Authors:

Jaakko Leppänen, Susanna Siitonen and Jan Weckström

Title:

The stability of Cladoceran communities in sub-Arctic NW Finnish Lapland lakes

The affiliations and addresses of the authors:

Corresponding author:

Jaakko Leppänen

Department of Environmental Sciences

P.O. Box 65, FIN-00014, University of Helsinki, Finland

Jaakko.leppanen@helsinki.fi

+358415439736

Susanna Siitonen

Department of Environmental Sciences

P.O. Box 65, FIN-00014, University of Helsinki, Finland

Jan Weckström

Department of Environmental Sciences

P.O. Box 65, FIN-00014, University of Helsinki, Finland

1

1

2

3

4

5

6

7

8

9

10

11

12

13

14

15

16

17

18

19

20

21

22

23

24

Abstract

It is difficult to plan restoration projects or study the amount of disturbance in aquatic ecosystems if

background conditions are not known. Zooplankton, especially cladocerans (water fleas), has

proven highly useful as a reliable indicator of environmental change. Cladocerans preserve well in

sediments and thus allow for the analysis of historical communities. To assess the stability of

cladoceran communities in lakes with low human impact, we compared pre-industrial and modern

cladoceran assemblages (top-bottom analysis) in 32 sub-Arctic lakes in NW Finnish Lapland. We

used a data set of measured environmental variables to determine their explanatory power on

cladoceran assemblages. While cladoceran assemblages at the community level have remained

relatively stable between the pre-industrial and modern samples, a clear change at the genus level

was observed with a significant proportional increase in Bosmina (Eubosmina) spp. (Wilcoxon

signed rank test z = 2.75 p = 0.006). The amount of organic matter in the sediment (measured as

loss on ignition (LOI)) explained the largest proportion of the variation in the cladoceran

community. Since LOI is strongly correlated to climatic factors, the increased abundance of B.

(Eubosmina) spp. may ultimately be related to climate warming. As the top-bottom approach is

comprised of two temporal snapshots, it cannot provide the exact time of community change. This

shortcoming is of special importance for restoration and management planning.

Keywords: Cladocera, community change, palaeolimnology, climate change, reference conditions,

Finland

2

25

26

27

28

29

30

31

32

33

34

35

36

37

38

39

40

41

42

43

44

45

46

47

Introduction

There is a long tradition of using (sub)fossil species assemblages to investigate the effects of both

natural and human-induced environmental disturbances. Zooplankton are known to respond

strongly to environmental changes (Jeppesen et al. 2011) and some groups even have potential to be

used as early warning organisms regarding ecosystem changes (Pace et al. 2013). Further,

zooplankton plays a key role in many restoration projects where the goal is to halt or reverse lake

eutrophication (Gulati et al. 2008), making it an important group for efforts which aim to improve

the quality of inland waters. In fact, Luoto et al. (2013) developed a cladoceran (Branchiopoda:

Phyllopoda) -based model, which can be used to estimate the ecological status of a given water

body and to define reference conditions. Also, cladocerans have been used to evaluate the success

of restoration projects in cases, where historical cladoceran community data have been available

(e.g. Louette et al. 2009). However, almost all surface waters in Europe have already changed

during the last centuries due to land use, contamination and climate change (Wetzel 1992; Bennion

and Batterbee 2007), but monitoring programs extending over decades are very rare. It is therefore

difficult to assess or to predict the effects of any disturbance or to succeed in restoration projects if

the environmental history or ongoing ecological trends are not assessed. Lake sediments have the

potential to store an enormous amount of environmental information and the palaeolimnological

approach can be used as a tool to uncover the historical conditions of past aquatic environments

(Smol 1992; European Union 2000). Cladocerans are regarded as one of the most useful

palaeolimnological tools to track environmental change (Eggermont and Martens 2011). Cladoceran

subfossils in families Chydoridae and Bosminidae preserve well in sediments and can be identified

in some cases to species group level (Frey 1987). Cladocerans have been used in

palaeolimnological research for more than 50 years with methods varying from simple descriptive

studies (Frey 1962) to computer-powered ecosystem modelling of historical environments (e.g.

Korhola et al. 2002). Cladoceran-based palaeolimnological studies include climate change research

3

48

49

50

51

52

53

54

55

56

57

58

59

60

61

62

63

64

65

66

67

68

69

70

71

72

(Lotter et al. 1997; Korhola 1999; Sarmaja−Korjonen et al. 2006), calcium decline research

(Jeziorski et al. 2008), reconstruction of water level fluctuations (Sarmaja−Korjonen and Alhonen

1999; Korhola et al. 2000; Siitonen et al. 2011), food web studies (Rawcliffe et al. 2010), and

reconstruction of trophic state (Korponai et al. 2011).

Lakes and rivers in NW Finnish Lapland are regarded as among the most pristine environments in

the world (Hettelingh et al. 1992; Rühling and Steinnes 2002). Because the level of anthropogenic

disturbance is extremely low, these ecosystems provide excellent opportunities to study baseline

conditions and the long-term stability of biological communities by using palaeolimnological

methods. Usually the fossil biota assemblages from a whole sediment sequence is studied to assess

possible past environmental trends (e.g. Manca et al. 2007), but when studying a large number of

lakes, the so called top-bottom or “before-after” approach is perhaps the most useful option

(Michelutti et al. 2001; Weckström et al. 2003). The topmost centimetre of lake sediment represents

the modern environmental conditions, whereas the “bottom” sample reflects a point of time in the

past, e.g. pre-industrial conditions. The top-bottom approach thus enables the assessment of system

stability on a regional scale. It should be noted, however, that this approach has a notable

shortcoming as it provides information of only two single periods of time, lacking the possibility to

track short-lived fluctuations between the two periods of interest.

In this study, we used a top-bottom data set consisting of 32 sub-Arctic lakes to 1) explore which

environmental factors exert the strongest impact on the cladoceran community structure, and 2) to

compare the species composition between the pre-industrial and modern samples in NW Finnish

Lapland. We aim to provide new information about the applicability of reference condition analysis

based on one temporal snapshot (the bottom sample) in some of the least disturbed regions in the

world. Further, our study intends to add new insights to the discussion regarding the stability of

zooplankton communities and environmental change during the last few centuries in NW Finnish

Lapland.

4

73

74

75

76

77

78

79

80

81

82

83

84

85

86

87

88

89

90

91

92

93

94

95

96

97

Materials and methods

Study area

The 32 lakes are situated in sub-Arctic NW Finnish Lapland, (except for one site located in

Norway), an area with a notable eco-climatic gradient (Fig. 1). The lakes span from the boreal

forest to the mountain birch woodland and further across the tree line to the tundra. The study lakes

are generally small (0.9–115 ha, mean 15 ha) and shallow (1-25 m, mean 6 m), they are relatively

neutral (pH ranges within 4.9–7.6, mean 6.6) and have low conductivity (0.4–5.1 mS/cm, mean 2.1

mS/cm). Total phosphorus (TP) varies between 1.5-46 µg/L (median 5 µg/L) and total nitrogen

(TN) between 54-1,500 µg/L (median 280 µg/L) (Table 1; Online Resource 1). According to the

dataset retrieved from the KNMI Climate Explorer (van Oldenborgh 1999) online data bank

(http://climexp.knmi.nl/), the annual mean temperatures (averages 1961-2011) in the study area

range from -1.2 ˚C in the south to -2.1 ˚C in the north. This is also reflected in the annual ice cover

period of the lakes varying from ca. 200 days in the south to 260 days in the north (Weckström et al.

2014). The study area is relatively pristine as it lacks big population centres, heavy industry, and the

effects of atmospheric transportation of pollutants are generally negligible (Paatero et al. 2008). The

air quality is considered as one of the cleanest in Europe (Hettelingh et al. 1992; Anttila et al. 2011).

According to weather data provided by the KNMI database, the annual temperature averages and

average daily precipitation have increased during the past decades in the study area (Fig. 1). Recent

climate change can thus be considered as the only regional environmental variable that has had an

impact on all study lakes during the past decades.

Fish populations

The important role of fish as a determinant of the cladoceran community structure has been shown

in many studies (e.g. Hrbacek et al. 1961; Brooks and Dodson 1965; Persson 1986), but in this

study it is assessed only at a general level because no exact data of possible fish introductions and

5

98

99

100

101

102

103

104

105

106

107

108

109

110

111

112

113

114

115

116

117

118

119

120

121

their timing are available. Most of our study lakes are either naturally inhabited by fish, or have

been stocked, and according to Tammi et al. (2003), the number of fish species in these lakes is

mostly between 1 and 3. However, the shallow (water depth < 1.5 m) and remote high altitude

hilltop lakes are most likely fishless. In our study lakes the most common fish species are whitefish

(Coregonus lavaretus), arctic char (Salvelinus alpinus), brown trout (Salmo trutta), and also perch

(Perca fluviatilis) especially in the forested catchments. Brown trout and arctic char are the most

common species able to inhabit the high altitude and cold tundra lakes, whereas whitefish is

generally restricted to lower altitude warmer water lakes (Tammi et al. 2003). Whitefish is probably

the most intensively introduced fish species in northern Finland (Tammi et al. 2003). However,

there are no reliable registers or data regarding the time, place and magnitude of fish introductions

available.

Sampling

Water samples were retrieved from 1 meter depth using a limnos sampler and geographical

characteristics were determined using topographic maps. The water samples (500 ml) were

collected in acid-washed polyethylene bottles and stored at 4 ºC for chemical analyses. Water

chemistry analyses were carried out using standard methods. For more information, see Weckström

et al. (1997) and Weckström and Korhola (2001).

Three parallel surface sediment cores were retrieved with a Limnos-type gravity corer from the

deepest part of each lake in autumn 2008. Sediment cores were combined in order to get enough

material for analyses and subsampled into 1 cm thick sequences, packed in small plastic bags and

stored in 4°C cold storage. Surface sediment samples (0-1 cm) are thought to represent the present,

and the 1 cm sediment slices from varying depths between 4 and 15 cm represent the pre-industrial

era. The retrieval depths of bottom samples were determined in the field and the assessment was

based on known sedimentation rates, local characteristics and visible sediment properties. In

6

122

123

124

125

126

127

128

129

130

131

132

133

134

135

136

137

138

139

140

141

142

143

144

145

general, at high altitude tundra lakes, the bottom sample was taken from an average depth of 9 cm,

whereas at lakes located in mountain birch vegetated catchment area, the bottom sample was taken

from an average depth of 13 cm. At lakes located in coniferous forest catchments, the bottom

sample was taken from an average depth of 14 cm. Sedimentation rates of these sub-Arctic lakes are

generally low and are well known in the region (e.g. Korhola and Weckström 2004; Siitonen 2005;

Weckström et al. 2014). The laboratory procedure and the identification of cladoceran is based on

Szeroczyńska and Sarmaja−Korjonen (2007). Cladoceran taxonomy is currently under a thorough

revision. In this study, the nomenclature is based on Szeroczyńska and Sarmaja−Korjonen (2007),

Van Damme and Dumont (2008), Sinev (2009), Korovchinsky (2016), and Sinev and Dumont

(2016). The sediment samples were prepared by heating and stirring 1 – 2 cm3 of sediment in 10%

KOH for 30 min and sieving through a 50 µm mesh with tap water. Cladoceran remains were

identified from permanent slides under a light microscope using 100-400 x magnification. The

counted number of individuals is based on the most common fragment of each species. The results

are expressed as relative abundances.

Data analysis

It has recently been proposed that a minimum number of 70-100 individuals should be counted

when studying claodoceran subfossils (Kurek et al. 2010). Here, at least 75 individuals per sample

were counted. The possible bias in species richness resulting from different total counts per sample

was corrected using rarefaction analysis (Birks and Line 1992). We used a Simple Mantel’s test

(Mantel 1967), which is a non-parametric test for correlation of two matrices, to study whether

environmentally similar lakes also have similar cladoceran communities. The Simple Mantel’s test

was applied to environmental factors (euclidean distance matrix) and cladoceran species

composition (Bray-Curtis dissimilarity matrix). Environmental data were Z-standardised and

cladoceran community data were square root-transformed prior to matrix calculations. Due to the

short gradient length of species compositional turnover along the first DCA axes (1.9 SD units), the

7

146

147

148

149

150

151

152

153

154

155

156

157

158

159

160

161

162

163

164

165

166

167

168

169

170

relationships between environmental variables and modern cladoceran assemblages were studied

using redundancy analysis (RDA). In RDA, the pre-industrial samples were treated as

supplementary variables. Skewed environmental data were log10(x+1) -transformed prior to

analysis. To reduce multicollinearity, variance inflation factors (VIFs < 20) were used to select the

final set of environmental variables. However, also the known ecological importance or

combination of the environmental variables was taken into account. A similarity matrix was

constructed using the Bray-Curtis similarity index (Bray and Curtis 1957), which was calculated

from square root-transformed species abundance data. The matrix was used to detect significant

differences between pre-industrial and modern cladoceran communities by the analysis of similarity

(ANOSIM) method. ANOSIM is a non-parametric test of significant difference between two groups

(Clarke 1993). The similarity matrix was further used to quantify compositional differences for each

lake between the pre-industrial and the modern period. For individual lake comparisons, the Bray-

Curtis dissimilarity index was used, where the value of 0 resembles identical cladoceran

communities. The Wilcoxon signed-rank test (Wilcoxon 1945) was conducted to determine if

species proportional abundances had changed significantly since the pre-industrial era. The

Wilcoxon signed-rank test is a nonparametric test analogous to the dependent t-test. RDA was

performed using CANOCO for Windows 5.01 (ter Braak and Šmilauer 1997-2012), ANOSIM,

Mantel’s test and the rarefication analyses were conducted using the PAST statistics 3.1. software

(Hammer et al. 2001) and the Wilcoxon signed-rank test was performed using the IBM SPSS

Statistics 22 software (IBM Corp 2013). To analyse the general environmental preferences of

cladoceran taxa, the study lakes were grouped into three catchment categories based on the

prevailing ecotone of the catchment area (coniferous forest, mountain birch woodland, and barren

tundra). These catchment categories consisted of 17, 7, and 8 lakes, respectively.

Results

Modern and pre-industrial cladoceran communities in NW Finnish Lapland

8

171

172

173

174

175

176

177

178

179

180

181

182

183

184

185

186

187

188

189

190

191

192

193

194

195

Fossil cladoceran remains were generally well preserved in the sediment samples. Out of 36 taxa

identified, Chydorus spp. and Bosmina (Eubosmina) spp. were most widely distributed and were

detected in all lakes both in pre-industrial and in modern samples. Bosmina (Eubosmina) spp. was

proportionally most abundant in 20 lakes in modern samples (average 37.6% SD ± 18.1 %) and in

16 lakes in pre-industrial samples (30.6 % SD ± 16.9 %). In modern samples, a total of 13

cladoceran taxa were present in all catchment vegetation types (Table 2). The rarefaction-corrected

number of taxa varied from 19 (lake 8) to 7 (lakes 12 and 49) in modern samples and from 18 (lake

9) to 6 (lake 6) in pre-industrial samples (Fig. 4).

Environmental variables and cladoceran assemblages

The Simple Mantel’s test exhibited positive (R = 0.40) and significant (p = 0.003) correlation

between similarity matrices of cladoceran communities and environmental factors. After screening

the original 31 environmental variables (Table 1; Online Resource 1) by VIF only 10 environmental

variables (mire area, LOI, sample depth, air temperature, pH, conductivity, calcium, total organic

carbon (TOC), total P, and total N) were included in RDA. These 10 environmental variables

explained 83.5% of the explanatory power of the 31 original environmental variables. After

variance partitioning, LOI was identified as the environmental variable explaining the largest part of

the variation in the cladoceran populations in our data set (Table 3). The correlation structure of

cladoceran populations and environmental variables is presented as an RDA biplot (Fig. 2). There,

the barren tundra lakes are plotted together indicating lower LOI, TOC, temperature and nutrients

values when compared to catchments with prevalent tree vegetation. According to RDA, no

common characteristics can be seen between the pre-industrial and modern samples (Fig. 3).

Cladoceran community changes since pre-industrial era

When all lakes were treated as one group, no significant differences were observed between pre-

industrial and modern cladoceran communities (ANOSIM R = -0.0066, p = 0.59). Results obtained

9

196

197

198

199

200

201

202

203

204

205

206

207

208

209

210

211

212

213

214

215

216

217

218

219

by similarity matrix analysis demonstrated that the average dissimilarity value between pre-

industrial and modern samples, when lakes were treated individually, was 0.29 SD ± 0.12. The

maximum dissimilarity value was 0.64 (Lake 62) and the minimum 0.13 (Lake 18). The largest

positive change in the rarefied species number between the pre-industrial and modern sample was in

lake 8, where the number of taxa increased by four. The largest negative change was recorded in

lake 26, where the number of taxa decreased by five (Fig. 4). The planktonic Bosmina (Eubosmina)

spp. increased significantly since the pre-industrial period (Wilcoxon signed rank test z = 2.7 p =

0.006), while changes concerning other species were not statistically significant. The proportion of

Bosmina (Eubosmina) spp. increased in 22 lakes by an average of 14.9 % and decreased in 10 lakes

by an average of -8.9 %. Further, the grouping of all identified planktonic taxa (Bosmina

(Eubosmina) spp., Polyphemus pediculus, Daphnia spp.) together, revealed a proportional increase

in 23 lakes by an average of 14.1 % and a decrease in nine lakes by an average of -8.9 %. The

change considering all planktonic species was significant (Wilcoxon signed rank test z = 2.8 p =

0.004). When lakes were grouped according to their catchment type (tundra, mountain birch,

confierous forest), the changes in community and species level were not significant.

Discussion

Environmental variables and cladoceran assemblages

Only Bosmina (Eubosmina) spp. and Chydorus spp. were found in all studied lakes. They are both

common in Northern Scandinavia (Korhola 1999; Rautio 2001; Brancelj et al. 2009). The overall

composition of cladoceran assemblages found in NW Lapland resembles those of the Central

Canadian treeline region (Sweetman et al. 2008) and Nova Scotia, Canada (Korosi and Smol 2011).

The clear correlation (Simple Mantel’s test R = 0.4, p = 0.003) regarding the degree of dissimilarity

between cladoceran communities and environmental parameters suggests that environmental factors

contribute strongly to species assemblages in our study lakes. Among the environmental variables

10

220

221

222

223

224

225

226

227

228

229

230

231

232

233

234

235

236

237

238

239

240

241

242

243

studied, only LOI explained a statistically significant portion of the variation in the species data.

LOI values provide a crude measure of the organic carbon content in sediments thus reflecting

primary production, catchment type and decomposition speed in the environment. Tundra lakes are

generally characterized by low LOI, TOC, temperature and nutrient concentrations (Fig. 2)

(Korhola and Weckström 2004). It has been suggested that fluctuations in LOI are connected to

changes in air temperature (Willemse and Törnquist 1999; Battarbee et al. 2001; Nesje and Dahl

2001; Kaplan et al. 2002). The correlation between climatic variables and LOI is also visible in this

data set (Table 1), where the role of eco-climatic gradients is clearly visible. High altitude and

latitude lakes, which are usually cool with low nutrient and low TOC concentrations, are

characterized by low LOI values, when compared to low altitude forest lakes. The fact that 17 taxa

were absent from tundra lakes, also reflects the effect of altitude and characteristics related to

altitude on the cladoceran species composition.

It is most likely that fish have some impact on cladoceran communities in our study lakes, although

our data do not clearly support this. Whitefish, especially the densely raked form (C. lavaretus

pallasi), feeds almost exclusively on zooplankton during all its life (e.g. Säisä et al. 2008), and may

thus have a high and direct impact on cladoceran communities. In contrast, as arctic char and brown

trout prefer larger prey items, such as invertebrates like gammarids and copepods (Crustacea), they

have an indirect impact on cladocerans by decreasing the pressure of invertebrate predation on

cladocerans (e.g. Seppovaara 1969; Milardi et al. 2016). However, in this study the impact of fish

on cladoceran communities cannot be quantified because no data on the dynamics of fish

populations are available. Moreover, because the dominant cladoceran species Bosmina

(Eubosmina) spp. is known to thrive in lakes with versatile fish communities (Tolonen 1997;

Amsinc et al. 2006), any generalizations regarding the effects of fish are very difficult.

In contrast, our results, concerning the role of primary production and climate-related

11

244

245

246

247

248

249

250

251

252

253

254

255

256

257

258

259

260

261

262

263

264

265

266

267

environmental variables on cladoceran species composition, are in good accordance with other

circumpolar studies (e.g. Korhola 1999; Brancelj et al. 2009; Sweetman et al. 2010; Korosi and

Smol 2011; Luoto et al. 2013). These studies indicate that nutrients, dissolved organic carbon and

lake water temperature are important variables controlling cladoceran community structure in

Canadian treeline region (Sweetman et al. 2010), lake depth and dissolved organic carbon in Nova

Scotia, Canada (Korosi and Smol 2011), lake depth, sediment organic content, epilimnetic summer

temperature, lake perimeter and lake catchment area in Finnish Lapland (Korhola 1999), and total

phosphorus in Finland (Luoto et al. 2013). In a study of 294 remote cold water lakes across Europe,

altitude was found to be the most important variable affecting the cladoceran community structure

(Brancelj et al. 2009).

Changes in cladoceran assemblages since the pre-industrial period

The lack of community level change between pre-industrial and modern samples suggests that

cladoceran communities have remained relatively stable during the recent centuries. Still, the

stability varied between lakes, and few lakes exhibited relatively high dissimilarities between pre-

industrial and modern samples (e.g. lakes 62 and 7). The most striking feature in our study lakes is

the increased relative abundance of planktonic Bosmina (Eubosmina) spp. in 22 out of 32 lakes,

whereas the corresponding decline in other taxa is highly variable. The reasons behind this shift are

most probably either changes in fish populations or climate warming. Fish may have high-

magnitude impacts on zooplankton communities (e.g. Brooks and Dodson 1965) and this has also

previously been detected in sub-Arctic lakes (Bøhn and Amundsen 1998; Donald et al. 2001;

Milardi et al. 2016). However, reliable historical records are not available and current fish data

concerning the study lakes are scarce. Planktivorous fish have been noted to prefer larger

cladoceran taxa, resulting in an overall decrease in the size structure of cladoceran communities e.g.

the shift from larger Eubosmina spp. to small Bosmina species (e.g. Stenson 1976). Such a shift,

however, is not detectable in our study lakes. The impact of predator fish on cladocerans is usually

12

268

269

270

271

272

273

274

275

276

277

278

279

280

281

282

283

284

285

286

287

288

289

290

291

292

not direct, but a result of trophic cascades (Brooks and Dodson 1965; Hall et al. 1976). The changes

in intensity of invertebrate predation can be detected as morphological changes in Bosmina

longirostris, but the applicability of Bosmina (Eubosmina) spp. in predation assessments is poor due

to contrasting results in literature (e.g. Sprules et al. 1984; Johnsen and Raddum 1987). In the

absence of species data of invertebrate predators, it is not possible to provide any information on

this issue. However, the minor changes in the cladoceran communities in most of our study lakes

since the pre-industrial time suggests that large-scale changes in fish population dynamics are not

likely.

The proportional increase in planktonic cladocera in the majority of the studied lakes is a significant

change that has occurred in the NW Finnish Lapland tree line region lakes during the last few

centuries indicating a presence of a regional baseline shift. The increasing abundance of planktonic

species, particularly Bosmina (Eubosmina) spp. in a relatively large geographical area suggest that

the shift may be a result of global climate change, which is reflected in NW Finnish Lapland as

increased temperatures and precipitation (Fig. 1). However, whereas lake surface water

temperatures in northern latitudes are increasing, the regional variation in warming trends suggests

that the connection between air and water temperatures is affected by local characteristics (O'Reilly

et al. 2015). Also, the climatic factors usually affect lake biota indirectly and the final impact

depends on lake and catchment characteristics of an individual lake (e.g. Battarbee 2000). The fact

that our study lakes may have responded to an increase in air temperatures and precipitation in a

number of ways, is also visible in our results (Fig. 3), where sample pairs do not exhibit any

common trends in relation to each other or to environmental variables. This may be the reason for

the low unique contributions of climatic factors showed in Table 3. However, some indications of

the impact of climate change on planktonic cladocerans can be seen. An increase in primary

production during the 20th century has already been recorded in Arctic lakes (Smol et al. 2005;

Michelutti et al. 2005). Further, the increase in planktonic diatom species since pre-industrial times

13

293

294

295

296

297

298

299

300

301

302

303

304

305

306

307

308

309

310

311

312

313

314

315

316

317

has been detected in the Canadian treeline region (Rühland et al. 2003) and in Finnish Lapland

(Sorvari and Korhola 1998; Korhola et al. 2002; Sorvari et al. 2002). Shifts in diatom communities

in the sub-Arctic region have been linked to shortening of the ice-cover period, more stable

stratification and a longer growing season due to climate warming (Smol et al. 2005). Planktonic

cladoceran species may have benefited from this elevated food availability. In addition to these

already observed changes related to primary production of lakes, there are further and potentially

important connections between climate change, primary production and cladoceran communities.

Higher temperatures may have enhanced the growth of edible bacteria near the surface (Simon and

Wünch 1998) and increased precipitation may have accelerated the flush of allochthonous carbon

into the lakes, which is an important component of winter food for cladocerans in Finnish Lapland

(Rautio et al. 2011). Bosmina (Eubosmina) spp. may adapt to changes in food availability easier

than some other cladoceran species, since it has a versatile feeding mechanism, which enables it to

feed both on large (Johnsen and Borsheim 1988) and small (Borsheim and Anderssen 1987) food

particles. In stratified lakes the increased production may also enhance oxygen depletion in the

hypolimnion, especially in high latitude lakes with prolonged ice cover. This, in turn, may suppress

the occurrence of benthic species and increases the proportion of planktonic cladoceran taxa (e.g.

Nevalainen and Luoto 2012). However, data regarding oxygen dynamics in our study lakes are not

available.

Our results are similar to Jeziorski et al. (2015), who compared pre-industrial and modern

cladoceran assemblages in 60 lakes of far north Ontario, Canada. They recorded a significant

proportional increase in pelagic cladoceran species. Also Desellas et al. (2011) detected an increase

in the relative abundance of pelagic cladoceran species since pre-industrial times in 42 lakes in

Ontario, Canada. Korosi and Smol (2012) compared modern cladoceran assemblages with pre-

industrial assemblages in Nova Scotia, Canada. They showed a proportional, but non-significant

increase of Bosmina (Eubosmina) spp. in 32 out of 48 lakes. However, Sweetman et al. (2008)

14

318

319

320

321

322

323

324

325

326

327

328

329

330

331

332

333

334

335

336

337

338

339

340

341

342

argued that cladoceran assemblages have not experienced any directional changes since pre-

industrial times in 50 tree-line region lakes in the central Canadian Arctic, despite a significant shift

towards planktonic species in the diatom communities. Although the top-bottom approach is highly

useful when assessing if changes in lake ecosystems have occurred since pre-industrial times on a

regional scale (a large number of lakes), it does not allow for pinpointing exactly when the

change(s) have occurred (Bennion et al. 2011). Especially for lake management purposes, a set of

chronological snapshots from the sediment sequences are needed. This is particularly important

when changes are rapid (e.g. due to pollution accidents), as it is impossible to detect any baseline

shifts prior to the accident without an adequate chronology of conditions.

In 10 out of 32 lakes the proportion of Bosmina (Eubosmina) spp. decreased. This opposite genus

level change may be caused by local environmental factors, which could have suppressed the

impact of regional stressors as suggested by Alric et al. (2013). Forestry (Bredesen et al. 2002),

fishing or fish introductions (Donald et al. 2001; Milardi et al. 2016) and reindeer herding

(Kuzmina and Leshko 2002) are likely the most important local human-induced factors that may

have had direct or indirect effects on cladoceran populations in our study lakes. The lakes

displaying a decreased proportion of Bosmina (Eubosmina) spp. are relatively shallow and represent

a wide spectrum of catchment variables. The average depth of these lakes was 4.5 m, while the

average depth of the other lakes was 8.7 m. In general, shallow lakes are more vulnerable to

environmental changes compared to deep lakes due to lower heat capacity (Shutner et al. 1983),

lower dilution capacity (Janse et al. 2008) and less diverse fish communities (Eloranta et al. 2015).

Conclusions

Cladoceran assemblages in NW Finnish Lapland have remained relatively stable during the last

centuries, however, some changes could be observed. The increased abundance of Bosmina

(Eubosmina) spp. in many of the lakes can be regarded as a baseline shift due to current climate

15

343

344

345

346

347

348

349

350

351

352

353

354

355

356

357

358

359

360

361

362

363

364

365

366

change. In contrast, some of the study lakes exhibited a decreased abundance of Bosmina

(Eubosmina) spp., which is likely related to local, catchment-related stressors. The top-bottom

approach is a powerful tool when a large number of sites are studied. However, in order to assess

the exact time, magnitude and speed of change(s) or baseline shift(s), either continuous sediment

series or a series of snapshots should be used instead. The recognition of directional changes and

the obtained set of multiple reconstructed past time slices may greatly assist in the planning of

restoration procedures.

Acknowledgements

This work was funded by Tellervo and Jussi Walden foundation. We thank Sanna Korkonen and

Juha Niemistö for help in the field.

References

Alric B, Jenny J-P, Berthon V, Arnaud F, Pignol C, Reyss J-L, Sabatier P, Perga M-E (2013) Local

forcing affect lake zooplankton vulnerability and response to climate warming. Ecology 94:

2767−2780

Amsinc SL, Strzelczak A, Bjerring R, Landkildehus F, Lauridsen TL, Christoffersen K, Jeppesen E

(2006) Lake depth rather than fish planktivory determines cladoceran community structure in

Faroese lakes – evidence from contemporary data and sediments. Freshw Biol 51: 2124−2142

Anttila P, Virkkula A, Ruosteenoja K, Hakola H, Vestenius M, Ryyppö T, Hellen H, Leppänen S

(2011) Assesment of the impacts of climate change on pollution transport to the arctic region −

Action 13 final report Finnish meteorological institute, Helsinki.

Battarbee RW (2000) Palaeolimnological approaches to climate change, with special regard to the

16

367

368

369

370

371

372

373

374

375

376

377

378

379

380

381

382

383

384

385

386

387

388

biological record. Quaternary Sci Rev 19: 107−124

Battarbee RW, Cameron NG, Golding P, Brooks SJ, Switsur R, Harkness D, Appleby P, Oldfield F,

Thompson R, Monteith DT, McGovern A (2001) Evidence for Holocene climate variability from

the sediments of a Scottish remote mountain lake. J Quaternary Sci 16: 339−346

Bennion H, Batterbee R (2007) The European Union water framework directive: Opportunities for

palaeolimnology. J Paleolimnol 38: 285−295

Bennion H, Battarbee RW, Sayer CD, Simpson GL, Davidson TA (2011) Defining reference and

restoration targets for lake ecosystems using paleolimnology: a synthesis. J Paleolimnol 45:

533−544

Birks HJB, Line JM (1992) The use of rarefaction analysis for estimating palynological richness

from Quaternary pollen−analytical data. The Holocene 2: 1−10

Borsheim K, Andersen S (1987) Grazing and food size selection by crustacean zooplankton

compared to production of bacteria and phytoplankton in a shallow Norwegian mountain lake. J

Plankton Res 9: 367−379

Brancelj A, Kernan M, Jeppesen E, Rautio M, Manca M, Sisko M, Alonso M, Stuchlik E (2009)

Cladocera remains from the sediments of remote cold lakes: A study of 294 lakes across Europe.

Adv Limnol 62: 239−264

Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin.

Ecology Monographs 27: 325−349

Bredesen EL, Bos DG, Laird KR, Cumming BF (2002) A cladoceran−based paleolimnological

assessment of the impact of forest harvesting on four lakes from the central interior of British

17

389

390

391

392

393

394

395

396

397

398

399

400

401

402

403

404

405

406

407

408

409

Columbia, Canada. J Paleolimnol 28: 389−402

Brooks JL, Dodson SI (1965) Predation, body size and composition of plankton. Science 150:

28−35

Bøhn T, Amundsen P-A (1998) Effects of invading vendace (Coregonus albula L.) on species

composition and body size in two zooplankton communities of the Pasvik River System, northern

Norway. J Plankton Res 20: 243−256

Clarke KR (1993) Non−parametric multivariate analysis of changes in community structure. Aust J

Ecol 18:117−143

Desellas AM, Paterson AM, Sweetman JN, Smol JP (2011) Assessing the effects of multiple

environmental stressors on zooplankton assemblages in boreal shield lakes since pre−industrial

times. J Limnol 70: 41−56

Donald DB, Vinebrooke RD, Anderson S, Syrgiannis J, Graham MD (2001) Recovery of

zooplankton assemblages in mountain lakes from the effect of introduced sport fish. Can J Fish

Aquat Sci 58: 1822−1830

Eggermont H, Martens K (2011) Preface: Cladocera crustaceans: sentinels of environmental

change. Hydrobiologia 676: 1−7

Eloranta AP, Kahilainen KK, Amundsen P-A, Kundsen R, Harrod C, Jones RI (2015) Lake size and

fish diversity determine resource use and trophic position of a top predator in high-latitude lakes.

Ecol Evol 5: 1664−1675

European Union (2000) Directive 2000/60/EC of the European Parliament and the council of 23

October 2000 on establishing a framework for community action in the field of water policy. Eur J

Commun L327: 1−72

18

410

411

412

413

414

415

416

417

418

419

420

421

422

423

424

425

426

427

428

429

430

431

Frey DG (1962) Cladocera from the Eemian interglacial of Denmark. J Paleontol 36: 1133−1154

Frey DG (1987) The taxonomy and biogeography of the Cladocera. Hydrobiologia 145: 5−17

Gulati RD, Pires LMD, Van Donk E (2008) Lake restoration studies: Failures, bottlenecks and

prospects of new ecotechnological failures. Limnologica 38: 233–247

Hall DJ, Threlkeld ST, Burns CW, Crowley PH (1976) The size-efficiency hypothesis and the size

structure of zooplankton communities. Ann Rev Ecol Syst 7: 177−208

Hammer Ø, Harper DAT, Ryan PD (2001) PAST. Paleontological statistics software package for

education and data analysis. Palaeontol Electron 4(1): 9

Hettelingh J−P, Downing RJ, de Smet P (1992) The critical loads concept for the control of

acidification. Stud Environ Sci 50: 161−174

Hrbacek J, Dvorakova M, Korinek V, Prochazkova L (1961) Demonstration of the effect of fish

stock on the species composition of zooplankton and the intensity of metabolism of the whole

plankton association. Int Ver Theor Angew Limnol Verh 14: 192–195

IBM Corp (2013) IBM SPSS Statistics for Windows, Version 22.0. Amonk, NY: IBM Corp

Janse JH, De Senerpont Domis LN, Scheffer M, Lijklema L, Van Liere L, Klinge M, Mooij WM

(2008) Critical phosphorus loading of different types of shallow lakes and the consequences for

management estimated with the ecosystem model PCLake. Limnologica 38: 203–219

Jeppesen E, Nõges P, Davidson T, Haberman J, Nõges T, Blank K, Lauridsen T, Søndergaard M,

Sayer C, Laugaste R, Johansson L, Bjerring R, Amsinck S (2011) Zooplankton as indicators in

lakes: a scientific−based plea for including zooplankton in the ecological quality assessment of

lakes according to the European Water Framework Directive (WFD). Hydrobiologia 676: 279–297

19

432

433

434

435

436

437

438

439

440

441

442

443

444

445

446

447

448

449

450

451

452

Jeziorski A, Yan ND, Paterson AM, DeSellas AM, Turner MA, Jeffries DS, Keller B, Weeber RC,

McNicol DK, Palmer ME, McIver K, Arseneau K, Ginn BK, Cumming BF, Smol JP (2008) The

widespread threat of calcium decline in fresh waters. Science 322: 1374−1377

Jeziorski A, Keller B, Dyer R, Paterson A, Smol J (2015) Differences among modern−day and

historical cladoceran communities from the “Ring of Fire” lake region in northern Ontario:

Identifying responses to climate warming. Fund Appl Limnol 186: 203− 216

Johnsen GH, Raddum GG (1987) A Morphological study of two populations of Bosmina longispina

exposed to different predation. J Plankton Res 9: 297−304

Johnsen G, Borsheim K (1988) Functional response and food selection of the water flea, Bosmina

longispina. J Plankton Res 10: 319−325

Kaplan MR, Wolfe AP, Miller AP (2002) Holocene environmental variability in southern

Greenland inferred from lake sediments. Quaternary Res 58: 149−159

Korhola A (1999) Distribution patterns of Cladocera in subarctic Fennoscandian lakes and their

potential in environmental reconstruction. Ecography 22: 357−373

Korhola A, Olander H, Blom T (2000) Cladoceran and chironomid assemblages as qualitative

indicators of water depth in subarctic Fennoscandian lakes. J Paleolimnol 24: 43−54

Korhola A, Sorvari S, Rautio M, Appleby PG, Dearing JA, Hu Y, Rose N, Lami A,

Cameron NG (2002) A multi−proxy analysis of climate impacts on the recent development of

subarctic Lake Saanajarvi in Finnish Lapland. J Paleolimnol 28: 59−77

Korhola A, Weckström J (2004) Paleolimnological studies in Arctic Fennoscandia and the Kola

Peninsula (Russia). Pages 381−418 In: Pienitz R, Douglas MSV, Smol JP (eds) Long-term

environmental change in Arctic and Antarctic lakes, Vol 8. Kluwer Academic Publishers, Dordrecht

20

453

454

455

456

457

458

459

460

461

462

463

464

465

466

467

468

469

470

471

472

473

474

Korosi JB, Smol JP (2011) Distribution of cladoceran assemblages across environmental gradients

in Nova Scotia (Canada) lakes. Hydrobiologia 663: 83−99

Korosi JB, Smol JP (2012) A comparison of present−day and pre−industrial cladoceran

assemblages from softwater Nova Scotia (Canada) lakes with different regional acidification

histories. J Paleolimnol 47: 43−54

Korovchinsky NM (2016) Redescription of Bythotrephes arcticus Lilljeborg, 1901

(Crustacea:Cladocera: Onychopoda) and confirmation of an independent species status of the

distant Transcaucasian populations of the genus Bythotrephes Leydig. Zootaxa 4138: 247−270

Korponai J, Varga KA, Lengre T, Papp I, Toth A, Braun M (2011) Paleolimnological

reconstruction of the trophic state in Lake Balaton (Hungary) using Cladocera remains.

Hydrobiologia 676: 237−248

Kurek J, Korosi JB, Jeziorski A, Smol JP (2010) Establishing reliable minimum count sizes for

cladoceran subfossils sampled from lake sediments. J Paleolimnol 44: 603−612

Kuzmina Y, Leshko Y (2002) Hydrobiological effects of gathering reindeer at an arctic lake in

Russia. Rangifer 13: 39−40

Lotter A, Birks H, Hofmann W, Marchetto A (1997) Modern diatom, cladocera, chironomid, and

chrysophyte cyst assemblages as quantitative indicators for the reconstruction of past environmental

conditions in the Alps. 1. Climate. J Paleolimnol 18: 395−420

Louette G, Declerc S, Vandekerkhove J, De Meester J (2009) Evalution of restoration measures in a

shallow lake through a comparison of present day zooplankton communities with historical

samples. Restor Ecol 17: 629−640

21

475

476

477

478

479

480

481

482

483

484

485

486

487

488

489

490

491

492

493

494

495

Luoto T, Nevalainen PL, Sarmaja−Korjonen K (2013) Zooplankton (Cladocera) in assessments of

biologic integrity and reference conditions: Appliance of sedimentary assemblages from shallow

boreal lakes. Hydrobiologia 707: 173−185

Manca M, Torretta B, Comoli P, Amsinck SL, Jeppesen E (2007) Major changes in trophic

dynamics in large, deep sub−alpine Lake Maggiore from 1940s to 2002: a high resolution

comparative palaeo−neolimnological study. Freshwater Biol 52: 2256−2269

Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer

Res 27: 209−220

Michelutti N, Laing TE, Smol JP (2001) Diatom assessment of past environmental changes in lakes

located near the Noril’sk (Siberia) smelters. Water Air Soil Poll 125: 231−241

Michelutti N, Wolfe AP, Vinebrooke RD, Rivard B, Briner JP (2005) Recent primary production

increases in arctic lakes. Geophys Res Lett 32: L19715

Milardi M, Siitonen S, Lappalainen J, Liljendahl A, Weckström J (2016) The impact of trout

introductions on macro− and microinvertebrate communities in fishless boreal lakes. J Paleolimnol

55: 273−287

Nesje A, Dahl SO (2001) The Greenland 8200 calendar years BP event detected in loss-on-ignition

profiles of Norwegian lacustrine sediment sequences. J Quaternary Sci 16: 155−166

Nevalainen L, Luoto TP (2012) Faunal (Chironomidae: Cladocera) responses to post−Little Ice Age

climate warming in the high Austrian Alps. J Paleolimnol 48: 711−724

O'Reilly CM, Sharma S, Gray DK, Hampton SE, Read JS, Rowley RJ, Schneider P, Lenters JD,

McIntyre PB, Kraemer BM, et al. (2015) Rapid and highly variable warming of lake surface waters

around the globe. Geophys Res Lett 42: 10773–10781

22

496

497

498

499

500

501

502

503

504

505

506

507

508

509

510

511

512

513

514

515

516

517

Paatero J, Dauvalter V, Derome J, Lehto J, Pasanen J, Vesala T, Miettinen J, Makkonen U, Kyrö E,

Jernström J, Isaeva L, Derome K (2008) Effects of Kola air pollution on the environment in the

western part of the Kola Peninsula and Finnish Lapland − Finnish Meteorological Institute Reports

2008/6 Helsinki

Pace ML, Carpenter SR, Johnson RA, Kurtzweil JT (2013) Zooplankton provide early warning of a

regime shift in a whole lake manipulation. Limnol Oceanogr 58: 525− 532

Persson L (1986) Effects if reduced interspecific competition on resource utilization in Perch

(Perca fluviatilis). Ecology 67: 355−364

Rautio M (2001) Zooplankton assemblages related to environmental characteristics in treeline

ponds in Finnish Lapland. Arct Antarct Alp Res 33: 289−298

Rautio M, Mariash H, Forsström L (2011) Seasonal shifts between autochthonous and

allochthonous carbon contributions to zooplankton diets in a subarctic lake. Limnol Oceanogr 56:

1513−1524

Rawcliffe R, Sayer CD, Woodward G, Grey J, Davidson TA, Jones JI (2010) Back to the future:

using palaeolimnology to infer long−term changes in shallow lake food webs. Freshwater Biol 55:

600−613

Rühland K, Priesnitz A, Smol J (2003) Paleolimnological evidence from diatoms for recent

environmental changes in 50 lakes across Canadian arctic treeline. Arct Antarct Alp Res 35:

110−123

Rühling Å, Steinnes E (2002) Heavy metals in surface soil in Fennoscandia. NORD 2002/4 Nordic

Council of Ministers, Copenhagen

23

518

519

520

521

522

523

524

525

526

527

528

529

530

531

532

533

534

535

536

537

538

Sarmaja−Korjonen K, Alhonen P (1999) Cladoceran and diatom evidence of lake−level fluctuations

from a Finnish lake and the effect of aquatic− moss layers on microfossil assemblages. J

Paleolimnol 22: 277−290

Sarmaja−Korjonen K, Nyman M, Kultti S, Väliranta M (2006) Palaeolimnological development of

Lake Njargajavri, northern Finnish Lapland, in a changing Holocene climate and environment. J

Paleolimnol 35: 65−81

Seppovaara O (1969) Nieriä (Salvelinus alpinus L.) ja sen kalataloudellinen merkitys suomessa.

Suomen Kalatalous 37. Maataloushallitus, Helsinki

Shutner BJ, Schlesinger DA, Zimmerman AP (1983) Empirical predictors of annual surface water

temperature cycles in North American lakes. Can J Fish Aquat Sci 40: 1838−1845

Siitonen S (2005) Vesikirput kahden Kilpisjärven alueen järven viimeaikaisen kehityksen

kuvaajina. MSc thesis. University of Helsinki, Helsinki

Siitonen S, Väliranta M, Weckström J, Juutinen S, Korhola A (2011) Comparison of Cladocera-

based water-depth reconstruction against other types of proxy data in Finnish Lapland.

Hydrobiologia 676: 155−172

Simon M, Wünch C (1998) Temperature control of bacterioplankton growth in a temperate lake.

Aquat Microb Ecol 16:119−130

Sinev AY (2009) Discrimination between two sibling species of Acroperus (Baird, 1843) from the

Palearctic (Cladocera: Anomopoda: Chydoridae). Zootaxa 2176: 1−21

Sinev AY, Dumont HJ (2016) Revision of the costata-group of Alona s. lato (Cladocera:

Anomopoda: Chydoridae) confirms its generic status. Europ J Taxon 223: 1−38

24

539

540

541

542

543

544

545

546

547

548

549

550

551

552

553

554

555

556

557

558

559

Smol JP (1992) Paleolimnology: an important tool for effective ecosystem management. Journal of

Aquatic Ecosystem Health 1: 49−58

Smol J, Wolfe A, Birks H, Douglas M, Jones V, Korhola A, Pienitz R, Ruhland K, Sorvari S,

Antoniades D, Brooks S, Fallu M, Hughes M, Keatley B, Laing T, Michelutti N, Nazarova L,

Nyman M, Paterson A, Perren B, Quinlan R, Rautio M, Saulnier−Talbot E, Siitonen S, Solovieva

N, Weckström J (2005) Climate−driven regime shifts in the biological communities of arctic lakes.

Proc Natl Acad Sci Usa 102: 4397−4402

Sorvari S, Korhola A (1998) Recent diatom assemblage changes in subarctic Lake Saanajärvi NW

Finnish Lapland, and their paleoenvironmental implications. J Paleolimnol 20: 205−215

Sorvari S, Korhola A, Thompson R (2002) Lake diatom response to recent Arctic warming in

Finnish Lapland. Global Change Biol 8: 171−181

Sprules WG, Carter JCH, Ramcharan CW (1984) Phenotypic associations in the Bosminidae

(Cladocera): Zoogeographic patterns. Limnol Oceanogr 29: 161−169

Stenson JAE (1976) Significance of predator influences on composition of Bosmina spp.

populations. Limnol Oceanogr 21: 814−822

Sweetman JN, LaFace E, Ruhland KM, Smol JP (2008) Evaluating the response of Cladocera to

recent environmental changes in lakes from the central Canadian Arctic treeline region. Arct

Antarct Alp Res 40: 584−591

Sweetman JN, Ruhland KM, Smol JP (2010) Environmental and spatial factors influencing the

distribution of cladocerans in lakes across the central Canadian Arctic treeline region. J Limnol 69:

76−87

Szeroczyńska K, Sarmaja−Korjonen K (2007) Atlas of subfossil cladocera from central and

northern Europe. Friends of the Lower Vistula society, Warzaw

25

560

561

562

563

564

565

566

567

568

569

570

571

572

573

574

575

576

577

578

579

580

581

582

Säisä M, Rönn J, Aho T, Björklund M, Pasanen P, Koljonen M-L (2008) Genetic differentiation

among European whitefish ecotypes based on microsatellite data. Hereditas 145: 69−83

Tammi J, Appelberg M, Beier U, Hesthagen T, Lappalainen A, Rask M (2003) Fish status survey of

Nordic Lakes: Effects of acidification, eutrophication and stocking activity on present fish species

composition. Ambio 32: 98−105

ter Braak CJF, Šmilauer P (2007-2012) Canoco reference manual and user’s guide: Software for

623 ordination version 50 Microcomputer power, Itaca

Tolonen A (1997) Size-specific food selection and growth in benthic whitefish (Coregonus

lavaretus (L.), in a subarctic lake. Boreal Environ Res 2: 387−399

Van Damme K, Dumont HJ (2008) Further division of Alona Baird, 1843: separation and position

of Coronatella Dybowski & Grochowski and Ovalona gen. n. (Crustacea: Cladocera). Zootaxa

1960: 1−44

van Oldenborgh GJ (1999) Koninklijk Nederlands Meteorologisch Instituut (KNMI). KNMI

Climate Explorer http://climexpknminl/ (accessed 1 December 2015)

Weckström J, Korhola A, Blom T (1997) The relationship between diatoms and water temperature

in thirty subarctic Fennoscandian lakes. Arct Antarct Alp Res 29: 75−92

Weckström J, Korhola A (2001) Patterns in the distribution, composition and diversity of diatom

assemblages in relation to ecoclimatic factors in Arctic Lapland. J Biogeogr 28: 31−45

Weckström J, Snyder JA, Korhola A, Laing TE, MacDonald GM (2003) Diatom inferred acidity

history of 32 lakes on the Kola Peninsula, Russia. Water Air Soil Poll 149: 339−361

Weckström J, Hanhijärvi ST, Forsström L, Kuusisto E, Korhola A (2014) Reconstructing lake ice

26

583

584

585

586

587

588

589

590

591

592

593

594

595

596

597

598

599

600

601

602

603

cover in subarctic lakes using a diatom- based inference model. Geophys Res Lett 41: 2026−2032

Wetzel RG (1992) Clean water: a fading resource. Hydrobiologia 243/244: 21−30

Wilcoxon F (1945) Individual comparisons by ranking methods. Biometrics Bull 1: 80−83

Willemse NW, Törnquist TE (1999) Holocene century-scale temperature variability from west

Greenland lake records. Geology 27: 580−584

Tables

Table 1 Summary of environmental variables of the studied lakes. Coordinates are in WGS84 coordinate system, Area

= lake area, LOI = loss on ignition, depth = maximum water depth, Airtemp = average July air temperature, Ptot = total

phosphorus and Ntot = total nitrogen in water samples. Lakes are presented in ascending altitudinal order. A more

comprehensive list of environmental variables (including lake perimeter, catchment area, distance to tree line,

alkalinity, concentrations of K, Ca, Na, Mg, TOC, NH4-N, PO4-P, Cl, NO23N, SiO2, turbidity, SO4 and CNR) is

available as supplementary data (Online Resource 1)

LakeLatitude

(N)Longitude

(E)Altitude (m.a.s.l)

Area (ha)

LOI (%)

Depth (m)

Airtemp (°C)

pHConductivity (mS/cm-1)

Ptot (µg/L-1)

Ntot

(µg/L-1)

25 69.070 20.880 930.9 1.69 41.4 3.35 8.50 6.24 0.60 4.00 120.00

62 69.240 21.507 897.0 6.03 24.8 9.50 8.60 6.93 2.60 1.50 69.00

58 69.266 21.189 895.0 1.15 14.16 3.50 9.60 6.99 1.80 4.00 110.00

54 69.030 21.125 796.4 9.33 33.6 8.00 9.20 6.80 1.40 1.50 110.00

49 69.080 20.670 776.3 16.10 16.9 12.10 9.40 6.69 0.90 1.50 54.00

55 69.056 21.047 774.0 20.44 34.04 2.00 9.30 6.98 2.00 1.50 140.00

63 69.191 21.454 704.3 100.35 14.3 21.50 9.70 7.59 4.70 4.00 77.00

18 68.920 20.970 526.0 3.85 55.0 1.45 10.80 7.13 3.40 5.00 270.00

48 68.700 21.500 487.9 28.04 35.1 12.60 11.20 7.09 2.30 5.00 150.00

21 68.700 21.480 480.6 18.01 28.1 25.00 11.30 7.15 3.40 1.50 130.00

17 68.900 21.070 463.0 6.05 48.3 1.70 11.30 6.90 2.50 3.00 240.00

20 68.850 21.200 449.1 115.18 28.7 5.15 11.30 6.98 2.40 1.50 200.00

26 69.180 20.720 355.0 7.21 59.6 3.40 11.10 6.97 3.40 4.00 290.00

15 68.480 22.170 346.0 12.89 68.1 1.75 12.20 7.12 2.90 1.50 360.00

31 68.470 22.970 344.0 2.22 63.0 5.30 12.30 7.06 3.00 4.00 230.00

27

604

605

606

607

608

609

610611612613614615

12 68.420 22.580 332.0 1.97 80.8 1.85 12.40 4.89 3.40 7.00 390.00

34 68.470 22.470 329.1 11.76 47.9 4.05 12.30 7.06 2.30 8.00 330.00

13 68.470 22.430 322.0 2.55 60.4 4.00 12.50 6.49 1.00 6.00 320.00

32 68.420 22.900 319.0 28.18 42.3 6.00 12.60 7.05 3.20 12.00 320.00

10 68.400 22.880 317.0 2.58 49.4 6.30 12.60 6.21 0.40 6.00 200.00

11 68.400 22.850 313.0 2.18 58.6 4.10 12.60 6.82 1.10 7.00 360.00

8 68.300 23.220 294.0 33.99 37.3 6.95 12.80 6.76 1.80 14.00 330.00

9 68.330 22.950 290.0 2.62 63.6 1.75 12.10 6.60 1.80 46.00 560.00

3 67.850 24.180 268.0 7.14 64.1 4.00 13.30 6.19 1.10 7.00 330.00

7 68.200 23.180 263.0 0.90 61.2 4.40 13.00 6.55 1.20 9.00 390.00

4 67.980 23.680 262.0 10.67 71.8 3.30 13.10 5.29 0.70 1.50 330.00

28 67.880 23.870 254.0 18.80 35.7 1.45 13.30 6.92 3.00 25.00 480.00

30 68.130 23.370 253.0 1.33 83.6 4.30 13.20 5.69 0.50 12.00 640.00

6 68.120 23.370 252.0 1.52 88.0 4.30 13.10 5.29 0.50 8.00 460.00

5 68.010 23.400 249.0 4.34 50.1 3.35 13.20 6.76 2.10 38.00 1500.00

29 68.100 23.420 249.0 4.01 42.3 9.60 13.20 6.78 5.10 14.00 190.00

2 67.820 24.870 197.5 2.90 84.5 6.30 13.80 6.12 0.70 3.00 260.00

Mean

    437.2 15.2 49.6 6.0 11.7 6.6 2.1 8.3 310.6

Table 2 Modern cladoceran taxa in lakes located in bare tundra, mountain birch woodland and coniferous forest –

vegetated catchment areas. The numbers preceding parentheses are average % of given species in all lakes situated in a

catchment vegetation type. Numbers within the parentheses indicate the number of lakes where the species was

detected. In the catchment vegetation type column the numbers indicate the total number of lakes in the ecotone

Barren

tundra (7)

Mountain

birch (8)

Coniferous

forest (17)

B. (Eubosmina) spp. 40.2 % (7) 39.9 % (8) 35.3 % (17)

Chydorus spp. 11.4 % (7) 4.0 % (8) 6.2 % (17)

Alonella nana 11.5 % (4) 17.1 % (8) 19.2 % (17)

Acroperus spp. 10.7 % (7) 3.1 % (7) 5.3 % (12)

28

616

617618619620

621

Alona affinis 0.1 % (1) 16.8 % (8) 16.7 % (17)

Eurycercus spp. 3.0 % (4) 4.5 % (8) 1.4 % (12)

Alonella excisa 1.6 % (3) 3.3 % (7) 1.1 % (9)

Alonopsis elongata 2.8 % (5) 0.8 % (5) 0.4 % (8)

Daphnia spp. 4.6 % (4) 0.6 % (3) 4.1 % (6)

Alona intermedia 2.3 % (5) 1.0 % (5) 0.4 % (8)

Ophryoxus gracilis 0.4 % (1) 1.2 % (4) 0.3 % (6)

Polyphemus pediculus 5.0 % (5) 3.0 % (8) 2.1 % (9)

Alona quadrangularis 3.0 % (2) 0.5 % (1) 0.8 % (5)

small Alona spp. 2.0 % (4) 0.7 % (3) 0.7 % (9)

Ceriodaphnia spp. 0.6 % (1) - 0.8 % (7)

Rhyncotalona falcata - 0.2 % (2) 0.1 % (2)

Flavalona rustica - 0.4 % (4) 0.9 % (7)

Sida crystallina - 0.4 % (4) 1.1 % (6)

Unapertura latens - 0.1 % (1) 0.2 % (4)

Camptocercus restricostris - 0.1 % (1) 0.1 % (2)

Graptoleberis testidunaria - 0.1 % (1) 0.4 % (4)

Coronatella rectangula - 0.1 % (1) 0.3 % (4)

Flavalona costata - 0.1 % (1) 0.1 % (1)

Alona guttata - 0.1 % (1) 0.1 % (2)

Paralona pigra - 0.1 % (1) 0.1 % (2)

Latona setifera - 0.1 % (1) 0.2 % (3)

Bythotrephes arcticus - 0.1 % (1) 0.1 % (1)

Ilyocryptus spp. - 0.1 % (1) -

Pleuroxus spp. - 0.1 % (1) -

Pleuroxus laevis - - 0.1 % (2)

Drepanothrix dentata - - 0.1 % (4)

Alonella exigua - - 0.1 % (1)

Number of taxa 15 28 30

Table 3 Summary of the results of variance partitioning for the screened 10 environmental variables

29

622

623

Figure captions

Fig. 1 a Location of the study lakes and weather stations, lake altitudes, air temperatures, catchment

vegetation types and regional temperature and precipitation trends. Circles represent lake locations

and triangles represent the locations of the weather stations. b Lake altitude, average July air

temperature and catchment type (1 coniferous forest, 2 mountain birch and 3 bare tundra). Lakes are

ordered based on latitude (low latitude at the bottom) for easy interpretation of the ecoclimatic

gradient. c Average annual temperatures and average daily precipitation subtracted from 1959-2014

(Kilpisjärvi and Muonio) and 1961-2011 (Karesuando) average

Fig. 2 Redundancy analysis (RDA) correlation biplots for modern (s) and pre-industrial (b)

cladoceran samples and 10 pre-screened environmental variables. Open circles represent

catchments dominated by coniferous forest, grey circles represent catchments dominated by

mountain birch woodland, and closed circles represent barren tundra catchments

Fig. 3 Arrows indicating differences between pre-industrial and modern samples in a coniferous

forest catchment, b mountain birch catchment and c barren tundra catchment. The arrows point

30

  Variance explained p= Covariation p= Unique

contribution Unexplained

Mire area 5.8 0.08 54 0.94 1 45LOI 20.1 0.001 48 0.002 7 45Sample Depth 14.0 0.001 51.4 0.11 3.6 45Air Temperature 10.8 0.001 52.3 0.28 2.7 45pH 11.2 0.003 52.1 0.23 2.9 45Conductivity 7.0 0.03 51.1 0.06 3.9 45Calsium 8.0 0.01 52.2 0.24 2.8 45TOC 14.2 0.003 51.3 0.08 3.7 45Ptot 3.4 0.36 53.4 0.67 1.6 45Ntot 6.8 0.04 51.4 0.11 3.6 45

624

625

626

627

628

629

630

631

632

633

634

635

636

637

638

639

640

641

642

643

644

645

646

from the pre-industrial towards the present sample reflecting the calculated change in cladoceran

community as a function of time. The explanation power and direction of change of the

environmental variables used in the analysis are presented in figure 2

Fig. 4 Stratigraphic diagram of differences in abundance regarding the 10 most common cladoceran

species detected in pre-industrial and modern samples and modern lake catchment vegetation types

(coniferous forest 1, mountain birch 2 and barren tundra 3), species richness and dissimilarity

values. Faunal change is presented as % abundances. Lakes are in altitudinal order (lowest elevation

at the bottom)

Figures

31

647

648

649

650

651

652

653

654

655

656

657

32

658

659

33

660