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The Influence of Variations in Salinity upon Photosynthesis in the Marine Alga Porphyra purpurea (ROTH) C. AG. (Rhodophyta, Bangiales)
Hartley Botanical Laboratories, University of Liverpool, P.O.Box 147, Liverpool, L69 3BX, Merseyside, U. K.
The Influence of Variations in Salinity upon Photosynthesis in the Marine Alga Porphyra purpurea (ROTH) C. AG. (Rhodophyta, Bangiales) R.
H.
REED,
J. C. COLLINS and G. RUSSELL
With 2 figures Received November 8, 1979 . Accepted December 31, 1979
Summary Steady-state photosynthetic responses of plants immersed in a range of concentrated and diluted seawaters have been determined. Net photosynthesis under hyposaline conditions was found to decrease in direct proportion to the reduction in salinity. Photosynthetic activity was increased in less extreme hypersaline media; in all other concentrated seawaters it was reduced. Photosynthetic activity of plants subjected to quasi-estuarine salinity fluctuations has been studied. Photosynthesis under such conditions was shown to decrease and increase in a synchronous manner, the rates of photosynthesis at any given point in time being similar to steady-state values for dilute seawaters of comparable salt content. Plants subjected to a single cycle of reduced salinity exhibited similar photosynthetic responses to those maintained under such conditions for 15 cycles. Key words: Porphyra, salinity, photosynthesis, quasi-estuarine salinity regimes.
The photosynthetic responses of species within the genus Porphyra have been investigated by several workers. Some studies suggest that photosynthetic activity is maximal in concentrated seawaters (e. g. OGATA and MATSUI, 1965) while others have shown that there is a depression of photosynthetic rate in all concentrated and dilute seawaters (e. g. ZAVODNIK, 1975). The present study was undertaken to examine photosynthesis in P. purpurea in a range of seawaters of varying salt content as part of a programme of research into aspects of the physiology of Porphyra under hyposaline and hypersaline conditions. The rate of net photosynthesis is of particular importance since it may directly influence the intracellular pool of «floridoside» (O-a-D galactopyranosyl-(l-+ 2)-glycerol, a primary photosynthetic product in the Bangiales). KAUSS (1969) has suggested that synthesis of «floridoside» due to increased photosynthetic activity in media of increasing salt content may provide a mechanism by which cellular solute concentration is altered in response to salinity Z. Pjlanzenphysiol. Bd. 98. S. 183-187. 1980.
184
R. H. REED, ]. C. COLLINS and G. RUSSELL
variation. This hypothesis is currently being tested and will form the basis of future research. Previous studies have been solely concerned with steady-state rates of photosynthesis following prolonged immersion in a variety of media. Data obtained from such experiments can only be related to certain specific conditions existing on marine rocky shores (e. g. to irregular salinity changes occurring in rock pools due to the effects of rainfall or evaporation; BIEBL, 1962). However, there are habitats which experience changes in salinity on a regular basis, these being the tidal mouths of rivers-«brackish» water estuaries (DEN HARTOG, 1971). Recently, DAVENPORT et al. (1975) described an apparatus which can be used to model quasi-tidal salinity changes similar to those found in fully-mixed estuaries. Such an apparatus has enabled us to study the effects of sinusoidal salinity fluctuations upon photosynthesis in P. purpurea. P. purpurea was collected from the mid-tidal region of the shore at Aberffraw, Anglesey, U.K. Discs were cut from healthy, non-reproductive portions of the monostromatic thalli using a cork borer. Plant material could be maintained in this form for more than 14 days in the laboratory. Net photosynthesis was measured using a thermostatically compensated oxygen electrode chamber at 288 K illuminated by means of a Bausch and Lomb type BDT projector fitted with a Thorn A1/8 bulb (at 35 X 10-5E . m-2 • S-l incident on the outer surface of the dlamber). An artificial seawater medium based on the ASP12 medium of PROVASOLI (1968), containing NaHCO a at 4 mol . m-a, was used throughout the present series of experiments. Media were prepared to give the following concentrations; X 1/16' X l/S' X 1/4, X 1/2 , X 3/4 X 1, X 1~, X 2, X 2~ and X 3 seawater. Discs of algal material were maintained in the above media for either 24 h or 168 h, with subsequent determination of photosynthetic rate. Photosynthesis under quasi-estuarine salinity regimes was also determined polarographically. An LKB 11300 Ultrograd Gradient Mixer was used in conjunction with a solenoid valve and mixing chamber to model salinity fluctuations as described in detail by DAVENPORT et al. (1975). The salinity regime used in the present study was a sinusoidal cycle, complete in 12 h, the amplitude of salinity change in this case being from X 1 to X 1/16 seawater since it was felt that repeated immersion in «freshwater» was unlikely to occur at the majority of estuarine sites in which P. purpurea has been recorded. Photosynthetic activity was assessed for plant material subjected to 1 cycle or 15 cycles of reduced salinity, thus giving comparable data to steady-state experiments.
Figure 1 a and 1 b represents the changes in photosynthetic rate of algal tissue immersed in a range of dilute and concentrated seawaters for 24 hand 168 h respectively. It is clear from Figure 1 a that photosynthetic activity is maximal in X 11/ 2 seawater, while all hyposaline and extreme hypersaline media result in a reduction in photosynthetic rate. Figure 1 b suggests that initial changes in photosynthesis in less extreme hyposaline and hypersaline media (X a/ 4 and X 11/ 2 seawater) may be transient since photosynthetic rates of plant material maintained for 168 h in such media are similar to those of X 1 seawater. In extremely dilute and concentrated seawater media (e. g. X 1/16 and X 3 seawater) the rate shows a decline rather than a recovery during the period 24-168 h following immersion. Z. Pflanzenphysiol. Ed. 98. S. 183-187. 1980.
Salinity and photosynthesis in Porphyra
185
3
..'e'. 1;
~ ODS!
1
~
0
...'2
4
u
t=====!====:±::====='==J b
~
.. • o
3
z
3 Seawater
Concentration
Fig. 1: Steady-state photosynthetic responses of Porphyra purpurea. Net O 2 production in a range of dilute and concentrated seawaters (X 1/16 to X 3 seawater) following immersion for (a) 24 h and (b) 168 h. Mean values (3 replicates) plus standard errors shown for each treatment.
It would seem that plants suffer permanent demage when maintained in X 1/16 seawater for 168 h. Light microscopic observations have revealed that up to 20 Ofo of the cells of tissues subjected to such treatment appear dead, having lost their phycobilin pigments and internal organization. Material equilibrated in X 1 seawater for 6 h following immersion in X 1/16 seawater for 168 h was subsequently found to photosynthesise at a rate which was less than 60 Ofo of the expected value for X 1 seawater. Plant material from X 3 seawater exhibited a greater recovery of photosynthetic rate on return to X 1 seawater after 168 h (to 80-95 Ofo of the expected rate).
Photosynthetic rates of material subjected to quasi-estuarine salinity regimes at 288 K under continuous illumination (4 X 10-5 E· m- 2 • S-1) for 1 cycle and 15 cycles are shown in Figure 2 a and 2 b respectively. Net photosynthesis is shown to undergo sinusoidal decreases and increases which are proportional to the extent of salinity Z. Pjlanzenphysiol. Bd. 98. S. 183-187. 1980.
186
R.
H.
REED,
J. C. COLLINS and G. RUSSELL
3
'.
N'
'~
!
'"S! K
1
~
01====±====:±====='======l
u
3
~
"~o
8
•
2
z
0+----+-----+------..-----1 o
9
6
Time
12
(h)
Fig. 2: Quasi-estuarine photosynthetic responses of Porphyra purpurea. Net O 2 production for plant material subjected to quasi-estuarine sinusoidal salinity regimes for (a) 1 cycle and (b) 15 cycles (X 1 to X 1/16 to X 1 seawater with a cycle time of 12 h) of reduced salinity. Data shown are individual values. change at any given point (c. f. Figures 1 and 2). It would seem that the time course for variations in salinity used in the present series of experiments was of sufficient duration to allow changes in photosynthetic rate to occur which are comparable to steady-state values. Figure 2 b shows that there is no evidence of a phase shift in the photosynthetic response, nor does the rate show any detectable degree of damping or enhancement after 15 cycles of reduced salinity. The data suggest that in estuarine habitats the rate of photosynthesis of P. purpurea will vary according to the external salinity, following a course which might have been predicted from the steady-state responses, although there was no a priori reason to suppose this to be the case. It has been stressed by DEN HARTOG (1967, 1971) that the salinity fluctuations occurring in estuaries may prevent many species, which can tolerate steady state reductions in salinity of similar proportion, from surviving in such habitats. MURRAY and LITTLER (1977) support this theory, maintaining that vegetation growing in habitats with fluctuating conditions is kept in a state of «disclimax». The present observations show that the photosynthetic rate of P. purpurea maintained for 168 h under quasi-estuarine conditions exhibits a slower decline than under steady-state hyposaline conditions (c. f. Figures 2 band 1 b). These observations do not support the theories of DEN HARTOG (1967, 1971) or MURRAY and LITTLER (1977). More data are required for a variety of algae under conditions of fluctuating salinity before these theoretical hypotheses can be adequately tested.
Z. Pjlanzenphysiol. Bd. 98. S. 183-187. 1980.
Salinity and photosynthesis in Porphyr'l
187
Acknowledgement This work is supported by a Science Research Council (U.K.) postgraduate award to R.H.R.
References BIEBL, R.: In: LEWIN, R. A. (Ed.): Physiology and Biochemistry of Algae, 799-815. Academic Press, New York and London, 1962. DAVENPORT, ]., LL.D. GRUFFYDD, and A. R. BEAUMONT: ]. Mar. BioI. Ass. U.K. 55, 391 (1975). HARTOG, C. DEN: Blumea 15, 31 (1967). HARTOG, C. DEN: Vie et Milieu 22, (supplement), 739 (1971). KAUSS, H.: Ber. Deut. Bot. Ges. 82, 115 (1969). MURRAY, S. N., and M. M. LITTLER: ]. Phycol. 13 (supplement), 47 (1977). OGATA, E. and T. MATSUI: Bot. Mar. 8,199 (1965). PROVASOLI, L.: In: WATANABE, A. and A. HATTORI (Eds.): Proc. U.S.-Japan Conf. Hakone, 63-75. lap. Soc. Plant Physiol., 1968. ZAVODNIK, N.: Bot. Mar. 18,245 (1975). R. H. REED, Hartley Botanical Laboratories, University of Liverpool, P.O.Box 147, Liverpool, L69 3BX, Merseyside, U.K.
Z. Pjlanzenphysiol. Bd. 98. S. 183-187. 1980.
The Influence of Variations in Salinity upon Photosynthesis in the Marine Alga Porphyra purpurea (ROTH) C. AG. (Rhodophyta, Bangiales) R.
H.
REED,
J. C. COLLINS and G. RUSSELL
With 2 figures Received November 8, 1979 . Accepted December 31, 1979
Summary Steady-state photosynthetic responses of plants immersed in a range of concentrated and diluted seawaters have been determined. Net photosynthesis under hyposaline conditions was found to decrease in direct proportion to the reduction in salinity. Photosynthetic activity was increased in less extreme hypersaline media; in all other concentrated seawaters it was reduced. Photosynthetic activity of plants subjected to quasi-estuarine salinity fluctuations has been studied. Photosynthesis under such conditions was shown to decrease and increase in a synchronous manner, the rates of photosynthesis at any given point in time being similar to steady-state values for dilute seawaters of comparable salt content. Plants subjected to a single cycle of reduced salinity exhibited similar photosynthetic responses to those maintained under such conditions for 15 cycles. Key words: Porphyra, salinity, photosynthesis, quasi-estuarine salinity regimes.
The photosynthetic responses of species within the genus Porphyra have been investigated by several workers. Some studies suggest that photosynthetic activity is maximal in concentrated seawaters (e. g. OGATA and MATSUI, 1965) while others have shown that there is a depression of photosynthetic rate in all concentrated and dilute seawaters (e. g. ZAVODNIK, 1975). The present study was undertaken to examine photosynthesis in P. purpurea in a range of seawaters of varying salt content as part of a programme of research into aspects of the physiology of Porphyra under hyposaline and hypersaline conditions. The rate of net photosynthesis is of particular importance since it may directly influence the intracellular pool of «floridoside» (O-a-D galactopyranosyl-(l-+ 2)-glycerol, a primary photosynthetic product in the Bangiales). KAUSS (1969) has suggested that synthesis of «floridoside» due to increased photosynthetic activity in media of increasing salt content may provide a mechanism by which cellular solute concentration is altered in response to salinity Z. Pjlanzenphysiol. Bd. 98. S. 183-187. 1980.
184
R. H. REED, ]. C. COLLINS and G. RUSSELL
variation. This hypothesis is currently being tested and will form the basis of future research. Previous studies have been solely concerned with steady-state rates of photosynthesis following prolonged immersion in a variety of media. Data obtained from such experiments can only be related to certain specific conditions existing on marine rocky shores (e. g. to irregular salinity changes occurring in rock pools due to the effects of rainfall or evaporation; BIEBL, 1962). However, there are habitats which experience changes in salinity on a regular basis, these being the tidal mouths of rivers-«brackish» water estuaries (DEN HARTOG, 1971). Recently, DAVENPORT et al. (1975) described an apparatus which can be used to model quasi-tidal salinity changes similar to those found in fully-mixed estuaries. Such an apparatus has enabled us to study the effects of sinusoidal salinity fluctuations upon photosynthesis in P. purpurea. P. purpurea was collected from the mid-tidal region of the shore at Aberffraw, Anglesey, U.K. Discs were cut from healthy, non-reproductive portions of the monostromatic thalli using a cork borer. Plant material could be maintained in this form for more than 14 days in the laboratory. Net photosynthesis was measured using a thermostatically compensated oxygen electrode chamber at 288 K illuminated by means of a Bausch and Lomb type BDT projector fitted with a Thorn A1/8 bulb (at 35 X 10-5E . m-2 • S-l incident on the outer surface of the dlamber). An artificial seawater medium based on the ASP12 medium of PROVASOLI (1968), containing NaHCO a at 4 mol . m-a, was used throughout the present series of experiments. Media were prepared to give the following concentrations; X 1/16' X l/S' X 1/4, X 1/2 , X 3/4 X 1, X 1~, X 2, X 2~ and X 3 seawater. Discs of algal material were maintained in the above media for either 24 h or 168 h, with subsequent determination of photosynthetic rate. Photosynthesis under quasi-estuarine salinity regimes was also determined polarographically. An LKB 11300 Ultrograd Gradient Mixer was used in conjunction with a solenoid valve and mixing chamber to model salinity fluctuations as described in detail by DAVENPORT et al. (1975). The salinity regime used in the present study was a sinusoidal cycle, complete in 12 h, the amplitude of salinity change in this case being from X 1 to X 1/16 seawater since it was felt that repeated immersion in «freshwater» was unlikely to occur at the majority of estuarine sites in which P. purpurea has been recorded. Photosynthetic activity was assessed for plant material subjected to 1 cycle or 15 cycles of reduced salinity, thus giving comparable data to steady-state experiments.
Figure 1 a and 1 b represents the changes in photosynthetic rate of algal tissue immersed in a range of dilute and concentrated seawaters for 24 hand 168 h respectively. It is clear from Figure 1 a that photosynthetic activity is maximal in X 11/ 2 seawater, while all hyposaline and extreme hypersaline media result in a reduction in photosynthetic rate. Figure 1 b suggests that initial changes in photosynthesis in less extreme hyposaline and hypersaline media (X a/ 4 and X 11/ 2 seawater) may be transient since photosynthetic rates of plant material maintained for 168 h in such media are similar to those of X 1 seawater. In extremely dilute and concentrated seawater media (e. g. X 1/16 and X 3 seawater) the rate shows a decline rather than a recovery during the period 24-168 h following immersion. Z. Pflanzenphysiol. Ed. 98. S. 183-187. 1980.
Salinity and photosynthesis in Porphyra
185
3
..'e'. 1;
~ ODS!
1
~
0
...'2
4
u
t=====!====:±::====='==J b
~
.. • o
3
z
3 Seawater
Concentration
Fig. 1: Steady-state photosynthetic responses of Porphyra purpurea. Net O 2 production in a range of dilute and concentrated seawaters (X 1/16 to X 3 seawater) following immersion for (a) 24 h and (b) 168 h. Mean values (3 replicates) plus standard errors shown for each treatment.
It would seem that plants suffer permanent demage when maintained in X 1/16 seawater for 168 h. Light microscopic observations have revealed that up to 20 Ofo of the cells of tissues subjected to such treatment appear dead, having lost their phycobilin pigments and internal organization. Material equilibrated in X 1 seawater for 6 h following immersion in X 1/16 seawater for 168 h was subsequently found to photosynthesise at a rate which was less than 60 Ofo of the expected value for X 1 seawater. Plant material from X 3 seawater exhibited a greater recovery of photosynthetic rate on return to X 1 seawater after 168 h (to 80-95 Ofo of the expected rate).
Photosynthetic rates of material subjected to quasi-estuarine salinity regimes at 288 K under continuous illumination (4 X 10-5 E· m- 2 • S-1) for 1 cycle and 15 cycles are shown in Figure 2 a and 2 b respectively. Net photosynthesis is shown to undergo sinusoidal decreases and increases which are proportional to the extent of salinity Z. Pjlanzenphysiol. Bd. 98. S. 183-187. 1980.
186
R.
H.
REED,
J. C. COLLINS and G. RUSSELL
3
'.
N'
'~
!
'"S! K
1
~
01====±====:±====='======l
u
3
~
"~o
8
•
2
z
0+----+-----+------..-----1 o
9
6
Time
12
(h)
Fig. 2: Quasi-estuarine photosynthetic responses of Porphyra purpurea. Net O 2 production for plant material subjected to quasi-estuarine sinusoidal salinity regimes for (a) 1 cycle and (b) 15 cycles (X 1 to X 1/16 to X 1 seawater with a cycle time of 12 h) of reduced salinity. Data shown are individual values. change at any given point (c. f. Figures 1 and 2). It would seem that the time course for variations in salinity used in the present series of experiments was of sufficient duration to allow changes in photosynthetic rate to occur which are comparable to steady-state values. Figure 2 b shows that there is no evidence of a phase shift in the photosynthetic response, nor does the rate show any detectable degree of damping or enhancement after 15 cycles of reduced salinity. The data suggest that in estuarine habitats the rate of photosynthesis of P. purpurea will vary according to the external salinity, following a course which might have been predicted from the steady-state responses, although there was no a priori reason to suppose this to be the case. It has been stressed by DEN HARTOG (1967, 1971) that the salinity fluctuations occurring in estuaries may prevent many species, which can tolerate steady state reductions in salinity of similar proportion, from surviving in such habitats. MURRAY and LITTLER (1977) support this theory, maintaining that vegetation growing in habitats with fluctuating conditions is kept in a state of «disclimax». The present observations show that the photosynthetic rate of P. purpurea maintained for 168 h under quasi-estuarine conditions exhibits a slower decline than under steady-state hyposaline conditions (c. f. Figures 2 band 1 b). These observations do not support the theories of DEN HARTOG (1967, 1971) or MURRAY and LITTLER (1977). More data are required for a variety of algae under conditions of fluctuating salinity before these theoretical hypotheses can be adequately tested.
Z. Pjlanzenphysiol. Bd. 98. S. 183-187. 1980.
Salinity and photosynthesis in Porphyr'l
187
Acknowledgement This work is supported by a Science Research Council (U.K.) postgraduate award to R.H.R.
References BIEBL, R.: In: LEWIN, R. A. (Ed.): Physiology and Biochemistry of Algae, 799-815. Academic Press, New York and London, 1962. DAVENPORT, ]., LL.D. GRUFFYDD, and A. R. BEAUMONT: ]. Mar. BioI. Ass. U.K. 55, 391 (1975). HARTOG, C. DEN: Blumea 15, 31 (1967). HARTOG, C. DEN: Vie et Milieu 22, (supplement), 739 (1971). KAUSS, H.: Ber. Deut. Bot. Ges. 82, 115 (1969). MURRAY, S. N., and M. M. LITTLER: ]. Phycol. 13 (supplement), 47 (1977). OGATA, E. and T. MATSUI: Bot. Mar. 8,199 (1965). PROVASOLI, L.: In: WATANABE, A. and A. HATTORI (Eds.): Proc. U.S.-Japan Conf. Hakone, 63-75. lap. Soc. Plant Physiol., 1968. ZAVODNIK, N.: Bot. Mar. 18,245 (1975). R. H. REED, Hartley Botanical Laboratories, University of Liverpool, P.O.Box 147, Liverpool, L69 3BX, Merseyside, U.K.
Z. Pjlanzenphysiol. Bd. 98. S. 183-187. 1980.