act as factors limiting the distribution of the endemic differences between the community composition at species in the lake. sampling site. The vertical and horizontal patterns in diatom Relative quantitative importance of environmental diversity and community structure closely resemble variables the spatial variability in sediment structure in the lake (e.g. Vogel et al., 2010). The sediment structure varies The results from the RDA analysis indicated that water along the whole basin, due to the complex geodynamic depth and water chemistry almost equally inﬂuence setting of the lake. The sediments from the western the spatial diatom community dynamics in Lake and eastern parts differ in the physical and chemical Ohrid. properties due to the presence of Mesozoic (Apulian) Diatom diversity and community structure in the and Paleozoic rocks (Pelagonian), respectively lake changed along the water depth gradients as (Robertson, 2004). Such variability may have impor- different species dominate the littoral and the sublit- tant inﬂuence on water chemistry and consequently, toral zones. The diatom communities in the sandy microhabitat structure in the lake. The observed littoral area, 0.5–1 m depth, are dominated by Ach- horizontal patterns in diatom diversity and community nanthidium sp., Amphora indistincta, A. pediculus, structure imply a presence of different habitats along Cocconeis placentula Ehrenberg, E. microcephala, 123 Hydrobiologia (2018) 819:197–215 211 Gomphonema sp., Navicula antonii Lange-Bertalot, diatom communities in the area of Kalishta, Struga Placoneis balcanica (Hustedt) Lange-Bertalot, Met- and Sateska reﬂects ongoing eutrophication and zeltin & Levkov, Pseudostaurosira sp. and S. pinnata. wastewater pollution in the northern part of the lake. Since the nearshore area is characterized as the most Lake Ohrid is a typical oligotrophic lake, however, dynamic part of lakes, it is expected to reﬂect the increasing pollution and nutrient loads from the presence of distinctive habitats, associated with surrounding settlements and the river tributaries, speciﬁc biogeochemical and/or metabolic processes, Sateska and Koselska, were already recognized as hence species communities (Lewis, 2009). The shal- the major source leading to eutrophication of the low water diatom communities in Lake Ohrid repre- northern lake area (Matzinger et al., 2007; Veljanoska- sent a mixture of ‘‘pioneering’’ taxa, which prefer Saraﬁloska et al., 2011; Trajanovska et al., 2014). Start sandy or macrophytic substrates (Levkov et al., of the human impact and eutrophication at * 1955 2007a). These communities appeared associated with AD was inffered from the analysis of several shallow a combination of multiple environmental factors, gravity cores recovered from the Kalishta spring area among others the concentration of ions, light avail- where changes in coastal sedimentation rate and ability, temperature and pH. The inﬂuence of the water increase in organic matter content was determined depth over diatom community structure in the upper (Matter et al., 2010). littoral and the sublittoral zone was evident from the The TP concentrations that we measured in the higher abundance of planktonic diatom taxa such as northern lake area were up to ten times higher than the Pantocsekiella ocellata complex. At greater water those measured in the eastern area (Table 1), and the depths, the recourses for benthic species become diatom communities were accordingly dominated by limited (e.g. light availability, temperature), to which nutrient tolerant (e.g. Kelly et al., 2008) and/or meso- species often respond with decreased abundances. In eutrophic species (e.g. Van Dam et al., 1994), such as contrast, these resources remain relatively stable in the E. microcephala, N. cryptotenella, Nitzschia linearis epilimnetic zone, possibly promoting high abundances Smith and P. ocellata ([ 10 lm). of planktonic species (Passy, 2008; Cantonati & Lowe, 2014). The strong inﬂuence of water depth in regulat- Implication for diatom ecology and palaeoecology ing the spatial diatom community patterns has also in Lake Ohrid been shown in other lakes studies (Yang & Duthie, 1995; Stone & Fritz, 2006; Laird et al., 2010; Wang Several studies showed that Lake Ohrid is under et al., 2012). increased human pressure which poses a threat to its The decline of diatom diversity in the lower littoral unique biota (Matzinger et al., 2007; Albrecht & part, however, can be associated with the substrate Wilke, 2008), and our results further corroborate these structure rather than any speciﬁc change of the ﬁndings. The signiﬁcant contribution of total phos- environmental factors. The lower littoral part of Lake phorus and nitrogen ammonia concentrations in Ohrid is characterized by dense growth of the macro- explaining the diatom distribution in the northern lake phytic algae from the genus Chara Linnaeus, forming area should raise serious concerns about the effects of submerged meadows extending between 5 and 10(15) the ongoing eutrophication and pollution over the lake m water depth (Trajanovska et al., 2014). The low diversity. diversity and communities dominated by epiphytic In the context of the Water Framework Directive diatoms, like C. placentula and E. microcephala, ‘WFD’ guidelines, diatoms have been suggested as the imply that the ‘‘Chara belt’’ might act as dispersal most appropriate bioindicators to be used in regular barrier for the diatom communities in the lake. The monitoring programs of the freshwater bodies in importance of the Chara belt as habitat for some Macedonia (Krstic et al., 2007). Although the infor- species and as barrier for others has been also stressed mation diatoms provide is rapid, reliable and cost by Radoman (1985). efﬁcient, the biological monitoring of Lake Ohrid still The group of environmental variables indicated that largely relies on macrophytes, invertebrates and ﬁsh, diatom distribution in Lake Ohrid is also driven by while diatoms were included only in short survey water chemistry (Fig. 6), particularly TP, NH -N and studies (e.g. Schneider et al., 2014). Despite the conductivity. The inﬂuence of TP and NH -N over the extensive ﬂoristic, taxonomic and palaeoecological 123 212 Hydrobiologia (2018) 819:197–215 diatom research, a systematic diatom-based ecological diversity. While the question how persistent and study on Lake Ohrid has not yet been performed. Our genetically different these phenotypes are remains study provides initial data for interactions between open for future studies, their presence in the fossil environment and spatial distribution of diatom com- record renders important palaeoecological informa- munities and thereby a baseline for establishing a more tion. Considering the here-provided information on accurate biomonitoring strategy for the lake. System- the environmental drivers of diatom community and atic diatom sampling and interpretation need to take diversity patterns in Lake Ohrid, future studies should the non-homogenous diatom distribution within the focus on constructing a reliable ‘within-lake’ diatom lake into account, hence a sampling strategy capturing calibration dataset for quantitative palaeoecological the communities across the vertical and horizontal reconstructions. Overall, a systematic assessment zones. integrating ecological and palaeoecological aspects Contrary to the diatom neo-ecology, Lake Ohrid is necessary to determine boundary conditions and to has been in the spotlight of palaeoecological research improve the action plans towards protection and after its inclusion as a target area of the International conservation of Lake Ohrid with its exceptional Continental Scientiﬁc Drilling Program, and the start biodiversity. of the interdisciplinary research project Scientiﬁc Collaboration on Past Speciation Conditions in Lake Conclusions Ohrid, SCOPSCO in 2009. Several sediment sequences, covering the last glacial–interglacial per- iod, were recovered within the project, prior an ICDP In this study, we demonstrated distinct spatial patterns deep drilling campaign took place in 2013 (Wagner of community and diversity in diatoms from Lake et al., 2014). A * 600-m-long master sediment Ohrid. The widespread and endemic species have sequence was retrieved from the deepest part of the limited distribution across the northern and eastern lake. Being one of the most abundant microfossils in part of the lake, which appear to be related to the the sedimentary archive of the lake, diatoms were presence of vertical and horizontal barriers. The intensively studied as one of the most important multivariate analyses reveal that the distribution of biological proxies which can provide information diatoms is related to variation in water depth and water about the past in-lake paleo-processes and the past chemistry gradients. Speciﬁcally, both variables environmental and climate conditions in the area appear to equally inﬂuence the diversity and the (Reed et al., 2010; Cvetkoska et al., 2012, 2016; extant community structure. The signiﬁcant inﬂuence Jovanovska et al., 2016; Zhang et al., 2016). of total phosphorus concentration on the diatoms in the However, in the lack of systematic diatom-based northern parts of the lake reﬂects the ongoing ecological data all these studies were limited to eutrophication as a result of the increased anthro- qualitative palaeoenvironmental interpretations. The pogenic nutrient loads. high degree of endemism and the lack of modern While this study provides initial insight into the analogue species, which represent a common chal- diatom distribution from the Macedonian side of Lake lenge for Quaternary palaeoecological interpretations Ohrid, future studies should expand the spatial scale of fossil diatom data from other ancient lakes (Mackay by including the whole lake and its spring area. et al., 2010, Wilke et al., 2016), are no exception in Moreover, integrating biotic and abiotic variables in Lake Ohrid. Furthermore, while all these studies were spatial and temporal dimension should be considered performed at high-resolution taxonomic level, an in order to unravel the assembly processes driving extraordinary phenotypic diversity was observed in extant diversity patterns in Lake Ohrid. some of the species complexes e.g. Pantocsekiella Acknowledgements The presented study would not have ocellata (Cvetkoska et al., 2012) but, the drivers been possible without the support of the Western Balkan behind it remain uncertain. The data presented here Environmental Network project (www.newenproject.org). The demonstrate that populations with different morpho- authors would like to thank Paul B. Hamilton and Timme H. logical traits are driven by different environmental Donders for their helpful discussions during the manuscript preparation. factors (e.g. P. ocellata morphs), corroborating the possibility for environmentally driven phenotypic 123 Hydrobiologia (2018) 819:197–215 213 Open Access This article is distributed under the terms of the Cvetkoska, A., J. Reed & Z. Levkov, 2012. Lake Ohrid diatoms Creative Commons Attribution 4.0 International License (http:// as palaeoclimate indicators of climate change during the creativecommons.org/licenses/by/4.0/), which permits unre- last glacial-interglacial cycle. Diatom Monographs 15: stricted use, distribution, and reproduction in any medium, 1–216. provided you give appropriate credit to the original Cvetkoska, A., P. B. Hamilton, N. Ognjanova-Rumenova & Z. author(s) and the source, provide a link to the Creative Com- Levkov, 2014. Observations of the genus Cyclotella mons license, and indicate if changes were made. (Ku ¨ tzing) Bre ´bisson in ancient lakes Ohrid and Prespa and a description of two new species C. paraocellata spec. nov. and C. prespanensis spec. nov. Nova Hedwigia 98: 313–340. Author contributions AP, AC, EJ and ZL conducted the ﬁeld Cvetkoska, A., E. Jovanovska, A. Francke, S. Toﬁlovska, H. work. AP counted the diatom slides, while AC and SB Vogel, Z. Levkov, T. H. Donders, B. Wagner & F. Wagner- performed the statistical analyses. AC wrote the manuscript Cremer, 2016. Ecosystem regimes and responses in a with contribution of all authors. The authors gave ﬁnal approval coupled ancient lake system from MIS 5b to present: the for publication. diatom record of lakes Ohrid and Prespa. Biogeosciences 13: 3147–3162. Fo ¨ ller, K., B. Stelbrink, T. Hauffe, C. Albrecht & T. Wilke, References 2015. Constant diversiﬁcation rates of endemic gastropods in ancient Lake Ohrid: ecosystem resilience likely buffers environmental ﬂuctuations. Biogeosciences 12: Albrecht, C. & T. Wilke, 2008. Ancient Lake Ohrid: biodiver- 7209–7222. sity and evolution. Hydrobiologia 615: 103–140. Fott, B., 1933. Die Schwebeﬂora des Ohrid-Sees. Bulletin de Allen, H. L. & B. T. Ocevski, 1976. Limnological studies in a l’Institut et du Jardin Botaniques de l’Universite de Beo- large, deep, oligotrophic lake (Lake Ohrid, Yugoslavia). grad 2: 153–175. Evaluation of nutrient availability and control of phyto- Fott, B., 1935. Phytoplanktonproduktion des Ohridsees. Ver- plankton production through in situ radio bioassay proce- handlungen der Internationalen Vereinigung fur Theo- dures. Archiv fu ¨ r Hydrobiologie 77: 1–21. retische und Angewandte Limnologie 7: 229–236. Allen, H. L. & B. T. Ocevski, 1977. Limnological studies in a Hammer, O., D. A. T. Harper & P. D. Ryan, 2001. PAST: large, deep, oligotrophic lake (Lake Ohrid, Yugoslavia). paleontological statistics software package for education Archiv fu ¨ r Hydrobiologie 53(1): 1–21. and data analysis. Paleontologia Electronica 4(1): 1–9. Anderson, M. J., T. O. Crist, J. M. Chase, M. Vellend, B. Hauffe, T., C. Albrecht, K. Schreiber, K. Birkhofer, S. Tra- D. Inouye, A. L. Freestone, N. J. Sanders, H. V. Cornell, L. janovski & T. Wilke, 2011. Spatially explicit analysis of S. Comita, K. F. Davies, S. P. Harrison, N. J. B. Kraft, J. gastropod biodiversity in ancient Lake Ohrid. Biogeo- C. Stegen & N. G. Swenson, 2011. Navigating the multiple sciences 8: 175–188. meanings of b diversity: a roadmap for the practicing Hauffe, T., C. Albrecht & T. Wilke, 2016. Assembly processes ecologist. Ecology Letters 14: 19–28. of gastropod community change with horizontal and ver- APHA - American Public Health Organization, 1998. Standard tical zonation in ancient Lake Ohrid: a metacommunity Methods for the Examination of Water and Wastewater, speciation perspective. Biogeosciences 13: 2901–2911. 20th ed. APHA - American Public Health Organization, Hustedt, F., 1945. Diatomeen aus Seen und Quellgebieten der Washington DC. Balkan-Halbinsel. Archiv fu ¨ r Hydrobiologie 40: 867–973. Battarbee, R. W., 1986. Diatom analysis. In Berglund, B. E. IPCC, 2014. Climate Change 2014: Impacts, Adaptation, and (ed.), Handbook of Holocene Palaeoecology and Palaeo- Vulnerability. Part B: Regional Aspects. In Barros, V. R., hydrology. Wiley, Chichester: 527–570. C. B. Field, D. J. Dokken, et al. (eds), Contribution of Borcard, D., P. Legendre & P. Drapeau, 1992. Partialling out the Working Group II to the Fifth Assessment Report of the spatial component of ecological variation. Ecology 73: Intergovernmental Panel on Climate Change. Cambridge 1045–1055. University Press, Cambridge. Brooks, J. L., 1950. Speciation in ancient lakes. Quarterly Jovanovska, E., T. Nakov & Z. Levkov, 2013. Observations of Review of Biology 25: 131–176. the genus Diploneis (Ehrenberg) Cleve from lake Ohrid, Cantonati, M. & L. R. Lowe, 2014. Lake benthic algae: toward Macedonia. Diatom Research 28: 237–262. an understanding of their ecology. Freshwater Science 33: Jovanovska, E., A. Cvetkoska, T. Hauffe, Z. Levkov, B. Wag- 475–486. ner, R. Sulpizio, A. Francke, C. Albrecht & T. Wilke, 2016. Clarke, K. & M. Ainsworth, 1993. A method of linking multi- Differential resilience of ancient sister lakes Ohrid and variate community structure to environmental variables. Prespa to environmental disturbances during the Late Marine Ecology-Progress Series 92: 205. Pleistocene. Biogeosciences 13: 1149–1161. Cocquyt, C., 2000. Biogeography and species diversity of dia- Jurilj, A., 1948. Nove diajtomeje- Surirellaceae - iz Ohridskog toms in the Northern Basin of Lake Tanganyika. Advances jezera i njihovo ﬁlogenetsko znacenje. Jugoslovenska in Ecological Research 31: 125–150. Akademija, Zagreb. Prirodnoslovnih Istrazivanja 24: Cristescu, M. E., S. J. Adamowicz, J. J. Vaillant & D. 171–260. G. Haffner, 2010. Ancient lakes revisited: from the ecology Jurilj, A., 1954. Flora i vegetacija dijatomeja Ohridskog jezera. to the genetics of speciation. Molecular Ecology 19: Jugoslovenska Akademija, Zagreb. Prirodnoslovnih 4837–4851. Istrazivanja 26: 99–190. 123 214 Hydrobiologia (2018) 819:197–215 Kelly, M., S. Juggins, R. Guthrie, S. Pritchard, J. Jamieson, B. Lindhorst, K., S. Krastel, K. Reicherter, M. Stipp, B. Wagner & Rippey, H. Hirst & M. Yallop, 2008. Assessment of eco- T. Schwenk, 2015. Sedimentary and tectonic evolution of logical status in U.K. rivers using diatoms. Freshwater Lake Ohrid (Macedonia/Albania). Basin Research 27: Biology 53: 403–422. 84–101. Kozarov, G., 1960. Lake Prespa phytoplankton investigations Mackay, A., B. M. Edlund & G. Khursevich, 2010. Diatoms in during the course of three years. Recueil des Travaux/ Ancient Lakes The Diatoms: Applications for the Envi- Station Hydrobiologique, Faculte ´ de Philosophie de ronmental and Earth Sciences, 2nd ed. Cambridge l’Universite ´ de Skopje 8: 1–57. University Press, Cambridge: 209–230. Kozarov, G., 1974. Characteristics of Lake Ohrid phytoplank- Martens, K., 1997. Speciation in ancient lakes (review). Trends ton. Proceedings of the Symposium on the Problems of the in Ecology and Evolution 12: 177–182. Regulation of Lake Ohrid. Macedonian Academy of Sci- Matter, M., F. S. Anselmetti, B. Jordanoska, B. Wagner, M. ence and Arts, Skopje: 363–369. Wessels & A. Wu ¨ est, 2010. Carbonate sedimentation and Krammer, K. & H. Lange-Bertalot, 1986. Naviculaceae. In Ettl, effects of eutrophication observed at the Kalis ˇta subaquatic H., J. Gerloff, H. Heynig & D. Mollenhauer (eds), springs in Lake Ohrid (Macedonia). Biogeosciences 7: Su ¨ ßwasserﬂora von mitteleuropa. Gustav Fischer-Verlag, 3755–3767. Stuttgart. Matzinger, A., M. Jordanoski, E. Veljanoska-Saraﬁloska, M. Krammer, K. & H. Lange-Bertalot, 1997. Bacillariaceae, Sturm, B. Mu ¨ ller & A. Wu ¨ est, 2006. Is Lake Prespa jeop- Ephitemiaceae, Surirellaceae. In Ettl, H., J. Gerloff, H. ardizing the ecosystem of ancient lake Ohrid? Hydrobi- Heynig & D. Mollenhauer (eds), Su ¨ ßwasserﬂora von mit- ologia 553: 89–109. teleuropa, 2nd ed. Gustav Fischer-Verlag, Stuttgart. Matzinger, A., M. Schmid, E. Veljanoska-Saraﬁloska, S. Pat- Krammer, K. & H. Lange-Bertalot, 2000. Centrales, Fragilari- ceva, D. Guseska, B. Wagner, B. Mu ¨ ller, M. Sturm & A. aceae, Eunotiaceae. In Ettl, H., J. Gerloff, H. Heynig & D. Wu ¨ est, 2007. Eutrophication of ancient Lake Ohrid: global Mollenhauer (eds), Su ¨ ßwasserﬂora von mitteleuropa, 2nd warming ampliﬁes detrimental effects of increased nutrient ed. Gustav Fischer-Verlag, Stuttgart. inputs. Limnology and Oceanography 52: 338–353. Krammer, K. & H. Lange-Bertalot, 2004. Achnanthaceae. Kri- Mitic, V., 1985. Vertical distribution of the biomass of Cy- tische erganzungen zu Achnanthes s.l., Navicula s. str., clotella fottii Hust. In Lake Ohrid during April-November Gomphonema. In Ettl, H., J. Gerloff, H. Heynig & D. 1981. Hidrobiol. Dept. Ed. Jululaire 1: 227–235 Mollenhauer (eds), Su ¨ ßwasserﬂora von mitteleuropa, 2nd Mitic ´, V., 1992. Phytoplankton of Lake Ohrid as indicator of ed. Gustav Fischer-Verlag, Stuttgart. water quality. The condition and the perspectives for pro- Krstic ´, S., Z. Svirc ˇev, Z. Levkov & T. Nakov, 2007. Selecting tection of the Lake Ohrid and its surroundings. pp. 49–51. appropriate bioindicator regarding the WFD guidelines for Moore, V. M., E. S. Hampton, L. R. Izmest’eva, E. A. Silow, E. freshwaters – a Macedonian experience. International V. Peshkova & B. K. Pavlov, 2009. Climate Change and Journal on Algae 9: 41–63. the World’s ‘‘Sacred Sea’’—Lake Baikal. Siberia. BioS- Laird, K. R., M. V. Kingsbury & B. F. Cumming, 2010. Diatom cience 59(5): 405–417. habitats, species diversity and water-depth inference NEN 6472. 1983. Water – Photometric determination of models across surface-sediment transects in Worth Lake, ammonium content. Dutch Normalization Institute. northwestern Ontario, Canada. Journal of Paleolimnology Passy, I. S., 2008. Continental diatom biodiversity in stream 44: 1009–1024. benthos declines as more nutrients become limiting. Pro- Legendre, P. & M. J. Anderson, 1999. Distance-based redun- ceedings of the Natural Academy of Sciences 105: dancy analysis: testing multispecies responses in multi- 9663–9667. factorial ecological experiments. Ecological Monographs Pavlov, A. & Z. Levkov, 2013. Diversity and distribution of 69: 1–24. Eunotia Ehrenberg in Macedonia. Phytotaxa 86: 1–117. Legendre, P. & L. Legendre, 1998. Numerical Ecology, 2nd ed. Radoman, P., 1985. Hydrobioidea a superfamily Prosobranchia Elsevier, Amsterdam. (Gastropoda), II. Origin, Zoogeography, Evolution in the Levkov, Z., 2009. Amphora sensu lato. Diatoms of Europe 5: Balkans and Asia Minor. Monographs Institute of Zoology 1–916. 1, Beograd. Levkov, Z. & D. M. Williams, 2011. Fifteen new diatom Rao, C. R., 1964. The use and interpretation of principal com- (Bacillariophyta) species from Lake Ohrid, Macedonia. ponent analysis in applied research. Sankhya ¯. The Indian Phytotaxa 30: 1–41. Journal of Statistics 26: 329–358. Levkov, Z. & D. M. Williams, 2012. Checklist of diatoms Reed, J. M., A. Cvetkoska, Z. Levkov, H. Vogel & B. Wagner, (Bacillariophyta) from Lake Ohrid and Lake Prespa 2010. The last glacial-interglacial cycle in Lake Ohrid (Macedonia), and their watersheds. Phytotaxa 45: 1–76. (Macedonia/Albania): testing diatom response to climate. Levkov, Z., S. Krstic, D. Metzeltin & T. Nakov, 2007a. Diatoms Biogeosciences 7: 3083–3094. of Lakes Prespa and Ohrid (Macedonia). Iconographia Robertson, A., 2004. Development of concepts concerning the Diatomologica 16: 1–603. genesis and emplacement of Tethyan ophiolites in the Levkov, Z., S. Blanco, S. Krstic ´, T. Nakov & L. Ector, 2007b. Eastern Mediterranean and Oman regions. Earth-Science Ecology of benthic diatoms from Lake Macro Prespa Reviews 66: 331–387. (Macedonia). Algological Studies 124: 71–83. Rossiter, A. & H. Kawanabe (eds), 2000. Ancient Lakes: Bio- Lewis, W. M., 2009. Ecological zonation in lakes. In Likens, G. diversity, Ecology and Evolution. Advances in Ecological E. (ed.), Encyclopedia of Inland Waters. Elsevier, Oxford: Research. Academic Press, LondonLondon and New York. 416–422. 123 Hydrobiologia (2018) 819:197–215 215 Schneider, S. C., M. Cara, T. E. Eriksen, B. B. Goreska, A. Wagner, B., T. Wilke, A. Francke, C. Albrecht, H. Baumgarten, Imeri, L. Kupe, T. Lokoska, S. Patceva, S. Trajanovska, S. A. Bertini, N. Combourieu-Nebout, A. Cvetkoska, M. Trajanovski, M. Talevska & E. V. Saraﬁloska, 2014. D’Addabbo, T. H. Donders, K. Fo ¨ ller, B. Giaccio, A. Eutrophication impacts littoral biota in Lake Ohrid while Grazhdani, T. Hauffe, J. Holtvoeth, S. Joannin, E. Jova- water phosphorus concentrations are low. Limnologica 44: novska, J. Just, K. Kouli, A. Koutsodendris, S. Krastel, J. 90–97. H. Lacey, N. Leicher, M. J. Leng, Z. Levkov, K. Lindhorst, Schreiber, K., T. Hauffe, C. Albrecht & T. Wilke, 2011. The role A. Masi, A. M. Mercuri, S. Nomade, N. Nowaczyk, K. of barriers and gradients in differentiation processes of Panagiotopoulos, O. Peyron, J. M. Reed, E. Regattieri, L. pyrgulinid microgastropods of Lake Ohrid. Hydrobiologia Sadori, L. Sagnotti, B. Stelbrink, R. Sulpizio, S. Toﬁ- 682: 61–73. lovska, P. Torri, H. Vogel, T. Wagner, F. Wagner-Cremer, Smilauer, P. & J. Leps ˇ, 2014. Multivariate Analysis of Eco- G. A. Wolff, T. Wonik, G. Zanchetta & X. S. Zhang, 2017. logical Data using Canoco 5, 2nd ed. Cambridge Univer- The environmental and evolutionary history of Lake Ohrid sity Press, Cambridge. (FYROM/Albania): interim results from the SCOPSCO Stankovic ´, S., 1960. The Balkan Lake Ohrid and its living world. deep drilling project. Biogeosciences 14: 2033–2054. Biol. IX, Uitgeverij, Dr. W. Junk, Den Haag, Netherlands, Wang, Q., X. Yang, P. B. Hamilton & E. Zhang, 2012. Linking Monog. spatial distributions of sediment diatom assemblages with StatSoft, 2011. STATISTICA, ver. 10. www.statsoft.com. hydrological depth proﬁles in a plateau deep–water lake Stone, J. R. & S. C. Fritz, 2006. Multidecadal drought and system of subtropical China. Fottea 12: 59–73. Holocene climate instability in the Rocky Mountains. Whittaker, R. H., 1960. Vegetation of the Siskiyou Mountains, Geology 34: 409–412. Oregon and California. Ecological Monographs 30: ter Braak C.J.F. & P. Smilauer, 2012. CANOCO Reference 279–338. Manual and User’s Guide: Software for Ordination (Ver- Whittaker, R. H., 1972. Evolution and measurement of species sion 5.0). Ithaca, NY, USA: Microcomputer Power. diversity. Taxon 21: 213–251. Trajanovska, S., M. Talevska, A. Imeri & S. C. Schneider, 2014. Wilke, T., B. Wagner, B. Van Bocxlaer, C. Albrecht, D. Ariz- Assessment of littoral eutrophication in Lake Ohrid by tegui, D. Delicado, A. Francke, M. Harzhauser, T. Hauffe, submerged macrophytes. Biologia 6: 756–764. J. Holtvoeth, J. Just, M. J. Leng, Z. Levkov, K. Penkman, L. Van Dam, H., A. Mertens & J. Sinkeldam, 1994. A coded Sadori, A. Skinner, B. Stelbrink, H. Vogel, F. Wesselingh checklist and ecological indicator values of freshwater & F. Wonik, 2016. Scientiﬁc drilling projects in ancient diatoms from The Netherlands. Netherlands Journal of lakes: integrating geological and biological histories. Aquatic Ecology 28: 117–133. Global and planetary change 143: 118–151. Veljanoska-Saraﬁloska, E., M. Jordanoski, T. Staﬁlov & M. Yang, J.-R. & H. C. Duthie, 1995. Regression and weighted Stefova, 2011. Study of organochlorine pesticide residues averaging models relating surﬁcial sedimentary diatom in water, sediment and ﬁsh tissue in Lake Ohrid (Mace- assemblages to water depth in Lake Ontario. Journal of donia/Albania). Macedonian Journal of Chemistry and Great Lakes Research 21: 84–94. Chemical Engineering 30: 163–179. Zhang, X. S., J. M. Reed, J. H. Lacey, A. Francke, M. J. Leng, Z. Vogel, H., M. Wessels, C. Albrecht, H.-B. Stich & B. Wagner, Levkov & B. Wagner, 2016. Complexity of diatom 2010. Spatial variability of recent sedimentation in Lake response to Lateglacial and Holocene climate and envi- Ohrid (Albania/Macedonia). Biogeosciences 7: ronmental change in ancient, deep and oligotrophic Lake 3333–3342. Ohrid (Macedonia and Albania). Biogeosciences 13: Wagner, B., T. Wilke, S. Krastel, G. Zanchetta, R. Sulpizio, K. 1351–1365. Reicherter, M. J. Leng, A. Grazhdani, S. Trajanovski, A. Zhang, Y., B. Qin, W. Hu, S. Wang, Y. Chen & W. Chen, 2006. Francke, K. Lindhorst, Z. Levkov, A. Cvetkoska, J. Temporal-spatial variations of euphotic depth of typical M. Reed, X. Zhang, J. H. Lacey, T. Wonik, H. Baumgarten lake regions in Lake Taihu and its ecological environ- & H. Vogel, 2014. The SCOPSCO drilling project recovers mental signiﬁcance. Science in China 49: 431–442. more than 1.2 million years of history from Lake Ohrid. Scientiﬁc Drilling 17: 19–29.
Hydrobiologia – Springer Journals
Published: May 14, 2018
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