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Hydrobiologia

, Volume 773, Issue 1, pp 177–191 | Cite as

Sharp differences in the δ13C values of organic matter and carbonate encrustations but not in ambient water DIC between two morphologically distinct charophytes

  • E. ProninEmail author
  • M. Pełechaty
  • K. Apolinarska
  • A. Pukacz
  • M. Frankowski
Open Access
Primary Research Paper

Abstract

The stable carbon isotope composition of the carbonate encrustations (δ13CCARB), organic matter (δ13CORG) and the dissolved inorganic carbon (δ13CDIC) in the ambient lake waters were analysed for two common but morphologically different and, thus, representing different growth forms of Chara species. We hypothesized that the relationships between δ13CCARB, δ13CORG and δ13CDIC are species specific and related to the different growth forms of the studied charophytes. For each species (Chara tomentosa and Chara globularis), 10 individuals and water samples from above the macrophytes were collected in five lakes at three sites per lake in mid-summer. Opposing shifts were found between δ13CCARB and δ13CDIC values with 13C enrichment in C. tomentosa and 13C depletion in C. globularis. In addition, C. globularis exhibited more negative values of δ13CORG than C. tomentosa, even under similar conditions. The δ13CCARB and δ13CORG values were positively correlated in both species, but δ13CCARB and δ13CDIC as well as δ13CORG and δ13CDIC were positively correlated in C. tomentosa only. The differences found result from the different proportions between 13C and 12C in DIC used as a CO2 source for photosynthesis, which is linked to the different growth forms represented by the two studied charophytes and, thus, are species specific as we hypothesized.

Keywords

Stable isotopes Characeae Organic matter Carbonate Encrustation 

Introduction

Charophytes (Charales; Charophyta) are aquatic macroscopic green algae of the family Characeae, whose members are distributed around the world and are found in various types of aquatic environments, including brackish and freshwaters, standing and floating water, and permanent and ephemeral waters (e.g., Hutchinson, 1975; Wade, 1990). However, charophytes prefer freshwater lakes, where they grow along a wide depth gradient depending on light availability (e.g., Martin et al., 2003). Charophytes can significantly modify the conditions of their environments, influencing both abiotic (e.g., pH, hardness, O2 concentration and water clarity) and biological (e.g., the structure of plankton community) components of aquatic ecosystems, particularly when they form dense and extensive meadows (Kufel & Kufel, 2002; Pentecost et al., 2006; Apolinarska et al., 2011; Pełechaty et al., 2013). The precipitation of CaCO3 as encrustations on the thalli surface, a feature typical of these macroalgae, results from photosynthetic CO2 assimilation from soluble bicarbonates (McConnaughey, 1998). According to different authors, the amount of CaCO3 on encrusted charophyte species may range from approximately 30% to over 80% of their dry mass (e.g., Pentecost, 1984; Krolikowska, 1997; Kufel & Kufel, 2002; Pełechaty et al., 2010; Urbaniak, 2010; Pełechaty et al., 2013). Thus, dense and extensive charophyte meadows contribute significantly to calcium carbonate precipitation and the deposition of lake marl sediments (Pełechaty et al., 2013).

The presence of carbonate encrustations promotes the preservation of charophyte remains in sediments and sedimentary rocks. The oldest charophyte fossils found date back to the Upper Silurian period (Croft, 1952). Thus, these macroalgae represent a potential archive for use in palaeoenvironmental studies (Apolinarska et al., 2011). Information regarding the precipitation of carbonate encrustation in Chara marl lakes and its possible application has increased over the last two decades. Coletta et al. (2001) postulated that the oxygen and carbon stable isotope values recorded in carbonate deposits on thalli could contain a record of the environmental conditions under which these carbonates precipitated. Furthermore, δ13C and δ18O measurements along the charophyte stem—the so-called isotope age gradient—can indicate seasonal changes in environmental conditions, including changes in the water temperature, the evaporative influence on the δ18O value of water or changes in the δ13C value of dissolved inorganic carbon (DIC) in water due to the photosynthetic activity of primary producers (Pentecost et al., 2006). In temperate climates, most calcification takes place during the summer months (Pentecost et al., 2006; Pełechaty et al., 2010). Therefore, stable isotope values tend to peak during the growing season. The use of charophyte carbonate δ13C and δ18O values as an environmental record is possible only if the relation between the carbon and oxygen isotope values of modern charophyte encrustations, as well as δ18OWATER and δ13CDIC, have been characterized.

Very little is known about the δ13C values of charophyte organic matter and their relationships with the δ13C values of DIC in surrounding waters and of carbonates precipitated by charophytes. Pentecost et al. (2006) defined the δ13C values of Chara hispida Linné 1753 organic matter but found only a weak and statistically insignificant correlation between the δ13C values of organic matter and of carbonates. Nuñez et al. (2002) studied the stable carbon isotope composition of bulk organic matter in sediment cores taken from a marl lake (Malham Tarn, NW England) and in peat and modern Chara samples for comparison. The authors emphasized the use of δ13C data biomarkers for the elucidation of environmental changes in lakes and their catchment areas.

In this study, we examine two Chara species widely distributed, Chara tomentosa Linné 1753 and Chara globularis Thuillier 1799, to determine whether there are species-related differences between the δ13C values of organic matter (δ13CORG), carbonate encrustations (δ13CCARB) and ambient dissolved inorganic carbon (δ13CDIC). Chara tomentosa is a tall branchy species that forms thick but sparser stands compared to C. globularis, a slender charophyte that grows in compact carpets close to the sediment. We hypothesized that there would exist species-specific relationships between the δ13C values of the above components resulting from the contrasting growth forms of the studied charophytes.

Materials and methods

Study sites

The study was carried out in seven lakes located in western Poland (Fig. 1), six in the Lubuskie Lake District and one in the Myśliborskie Lake District. For each of the studied species, C. tomentosa and C. globularis, individual thalli were sampled in five lakes and at three sites per lake (Chara stands). In three lakes, the two species co-occurred. In the other four lakes, the species occurred separately, each in two lakes. Altogether, the study was carried out at 30 sites (15 sites in five lakes for each of the studied species). The lakes differed in terms of morphology, water flow and catchment area (Table 1). This study included both shallow, small, polymictic lakes and deep, large, stratified water bodies (Table 1). The residence time of the water varied from approximately 0.5, 2.8 and 3.3 years in Lakes Malcz, Jasne and Karskie Wielkie, respectively, to about 5 years in other lakes (no reliable data exist for Lake Męcko Duże). With the exception of Lake Karskie Wielkie, which is slightly eutrophicated, the studied lakes are mesotrophic bodies of water. All lakes are characterized by well-developed aquatic vegetation dominated by charophyte meadows (Table 1) and as such represent the Chara-lake group. Furthermore, the studied lakes are characterized by high water clarity, with the highest Secchi depth values exceeding 6 m in Lake Pierwsze (Pełechaty et al., 2007) and Lake Męcko Duże (this study). Water clarity exceeding 5 m was measured in Lakes Jasne, Niesłysz and Złoty Potok (Pełechaty et al., 2007). Five of the investigated lakes have a direct catchment area covered mostly by forest. In contrast, the catchments of Lake Niesłysz and Lake Karskie Wielkie are primarily used for agricultural and recreational purposes. Three of the studied lakes, Lake Pierwsze, Lake Męcko Duże and Lake Malcz, are located near the Wędrzyn Military Training Ground. In this territory, human activity is regulated by the armed forces and is therefore substantially restricted.
Fig. 1

Locations of the lakes in which Chara tomentosa and Chara globularis stands were investigated. 1 Lake Karskie Wielkie; 2 Lake Pierwsze; 3 Lake Jasne; 4 Lake Męcko Duże; 5 Lake Malcz; 6 Lake Niesłysz; 7 Lake Złoty Potok

Table 1

Selected habitat characteristics of investigated lakes

Lake

Geographical coordinates

Area (ha)

Max. depth (m)

Mean depth (m)

Character of flow

No. of charophytes forming extensive stands

Męcko Dużea,b

52°22′0″N, 15°11′2″E

40.9

22.7

9.2

Closed

7

Karskie Wielkiea,c

52°55′4″N, 15°04′8″E

150

17.6

6.2

Outflow

4

Jasnea,d,e

52°17′7″N, 15°03′06″E

15.1

9.5

4.3

Closed

7

Niesłysza,f

52°13′9″N, 15°23′8″E

486.2

34.7

7.8

Throughflow

5

Złoty Potoka,f

52°13′0″N, 15°22′5″E

32.8

13.7

5.9

Closed

5

Malcza,b

52°21′1″N, 15°13′3″E

36.2

7.3

3.4

Throughflow

4

Pierwszea,f

52°23′11″N, 15°09′18″E

19.3

10.7

4.7

Closed

6

Data sources a Jańczak (1996), b Pełechaty & Pukacz (2006), c Cyrwus (2008, unpublished data), d Pełechaty et al. (2010), e Pukacz & Pełechaty (2013), f Pełechaty et al. (2007)

Chara tomentosa and Chara globularis stand structure

Environmental samples were collected from two different types of macrophyte stands dominated either by C. tomentosa or by C. globularis. According to a preliminary study performed prior to sample collection, both types of stands were well developed in the form of extensive charophyte meadows. In five out of the 15 Chara tomentosa stands studied, cover reached 100%, whereas at seven stands it was at least 70%. In the other three stands, the species coverage was 50% (Table 2). Regardless of the exact coverage of C. tomentosa in the stands studied, the species was the dominant taxon, with minor or negligible contributions by vascular plants and mosses.
Table 2

Carbon stable isotope composition of DIC (δ13CDIC), carbonates (δ13CCARB) and organic matter (δ13CORG) of Chara tomentosa (CT) and Chara globularis (CG)

Lake

Stand

Depth (m)

Coverage (%)

δ13CDIC (‰ V-PDB)

δ13CCARB (‰ V-PDB)

δ13CORG (‰ V-PDB)

Męcko Duże

CT1

3

50

0.20

1.75

−15.75

CT2

3

50

−0.06

1.71

−15.38

CT3

3

80

−0.04

1.54

−15.09

CG1

4

100

−0.02

−2.45

−23.40

CG2

4

100

0.19

−3.14

−24.50

CG3

4

100

−0.02

−2.15

−23.60

Karskie Wielkie

CT1

3

70

−5.27

−3.58

−20.91

CT2

3

80

−5.11

−3.83

−21.85

CT3

3

80

−5.12

−3.53

−20.47

CG1

3

70

−5.53

−6.69

−27.90

CG2

3

70

−5.53

−6.56

−27.60

CG3

3

40

−4.97

−6.90

−27.60

Jasne

CT1

3

100

0.17

0.91

−14.72

CT2

3

100

−0.03

1.54

−13.64

CT3

3

100

0.10

1.33

−13.59

CG1

4

100

0.01

−10.59

−35.40

CG2

4

100

−0.05

−7.78

−30.20

CG3

4

100

−0.07

−7.32

−29.20

Niesłysz

CT1

2

80

−1.30

−0.35

−14.28

CT2

2

80

−1.51

−0.44

−14.44

CT3

2

50

−1.47

−0.59

−13.90

Złoty Potok

CT1

2

90

−3.24

−1.69

−17.53

CT2

2

100

−2.93

−1.64

−18.30

CT3

2

100

−3.21

−1.44

−17.98

Malcz

CG1

3

80

0.28

−1.51

−22.20

CG2

3

80

0.31

−2.04

−21.60

CG3

3

80

0.30

−0.20

−20.70

Pierwsze

CG1

4

100

−1.26

−3.93

−20.10

CG2

4

100

−0.69

−2.12

−19.80

CG3

4

100

−1.11

−2.51

−18.50

The depth and vegetation coverage of the studied stands are also provided

Compared to Chara tomentosa, Chara globularis coverage was in many cases more extensive. In nine out of the 15 studied stands, this species covered 100% of the studied stand area, and in five stands the coverage reached or even exceeded 70%. At one site, the coverage was only 40% (Table 2). Similar to C. tomentosa, C. globularis was always the dominant species in a milieu containing far less abundant vascular plants and mosses.

The water quality parameters measured during the study period (Table 3) confirmed the results of earlier studies, which characterized the investigated lakes as hardwater ecosystems with moderate nutrient availability and high transparency (Pełechaty et al., 2007 and references therein; Kraska, 2009; Cyrwus 2008, unpublished data; Pełechaty et al., 2015). The aforementioned environmental conditions promote charophyte dominance in the form of submerged vegetation (Dąmbska, 1964; Hutchinson, 1975; Krause, 1981, 1997; Blindow, 1992a, b), including extensive meadows formed by both of the species studied.
Table 3

Physical and chemical characteristics of water sampled above Chara tomentosa (CT) and Chara globularis (CG) stands studied in July 2012

Lake

Stand

Temperature (°C)

Oxygen (mg l−1)

pH

Conductivity (µS cm−1)

Alkalinity (mmol l−1)

Total hardness (mg CaCO3 l−1)

HCO3 (mg l−1)

Męcko Duże

CT

18.97 ± 0.05

7.50 ± 0.29

8.75 ± 0.04

261.00 ± 1.41

1.77 ± 0.05

109.67 ± 0.47

107.77 ± 2.88

CG

19.07 ± 0.21

7.33 ± 0.09

8.70 ± 0.08

264.33 ± 3.86

1.70 ± 0.00

109.73 ± 1.32

103.70 ± 0.00

Karskie Wielkie

CT

20.33 ± 0.05

7.50 ± 0.29

8.53 ± 0.05

595.00 ± 5.35

2.77 ± 0.05

234.80 ± 3.22

168.77 ± 2.88

CG

20.00 ± 0.08

7.73 ± 0.09

8.50 ± 0.08

586.67 ± 13.12

2.73 ± 0.05

232.67 ± 4.11

166.73 ± 2.88

Jasne

CT

21.90 ± 0.08

6.27 ± 0.17

8.50 ± 0.08

294.33 ± 4.03

1.53 ± 0.05

130.53 ± 387

93.53 ± 2.88

CG

21.77 ± 0.24

5.80 ± 0.42

8.50 ± 0.00

314.00 ± 9.42

1.63 ± 0.05

129.53 ± 2.76

99.63 ± 2.88

Niesłysz

CT

22.17 ± 0.15

8.17 ± 0.58

8.57 ± 0.15

317.67 ± 18.50

1.90 ± 0.00

131.40 ± 4.08

115.90 ± 0.00

Złoty Potok

CT

22.06 ± 0.11

6.97 ± 0.20

8.57 ± 0.06

332.00 ± 5.56

2.17 ± 0.06

148.13 ± 1.90

132.17 ± 3.52

Malcz

CG

23.10 ± 0.30

5.30 ± 0.10

8.47 ± 0.12

266.00 ± 6.60

1.87 ± 0.06

106.47 ± 1.10

113.87 ± 3.52

Pierwsze

CG

21.40 ± 0.44

6.97 ± 0.21

8.97 ± 0.06

158.30 ± 5.77

1.17 ± 0.06

65.07 ± 1.68

71.17 ± 3.52

Lake

Stand

Ca2+ (mg l−1)

Mg2+ (mg l−1)

TP (mg l−1)

TN (mg l−1)

SO4 2− (mg l−1)

Cl (mg l−1)

SI

Visibility (m)

Męcko Duże

CT

40.29 ± 0.30

2.22 ± 0.30

0.05 ± 0.00

1.35 ± 0.00

15.00 ± 0.00

6.33 ± 0.47

0.87 ± 0.05

6.5

CG

40.48 ± 0.58

2.13 ± 0.46

0.04 ± 0.00

1.35 ± 0.00

15.00 ± 0.00

6.57 ± 0.47

0.81 ± 0.08

 

Karskie Wielkie

CT

78.42 ± 1.26

9.51 ± 1.50

0.04 ± 0.00

1.86 ± 0.03

40.00 ± 0.00

25.67 ± 0.94

1.11 ± 0.06

3.1

CG

77.19 ± 0.17

9.74 ± 0.97

0.05 ± 0.00

1.82 ± 0.03

35.00 ± 4.08

23.00 ± 1.41

1.06 ± 0.08

 

Jasne

CT

47.78 ± 1.59

2.76 ± 0.58

0.05 ± 0.00

1.65 ± 0.03

16.67 ± 2.36

7.67 ± 0.47

0.67 ± 0.11

3.0

CG

47.00 ± 0.49

2.98 ± 0.49

0.05 ± 0.00

1.63 ± 0.06

20.00 ± 0.00

8.33 ± 0.47

0.69 ± 0.01

 

Niesłysz

CT

43.96 ± 0.23

5.29 ± 0.96

0.08 ± 0.01

1.80 ± 0.06

16.67 ± 2.36

12.33 ± 0.47

0.79 ± 0.13

4.2

Złoty Potok

CT

49.73 ± 1.01

5.85 ± 0.22

0.06 ± 0.00

1.16 ± 0.07

30.00 ± 0.00

9.33 ± 0.47

0.89 ± 0.06

4.3

Malcz

CG

38.27 ± 0.30

2.67 ± 0.30

0.05 ± 0.02

1.91 ± 0.05

10.00 ± 0.00

7.00 ± 0.00

0.65 ± 0.10

3.8

Pierwsze

CG

22.58 ± 0.24

2.12 ± 0.50

0.06 ± 0.01

1.32 ± 0.12

10.00 ± 0.00

7.67 ± 0.47

0.72 ± 0.07

5.4

Means ± standard deviations (N = 3). Visibility was measured at macrophyte-free pelagic sites

SI saturation index

As the smaller, slenderer and more densely growing charophyte species, Chara globularis formed very compact patches concentrated near the bottoms of the lakes studied (depths of 3–4 m). Thus, the species came into contact with deeper waters rather than the more homogeneous waters above the charophyte stand. In contrast, the taller, thicker and branched thallus Chara tomentosa formed communities, which, compared to C. globularis patches, contacted more surface water and was less influenced by near-sediment conditions. Moreover, C. tomentosa patches were not as compact as those of C. globularis, allowing waters from above the patch to penetrate (stand depths were 2–3 m).

In published studies, both species are characterized by a high and comparable productivity. Pentecost (1984) showed that the biomass produced by C. globularis can exceed 1.1 kg DW m−2 (0.89 kg DW m−2 on average), although lower biomass values with a maximum of 0.305 kg DW m−2 were also recorded (Fernández-Aláez et al., 2002). For C. tomentosa, Blindow et al. (2002) recorded values between 0.7 and 0.8 kg DW m−2, which are comparable to those of C. globularis recorded by Pentecost (1984). However, Krolikowska (1997) determined a C. tomentosa biomass of 1.2 kg DW m−2 in a compact monospecific community. The similarity of the two species in terms of biomass production, despite their morphological differences, emphasizes the greater density of C. globularis stands compared to those formed by C. tomentosa.

Field sampling

At each study site, 10 individual charophytes from an area of 4 m2 were collected, and water from the immediate environment was sampled for isotopic analyses in July 2012. Prior to charophyte sampling, the basic physical and chemical properties of the water just above each studied charophyte patch were measured (water temperature, oxygen concentration, conductivity, pH) using portable field measurement equipment (Elmetron CX-401; Elmetron Sp. j., Zabrze, Poland, CyberScan 200 and CyberScan 20; Eutech Instruments Europe BV, Nijkerk, The Netherlands, respectively). Water samples for laboratory analyses were collected from above the macrophytes using a bathometer in a one-litre plastic bottle and preserved with chloroform. Water samples for stable carbon isotope analysis of DIC were collected in 10-ml glass septa test tubes and preserved with two drops of HgCl2. All charophyte samples were collected by diving. In addition to the aforementioned in situ measurements, water visibility was determined by Secchi disc at a vegetation-free pelagic region in each lake studied.

Laboratory work and analyses

The air-dried Chara samples were kept on paper sheets until further treatment. The thalli of charophytes with calcite encrustations were homogenized using a mortar and pestle. Prior to the isotope analysis of Chara organic matter (δ13CORG), the samples were decalcified in 15% HCl for 2 h to remove carbonates and then rinsed with distilled water. The procedure was repeated three times. Finally, after centrifugation and water removal, the samples were dried at a temperature of 50°C for 12 h and then homogenized and pulverized using an agate mortar.

The stable C isotope composition of charophyte carbonates (δ13CCARB) and dissolved inorganic carbon (δ13CDIC) were measured at the Isotope Dating and Environment Research Laboratory in Warsaw, Poland. Carbonates were dissolved in 100% phosphoric acid (density 1.9) at 75°C using a Kiel IV online carbonate preparation line connected to a ThermoFinnigan Delta + mass spectrometer. All values are reported per mil relative to V-PDB by assigning a δ13C value of 1.95‰ to NBS19. The reproducibility was tested by replicate analysis of laboratory standards and was found to be better than ±0.03‰.

The δ13CDIC analyses were conducted using a GasBench-II headspace autosampler connected to a Finnigan MAT 253 isotope ratio mass spectrometer (IRMS). During the δ13CDIC determination procedure, septum-sealed sample vials were filled with 3–4 drops of phosphoric acid (98%) and then flushed with a continuous flow of He to replace the air in the vials. Then, the samples were injected into the vials with a syringe, and CO2 was released by contact with acid. The CO2 and He mixture was left to equilibrate for 18 h, and after purification (removal of water vapour) and separation on a GC column, CO2 was measured in the IRMS using a sample or a reference gas as a comparison. To ensure the precision of the results, four international carbonate standards were measured in each series of samples: NBS 18, NBS 19, LSVEC and IAEA-CO-9.

The Chara organic matter (δ13CORG) samples were analysed at the Institute of Geosciences, Goethe University in Frankfurt, Germany. Carbon isotope analysis of organic matter was performed using a Flash Elemental Analyser 1112 (ThermoQuest) connected to the continuous flow inlet system of a MAT 253 gas source mass spectrometer (ThermoQuest). In addition to IAEA and NBS reference materials (NBS 18, NBS 19, LSVEC), a USGS 24 standard was analysed along with the samples in order to prove accuracy and precision. The reproducibility of both samples and standards was tested and was found to be better than ±0.2‰ for δ13CORG (van de Schootbrugge et al., 2008).

The water samples used for hydrochemical analyses were stored in the refrigerator until further treatment. The total alkalinity was determined by titration of a 0.1 mol l−1 HCl-acidified water sample against the indicator methyl orange. The bicarbonate concentration was calculated by multiplying the alkalinity by 61 gmol−1 (the molar mass of HCO3 ). Total water hardness and Ca2+ concentration were determined using the versenate method, while Mg2+ concentration was calculated as the difference between the total hardness and the concentration of Ca2+ ions. The anions Cl and SO4 2− were determined by ion chromatography using the Thermo Scientific Dionex IonPac AS22 Carbonate Eluent Anion-Exchange Column (Thermo Scientific, USA). Total nitrogen was determined using a TOC-L Shimadzu analyser with a TNM-L unit via catalytic thermal decomposition and chemiluminescence methods (Shimadzu, Japan). Total phosphorous was determined using an ICP-OES 9820 (Shimadzu, Japan).

The calcite saturation index (SI) was calculated for each study site in order to determine whether conditions of HCO3 ion supersaturation occurred. The following formula was applied (Kelts & Hsü, 1978):
$${\text{SI}} = \log {\text{IAP}}/K_{\text{C}},$$
where IAP is the Ca2+ and CO3 2− ion activity product and K C is the equilibrium constant for the following reaction:
$${\text{CaCO}}_{3} \leftrightarrow {\text{Ca}}_{{({\text{aq}})}}^{2 + } + {\text{CO}}_{{3\,({\text{aq}})}}^{{2 - }} .$$

The study results were assessed statistically using Statistica 10 software (StatSoft Inc., Tulsa, OK, USA). A scatter plot of the relation between δ13CCARB, δ13CDIC and δ13CORG was used for data presentation. Additionally, the Pearson’s correlation between δ13CCARB and δ13CORG, δ13CCARB and δ13CDIC as well as δ13CDIC and δ13CORG was calculated and presented in a scatter biplot. Differences in isotopic composition between the studied species were determined via t test. For all the statistics, P < 0.05 was used to determine significance.

Results

The δ13CDIC values above Chara tomentosa and Chara globularis stands

The δ13CDIC values of the waters above Chara globularis stands were in many cases similar to the δ13CDIC values observed in C. tomentosa stands, especially in lakes where both species co-occurred (any differences were statistically insignificant; t test, P > 0.05, Fig. 2a). The most negative values for both investigated species were found in Lake Karskie Wielkie (Fig. 3; Table 2), while the most positive values were found in Lake Malcz for C. globularis and in Lakes Jasne and Męcko Duże for both species (Fig. 3; Table 2).
Fig. 2

Differences in carbon stable isotope values between a DIC (dissolved inorganic carbon) in the C. tomentosa and C. globularis stands, b carbonate encrustations of C. tomentosa and C. globularis, and c organic matter of C. tomentosa and C. globularis. Carbon stable isotope values were measured in nine stands (N = 9) for each species in the lakes where both species co-occurred. Median, box 25–75% and min–max; except for δ13CDIC, the differences between species were statistically significant (t test, P < 0.05)

Fig. 3

Relation between the δ13C values of charophyte carbonates (grey squares and rhombuses), δ13C values of DIC (white squares and rhombuses) and δ13C values of organic matter (black squares and rhombuses) for a Chara tomentosa stands (N = 15) and b Chara globularis stands (N = 15)

The δ13C values of Chara tomentosa and Chara globularis organic matter and carbonate encrustations

The carbonate encrustations of C. tomentosa had substantially higher δ13C values in comparison to C. globularis (Table 2). In lakes where both species co-occurred, the difference was statistically significant (t test, P < 0.001, Fig. 2b). The greatest differences in the δ13CCARB values of the studied species were noted in Lake Jasne, where the most negative values for C. globularis and the second most positive values for C. tomentosa were observed (Fig. 3a, b; Table 2).

Substantially higher δ13C values for organic matter were also revealed by C. tomentosa. The most negative values for C. tomentosa were found in Lake Karskie Wielkie and for C. globularis in Lake Jasne (Fig. 3; Table 2). Conversely, in Lake Jasne and Lake Męcko Duże, C. tomentosa revealed the most positive δ13CORG values, while for C. globularis the most positive δ13CORG values were noted in Lake Pierwsze (Fig. 3; Table 2). Again, the highest contrast in the carbon stable isotope signal was noted in Lake Jasne. In lakes where both Chara species co-occurred, the difference in the δ13CORG values between the studied species was statistically significant (t test, P < 0.00001; Figs. 2c, 3a, b).

The relationships between the δ13CDIC, δ13CCARB and δ13CORG values of the studied species are presented in scatter plots (Fig. 3). Compared to DIC, carbonate encrustations of C. tomentosa were enriched in 13C, while those involving C. globularis were 13C depleted (Fig. 3a, b). This shift was apparent in all studied lakes. In both studied species, the organic matter was 13C depleted relative to both DIC and carbonates, a trend that was valid for all lakes (Fig. 3a, b).

A close relationship between the δ13CCARB and δ13CORG values was reflected in their high correlation coefficients (Fig. 4a). We also found a close relationship between the δ13CCARB and δ13CDIC values for C. tomentosa, while the relationship between the δ13CCARB and δ13CDIC values of C. globularis was weak and statistically insignificant (Fig. 4b). Similar observations were made concerning the relationship between δ13CORG and δ13CDIC values: a high correlation coefficient was obtained for C. tomentosa but not for C. globularis (Fig. 4c).
Fig. 4

Correlations between the stable isotope values of a carbonate encrustations and organic matter, b carbonate encrustations and dissolved inorganic carbon, and c organic matter and dissolved inorganic carbon of Chara tomentosa (grey squares, N = 15) and Chara globularis (black rhombuses, N = 15) stands

Discussion

Main factors controlling the composition of carbon stable isotope for DIC, charophyte encrustation and organic matter

Taking into account the complexity of lake ecosystems, a number of fractionation factors that influence the carbon stable isotope composition of DIC can be specified. The isotope composition of inflowing waters (i.e., surface and ground waters), CO2 exchange with the atmosphere and the time of water exchange in a lake are of prime importance for the δ13CDIC values (Leng & Marshall, 2004 Myrbo & Shapley, 2006 and references in both cited papers). Additionally, δ13CDIC values are related to the rate and intensity of photosynthesis because aquatic autotrophic organisms preferentially uptake 12CO2, leaving ambient DIC 13C enriched (e.g., Pentecost & Spiro, 1990; Andrews et al., 1997; McConnaughey & Whelan, 1997; Leng & Marshall, 2004 and references therein). Therefore, δ13CDIC values vary both horizontally (e.g., shallow littoral waters vs. deep pelagic regions) and vertically within the water column, where the epilimnetic layer is usually 13C enriched compared to hypolimnetic waters. Under aerobic conditions, the near-bottom waters are 13C depleted due to 12CO2 release resulting from sedimentary organic matter decomposition (Myrbo & Shapley, 2006 and reference therein). Thus, aquatic macrophytes, including charophytes at deeper sites or concentrated near lake-floor sediment can utilize this 13C-depleted source of CO2 for photosynthesis. Under anaerobic conditions, δ13CDIC in pore and near-bottom water is strongly dependent on the degradation of sedimentary organic matter stored in carbon-rich sediments (Gu et al., 2004). Bacterial methane production, depending on the resultant product, CH4 or CO2, may cause the 13C depletion or 13C enrichment of pore and near-bottom water, respectively. However, the lakes included in this study are not significantly fertile (i.e., clear-water mesotrophic lakes, and only Lake Karskie Wielkie is slightly eutrophicated) and contain abundant submerged vegetation dominated by charophytes (indicative of a low trophy state; Krause, 1981), out of which many species can overwinter. In addition, charophytes are characterized by low decomposition ratios compared to vascular plants (Kufel & Kufel, 2002). Therefore, methanogenesis, in our opinion, can be considered a less significant 13C fractionation factor in these lakes.

In aquatic environments, inorganic C can be assimilated in two forms, CO2 and HCO3 (Smith & Walker, 1980). As evidenced for the marine environment, CO2 is 13C depleted compared to other components of DIC (H2CO3, HCO3 , CO3 2−) by typically 8–12‰ (Mook et al., 1974). The difference between the stable isotopic composition values of HCO3 and CO2 is temperature dependent. The δ13C values of CO2 are 12‰ lower than those of HCO3 at 0°C and 8.4‰ lower at 30°C (Mook et al., 1974). For this reason, Fry (1996) assumed that under isotopic equilibrium the cells using CO2 should have δ13C values 8–12‰ lower than cells using HCO3 . Thus, the δ13C values of ambient DIC depend not only on the character of a lake but also on the variable in time and space, temperature, and the pH-dependent proportions of CO2, HCO3 and CO3 2− (Smith & Walker, 1980; Zhang et al., 1995). Therefore, in addition to lake morphology and the related residence time of water, other environmental conditions, including water physical and chemical properties, should be taken into consideration. In this study, no direct effects of the lake morphology and the rate of water exchange on the δ13CDIC values were identified. In addition, the pH values of waters, almost equal in all lakes studied, exceeded 8 at each study site (Table 3), permitting the assumption that HCO3 ions were the form of inorganic carbon in all waters sampled above charophyte beds. This was unequivocally confirmed by C species modelling performed with MINEQL 4.6 software (Environmental Research Software, Hallowell, ME, USA; since the developed model is of minor relevance to the study aim, we have avoided it). Additionally, HCO3 ion accessibility for autotrophs in the studied lakes was reflected in the abundant encrustation present on the charophyte thalli and in the calculated values of the calcite saturation index (SI, Table 3). The SI values indicate supersaturation with respect to HCO3 ions, which further indicates favourable conditions for calcium carbonate precipitation in all studied lakes. What differentiates the lakes is the character of flow (Table 1). Compared to other lakes, the most negative δ13C DIC values were found in Lake Karskie Wielkie (Table 2), the only outflow lake included in this study (Table 1). In addition to the flow character, the waters of Lake Karskie Wielkie revealed distinctive chemical properties (i.e., much higher conductivity, alkalinity and hardness as well as Ca2+, SO4 2− and Cl concentrations) compared to the other lakes. Importantly, the second most negative δ13CDIC values were measured in Lake Złoty Potok (Table 2), which, similar to Lake Karskie, exhibited a higher alkalinity, hardness and SO4 2− concentration than the other lakes (Table 3), in which the δ13CDIC values were relatively similar. The aforementioned chemical water characteristics are related to the ground waters that feed the lakes. According to the data available, including the most negative δ18O values in the group of studied lakes (unpublished data), it is reasonable to suggest that ground waters significantly contribute to the water budget of Lakes Karskie Wielkie and Złoty Potok, and the δ13C DIC values are strongly dependent on the δ13C DIC values of inflowing waters. The moderately higher fertility of Lake Karskie Wielkie and the agricultural character of its catchment basin may also point to a contribution of surface inflow from arable fields to the water chemistry and isotopic composition of this lake.

Apart from the δ13C values of ambient DIC, the so-called ‘vital effect’ is regarded as an important factor to control the δ13C values of biogenically precipitated carbonates in lakes (Leng & Marshall, 2004 and references therein). Above the charophyte stands, DIC is strongly 13C enriched by the photosynthetic activity of these macroalgae (Coletta et al., 2001; Pełechaty et al., 2010; Apolinarska et al., 2011). As a consequence, elevated δ13CDIC values are recorded in the carbonate encrustations of these charophytes.

The δ13C values of organic matter (δ13CORG) depend on the carbon source utilized (e.g., CO2(aq), HCO3 ), the isotope effects associated with the assimilation of carbon, the photosynthesis pathway performed by the photosynthesizing organism and the cellular carbon budget (Hayes, 1993). For aquatic environments, many authors have recorded different δ13CORG values of autotrophic organisms such as marine phytoplankton or freshwater macrophytes and found smaller and larger offsets of δ13CORG within the same investigated groups of organisms (e.g., Keeley, & Sandquist, 1992 and reference therein; Rau et al., 1992; Fry, 1996 and reference therein; Rau et al., 2001; Herzschuh et al., 2010; Mendonça et al., 2013). In the following discussion, we will try to explain the observed differences between the δ13CCARB, δ13CORG and δ13CDIC values of the two studied charophyte species in light of CO2 source used for their photosynthetic activity, 13C-enriched DIC from well-mixed waters above and penetrating Chara tomentosa stand and, for Chara globularis, 13C-depleted DIC from near-bottom waters with a higher proportion of 12C released by organic matter decomposition and carbonate dissolution in surface sediments. The proportion between 13C and 12C in C taken up by the two charophytes seems related to their growth forms.

δ13CCARB versus δ13CDIC

This study revealed opposing tendencies in the shift between the δ13CCARB and the δ13CDIC values of the studied species (Fig. 3a, b). We postulate that this contradictory shift results from the different growth forms represented by the studied species. C. tomentosa is a bigger and more highly branched Chara species with a much longer thallus compared to C. globularis (Dąmbska, 1964; Krause, 1981, 1997; Torn et al., 2006; Pełechaty & Pukacz, 2008). The length of C. tomentosa thallus can exceed 140 cm, whereas C. globularis thalli are usually 20 cm long. C. tomentosa is often found at more shallow depths than C. globularis. The latter species forms more compact stands near the bottom of lakes compared to the less compact stands of C. tomentosa. Considering these characteristics, we suggest that the encrustation of C. globularis was 13C depleted compared with the δ13C values measured in DIC due to the assimilation of carbon from waters near the bottom of the lake rather than the well-mixed water above the stands. The near-bottom water is usually enriched with 12C derived from organic matter decomposition in the surface sediment. The lack of correlation between δ13CCARB and δ13CDIC values in C. globularis stands (Fig. 4b) seems to confirm this hypothesis. In contrast, a strong correlation between the δ13C values of C. tomentosa encrustations and those of DIC (Fig. 4b) emphasizes a significant relationship between CCARB and CDIC in homogenous ambient water. In addition, this strong correlation may suggest that in contrast to C. globularis, C. tomentosa precipitated encrustation in or close to an isotopic equilibrium with DIC from the immediate environment.

Due to the higher proportion of 12CO2 assimilated preferentially during photosynthesis, the remaining water DIC becomes 13C-enriched DIC source for the calcite precipitated as an encrustation by charophytes (cf. Pentecost & Spiro, 1990; Andrews et al., 1997). This relationship has been reported also by Pełechaty et al. (2010) for C. rudis, a species morphologically similar to C. tomentosa. In addition, the δ13CCARB values of C. tomentosa collected in this study from Lake Jasne were comparable to those shown by Pełechaty et al. (2010) for C. rudis in the same lake. By contrast, the δ13CCARB values recorded for C. globularis in Lake Jasne were significantly different from those reported for C. tomentosa (13C depleted), exceeding 12‰ at one stand, and this tendency was also valid for other studied lakes. Pukacz et al. (2014) reported the horizontal homogeneity of physical and chemical water properties in Lake Jasne, with no significant differences between pelagic open waters and charophyte stands. Thus, it can be assumed that the relatively homogeneous waters of Lake Jasne should counteract the difference in isotopic values between the studied species. The existence of this difference, therefore, seems to confirm that the δ13CCARB of C. globularis was 13C depleted, because this species uses the DIC of the near-bottom waters rather than of the water above the studied stands (which was sampled in this study). In summary, by creating a dense community just off the bottom sediment, C. globularis appears to use a DIC stock enriched in 12C derived from decomposition in sediments. As a result, the C. globularis δ13CCARB value reveals significant 13C depletion compared not only to C. tomentosa but also to DIC in water sampled above C. globularis stands.

δ13CORG of charophytes as an indicator of C source

The carbon stable isotope values of organic matter were higher in C. tomentosa compared to C. globularis (Figs. 2e, 3a, 4a; Table 2). These differences were significant in all lakes in which the two species co-occurred and exceeded 20‰ in Lake Jasne (Fig. 3a, b; Table 2).

This study presents strong and statistically significant positive correlations between the δ13CCARB and δ13CORG values for both species (Fig. 4a). In contrast to our findings, Pentecost et al. (2006) recorded a week and insignificant positive correlation between the C. hispida δ13C values of encrustation and organic matter. In that study, the δ13CORG values of C. hispida, recorded in July and August, ranged between approximately −19.0 and −17.0‰, but the mean value over the investigated period (from February to August) was −19.7‰. In our study, the mean δ13CORG value of C. tomentosa, the species most similar to C. hispida in terms of size and morphology (i.e., −16.5‰), corresponded to the above data for C. hispida, while the mean δ13CORG value of C. globularis (i.e., −24.8‰) emphasized the difference between this species and the above two large Chara species.

Interestingly, the δ13CORG values obtained for C. tomentosa are similar to those of 13C-enriched vascular macrophytes, which have an average value of −13.5‰ (Mendonça et al., 2013). On the other hand, the cited authors provide a value of −27.2‰ as the average δ13C value of 13C-depleted plants, similar to our results for C. globularis. Thus, the difference in the δ13C values for organic matter between C. tomentosa and C. globularis is similar to that between 13C-enriched C4 plants, with δ13C values ranging from −16 to −10‰, and C3 plants, with δ13C values ranging from −32 to −22‰ (e.g., O’Leary et al., 1992; Hayes, 1993; Fry, 1996 and reference therein). Because both studied Chara species are members of the same genus and exhibit similar physiological photosynthetic patterns, the aforementioned comparisons point to the possible risk of misinterpreting the carbon source in palaeoecological studies. In terrestrial plants, the differing δ13C values of organic matter are the result of the photosynthetic pathways used for CO2 fixation and the isotopic signature of the atmospheric CO2 used for photosynthesis (Fry, 1996 and references therein; Mendonça et al., 2013). In C3 plants, large fractionation associated with the enzyme ribulose bisphosphate carboxylase/oxygenase (Rubisco), which catalyses the first step in CO2 fixation, are observed (e.g., O’Leary et al., 1992; Hayes, 1993; Fry, 1996 and reference therein). During photosynthetic carbon fixation in the C4 pathway, phosphoenolpyruvate carboxylase catalyses the first carbon fixation step, which is associated with a smaller carbon isotope fractionation compared to that of Rubisco (e.g., O’Leary et al., 1992; Hayes, 1993). For aquatic plants, the carbon source (CO2 vs. HCO3 ) seems to be a key isotope discrimination factor. The average difference in the δ13CORG values between C. tomentosa and C. globularis (8.3‰) is close to the difference reported by Mook et al. (1974) between the δ13C values of HCO3 and the δ13C values of dissolved CO2, falling within the range between 8 and 12‰ and reaching 9‰ at 25°C. These data prompt us to suggest that 13C-enriched HCO3 from above- and within-stand waters is the main source of C for C. tomentosa, while 12CO2 released from organic matter decomposing in lake bottom sediments and 13C-depleted HCO3 ions are likely to serve as C sources for C. globularis. Thus, the C source utilized is species specific and appears to be inseparably related to the growth form of each species. Additional detailed field investigations of a range of species representing different growth forms and a range of conditions above, within and beneath a charophyte stand as well as laboratory testing the exact CO2 acquisition for photosynthesis and membrane transport mechanisms (e.g., Ray et al., 2003; Beilby & Casanova, 2014), and respiration effects would explicitly verify our assumption. This is particularly important in the context of the aforementioned use of δ13C values in palaeoecological studies as an indication of the source of matter in sediment deposits.

Conclusions

In the present study:
  • We found opposing shifts between δ13CCARB and δ13CDIC values:
    • 13C enrichment in Chara tomentosa

    • 13C depletion in Chara globularis.

  • A strong positive correlation was found between δ13CCARB and δ13CDIC as well as between δ13CORG and δ13CDIC for C. tomentosa but not for C. globularis.

  • The δ13CCARB and δ13CORG values were strongly positively correlated in both species.

  • C. globularis samples exhibited more negative values of δ13CORG than did C. tomentosa, particularly in lakes where the two species co-occurred.

  • The differences between the isotope values of carbonate encrustations and the organic matter of the studied charophyte species were statistically significant.

  • The differences in isotope signatures were repetitive at each site and in each investigated lake.

  • The proportion between 13C and 12C used for photosynthesis from 13C-enriched DIC for C. tomentosa and 13C-depleted DIC for C. globularis is postulated to be a key factor influencing the isotope values recorded in the carbonates and organic matter of the species and may be useful in future palaeoecological studies.

Notes

Acknowledgements

This paper utilizes results obtained during the research project No. N304 0425 39, which was supported financially by the Polish Ministry of Science and Higher Education during the years 2010–2013. Financial resources earmarked for statutory activities of the Department of Hydrobiology, Faculty of Biology, Adam Mickiewicz University, are also acknowledged. Two anonymous peer reviewers are kindly acknowledged for their comments and suggestions, which helped to improve the manuscript.

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© The Author(s) 2016

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.

Authors and Affiliations

  • E. Pronin
    • 1
    Email author
  • M. Pełechaty
    • 1
  • K. Apolinarska
    • 2
  • A. Pukacz
    • 3
  • M. Frankowski
    • 4
  1. 1.Department of Hydrobiology, Faculty of BiologyAdam Mickiewicz UniversityPoznanPoland
  2. 2.Institute of Geology, Faculty of Geographical and Geological SciencesAdam Mickiewicz UniversityPoznanPoland
  3. 3.Polish-German Research Institute, Collegium PolonicumAdam Mickiewicz University in Poznań – European University Viadrina in Frankfurt/OderSłubicePoland
  4. 4.Department of Water and Soil Analysis, Faculty of ChemistryAdam Mickiewicz UniversityPoznanPoland

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