- Original Article
- Open Access
Distribution patterns of epilithic diatoms along climatic, spatial and physicochemical variables in the Baltic Sea
© The Author(s) 2017
- Received: 22 March 2017
- Accepted: 7 September 2017
- Published: 19 September 2017
The species richness and community composition of the diatom communities were studied in the Baltic Sea, Northern Europe, to enhance knowledge about the diversity of these organisms in a brackish water ecosystem. Many organisms in the Baltic Sea have been studied extensively, but studies investigating littoral diatoms are scarce. The goal of this study was to examine the importance of climatic, spatial and water physicochemical variables as drivers of epilithic diatoms in the Gulf of Finland and the Gulf of Bothnia. The variation in species richness was best explained by pH, total phosphorus and total nitrogen. Redundancy Analysis indicated that the most important factors correlating with species composition were air temperature, silicon, total phosphorus, water temperature, salinity and pH. Variation Partitioning showed that the species composition was mostly affected by climatic and spatial variables, whereas physicochemical variables had little impact. However, the strongest factor was the combined influence of climatic, spatial and physicochemical variables. The results suggest that diatom species richness in the northern Baltic Sea is primarily regulated by local factors, while climatic and spatial variables have little impact on richness. Species composition is mostly affected by climatic and spatial variables. We conclude that understanding the distribution patterns of Baltic Sea diatoms requires the inclusion of climatic, spatial and water chemistry variables.
- Baltic Sea
Diatoms provide ca. 40% of the global marine primary production, and thus they play a fundamental role in food webs and chemical cycles in the aquatic ecosystems . Changes in the diatom composition therefore affect entire ecosystems. The variation in diatom composition and species richness has been the subject of a large body of research both in marine and fresh waters [e.g. 2, 3]. Traditionally, diatoms are thought to respond merely to local environmental variables, such as water chemistry, and in many cases, water chemistry variables, such as nutrients (nitrogen, phosphorus and silicon), pH, salinity and conductivity have been found to be the most important explanatory variables for diatom composition [e.g. 1, 2, 4]. However, the roles of climate and dispersal limitation have recently also been emphasized in explaining diatom distributions . Organisms have distinct regional pools of species, and both climate and local physicochemical factors act as filters that determine the species composition in local communities [3, 5]. The relative importance of climatic factors and local physicochemical factors varies with study scale: climatic factors may override the local physicochemical factors at continental scales, while at regional scales (100–3000 km) diatom communities are influenced by both climatic and local factors .
The Baltic Sea is one of the world’s three large brackish water seas. Its surface water salinity ranges from ca. 9 in the South-West to almost zero in the North-East . Such a decrease in salinity is caused by the restricted exchange of water with the North Sea through the narrow Danish Straits. A number of rivers also discharge from the catchment to different parts of the Baltic Sea—mostly to the Gulf of Bothnia, the Gulf of Finland and the Gulf of Riga. The largest annual total river runoff flows into the Gulf of Bothnia and the Gulf of Finland , which explains their low salinities. The Gulf of Bothnia and the Gulf of Finland also receive most of the incoming nutrient loads and organic material due to river runoffs. Anthropogenic nutrient inputs result in serious eutrophication including internal loading and hypoxia .
The Baltic Sea is a young formation with a low biodiversity . Present conditions have only prevailed for ca. 3000 years, which is too short a period for brackish water communities to develop, and thus only a few freshwater or marine species have been able to adapt to live in the Baltic Sea . Consequently, most important marine animal and algae groups are missing. This situation makes the whole ecosystem sensitive to disturbances as the extinction of a keystone species may affect the entire ecosystem .
Although diatoms are highly useful in indicating various environmental changes and they are used as standards in freshwater biomonitoring, diatom research has been somewhat scarce in the Baltic Sea. However, there have been important studies of benthic diatoms by Leskinen and Hällfors in the southernmost Finland [e.g. 11–13], Vilbaste et al. [14, 15] in the Gulf of Riga and the coastal area of Estonia, Sommer in the coastal area of Germany , and Snoeijs, Busse and Ulanova in the coastal area of Sweden [e.g. 17, 18]. However, sampling has usually covered only a limited spatial scale with the exception of the study by Ulanova et al. . Thus, there is a lack of broad research studies investigating the effects of climatic, spatial and water physicochemical variables on benthic diatoms in the Baltic Sea.
The aim of this study was to determine the most important climatic, spatial and physicochemical variables that explain variation in diatom species richness and composition in the Baltic Sea, using epilithic (i.e. growing on stones) diatom data collected in the littoral zone of the Gulf of Finland and the Gulf of Bothnia. Sampling covered the entire Finnish coastline, and explanatory variables were represented by climatic (July air temperature and precipitation), spatial (latitude, longitude and coast line exposition) and water physicochemical (total nitrogen, total phosphorus, pH, salinity, dissolved oxygen, silicon and water temperature) variables.
The Gulf of Finland is the easternmost part of the Baltic Sea and is bounded by Finland, Estonia and Russia. Unlike several other parts of the Baltic Sea, the western outline of the Gulf of Finland does not form a hydrographic threshold . The Finnish archipelago in the Gulf of Finland is shallow, disintegrated and contains many islands. The Neva River in the eastern end of the Gulf of Finland produces the largest single fresh water inflow into the Baltic Sea . The Bothnian Sea and the Bothnian Bay belong to the Gulf of Bothnia, which is a northern extension of the Baltic Sea. The Gulf of Bothnia is isolated from the rest of the Baltic Sea by an archipelago and a hydrographic threshold, which leads to substantially different environmental features . River discharges lower the salinity in the Gulf of Bothnia (ca. 0 in the North and ca. 6 in the South) and the Gulf of Finland (<2 in the East and ca. 6 in the West) [20, 21] and bring most of the nutrient loads thus increasing the nutrient levels especially in the littoral zone . Both gulfs suffer from eutrophication and water quality deterioration, but the issue is even more severe in the Gulf of Finland.
Biogeographically, the studied area belongs to the boreal ecoregion. The climate represents an ecotone between continental and oceanic climate zones . The variation in annual mean temperatures is from 1.6 °C (Kemi) to 6.0 °C (Hanko), and the annual precipitation varies between 580 mm and 768 mm .
Diatom sampling and laboratory analysis
The diatom samples were collected between the 1st and 15th of July 2013 in sheltered bays to minimize the effect of waves. The distance between sampling sites was ca. 30 km (Fig. 1), but large river mouths with ample nutrient loads were avoided so that minimum distance to river mouths was kept to 1 km. The diatom sampling complied with a standard SFS-EN 13946 adapted by Eloranta et al. . Five stones with a diameter of at least 10 cm were randomly collected from each site from depths of 20–50 cm, and diatoms were sampled with a toothbrush from a 25 cm2 surface area of each stone. The samples were preserved with ethanol in the field.
The samples were processed according to the SFS-EN 13946 standard. Organic material was removed from the samples by boiling with hydrogen peroxide (30% H2O2). Cleaned diatoms were mounted on slides using Naphrax . To ensure an adequate number of counted valves per sample, two slides were prepared for each sample. Approximately 300 valves per sample were counted and identified to species level (when possible) with a light microscope (magnification 1000×) according to Krammer and Lange-Bertalot . The most recent names of the taxa were verified using AlgaeBase . The counting of 300 valves per sample was documented to be an adequate number for a reliable diatom community analysis in most environments .
Water sampling and laboratory analyses
Water samples (0.5 l) were collected simultaneously with diatom sampling and they were used for the analysis of total phosphorus complying to standard SFS-EN 1189. Water temperature and conductivity were measured in situ using Mettler Toledo MX300 probe. Conductivity was used to calculate the salinity complying the UNESCO formula .
In order to include a higher number of potentially important explanatory variables, we also collected environmental data from existing databases. The values of total nitrogen, pH, dissolved oxygen and silicon for sampling sites were interpolated from the materials of the Finnish Environment Institute (2013, raster, spatial resolution 20 m). The coast line exposition was also interpolated from the materials of the Finnish Environment Institute (2004, raster, spatial resolution 20 m). July air temperature and July precipitation were calculated using data from the Finnish Meteorological Institute (1981–2010, grid, spatial resolution 10 m)  with the Spatial Analyst tools of ArcGIS 10.2.1, Arcmap-applications . For a list of all the explanatory variables, see Additional file 1.
Intercorrelations among the explanatory variables were assessed using Spearman’s rank correlation coefficient (rs). Six of the correlations were diagnosed as strongly correlated (rs < −0.7 or > 0.7, p < 0.001)  (see Additional file 2 for details), and thus silicon, latitude, and air temperature were excluded from species richness analyses.
Correlograms with Moran’s I  were constructed to examine the degree of spatial autocorrelation in the environmental variables and diatom species richness. The correlograms show correlation values in the range of [−1, 1], where values near −1 signify strong negative spatial autocorrelation, 0 complete randomness, and values near 1 strong positive spatial autocorrelation . Autocorrelation coefficients were calculated for distance classes with 80 km intervals generating a spatial correlogram with 9 distance classes. The significance of the spatial autocorrelation in the distance classes was tested using the Bonferroni criterion α = 0.05/k, where k is the number of distance classes used . Thus, the corrected level of significance was set at α = 0.05/9 = 0.00556.
Generalized Additive Models (GAM) were used to study the relationship between species richness and explanatory variables [35, 36]. GAMs are likelihood-based regression models that replace the linear function by an additive function . Thus, they uncover the nonlinear covariate effects by estimating the shape of a smooth curve directly from the data . GAMs were fitted using the R statistics package mgcv with maximum degrees of smoothing restricted to 3 . The significance of the GAMs was analyzed using F-tests and Chi square tests .
Prior to statistical species composition analyses, water quality variables (except pH), climate variables and coast line exposition were log-transformed (log10(x)) to reduce their skewed distributions, and diatom species composition data were Hellinger-transformed , because this method produces more precise estimates of the percentage of variation explained by the predictor variables .
As a constrained ordination, Redundancy Analysis (RDA)  was used to study the effects of climatic, spatial and water physicochemical variables on the diatom composition. Multicollinearity among the variables was assessed by determining variance inflation factors (VIF) , and values of VIF > 10 were considered to represent high collinearity and thus removed from the analysis . Due to high VIF, latitude was omitted from the RDA analysis.
Furthermore, variation partitioning was conducted to partition the variation in diatom community compositions with respect to all climatic (July air temperature and July precipitation), spatial (exposition, latitude and longitude) and water physicochemical variables (total phosphorus, total nitrogen, pH, salinity, oxygen, silicon and water temperature) and their combined effects . Variation partitioning, based on and utilizing the eigenvalues of Redundancy Analysis, enables the determination of the individual and combined effects of local and regional explanatory variables and the proportion of unexplainable variation. All statistical analyses were conducted in the R environment  using packages mgcv , ncf , rda  and vegan .
We then conducted Mantel tests to examine community turnover along geographical gradients . The Mantel test is a method for modeling pairwise community dissimilarities as a function of pairwise spatial distances. Overall, the Mantel statistic r is a correlation between two dissimilarity or distance matrices.
Spatial autocorrelation in explanatory variables
Characteristics of diatom assemblages
Diatom taxa for which average abundance in sampling sites exceeded 1.0%. Mean and range of the species’ relative abundance (%) and the percentage of sampling sites are also shown
Sampling sites (%)
Diatoma tenuis Agardh
Nitzschia frustulum (Kützing) Grunow
Fragilariforma virescens var. subsalina Grunow
Achnanthidium minutissimum (Kützing) Grunow
Rhoicosphenia abbreviata (Agardh) Lange-Bertalot
Fragilaria capucina Desmazières
Nitzschia liebetruthii Rabenhorst
Staurosirella pinnata (Ehrenberg) D.M.Williams & Round
Fragilaria construens (Ehrenberg) Grunow
Achnanthes oblongella Oestrup
Fragilaria fasciculata (Agardh) Lange-Bertalot
Nitzschia perminuta (Grunow) Peragallo
Achnantheiopsis delicatula (Kützing) Lange-Bertalot
Epithemia sorex Kützing
Nitzschia inconspicua Grunow
Navicula gregaria Donkin
Cocconeis placentula var. placentula Ehrenberg
Navicula incertata Lange-Bertalot
Navicula margalithii Lange-Bertalot
Halamphora coffeiformis (Agardh) Levkov
Nitzschia fonticola (Grunow) Grunow
Results of the best approximating Generalized Additive Model for explaining variation in diatom species richness
Redundancy analysis and variation partitioning
The Mantel test indicated that the community dissimilarity of diatoms was significantly correlated with geographical distance (see Additional file 4 for details).
Our analyses showed that diatom species richness was related to three water chemistry variables: pH, total phosphorus and total nitrogen. The importance of pH on the diatom species richness in the Baltic Sea is in accordance with several earlier studies [e.g. 51]. However, our result of a U-shaped relationship between species richness and pH disagrees with some other studies, which have shown a unimodal relationship [e.g. 52]. We speculate that our different result may be due to some unmeasured environmental variables, such as trace metals or organic solvents. We also expect that covering a wider pH range would have further emphasized the importance of pH in regulating the species richness.
Previous studies investigating the effect of nutrients on diatom and phytoplankton species richness have settled upon contradictory results, and concluded that the role of nutrients varies between regions . Marine environments are usually considered as nitrogen limited , while freshwaters are often thought as phosphorus limited . Previous studies have found differences in nutrient limitation between the Baltic Sea basins: the Bothnian Bay in the North seems to be phosphorus limited throughout the year, and the Gulf of Finland seems to be nitrogen limited, with the exception of some high nitrogen peaks in autumn. The nutrient limitation of the Bothnian Sea varies within the year  (see also  about joint limitation by N and P). Thus, we assumed that both total phosphorus and total nitrogen would be among the most important explanatory variables for diatom richness in our study [e.g. 11, 17]. However, we found that the effect of phosphorus on richness was slightly stronger than the nitrogen effect, which agrees with the findings of Blomqvist et al. . This finding may reflect the fact that salinity in our study area was closer to freshwater than marine. Some earlier studies have observed a unimodal relationship between nutrients and diatom species richness, stemming from P limitation in low nutrient levels leading to increased P competition, and high pH in high P values [53, 59]. The nutrient levels in our sampling sites remained moderate, thus leading to positive, however leveling off, dependence between total phosphorus and species richness, and total nitrogen and species richness.
RDA showed that salinity was one of the key variables affecting diatom composition on the first axis, albeit its effect was somewhat weaker than air and water temperature, silicon and total phosphorus. The salinity gradient in our study area was 0.1–6.1, thus making the RDA result consistent with previous studies. Busse and Snoeijs , Ulanova and Snoeijs , and Ulanova et al.  studied the Swedish coast (salinity gradient approx. 0.4–11.4) and emphasized the role of salinity as one of the most important explanatory variables for diatoms. Clarke et al.  studied the Danish Straits (salinity gradient 2.7–31.1) and noted a similar strong impact of salinity on diatoms. In contrast, Weckström and Juggins  (salinity gradient 0.7–6.4), and Leskinen and Hällfors  (salinity ca. 6) studied the Gulf of Finland and reported salinity to have only a minor effect on diatom communities. In conclusion, these studies show how both the extent of the salinity gradient and study area seem to affect the importance of salinity on diatoms.
RDA also showed that water and air temperatures were important variables for diatom compositions. Temperature may affect diatoms directly by influencing metabolism, growth and reproduction , or indirectly by changing the physical, chemical and biological characteristics of the water. Therefore, some earlier studies have noted air and water temperatures to be influential to diatoms [e.g. 62]. We also showed silicon to exert a strong effect on littoral diatom composition, which is inconsistent with several previous studies suggesting that silicon is a limiting nutrient only in the pelagic areas [12, 19].
Due to these driving variables, RDA clearly separated the southern and northern study areas based on their diatom communities. The southern sampling sites in the Gulf of Finland and the Archipelago Sea were characterized by high temperatures, salinity, pH and concentrations of total phosphorus, but low concentrations of silicon. Diatom samples collected from the southern area were dominated e.g. by Navicula incertata, which is a brackish water species tolerating somewhat high salinities, and Nitzschia frustulum, Nitzschia liebetruthii and Diatoma monoliformis, which thrive in eutrophic waters and indicate high nutrient levels. Samples from the Bothnian Bay in the North, were dominated by the freshwater species Encyonema silesiacum and Nitzschia fonticola. Such regional segregation of species is typical for diatom studies [e.g. 63] due to climatic variation, restricted dispersal and regional differences in water chemistry.
According to the traditional view, unicellular organisms are ubiquitous and their community compositions are only regulated by local water chemistry variables [e.g. 64]. During the past decades, however, the traditional view has been questioned, and particularly the seminal approach of variation partitioning by Borcard et al.  has given rise to research concerning the role of local and regional variables affecting diatom community composition [e.g. 63, 65]. In particular, benthic algae have been documented to exhibit spatially more restricted distributions than previously believed, possibly because they are less exposed to wind and currents than planktonic algae . In our variation partitioning, only 0.6% of variation in community composition was explained solely by local water physicochemical variables, whereas the spatial variables explained purely 1.7% of the variation and the combined effect of all explaining variables was 8.8%. Such a spatial component was also evident in Mantel test in which community dissimilarity was correlated with geographical distance. This may reflect either dispersal limitation or spatially structured environmental variation. For example, Heino et al.  and Potapova and Charles  also reported that spatial variables had stronger influence on communities than water chemistry variables in boreal and North American streams, respectively. The importance of spatial variables on diatom community composition has been criticized, however, because spatial effect may also include the effects of any spatially structured, unmeasured environmental variables . However, in our study, we included water chemistry variables that have been previously documented to be the most important drivers for diatom communities (e.g. pH, salinity, total nitrogen, total phosphorus) [e.g. 18]. Therefore, we assume that the importance of regional variables is not solely due to unmeasured water chemistry variables. In our study, climatic variables explained 1.8% of variation, i.e. slightly more than spatial variables. Previous studies taking into account the effect of climate on diatom composition are rare, but these studies have suggested that climate may be influential for diatoms . Our study confirms that it is important for future diatom studies to consider climatic variables.
Our variation partitioning showed that 81.5% of variation remained unexplained. Such a high value is typical for corresponding studies [e.g. 67], and it may be due to the fact that we missed some abiotic (e.g. calcium and magnesium concentrations) or biotic (e.g. grazing pressure) factors that may have been influential to the community composition. While the individual effects of variable groups remained admittedly low here, the combined effects proved to be important. This result was to be expected, as spatial and climatic variables are strongly related, and both also affect water chemistry. In general, this shows that most of the variables act in concert to influence diatoms and any individual effect of a single variable is not easily disentangled.
The usefulness of diatoms in indicating the local environment has been recognized, and diatoms are increasingly utilized in monitoring the state of the aquatic ecosystems. The Baltic Sea is a unique and vulnerable ecosystem with low salinity and biodiversity, and thus demands continuous research to support conservation efforts and monitoring programs. However, previous research on large-scale distribution patterns of diatoms in the Baltic Sea is scarce. Here, we showed that the most important variables affecting diatom species richness were pH, total phosphorus and total nitrogen. The most important variable groups affecting diatom composition were climatic and spatial variables, whereas the effect of water physicochemical variables was surprisingly weak. The combined effects of climatic, spatial and water physicochemical variables were, however, stronger. Therefore, we conclude that explanatory variables affecting diatom species richness and composition are diverse, and understanding the distribution of diatoms requires the inclusion of not only the local water physicochemical variables, but also regional explanatory variables such as climatic and spatial variables.
LV and JS designed the study in cooperation. LV collected and analyzed the diatom and water samples, performed the data analyses, and was a major contributor in writing the manuscript. JS gave useful comments concerning the manuscript. Both authors read and approved the final manuscript.
We thank the Walter and Andrée de Nottbeck Foundation for financial support. We are thankful for Hanna Reijola, Tuija Vaahtojärvi and Juhani Virkanen at the Environmental Laboratory of the Department of Geosciences and Geography (University of Helsinki) for the assistance with the analyses of water samples. We also thank Elina Virtanen (Finnish Environment Institute) and Miska Luoto (University of Helsinki) for providing us with useful data.
The authors declare that they have no competing interests.
Availability of data and materials
The datasets generated and analyzed during the current study are available from the corresponding author on request, and will be available in ResearchGate after publication of the article.
Consent for publication
Ethics approval and consent to participate
Funding for the research has been received from the Walter and Andrée de Nottbeck Foundation.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
- Sanders R, Brown L, Henson S, Lucas M. New production in the Irminger Basin during 2002. J Marine Syst. 2005;55:291–310.View ArticleGoogle Scholar
- Sorokin YI, Sorokin PY. Production in the Sea of Okhotsk. J Plankton Res. 1999;21:201–30.View ArticleGoogle Scholar
- Pajunen V, Luoto M, Soininen J. Climate is an important driver for stream diatom distributions. Glob Ecol Biogeogr. 2016;25:198–206.View ArticleGoogle Scholar
- Hillebrand H, Sommer U. Diversity of benthic microalgae in response to colonization time and eutrophication. Aquat Bot. 2000;67:221–36.View ArticleGoogle Scholar
- Martiny JBH, Bohannan JM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Øvreås L, Reysenbach AL, Smith VH, Staley JT. Microbial biogeography: putting microorganisms on the map. Microbiol Mol Biol R. 2006;4:102–12.Google Scholar
- Meier HEM, Kauker F. Sensitivity of the Baltic Sea salinity to the freshwater supply. Clim Res. 2003;24:231–42.View ArticleGoogle Scholar
- Leppäranta M, Myrberg K. Physical Oceanography of the Baltic Sea. Chicester: Springer; 2009.View ArticleGoogle Scholar
- Zander CD, Reimer LW. Parasitism at the ecosystem level in the Baltic Sea. Parasitology. 2002;124:119–35.View ArticleGoogle Scholar
- Johannesson K, Smolarz K, Grahn M, Andre C. The future of Baltic Sea populations: local extinction or evolutionary rescue? Ambio. 2011;40:179–90.View ArticlePubMedPubMed CentralGoogle Scholar
- Elmgren R. Trophic dynamics in the enclosed, brackish Baltic Sea. Rapp. P.-V. Réun. Cons. Int. Explor. Mer. 1984;183:152–69.Google Scholar
- Leskinen E, Hällfors G. Community structure of epiphytic diatoms in relation to eutrophication on the Hanko Peninsula, south coast of Finland. 10th Diatom-Symposium 323–333; 1988.Google Scholar
- Leskinen E, Hällfors G. Dynamics of epiphytic diatoms on Cladophora glomerata in the Tvärminne archipelago, northern Baltic Sea. in Proceedings of the 11th International Diatom Symposium; 1994.Google Scholar
- Leskinen E, Hällfors G. Tabularia waernii (Diatomophyceae) in the northern Baltic Sea. Ann Bot Fennici. 1997;34:141–7.Google Scholar
- Vilbaste S. The epiphytic and microphytobenthic diatoms in Estonian coastal waters (the Baltic Sea). in Proceedings of the Thirteenth International Diatom Symposium. 1995; 259–69.Google Scholar
- Vilbaste S, Sundback K, Nilsson C, Truu J. Distribution of benthic diatoms in the littoral zone of the Gulf of Riga, the Baltic Sea. Eur J Phycol. 2000;35:373–85.View ArticleGoogle Scholar
- Sommer U. Nutrient competition experiments with periphyton from the Baltic Sea. Mar Ecol Prog Ser. 1996;140:161–7.View ArticleGoogle Scholar
- Busse S, Snoeijs P. Gradient responses of diatom communities in the Bothnian Sea (northern Baltic Sea), with emphasis on responses to water movement. Phycologia. 2003;42:451–64.View ArticleGoogle Scholar
- Ulanova A, Snoeijs P. Gradient responses of epilithic diatom communities in the Baltic Sea proper. Estuar Coast Shelf Sci. 2006;68:661–74.View ArticleGoogle Scholar
- Ulanova A, Busse S, Snoeijs P. Coastal diatom-environment relationships in the brackish Baltic Sea. J Phycol. 2009;45:54–68.View ArticlePubMedGoogle Scholar
- Andrejev O, Myrberg K, Alenius P, Lundberg PA. Mean circulation and water exchange in the Gulf of Finland: a study based on three-dimensional modelling. Boreal Environ Res. 2004;9:1–16.Google Scholar
- Håkansson B, Alenius P, Brydsten L. Physical environment in the Gulf of Bothnia. Ambio Special Report Number. 1996;8: 5–12.Google Scholar
- Cederwall H, Elmgren R. Biological effects of eutrophication in the Baltic Sea, particularly the coastal zone. Ambio. 1990;19:109–12.Google Scholar
- Meier HEM. Baltic Sea climate in the late twenty-first century: a dynamical downscaling approach using two global models and two emission scenarios. Clim Dyn. 2006;27:39–68.View ArticleGoogle Scholar
- Pirinen P, Simola H, Aalto J, Kaukoranta J-P, Karlsson P, Ruuhela R. Tilastoja Suomen ilmastosta 1981–2010. Ilmatieteen laitoksen raportteja 2012: 1. Helsinki: Finnish Meteorological Institute.Google Scholar
- Eloranta P, Karjalainen SM, Vuori KM. Piileväyhteisöt jokivesien ekologisen tilan luokittelussa ja seurannassa—menetelmäohjeet. Oulu: Painotupa ky; 2007.Google Scholar
- Krammer K, Lange-Bertalot H. Bacillariophyceae. Süßwasserflora von Mitteleuropa 2 (1–4). Stuttgart: Gustav Fischer Verlag; 1986–1991.Google Scholar
- Guiry MD, Guiry GM. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. 2017. http://www.algaebase.org. Accessed 15 June 2017.
- Teittinen A, Taka M, Ruth O, Soininen J. Variation in stream diatom communities in relation to water quality and catchment variables in boreal, urbanized region. Sci Total Environ. 2015;530–531:279–89.View ArticlePubMedGoogle Scholar
- UNESCO. Algorithms for computation of fundamental properties of seawater. UNESCO technical papers in marine science. 44; 1983.Google Scholar
- ESRI. ArcGIS 10.2.1 for Desktop. Redlands, CA: Environmental System Research Institute; 2014.Google Scholar
- Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, García Marquéz JR, Gruber B, Lafourcade B, Leitão PJ, Mündemüller T, McClean C, Osborne PE, Reineking J, Schröder B, Skidmore AK, Zurell D, Lautenbach S. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography. 2013;36:27–46.View ArticleGoogle Scholar
- Moran PAP. The interpretation of statistical maps. J R Stat Soc B (Methodological). 1948;10:243–51.Google Scholar
- Waldhör T. The spatial autocorrelation coefficient Moran’s I under heteroscedasticity. Stat Med. 1996;15:887–92.View ArticlePubMedGoogle Scholar
- Bland JM, Altman DG. Multiple significance tests: the Bonferroni method. BMJ. 1995;310:170.View ArticlePubMedPubMed CentralGoogle Scholar
- Hastie T, Tibshirani R. Generalized additive models. Stat Sci. 1986;1:297–318.View ArticleGoogle Scholar
- Guisan A, Edwards TC, Hastie T. Generalized linear and generalized additive models in studies of species distributions: setting the scene. Ecol Model. 2002;157:89–100.View ArticleGoogle Scholar
- Benedetti A, Abrahamowicz M, Goldberg MS. Accounting for data-dependent degrees of freedom selection when testing the effect of a continuous covariate in generalized additive models. Commun Stat Simul. 2009;38(5):1115–35.View ArticleGoogle Scholar
- Wald A. A note on regression analysis. Ann Math Stat. 1947;18:586–9.View ArticleGoogle Scholar
- Legendre P, Gallagher ED. Ecologically meaningful transformations for ordination of species data. Oecologia. 2001;129:271–80.View ArticlePubMedGoogle Scholar
- Peres-Neto PR, Legendre P, Dray S, Borcard D. Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology. 2006;87:2614–25.View ArticlePubMedGoogle Scholar
- Van den Wollenberg AL. Redundancy analysis an alternative for canonical correlation analysis. Psychometrika. 1977;42:207–19.View ArticleGoogle Scholar
- O’Brien RM. A caution regarding rules of thumb for variance inflation factors. Qual Quant. 2007;41:673–90.View ArticleGoogle Scholar
- Stine RA. Graphical interpretation of variance inflation factors. Am Stat. 1995;49:53–6.Google Scholar
- Borcard D, Legendre P, Drapeau P. Partialling out the spatial component of ecological variation. Ecology. 1992;73:1045–55.View ArticleGoogle Scholar
- R Development Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. 2013. http://www.Rproject.org. Accessed 21 Feb 2016.
- Wood, S. Mixed GAM Computation Vehicle with GCV/AIC/REML Smoothness Estimation. 2016. https://cran.r-project.org/web/packages/mgcv/mgcv.pdf. Accessed 8 Feb 2016.
- Bjornstad ON. Spatial Nonparametric Covariance Functions. 2015. https://cran.r-project.org/web/packages/ncf/ncf.pdf. Accessed 8 Feb 2016.
- Guo Y, Hastie T, Tibshirani R. Shrunken Centroids Regularized Discriminant Analysis. 2015. https://cran.r-project.org/web/packages/rda/rda.pdf. Accessed 8 Feb 2016.
- Oksanen J, Blanchet FG, KindT R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H. Vegan: Community ecology package. 2016. https://cran.r-project.org/web/packages/vegan/vegan.pdf. Accessed 8 Feb 2016.
- Mantel N. The detection of disease clustering and a generalized regression approach. Cancer Res. 1967;27:209–20.PubMedGoogle Scholar
- Barinova S, Stenina A. Diatom diversity and ecological variables in the Arctic lakes of the Kostyanoi Nos Cape (Nenetsky Natural Reserve, Russian North). Plant Biosyst. 2013;2:397–410.View ArticleGoogle Scholar
- Soininen J. Responses of epilithic diatom communities to environmental gradients in some Finnish rivers. Int Rev Hydrobiol. 2002;87:11–24.View ArticleGoogle Scholar
- Soininen J. Is diatom diversity driven by productivity in boreal streams? Diatom Res. 2009;24:197–207.View ArticleGoogle Scholar
- Nixon SW, Ammerman JW, Atkinson LP, Berounsky VM, Billen G, Boicourt WC, Boynton WR, Church TM, Ditoro DM, Elmgren R, Garber JH, Giblin AE, Jahnke RA, Owens NJP, Pilson MEWQ, Seitzinger SP. The fate of nitrogen and phosphorus at the land–sea margin of the North Atlantic Ocean. Biochemistry. 1996;35:141–80.Google Scholar
- Schindler DW. Eutrophication and recovery in experimental lakes: implications for lake management. Science. 1974;184(4139):897–9.View ArticlePubMedGoogle Scholar
- Danielsson Å, Papush L, Rahm L. Alterations in nutrient limitations—scenarios of a changing Baltic Sea. J Marine Syst. 2008;73:263–83.View ArticleGoogle Scholar
- Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett. 2007;10:1135–42.View ArticlePubMedGoogle Scholar
- Blomqvist S, Gunnars A, Elmgren R. Why the limiting nutrient differs between temperate coastal seas and freshwater lakes: a matter of salt. Limnol Oceanogr. 2004;49:2236–41.View ArticleGoogle Scholar
- Weckström K, Juggins S. Coastal diatom-environment relationships from the Gulf of Finland, Baltic Sea. J Phycol. 2005;42:21–35.View ArticleGoogle Scholar
- Clarke A, Juggins S, Conley D. A 150-year reconstruction of the history of coastal eutrophication in Roskilde Fjord, Denmark. Mar Pollut Bull. 2003;46:1615–8.View ArticlePubMedGoogle Scholar
- Bothwell ML. Growth-rate responses of lotic periphytic diatoms to experimental phosphorus enrichment: the influence of temperature and light. Can J Fish Aquat Sci. 1988;45:261–70.View ArticleGoogle Scholar
- Leland HV. Distribution of phytobenthos in the Yakima River basin, Washington, in relation to geology, land-use, and other environmental-factors. Can J Fish Aquat Sci. 1995;52:1108–29.View ArticleGoogle Scholar
- Soininen J, Paavola R, Muotka T. Benthic diatom communities in boreal streams: community structure in relation to environmental and spatial gradients. Ecography. 2004;27:330–42.View ArticleGoogle Scholar
- Finlay BJ. Global dispersal of free-living microbial eukaryote species. Science. 2002;296:1061–3.View ArticlePubMedGoogle Scholar
- Potapova MG, Charles DF. Benthic diatoms in USA rivers: distributions along spatial and environmental gradients. J Biogeogr. 2002;29:167–87.View ArticleGoogle Scholar
- Soininen J. Assessing the current related heterogeneity and diversity patterns of benthic diatom communities in a turbid and a clear water river. Aquat Ecol. 2004;38:495–501.View ArticleGoogle Scholar
- Heino J, Bin LM, Karjalainen SM, Mykrä H, Soininen J, Vieira LCG, Diniz JAF. Geographical patterns of micro-organismal community structure: are diatoms ubiquitously distributed across boreal streams? Oikos. 2010;119:129–37.View ArticleGoogle Scholar
- Clarke G, Kernan M, Marchetto A, Sorvari S, Catalan J. Using diatoms to assess geographical patterns of change in high-altitude European lakes from pre-industrial times to the present day. Aquat Sci. 2005;67:224–36.View ArticleGoogle Scholar