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Classifying aquatic macrophytes as indicators of eutrophication in European lakes

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Abstract

Aquatic macrophytes are one of the biological quality elements in the Water Framework Directive (WFD) for which status assessments must be defined. We tested two methods to classify macrophyte species and their response to eutrophication pressure: one based on percentiles of occurrence along a phosphorous gradient and another based on trophic ranking of species using Canonical Correspondence Analyses in the ranking procedure. The methods were tested at Europe-wide, regional and national scale as well as by alkalinity category, using 1,147 lakes from 12 European states. The grouping of species as sensitive, tolerant or indifferent to eutrophication was evaluated for some taxa, such as the sensitive Chara spp. and the large isoetids, by analysing the (non-linear) response curve along a phosphorous gradient. These thresholds revealed in these response curves can be used to set boundaries among different ecological status classes. In total 48 taxa out of 114 taxa were classified identically regardless of dataset or classification method. These taxa can be considered the most consistent and reliable indicators of sensitivity or tolerance to eutrophication at European scale. Although the general response of well known indicator species seems to hold, there are many species that were evaluated differently according to the database selection and classification methods. This hampers a Europe-wide comparison of classified species lists as used for the status assessment within the WFD implementation process.

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Acknowledgements

REBECCA was funded by the European Commission under the 6th Framework Program, Contract No.: SSP1-CT-2003-502158—REBECCA. The authors thank all intercalibration representatives who contributed to the realisation of the database and the formulation of ideas and concepts during discussions in REBECCA and GIG meetings, specifically Laszlo Tóth (JRC) and Deirdre Tierney (EPA, Ireland). We are grateful to those who supplied data to the REBECCA dataset of European macrophyte data: Heikki Toivonen (SYKE, Finland); Tapio Rintanen (Finland); Helle Mäemets (Centre for Limnology, Estonia), Luc DeNeijs (Institute of Nature Conservation, Belgium); Vaida Olsauskyte (Lithuanian Environmental Protection Agency, Lithuania); Hanna Soszka (Institute of Environmental Protection, Poland); Arie Naber (Institute for Inland Water Management and Waste Water Treatment, the Netherlands). Gary Free (EPA, Ireland) and Eddy Lammens (Institute for Inland Water Management and Waste Water Treatment, the Netherlands) provided valuable comments on earlier versions of this manuscript.

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Correspondence to W. Ellis Penning.

Appendix

Appendix

List of species per species group included in REBECCA macrophyte study, with results of classifications. Column headings ‘P’ and ‘L’ represent methods based on percentiles or on LEAFPACS, respectively, and ‘n’ is the number of lakes in which a species occurred

 

Species

All

N-GIG

C-GIG

CH

CL

NH

NL

Norway

Finland

Latvia

P

n

P

n

P

n

P

L

n

P

L

n

P

L

n

P

L

n

P

n

P

n

P

n

I

Baldellia ranunculoides

o

8

+

5

 

1

     

1

+

+

4

  

1

      

I

Crassula aquatica

o

24

o

24

           

o

+

24

8

o

8

  

I

Elatine hexandra

20

o

8

5

  

1

+

+

4

   

o

+

8

 

3

    

I

Elatine hydropiper

131

128

 

1

  

1

      

+

124

o

13

74

  

I

Elatine orthosperma

 

3

 

3

             

3

 

3

    

I

Elatine triandra

o

57

o

57

           

+

+

56

+

5

o

41

  

I

Eleocharis acicularis

394

372

18

11

7

+

+

31

328

56

189

9

I

Eriocaulon aquaticum

20

 

1

             

1

      

I

Isoetes echinospora

380

378

          

2

365

101

186

  

I

Isoetes lacustris

487

424

13

  

2

11

  

3

405

117

197

7

I

Limosella aquatica

23

o

23

          

1

22

11

o

4

  

I

Littorella uniflora

207

130

16

− −

7

9

+

+

12

118

55

16

  

I

Lobelia dortmanna

292

260

4

   

4

+

6

251

81

102

  

I

Lythrum portula

o

13

12

 

1

     

1

  

1

o

+

11

o

7

    

I

Ranunculus reptans

462

462

        

+

21

419

88

256

  

I

Subularia aquatica

323

319

 

3

     

3

  

2

302

75

157

  

E

Callitriche cophocarpa

o

25

+

25

          

3

+

+

21

+

9

+

14

  

E

Callitriche hamulata

93

78

o

5

  

1

4

  

2

76

63

 

1

  

E

Callitriche hermaphroditica

o

101

79

o

13

o

8

+

+

5

+

19

+

58

27

24

  

E

Callitriche palustris

o

224

223

 

1

  

1

   

o

4

210

46

o

112

  

E

Callitriche stagnalis

o

15

o

8

o

5

  

3

  

2

   

o

+

8

o

6

    

E

Ceratophyllum demersum

+

184

+

90

+

87

+

+

83

+

+

4

+

+

33

+

+

53

+

17

o

30

+

61

E

Elodea canadensis

o

237

o

107

o

78

o

60

+

+

18

+

+

30

+

75

o

23

o

39

o

49

E

Elodea nuttallii

+

20

 

2

+

15

+

+

14

  

1

     

2

      

E

Hydrilla verticillata

 

2

   

2

  

2

              

2

E

Myriophyllum alterniflorum

482

419

24

− −

11

13

o

− −

22

387

115

185

12

E

Myriophyllum sibiricum

45

45

        

6

+

37

15

30

  

E

Myriophyllum spicatum

+

184

+

68

o

90

o

+

79

o

+

11

+

+

44

+

+

24

+

9

  

o

56

E

Myriophyllum verticillatum

+

79

+

53

+

26

+

+

24

  

2

+

+

13

+

+

38

+

5

+

28

+

16

E

Najas flexilis

o

11

+

7

          

3

+

+

4

 

2

 

1

  

E

Najas marina

+

24

  

+

24

+

24

               

E

Najas tenuissima

3

 

3

             

3

   

3

  

E

Potamogeton acutifolius

 

2

   

2

  

2

               

E

Potamogeton alpinus

311

296

8

  

3

5

− −

29

+

255

o

90

o

144

  

E

Potamogeton berchtoldii

322

o

284

8

  

2

o

+

6

+

27

+

245

o

83

138

  

E

Potamogeton compressus

o

83

o

65

+

18

o

+

18

   

+

+

12

o

+

51

 

2

30

o

6

E

Potamogeton crispus

+

94

+

52

o

31

+

+

28

  

3

+

+

24

o

+

28

+

7

 

4

+

5

E

Potamogeton filiformis

82

63

11

− −

9

  

2

30

33

38

11

  

E

Potamogeton friesii

o

61

o

45

o

14

o

14

   

+

+

36

+

9

+

21

   

2

E

Potamogeton gramineus

317

285

20

o

11

9

o

33

+

245

66

128

+

8

E

Potamogeton lucens

o

181

+

64

o

93

o

84

+

+

9

+

+

37

+

26

+

11

5

o

74

E

Potamogeton obtusifolius

o

177

+

151

+

11

+

+

7

+

+

4

+

+

28

+

+

120

+

30

+

55

 

1

E

Potamogeton pectinatus

+

128

+

45

+

71

+

+

68

  

3

+

+

30

o

+

15

+

10

 

1

o

9

E

Potamogeton perfoliatus

o

627

470

o

115

o

99

o

+

16

o

56

+

394

o

73

239

75

E

Potamogeton polygonifolius

23

18

 

1

  

1

     

 

− −

18

16

    

E

Potamogeton praelongus

224

199

22

16

o

+

6

o

43

+

153

47

62

18

E

Potamogeton pusillus

+

56

o

19

+

30

+

+

29

  

1

+

+

7

+

12

+

4

+

6

  

E

Potamogeton rutilus

o

23

o

17

o

5

  

3

  

2

+

+

5

o

+

12

+

9

+

4

 

1

E

Potamogeton trichoides

+

10

  

+

10

+

+

10

               

E

Potamogeton vaginatus

 

2

 

2

          

1

  

1

 

1

 

1

  

E

Potamogeton gramineus × perfoliatus

o

39

o

31

o

6

o

4

  

2

+

14

+

17

12

   

1

E

Potamogeton gramineus × natans

4

4

           

4

 

3

    

E

Potamogeton filiformis × pectinatus

 

3

 

3

          

2

  

1

 

3

 

 

 

 

E

Potamogeton gramineus × lucens

25

24

        

10

+

14

 

3

    

E

Ranunculus aquatilis

o

58

o

25

31

29

  

2

+

+

10

+

15

o

12

  

24

E

Ranunculus baudoti

 

3

   

2

  

2

               

E

Ranunculus circinatus

+

36

+

25

+

10

+

+

9

  

1

+

+

20

+

+

5

      

E

Ranunculus confervoides

43

43

        

− −

9

34

32

4

  

E

Ranunculus peltatus

249

249

        

+

18

222

29

133

  

E

Ranunculus penicillatus

 

1

                      

E

Utricularia australis

7

7

           

+

7

  

7

  

E

Utricularia intermedia

130

127

        

7

114

38

o

57

  

E

Utricularia minor

85

83

 

1

     

1

4

77

50

o

24

 

1

E

Utricularia ochroleuca

30

30

           

− −

30

27

 

3

  

E

Utricularia vulgaris

o

418

364

o

38

o

34

o

+

4

+

41

+

308

53

o

173

25

E

Zannichellia palustris

+

36

+

15

+

20

+

+

17

  

3

+

+

8

+

+

7

 

2

    

N

Nuphar lutea

o

766

o

572

o

154

o

122

+

+

32

+

+

73

+

473

o

111

o

248

+

118

N

Nuphar pumila

o

206

178

o

25

o

14

+

+

11

  

3

+

165

19

o

117

+

24

N

Nuphar lutea × pumila

174

172

 

2

  

1

  

1

   

154

  

134

  

N

Nymphaea alba

o

454

o

416

o

26

o

+

22

o

+

4

56

+

350

o

109

o

163

11

N

Nymphaea candida × tetragona

 

2

 

2

             

2

   

2

  

N

Nymphaea candida

o

86

o

30

o

56

o

+

46

+

+

10

  

3

+

27

    

50

N

Nymphaea tetragona

o

24

o

24

           

o

+

23

  

o

24

  

N

Nymphaea alba × candida

 

3

   

3

  

3

               

N

Nymphoides peltata

+

4

  

+

4

+

+

4

     

 

  

 

 

 

 

 

 

 

N

Persicaria amphibia

o

208

o

184

13

8

+

+

5

+

+

43

o

+

140

o

35

o

63

 

 

N

Potamogeton natans

o

669

o

513

129

o

102

+

+

27

83

o

+

422

o

133

o

189

o

107

N

Sagittaria natans

o

68

o

68

          

 

o

+

66

 

 

o

53

 

 

N

Sagittaria sagittifolia × natans

+

8

+

8

          

 

+

+

7

 

 

+

8

 

 

N

Sparganium angustifolium

396

388

 

2

     

2

− −

15

348

147

196

 

 

N

Sparganium gramineum

o

205

o

205

          

2

o

+

201

 

1

o

138

 

 

N

Sparganium hyperboreum

27

27

          

1

− −

26

20

6

 

 

N

Sparganium natans

o

99

o

97

        

5

o

+

88

12

o

54

 

 

N

Sparganium angustifolium × gramineum

21

21

        

 

 

 

+

21

 

 

 

2

 

 

L

Hydrocharis morsus-ranae

+

120

+

76

+

44

+

+

37

+

+

7

+

+

25

+

+

48

 

 

+

30

+

25

L

Lemna gibba

+

7

 

2

o

5

o

+

5

     

1

  

1

 

 

 

 

 

1

L

Lemna minor

+

264

+

215

+

47

+

+

42

+

+

5

+

+

53

+

+

158

+

56

+

81

+

18

L

Lemna trisulca

+

146

+

78

+

36

+

+

33

  

3

+

+

26

+

+

51

+

4

+

23

o

14

L

Salvinia natans

+

7

  

+

7

+

+

7

     

 

  

 

 

 

 

 

 

 

L

Spirodela polyrhiza

+

84

+

58

+

26

+

+

24

  

2

+

+

22

+

+

34

+

13

+

19

+

9

L

Stratiotes aloides

+

60

+

56

+

4

+

+

4

   

+

+

26

o

+

28

 

 

o

13

 

 

L

Trapa natans

+

5

  

+

5

+

+

4

  

1

 

 

 

 

 

 

 

 

 

 

 

2

C

Chara aspera

o

76

o

49

23

− −

21

  

2

o

28

+

20

o

12

11

 

3

C

Chara connivens

+

15

  

15

− −

15

     

 

  

 

 

 

 

 

 

 

C

Chara contraria

o

47

o

22

25

− −

24

  

1

o

16

o

+

6

5

 

 

5

C

Chara delicatula

15

12

 

3

  

3

   

9

  

3

10

 

 

 

 

C

Chara filiformis

 

2

 

1

 

1

  

1

     

1

  

 

 

 

 

 

 

 

C

Chara fragilis

o

10

o

10

          

1

o

+

9

 

 

o

6

 

 

C

Chara globularis

o

135

97

33

26

+

7

o

30

+

63

40

25

 

 

C

Chara hispida

o

22

o

7

14

− −

14

   

o

4

  

3

 

 

 

 

4

C

Chara intermedia

 

2

 

1

 

1

  

1

     

1

  

 

 

1

 

 

 

1

C

Chara rudis

o

20

15

5

− −

5

   

14

  

1

11

 

 

 

2

C

Chara strigosa

7

6

 

1

  

1

     

3

  

3

6

 

 

 

 

C

Chara tomentosa

o

24

+

10

o

14

o

− −

14

   

9

  

1

+

4

 

 

o

9

C

Chara vulgaris

o

12

  

10

10

     

 

  

 

 

 

 

 

 

2

C

Nitella confervacea

 

2

 

2

          

 

  

2

 

1

 

1

 

 

C

Nitella flexilis

o

48

29

o

10

+

6

+

4

  

 

+

27

 

 

25

 

 

C

Nitella mucronata

o

8

 

2

+

6

o

+

6

     

 

  

2

 

2

 

 

 

 

C

Nitella opaca

142

132

o

6

  

3

  

3

o

6

121

67

51

 

 

C

Nitella translucens

 

3

 

2

 

1

     

1

  

 

  

2

 

 

 

 

 

 

C

Nitella wahlbergiana

 

3

 

3

          

 

  

3

 

 

 

2

 

 

C

Nitellopsis obtuse

+

41

 

1

+

40

+

+

40

     

1

  

 

 

 

 

 

o

10

C

Tolypella canadensis

5

5

          

 

− −

5

5

 

 

 

 

C

Tolypella glomerata

 

3

   

2

  

2

   

 

 

 

 

 

 

 

 

 

 

 

 

  1. Classifications in the percentiles method are Sensitive (−), Tolerant (+) and Indifferent (o). LEAFPACS classifications are positive responder (+), negative responder (−), or strongly negative responder (− −).C = Central GIG, N = Northern GIG, H = High alkalinity, L = Low-moderate alkalinity. Species groups: I—isoetids, E—elodeids, N—nymphaeids, L—lemnids, C—charids

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Penning, W.E., Mjelde, M., Dudley, B. et al. Classifying aquatic macrophytes as indicators of eutrophication in European lakes. Aquat Ecol 42, 237–251 (2008). https://doi.org/10.1007/s10452-008-9182-y

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