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Article

Photosynthetic Responses of Freshwater Macrophytes to the Daily Light Cycle in Songkhla Lagoon

by
Ponlachart Chotikarn
1,2,3,
Pathompong Pramneechote
1,3 and
Sutinee Sinutok
2,3,*
1
Marine and Coastal Resources Institute, Faculty of Environmental Management, Prince of Songkla University, Songkhla 90110, Thailand
2
Faculty of Environmental Management, Prince of Songkla University, Songkhla 90110, Thailand
3
Coastal Oceanography and Climate Change Research Center, Prince of Songkla University, Songkhla 90110, Thailand
*
Author to whom correspondence should be addressed.
Plants 2022, 11(21), 2806; https://0-doi-org.brum.beds.ac.uk/10.3390/plants11212806
Submission received: 25 August 2022 / Revised: 7 October 2022 / Accepted: 17 October 2022 / Published: 22 October 2022
(This article belongs to the Section Plant Physiology and Metabolism)
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Abstract

:
Macrophytes play an important role in the freshwater ecosystem. However, human activities and climate change are currently affecting aquatic lakes and species in various ways. The heterogeneity of macrophyte ecophysiology might lead to different responses to changing environments. To understand the photosynthetic responses of freshwater macrophytes to changes in light, six freshwater macrophyte species from Songkhla Lagoon were investigated. The results showed that there was a diurnal response of photosynthetic activities in all species. The Fv/Fm and ∆F/Fm′ of all species decreased at midday (9 a.m.–3 p.m.) then recovered at 6 p.m. close to the 6 a.m. level. As well as alpha, the positive relation between alpha and light showed the adaptation of plants. The saturating irradiance (Ik) revealed that plants from different light regimes showed different responses to light and temperature changes. To maintain a positive carbon balance and cope with light and temperature conditions, macrophytes had strategies such as modifying light harvesting capacity and light use. This study provides a better understanding of the vulnerability of each species to environmental changes and photosynthetic responses that enable species from different light regime to adapt to changing light environments.

1. Introduction

Macrophytes play an important role in the function of freshwater ecosystems by maintaining biological diversity, acting as ecosystem engineers [1]; habitat structure for other aquatic organisms [2]; and affecting lake nutrient status, sediment resuspension, and water turbidity [3,4]. However, human activities and climate change are currently affecting aquatic lakes and species through several factors, such as eutrophication, habitat destruction, and changes in water chemistry and physical properties [5].
Thale Noi is one of four interconnected water bodies in the Songkhla Lagoon, which is a tropical estuarine lagoon system covering 27 km2. Thale Noi, listed as a Ramsar site, is a valuable freshwater habitat supporting not only biodiversity, but also local inhabitants whose livelihoods depend on that biodiversity via fishery, aquaculture, and tourism [6,7,8]. As Thale Noi receives runoff and wastewater including sediments from the surrounding watershed, they are currently facing serious water pollution and eutrophication problems, which may lead to losing their valuable ecosystem services and function [6,7]. Eighteen dominant species of macrophytes have been listed in Songkhla Lagoon, including floating plants Eichhornia crassipes and Salvinia cucullata; plants with roots with floating leaves Nymphaea lotus and Nymphaea stellata; and submerged plants Ceratophyllum demersum and Chara zeylanica [8,9,10]. These systems are dynamic because of their complex physical and chemical processes in water bodies and sediment. Variations in environmental factors affect aquatic macrophytes in many ways, including distribution and abundance [11]. Some macrophytes can grow very well, which leads to overgrowth that might disturb the ecosystem. Several environmental parameters reveal the dynamics in terms of diurnal such as light and temperature, which affect the growth and photosynthetic activities of macrophytes [12,13].
Rapid light curves (RLCs) are a useful tool for evaluating a plant’s photosynthetic response to varying light conditions based on the background light to which they have been acclimated [14,15]. Jiang et al. [16] found that at midday under ambient light, the maximum quantum yield (Fv/Fm) of six submerged macrophytes decreased, but did not significant change under shade; Fv/Fm was negatively correlated with photon radiance. Shading decreased the net photosynthesis in C. aspera and C. canescens within 24 h; however, their photosynthetic performance was recovered within a short period [17]. Chen et al. [12] revealed that Potamogeton maackianus and Vallisneria natans decreased their minimum saturating irradiance (Ek) and maximum relative electron transport rate (rETRmax) and increased their initial slope (α) of RLCs under low light stress.
The heterogeneity of macrophyte morphology (e.g., emerged, floating, roots with floating leaves, and submerged plants) is related to water velocity and light regime [18,19]. Light and temperature are two of the most important factors controlling the growth, productivity, abundance, distribution, and survival of different groups of aquatic macrophytes [20,21,22]. The ecophysiological response of macrophytes to light and temperature depends upon their life form, traits, photosynthetic structure, and mechanisms, e.g., pigment contents, C3 and C4 plants, and their acclimation capacity to changing light and temperature [23,24,25]. The loading of sediment and nutrients and epiphytic algae can also reduce light availability and inhibit physiological processes [22]. Emergent and floating-leaved, and low-light-tolerant submerged species are commonly found in turbid water, where the presence of other submerged species is limited [3]. The temperature and minimum light requirements of a species can also determine the macrophyte depth zonation [26,27].
Understanding the photosynthetic responses of freshwater macrophytes to changes in light may explain the dynamics of these ecosystems. In this study, we investigated the photosynthetic responses of six freshwater macrophyte species from different light regimes (Eichhornia crassipes, Salvinia cucullata, Nymphaea lotus, Nymphaea stellata, Ceratophyllum demersum, and Chara zeylanica) from Thale Noi, Songkhla Lagoon. This study focused on the photosynthetic strategies that enable species to adapt to changing light environments.

2. Results

2.1. Physical Parameters

The average air and surface water temperatures were 31.21 ± 1.04 and 32.89 °C ± 0.63 °C, respectively. The average light intensity of surface water and air were 863.52 ± 221.02 and 1323.32 ± 309.63 µmol photons m−2 s−1, respectively. The highest surface water and air temperatures were 36 °C at 12 – 3 p.m. and 37 °C at 1 p.m., respectively. The light intensity of the surface water and air was highest at 1 p.m. (2060.67 µmol photons m−2 s−1) and 12 p.m. (2700 µmol photons m−2 s−1), respectively (Figure 1).

2.2. Maximum Quantum Yield (Fv/Fm)

At 6 a.m., Fv/Fm of C. demersum, N. stellata, C. zeylanica, S. cucullata, E. crassipes, and N. lotus were 0.71 ± 0.01, 0.72 ± 0.02, 0.73 ± 0.02, 0.77 ± 0.00, 0.77 ± 0.03, and 0.78 ± 0.03, respectively (Figure 2). A significant difference of Fv/Fm among species and time were observed (p < 0.05) (Table 1) where Fv/Fm of submerged plants (C. demersum and C. zeylanica) was significantly lower than the floating plants (Eichhornia crassipes, Salvinia cucullata) and root with floating leaf plant (Nymphaea lotus, Nymphaea stellata) (p < 0.05). Results showed that there was no difference between 6 a.m. and 6 p.m. and 9 a.m. and 3 p.m. (p > 0.05), revealing diurnal recovery and down-regulation in midday, respectively. A comparison among species found that roots with floating leaves (N. lotus and N. stellata) and floating plants (E. crassipes and S. cucullata) had a decreased tendency in Fv/Fm at midday, while submerged plants (C. demersum and C. zeylanica) showed various trends.

2.3. Rapid Light Curves (RLCs)

The RLCs showed responses to the light regime and revealed downregulation of photosynthesis for each submerged plant. C. demersum had the highest relative electron transport rate (rETR) at 9 a.m., while N. lotus and N. stellata had the highest at 3 and 12 p.m., respectively. The rETR of C. zeylanica, S. cucullata, and E. crassipes was high in the range of 6 a.m.–12 p.m., 6–9 a.m., and 12–3 p.m., respectively (Figure 3). However, all species had a low rETR at 6 p.m.

2.3.1. Effective Quantum Yield (∆F/Fm′)

There were significant changes in the ∆F/Fm′ in all species (p < 0.05) except for S. cucullata during the day (p > 0.05). At 6 a.m., the ∆F/Fm′ of C. zeylanica, S. cucullata, C. demersum, E. crassipes, N. stellata, and N. lotus were 0.66 ± 0.03, 0.72 ± 0.02, 0.73 ± 0.02, 0.77 ± 0.00, 0.79 ± 0.01, and 0.81 ± 0.00, respectively (Figure 4a). Then, the ∆F/Fm′ of C. demersum, E. crassipes, and N. lotus significantly decreased from 6 a.m. to 3 p.m. and significantly increased at 6 p.m., while the ∆F/Fm′ of N. stellata and C. zeylanica significantly increased at 3 p.m. The ∆F/Fm′ was different among species and time (p < 0.05) (Table 1), where the ∆F/Fm′ of submerged plants (C. demersum and C. zeylanica) was significantly lower than that of the other species (p < 0.05). In all species except C. zeylanica, the ∆F/Fm′ at 6 a.m. and 6 p.m. was not significantly different, indicating the recovery of photosynthetic efficiency.

2.3.2. Alpha (α)

At 6 a.m., the α values of C. demersum, C. zeylanica, S. cucullata, N. stellata, N. lotus, and E. crassipes were 0.08 ± 0.02, 0.16 ± 0.00, 0.16 ± 0.01, 0.17 ± 0.03, 0.20 ± 0.02, and 0.22 ± 0.01, respectively (Figure 4b). The α in all species significantly decreased over time at midday (p < 0.05), except in N. lotus (p > 0.05), which showed a slightly stable trend. The α was different among species and time (p < 0.05) (Table 1), where N. lotus and N. stellata showed the slowest change in α, while the fastest change occurred in submerged plants (C. demersum and C. zeylanica). There was no difference in the α between 6 a.m. and 6 p.m. (p > 0.05), revealing that all plants could adapt to cope with ambient light and return to their normal state.

2.3.3. Saturating Irradiance (Ik)

At 6 a.m., the saturating irradiance (Ik) of C. zeylanica, C. demersum, E. crassipes, N. lotus, S. cucullata and N. stellata was 125.04 ± 15.76, 143.81 ± 24.01, 145.71 ± 21.85, 147.45 ± 49.82, 185.60 ± 32.21, and 188.69 ± 30.93 μmol photons m−2 s−1, respectively (Figure 4c). There were significant changes in the Ik in all species (p < 0.05), except for S. cucullata and C. zeylanica (p > 0.05). The Ik of submerged plants (C. demersum and C. zeylanica) decreased at noon, the Ik of E. crassipes and S. cucullata decreased at 9 a.m. and 6 p.m., and the Ik of N. lotus and N. stellata decreased only at 6 p.m. The Ik significantly differed among species and time (p < 0.05) (Table 1). The Ik at 6 p.m. was not significantly different from the Ik at 6 and 9 a.m., indicating the recovery of photosynthetic efficiency.

2.3.4. Maximum Relative Electron Transport Rates (rETRmax)

At 6 a.m., the rETRmax of C. demersum, C. zeylanica, N. lotus, N. stellata, S. cucullata, E. crassipes was 10.62 ± 1.37, 20.62 ± 2.90, 26.66 ± 6.06, 29.84 ± 3.70, 29.88 ± 6.25, and 31.66 ± 4.28 µmol electrons m−2 s−1, respectively (Figure 4d). There were significant changes in the rETRmax over time in all species (p < 0.05). The rETRmax showed various patterns for each species, in which C. demersum and N. stellata had the highest rETRmax at 9 a.m., those of E. crassipes and N. lotus were highest at 3 p.m., and those of S. cucullata and C. zeylanica were the highest at 6 a.m.–12 p.m., which then decreased after the peak (Figure 4d). The rETRmax was significantly different among species and time (p < 0.05) (Table 1).

3. Discussion

Photosynthetic responses to the daily light cycle in six freshwater macrophyte species, Eichhornia crassipes, Salvinia cucullata, Nymphaea lotus, Nymphaea stellata, Ceratophyllum demersum, and Chara zeylanica at Thale Noi, Songkhla Lake, were investigated. We observed a diurnal response of photosynthetic activities in all species.
The maximum quantum yield (Fv/Fm) and effective quantum yield (∆F/Fm′) indicate the diurnal change in which photosynthetic efficiency decreases during midday and returns to the morning level at the end of the day due to photoinhibition, photoprotection, and photoadaptation [16,27,28]. Diurnal changes in Fv/Fm were also observed in Lagarosiphon major, indicating the dynamic photoinhibition of PSII [27]. Excessive photosynthetically active radiation (PAR) and a high air temperature during midday might lead to the downregulation of photosynthesis and a change in the balance of energy absorption and dissipation of PSII, resulting in photoprotection against photodamage [16]. This is consistent with the results of the study conducted by Chotikarn et al. [29], reporting that an elevated temperature of 36 °C resulted in the downregulation of photosynthesis in C. demersum. Such high air and water temperatures might degrade photosystem II in the photosynthetic apparatus [29]. Furthermore, the recovery of Fv/Fm at 6 p.m. indicated the reversible photoinhibition, effective photoprotection, and photoadaptation of PSII of these macrophyte species. The ability of aquatic plants to survive under various conditions of light availability is partly related to their form, traits, photosynthetic structure, and mechanisms such as pigment contents, C3 and C4, and acclimation capacity to changing light and temperature [11,23,24,25,30]. These species contain chlorophyll a and b as light harvesting pigments and carotenoid as a photoprotection mechanism. Prior studies reported that the chlorophyll a to chlorophyll b ratio and chlorophyll a to carotenoid ratio indicate the size of light harvesting complexes and photoprotection capacity [31] and vary according to light and temperature changes. Changes in the pigment contents and these ratios may be further analyzed to confirm the photosynthetic strategy of these macrophytes.
The saturating irradiance (Ik) reflects the minimum light that saturates a plants’ capacity for photosynthesis. The results showed that the responses of plants located in the same position in the water exposed to a similar light regime were similar; for example, floating plants and roots with floating leaves that were light-adapted showed an increased Ik when light intensity was high. In contrast, the Ik of the submerged plants that were shade-adapted had a negative relationship with light intensity, and the Ik increased again at 6 p.m. due to the plants’ acclimation to prevent photodamage by excessive light. There is a different light intensity between under and above water surfaces, and underwater light was in the range of 40–80% of the ambient surface light in this study. This resulted in plants in different positions experiencing different light regimes. Lacoul and Freedman [11] reviewed that some species of submerged macrophytes are highly intolerant to shading, such as Chara spp. and Potamogeton alpinus, while others may grow in gaps beneath a well-established canopy, such as Ceratophyllum demersum, Hydrilla verticillata, Myriophyllum spicatum, Potamogeton crispus, P. pectinatus, and Urtricularia vulgaris [32,33].
To maintain a positive carbon balance and cope with light conditions, macrophytes have developed strategies such as modifying light harvesting capacity, light use efficiency, and rates of growth [34]. For example, when light is limited, plants might increase their chlorophyll content to enhance photosynthesis efficiency. In contrast, chlorophyll content may be decreased due to photodamage under high light conditions. For S. cucullata, there was no change in the Ik during the daily light cycle. However, there was an adjustment in photophysiology. The decrease in alpha (α) revealed that S. cucullata has a wide range of light tolerance.
The ∆F/Fm′ differed between species, which might indicate differences in light harvesting efficiency. In this study, the change in alpha revealed plants’ adaptation related to light use efficiency and flexibility to cope with different light regimes. There was a change in alpha for all species except N. lotus, revealing that N. lotus might be a wide-range light-tolerant plant whose photosynthesis efficiency is high even in full sunlight at 12 p.m. N. lotus exhibits sun plant characteristic and is able to maintain high rates of photosynthesis in full sunlight [35]. A similar study was conducted by Ritchie [35], who found that the Fv/Fm, rETRmax, and quantum efficiency of Nymphaea caerulea Saligny all vary on a diurnal cycle. The maximum relative electron transport rate (rETRmax) showed various responses, which depended on each species [35]. The highest rETRmax for each species in this study occurred at different times and, in all species, was related to ∆F/Fm′. After the rETRmax reached the peak, the ∆F/Fm′ of E. crassipes, and S. cucullata decreased at 3 p.m. and 6 a.m., respectively; those of N. lotus and N. stellata decreased at 3 p.m. and 9 a.m., respectively; and those of C. demersum and C. zeylanica decreased at 9 a.m. and 12 p.m., respectively. This relationship revealed a downregulation of photosynthesis, which decreased the light harvesting efficiency of plants [16].
Comparing the species, strategy for each species, and diurnal photosynthesis response, we found that E. crassipes, with their light stress tolerance and rapid growth rate, was a competing plant in the lake and tend to dominate in Songkhla Lagoon. This free-floating plant can monopolize light and absorb nutrients from the water column [36]. The extensive growth of E. crassipes has negative impacts on socioeconomic perspectives such as boating access, navigability and recreation, access to water supply for agriculture, and disturbed breeding or feeding in some living organisms. Thus, Songkhla Lagoon management should focus on controlling E. crassipes. Various applications of E. crassipes as biomass and biodiesel [37,38], electrode material [39,40], and heavy metal remover [41] have been investigated. However, high light exposure for submerged macrophytes should be avoided during lake restoration to prevent photoinhibition and photodamage. This study provides a better understanding of the photosynthetic response that enables species to adapt to changing light environments.

4. Materials and Methods

4.1. Study Site

Study site was located in Thale Noi (7º47′06″ N and 100º8′9.999″ E), Songkhla Lagoon, Thailand. Photosynthetic responses of six freshwater macrophyte species (Eichhornia crassipes, Salvinia cucullata, Nymphaea lotus, Nymphaea stellata, Ceratophyllum demersum, and Chara zeylanica) were investigated in April 2017. All six macrophyte species were collected (n = 4) from the same area, so interspecies comparisons of photobiology were therefore possible. Samples were maintained in freshwater during measurements. The measurement of maximum quantum yield of PSII (Fv/Fm) was made on the plant leaves after dark adaptation, and the rapid light curves (RLCs) measurements were made within 5 min of collection. Air and surface water temperature and irradiance were recorded hourly from 6 a.m. to 7 p.m. using a YSI Pro Plus multiparameter (YSI Incorporated, Ohio, USA) and Light Sensor Logger (LI-1500, LI-COR Environment, Nebraska, USA) (n = 3).

4.2. Maximum Quantum Yield (Fv/Fm)

Photosynthetic activity, as maximum quantum yield (Fv/Fm), was recorded by estimating chlorophyll a fluorescence using a Pulse Amplitude Modulated (MINI-PAM) fluorometer (Walz, Germany). Dark-adapted photosystem II (PSII) photochemical efficiency was measured as maximum quantum yield (Fv/Fm) after using a dark-adapted chamber for 15 min (n = 4). Fv/Fm was calculated from (Fm − F0)/Fm, where F0 represents the minimum fluorescence of dark-adapted biological materials, and Fm represents the maximum fluorescence after a saturating pulse is applied [42]

4.3. Rapid Light Curves (RLCs)

The photosynthetic performance of all six species was examined by performing RLCs using a PAM fluorometer (MIMI-PAM, Walz, Germany) (n = 4). RLCs with 9 increasing actinic light intensities (0, 66, 90, 125, 190, 285, 420, 625, and 820 μmol photons m−2 s−1) were applied, with 0.8 s saturating flashes (>4500 μmol photons m−2 s−1) between each actinic light intensity every 10 s [43]. The effective quantum yield of PSII (ΔF/Fm′ was calculated from (Fm′ – F)/ Fm′, where F represents the minimum fluorescence of light-adapted biological materials, and Fm′ represents the maximum fluorescence after a saturating pulse is applied [44]). The maximum relative electron transport rate (rETRmax) was calculated using ΔF/Fm′ × photosynthetically active radiation (PAR, measured in μmol photon m−2 s−1). The minimum saturating irradiance (Ik) and initial slope (α) of the RLCs were calculated using the curve fitting protocols outlined by Ralph and Gademann [14] and Sinutok et al. [43].

4.4. Data Analysis

Repeated ANOVA tests were performed to determine any significant differences in chlorophyll fluorescence parameters (ΔF/Fm′, rETRmax, Ik, α) among times and species, with a significant level of 95%. If data did not meet the assumptions of normality (Kolmogorov–Smirnov test) and equal variance (Levene’s test), the data were transformed using log10 or square root.

5. Conclusions

The photosynthetic responses of six freshwater macrophyte species were investigated. There was a significant difference among species and times, which revealed diurnal response and adaptation. The Fv/Fm and ∆F/Fm′ of all species decreased at midday (9 a.m.–3 p.m.), then returned to 6 a.m. levels by 6 p.m. Our results revealed that submerged plants and water surface plants showed different responses to cope with the light regimes. Changing light intensity and temperature in the future due to climate and anthropogenic changes might affect species composition and zonation in lakes. Further research on biochemical and physiological stress responses, photoprotective pigments, and enzyme activity for each species is thus warranted.

Author Contributions

Conceptualization, P.C. and S.S.; methodology, P.C. and S.S.; software, P.C. and S.S.; validation, P.C., S.S. and P.P.; formal analysis, P.C., S.S. and P.P.; investigation, P.C., S.S. and P.P.; resources, P.C. and S.S.; data curation, P.C., S.S. and P.P.; writing—original draft preparation, P.C., S.S. and P.P.; writing—review and editing, P.C., S.S. and P.P.; visualization, P.C., S.S. and P.P.; supervision, S.S.; project administration, S.S.; funding acquisition, P.C. and S.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was financially supported by the Thailand Research Fund and cofunded by The Commission of Higher Education (grant number: MRG6080129) and the Institute for the Promotion of Teaching Science and Technology (IPST) (grant number: 026/2559).

Data Availability Statement

Data available from corresponding author upon request.

Acknowledgments

We thank Raymond Ritchies and Anchana Prathep for their valuable support and access to Junior-PAM and light sensor and Faculty of Environmental Management, Marine and Coastal Resources Institute, and Coastal Oceanography and Climate Change Research Center for research facilities.

Conflicts of Interest

The authors declare no conflict of interest.

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Plants 11 02806 g001 550
Figure 1. Air and water temperatures (a) and light intensity of air and water (b) at Thale Noi, Songkhla Lake from 6 a.m. to 7 p.m. (n = 3). Data represent mean ± SE.
Figure 1. Air and water temperatures (a) and light intensity of air and water (b) at Thale Noi, Songkhla Lake from 6 a.m. to 7 p.m. (n = 3). Data represent mean ± SE.
Plants 11 02806 g001
Plants 11 02806 g002 550
Figure 2. Fv/Fm of six macrophyte species at Thale Noi, Songkhla Lake, from 6 a.m. to 6 p.m. for each species (n = 4). Data represent mean ± SE.
Figure 2. Fv/Fm of six macrophyte species at Thale Noi, Songkhla Lake, from 6 a.m. to 6 p.m. for each species (n = 4). Data represent mean ± SE.
Plants 11 02806 g002
Plants 11 02806 g003 550
Figure 3. RLCs of six macrophyte species at Thale Noi, Songkhla Lake, from 6 a.m. to 6 p.m. for Ceratophyllum demersum (a), Chara zeylanica (b), Nymphaea lotus (c), Nymphaea stellata (d), Eichhornia crassipes (e), and Salvinia cucullata (f) (n = 4). Data represent mean ± SE.
Figure 3. RLCs of six macrophyte species at Thale Noi, Songkhla Lake, from 6 a.m. to 6 p.m. for Ceratophyllum demersum (a), Chara zeylanica (b), Nymphaea lotus (c), Nymphaea stellata (d), Eichhornia crassipes (e), and Salvinia cucullata (f) (n = 4). Data represent mean ± SE.
Plants 11 02806 g003
Plants 11 02806 g004 550
Figure 4. ∆F/Fm′ (a), alpha (b), Ik (c), and rETRmax (d) of six macrophyte species at Thale Noi, Songkhla Lake, from 6 a.m. to 6 p.m. for each species (n = 4). Data represent mean ± SE.
Figure 4. ∆F/Fm′ (a), alpha (b), Ik (c), and rETRmax (d) of six macrophyte species at Thale Noi, Songkhla Lake, from 6 a.m. to 6 p.m. for each species (n = 4). Data represent mean ± SE.
Plants 11 02806 g004
Table
Table 1. Two-way repeated ANOVA summary table.
Table 1. Two-way repeated ANOVA summary table.
ParametersInteractionSSdfMSFp
Fv/FmSpecies0.23650.04736.714<0.001*
Error (Species)0.023180.001
Time0.06040.01514.619<0.001*
Species * Time0.094200.0054.568<0.001*
Error (Time)0.074720.001
∆F/Fm′Species0.32650.06526.376<0.001*
Error (Species)0.045180.002
Time0.14340.03614.572<0.001*
Species * Time0.335200.0176.827<0.001*
Error (Time)0.177720.002
alphaSpecies0.27250.05422.299<0.001*
Error (Species)0.044180.002
Time0.1211.4790.0828.7340.003*
Species * Time0.1197.3970.0161.7180.144
Error (Time)0.24926.6280.009
IkSpecies194592.651538918.53011.212<0.001*
Error (Species)62480.808183471.156
Time86722.464421680.6165.5490.001*
Species * Time378151.5752018907.5794.839<0.001*
Error (Time)281300.345723906.949
rETRmaxSpecies27906.05355581.21156.787<0.001*
Error (Species)1769.1041898.284
Time14831.34143707.83539.288<0.001*
Species * Time21566.338201078.31711.426<0.001*
Error (Time)6795.0257294.375
* Significant difference.
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Chotikarn, P.; Pramneechote, P.; Sinutok, S. Photosynthetic Responses of Freshwater Macrophytes to the Daily Light Cycle in Songkhla Lagoon. Plants 2022, 11, 2806. https://0-doi-org.brum.beds.ac.uk/10.3390/plants11212806

AMA Style

Chotikarn P, Pramneechote P, Sinutok S. Photosynthetic Responses of Freshwater Macrophytes to the Daily Light Cycle in Songkhla Lagoon. Plants. 2022; 11(21):2806. https://0-doi-org.brum.beds.ac.uk/10.3390/plants11212806

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Chotikarn, Ponlachart, Pathompong Pramneechote, and Sutinee Sinutok. 2022. "Photosynthetic Responses of Freshwater Macrophytes to the Daily Light Cycle in Songkhla Lagoon" Plants 11, no. 21: 2806. https://0-doi-org.brum.beds.ac.uk/10.3390/plants11212806

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