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Doty 1946). For latitudinal distances, marine algal distribu- tions span hundreds of kilometers of coastline, and many algae have been identified as warm- or ...
Oecologia 9 Springer-Verlag1986

Oecologia (Berlin) (1986) 70:6-12

Recovery of photosynthesis after exposure of intertidal algae to osmotic and temperature stresses: comparative studies of species with differing distributional limits Celia M. Smith 1., and Joseph A. Berry 2 1 Hopkins Marine Station of Stanford University, Pacific Grove, CA 93950, USA 2 Carnegie Institution of Washington, Department of Plant Biology, Stanford, CA 94305, USA

Summary. This study examines possible relationships between stress tolerance by marine algae and distributions of these species. The ability to recover photosynthetic activity following dehydration or temperature treatments was the assay used to evaluate stress tolerance, and Porphyra perforata, Rhodoglossum affine, Gelidium coulteri, and Smithora naiadum differed in thresholds of tolerance, even though plants were collected from low tidal sites. Limits of dehydration tolerance were well correlated with limits o f tidal distribution for these species. Additionally, other high tidal species tolerated severe dehydration while subtidal and low tidal species were sensitive to dehydration. High tidal individuals of P. perforata were also more tolerant of dehydration than were low tidal thalli of P. perforata. Limits of high or low temperature tolerance were not well correlated with tidal elevation for any groups of algae studied. However, cold-tolerant species had more northerly extensions, and warm-tolerant species had more southerly distributions. Thus, differential tolerance to temperature extremes may be an important influence for latitudinal ranges of species. By comparing the experimentally determined thresholds of stress with distributions of species, we test the role of stress in influencing photosynthesis and ultimately distributions of marine algae. Key words: Photosynthesis - Osmotic stress - Temperature Stress - Algae - Intertidal region - Porphyra perforata Rhodoglossum affine - Gelidium coulteri- Smithora naiadum

Biological interactions and environmental stress (Connell 1972; Dring and Brown 1982; Druehl 1982; Underwood and Denley 1984) are thought to influence the occurrence of marine algae and result in discrete distributions of species. In the intertidal region algae are distributed in relatively narrow zones, where at upper elevations high tidal species are wetted by high tides, and at lower elevations low tidal species are rarely exposed by low tides (Chapman 1942;

* Present address and offprint requests to: Department of Botany, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA

Doty 1946). For latitudinal distances, marine algal distributions span hundreds of kilometers of coastline, and many algae have been identified as warm- or cold-water species (Biebl 1970, 1972; Druehl 1982). Several physiological studies suggest that differences in the abilities of species to tolerate stress are responsible for observed differences in algal distributions (Chapman 1966; Johnson et al. 1974; Quadir et al. 1979; Dring and Brown 1982). Few studies have compared stress tolerances and the distribution of algae at more than one tidal elevation. This shortcoming may be the result of time-consuming limitations by conventional techniques. In this study, we introduce a reproducible and rapid assay to detect thresholds of photosynthetic tolerance to dehydration and temperature extremes. By comparing physiological tolerances with distributions for algal species, we test current hypotheses on stress responses in several species occurring in various intertidal and latitudinal ranges. Materials and methods

Plant collections Tidal elevations of sites were determined by surveying from USGS benchmark "Station Mussell 1932" at Hopkins Marine Station, Pacific Grove, California to the areas of interest. To determine tidal ranges for common algae, transects from 0.3 to 1.8 m elevations were run with 20 • 25 c m 2 quadrats. This survey was conducted at the same field site and season from which samples were collected for physiological studies. Fresh plant samples were collected from surveyed tidal elevations, and used within 8 hr of collection for photosynthetic measurements. Sections of vegetative blades of Macroeystis pyrifera growing less than one meter below the canopy's surface were collected from plants in the inner fringe of the kelp forest at Hopkins. All other subtidal samples were collected at a depth greater than 8 m. All collections were maintained for 1-8 hr in tanks with flowing seawater under ambient irradiance at 14+ i ~ C. Any intertidal species collected during low tides were rehydrated for at least 1 hr before use. Vegetative tissues were cut from thalli, and weighed immediately before photosynthetic measurements. Discs

0.37 cm 2 were punched from thalli of Fucus distichus L., Gigartina corymbifera (Kutz.) J. Ag., Hesperophycus harveyanus (Decne.) S. & G., Iridaea flaccida (S. & G.) Silva, Macrocystis pyrifera (L.) C. Ag., Mastocarpus papillatus (C. Ag.) J. Ag., Porphyra perforata J. Ag., Porphyra nereocystis Anders., Smithora naiadum Hollenb., and Ulva taeniata (Setch.) S. & G. For branched species, Endocladia muricata (Post. & Rupr.) J. Ag., Gigartina canaliculata Harv., Gelidium coulteri Harv., Rhodoglossum affine (Harv.) Kyt., and Pelvetiafastigata (J. Ag.) De Toni, apical tips or lateral branches were used.

Photosynthesis measurements Rates of photosynthesis were measured polarographicatly at 15~ C, with a temperature-controlled, water-jacketed, Clark type oxygen electrode (Rank Bros., Cambridge, England). The electronics were modified to have the usual output of the electrode and a 10 x expanded scale output with an adjustable offset bias. Both signals were recorded on a 2 channel potentiometric recorder (E & K Scientific Products, Saratoga CA). A tungsten halogen lamp (GTE Sylvania) served as a light source. Tissues were mounted on a 1.0 cm 2 stainless steel grid attached to the chamber seal. The grid allowed tissues to be oriented perpendicular to incoming light and held tissue stationary within the stirred electrode compartment. Appropriate fluence rates of light were selected with neutral density filters (Ditric Optics, Hudson MA), and measured with a quantum sensor (Licor Inst Corp, Lincoln NB). For photosynthetic measurments, seawater was modified by addition of 45 mM hydroxyethlypiperazine - ethanesulfonic acid (HEPES) buffer and acidified with concentrated hydrochloric acid to pH 3. It was then diluted with distilled water to normal salinity, 34 0/00, and bubbled with nitrogen gas for 24 h. This CO2 free medium was titrated to an appropriate pH with saturated (CO2 free) sodium hydroxide. Bicarbonate was added from 1 M stock solutions to the appropriate final concentrations and pH 8.20 for medium, in the electrode chamber. Media used to determine photosynthetic response to salinity contained appropriate amounts of salt for the range 0.27 to 1.66 M sodium chloride in seawater. Tissues were allowed to equilibrate for 10 rain in low light before measurement of photosynthesis. Steady state rates were determined by following the rate of oxygen evolution in 4.8 ml of medium containing 20.8 mM bicarbonate and 50 gmol dissolved O2, for 20 to 30 min. Saturating but not damaging fluence rate of 700 gmol quanta m - 2 s- 1 was used to surveys species. Media was changed about every 10 min to minimize bicarbonate depletion.

mental conditions. Osmotic treatments were conducted at 21 ~ C. Temperature treatments were imposed in seawater at normal salinity. All treatments were conducted at approximately 15 gmol quanta m -2 s 1 in air saturated seawater. Unless otherwise stated, 10 rain treatments were used for these assays. Algal samples were then transferred to the oxygen electrode (with fresh medium at normal salinity and temperature) and any remaining photosynthetic activity was measured for 30 min. A final rate was expressed as a percent of the pretreatment rate measured for that sample. Means of three to five replicates are presented for each treatment. Replicates were measured in a rotating order over several days to minimize any possible influences of circadian or tidal rhythms.

Results

Photosynthetic responses by Porphyra perforata to environmental factors The fluence rate required to saturate photosynthesis of the widely distributed intertidal alga, Porphyra perforata, at 15~ was approximately 30011mol quanta m - 2 s 1 (Fig. t A). These rates were stable when measured at fluence rates as high as 1,000 gmol quanta m 2 s - l , and 15~ C. At ambient oxygen concentration, photosynthesis was about half saturated at 2.1 mM bicarbonate - ambient seawater concentration. The requirement for bicarbonate was lower at reduced oxygen concentrations, but at high bicarbonate concentrations low and ambient oxygen concentrations had little effect on the maximum rate of photosynthesis (Fig. 1 B). At normal salinity, photosynthesis was maximal (Fig. 1 C), while the rate of photosynthesis under hyperosmotic conditions reached about 50% at 0.96 M NaC1 in seawater. Temperature needed for optimal photosynthetic performance ranged from about 20 to 30~ (Fig. 1D), while the rate of photosynthesis at local ambient seawater temperature, 15~ C, was about 85% of maximal performance. Above 30~ or below 15~ C, photosynthesis declined. Saturating light and bicarbonate levels and low oxygen concentration were used in subsequent analyses of photosynthesis to minimize variations in the photosynthetic activity that might occur with small variations in carbon and oxygen concentrations. In order to assess the variability of photosynthetic activity, 12 discs were sampled from 6 plants of P. perforata at the same tidal site. These discs had a mean fresh weight of 7.32 + 0.87 mg cm-2 of blade area and gave a mean photosynthetic rate of 8.30 _+0.57 gmol oxygen evolved an- 2 s I (mean _+1 SD). -

Stress treatments For hyperosmotic treatments, separate solutions of selected osmotic strengths were prepared by the addition of appropriate amounts of salt for 0.7 to 5.4 M sodium chloride in seawater, and buffered to pH 8.20. Calculated increases in salinities were checked with a Goldberg temperature compensated refractometer (A & O Corp, Buffalo NY). Stress treatments were imposed on algal samples allowed to reach steady state rates of photosynthesis by quickly transfering the tissue to a second electrode chamber. This second chamber was maintained at appropriate experi-

Effects of temperature treatments on photosynthetic recovery The effects of exposing tissues to extreme temperature encountered by P. perforata during low tides in central California were investigated by following subsequent photosynthetic performance. For unstressed samples, maximal photosynthetic rate at 15~ was reached within 20 min after beginning illumination (Fig. 2A). Recovery of discs treated at 37~ was damaged, as evident from reduced capacity

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Fig. 1 A-D. Response of photosynthesis to different factors: A Light response of photosynthesis for discs punched from blades of Porphyra perforata. Photosynthesis was measured at 15~ C, ambient salinity (34 0/00), pH 8.20, 20.8 mM bicarbonate, and low (20 to 50 gmol) dissolved 02. Data are expressed as ~tmol oxygen evolved m-z s-1. B Response of photosynthesis to bicarbonate and oxygen. Photosynthesis was measured at 800 gmol quanta m- z s 1 fluence rate, and experimental concentrations of bicarbonate and oxygen. All else as in A. C Response of photosynthesis to osmotic dehydration. Photosynthesis was measured at experimental osmotic concentrations, and 800 gmol quanta m -a s- 1 fluence rate. All else as in A. D Response of photosynthesis to temperature. Photosynthesis was measured at experimental temperatures, and 800 gmol m 2 s- 1 fluence rate. All else as in A

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Effects of dehydration treatments on photosynthetic recovery The effects of exposing tissues to a range of dehydration encountered by P. perforata during low tides in central California were investigated by following subsequent photosynthetic recovery (Fig. 3A). Photosynthetic recovery, after 10 rain exposures to select dehydration treatments, was substantially lower than those of the controls (Fig. 3A). A threshold of tolerance to dehydration was detected (Fig. 3 B). This threshold extended beyond the range over which photosynthetic activity was measureable for P. perforata (compare Figs. 1 C and 3 B). This study of dehydration tolerance was extended to other low tidal species that differ in upper limits of tidal distribution (Table 2). Low tidal thalli of P. perforata were more tolerant of dehydration (Fig. 3 B) than were the other low tidal species. Our next study assessed the responses of a variety of species to routine levels of tissue dehydration for high tidal algae during midday low tides in central California. Individuals of P. perforata (Table 3) and of 11 other species (Table 4) were collected from several tidal elevations. Osmotic concentrations were chosen from results of preliminary tests which showed that the selected level of dehydration could probe the sensitivity of low and mid-tidal algae to dehydration, but not eliminate their responses (data not shown). Results of these surveys suggest that tolerance of dehydration is well correlated with tidal elevation at which thalli were collected. For example, high tidal individuals of P. perforata, and other high tidal species were tolerant of severe dehydration. Low tidal individuals of P. perforata

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Table 1. P r e t r e a t m e n t rates o f photosynthesis and percent o f p h o t o synthesis recovered after 10 rain treatments at 3 7 ~ in seawater for individuals o f Porphyra perforata from different tidal elevations. Recoveries are expressed as a percent o f p r e t r e a t m e n t performance that was re-established after 30 rain at 15 ~ C and ambient salinity. See text for discussion o f infected thalli at 0.3 m. M e a n rates o f photosynthesis are given as gmol oxygen evolved m - 2 s~ i • SE, n = 5 Elevation m

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Table 2. Distribution characteristics for four low tidal algae at H o p k i n s Marine Station

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and other species restricted to low tidal elevations, were impaired by this treatment. Species, such as Maerocystis pyrifera or Gigartina canaliculata, found only in areas that are never or rarely exposed, were sensitive to severe dehyd r a t i o n (Table 4).

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Fig. 4A, B. Comparisons of ranges in physiological tolerances with distributions of species along environmental gradients : A Comparison of ranges in dehydration tolerated by four species, with their respective uppermost tidal distributions at Monterey Bay, California (taken from Table 2). B Comparison of temperatures tolerated by four species with their respective latitudinal distributions north and south of Monterey Bay, California (Conway et al. 1975; Abbott and Hollenberg 1976)

Table 3. Pretreatment rates of photosynthesis by individuals of Porphyra perforata from different tidal elevations, and percent of photosynthetic rate recovered after a 10 min treatment to a select dehydration level (4,1 M NaC1 in seawater). Recovery is given as a percent of pretreatment performance that was re-established after 30 min at 15~ C and ambient salinity. Mean rates of photosynthesis are expressed as pmol oxygen evolved m -2 s-1, • ] SE, n= 5

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The significance o f results from our osmotic d e h y d r a t i o n studies is best u n d e r s t o o d in the context o f how these treatments relate to tissue d e h y d r a t i o n experienced by algae in the field. The rationale behind using osmotic d e h y d r a t i o n comes from observations that air-drying tissues of intertidal algae concentrates salts in cell walls. W e reasoned that immersing tissues in hyperosmotic solutions o f salt in seawater m a y have effects similar to air-drying. Several lines o f evidence support the suggestion that air-drying and osmotic d e h y d r a t i o n have similar effects on algal tissues. Cell volumes decrease after treatment to b o t h types o f drying (Smith et al. 1986). Fluorescence emission from the photosynthetic a p p a r a t u s o f P. perforata is recovered after treatment to both types o f drying (Smith et al. 1982). Fluorescence emission from the photosynthetic apparatus o f a subtidal species is disrupted after treatment to both types of drying (Smith et al. 1982). High tidal species are tolerant while low and subtidal species are intolerant of b o t h types o f drying (Biebl 1952). The extent o f water loss experienced by algae in the field varies with timing of tide (early morning, midday, late afternoon, evening), and d u r a t i o n o f exposure (Isaac 1933; C h a p m a n 1962; G l y n n 1965; Smith unpublished work). During a typical m i d d a y low tide in central California, low tidal plants m a y be exposed for only 1 h and dehydrate to 85% R W C (Smith 1984b). During the same day, high intertidal algae can be exposed for 6 or more h. Three h o f drying is sufficient exposure to dehydrate tissues from 100% relative water content ( R W C ) to a b o u t 15% R W C

11 (Smith 1984 b), and to bring water potentials from - 2 MPa to - 9 MPa (Smith unpublished work). These thalli usually have a layer of salt on thallus surfaces, and remain at very low water content until an incoming tide rehydrates tissues. It is likely that salts in cell walls of drying thalli withdraws water from cells to a water potential defined by the hypersaline solution. Consequently, immersion of algal tissues in highly saline solutions ( > 3 M NaC1 in seawater) in some ways mimics dehydration of tissues to low water potentials experienced by algae in the field. The use of this technique assumes that solutions do not cause damage by ion-specific effects, and use of other osmotica, such as sorbital, gave similar results.

Significance of dehydration to algal distributions Dehydration intolerance is hypothesized to be a major factor determining upper limits of distribution for intertidal algae (Doty 1946; Chapman 1966; Dring and Brown 1982). To test this hypothesis, we compared known tidal distributions (Table 2) with photosynthetic tolerances of dehydration (Fig. 4A). These results, and all of our survey results are consistent with the suggestion that dehydration intolerance limits upper distributions of low and mid-tidal species. High tidal algae are tolerant of long periods of severe dehydration (Isaac 1933; Biebl 1950; Chapman 1962; Dring and Brown 1982). The uppermost limit is likely to be the result of secondary effects from tissue dehydration: insufficient carbon gain when tissues are drying, reduced photosynthetic capacity when tissues are fully hydrated (this study), and reduced growth (Edwards 1977; Chock and Mathieson 1976; Smith 1984a). The physiological limitations which restrict subtidal and low tidal species from higher tidal areas can probably be accounted for by damage to primary processes of photosynthesis from severe dehydration (Wiltens etal. 1978; Hodgson 1981; Smith etal. 1982; Smith et al. 1986). Tolerance of tissue dehydration increases with tidal exposure for individuals of P. perforata from different tidal elevations. Part of the success of species with wide tidal distributions may be the ability of individuals to physiologically adjust to varying levels of stress at particular tidal elevations. Results of transplantation experiments also suggest this possibility (Schonbeck and Norton 1978). Biological interactions among species (Connell 1972; Hruby ] 976; Hodgson 1980) are generally thought to maintain usual lower limits of tidal distribution for algae. Yet, P. perforata is not found in less exposed tidal elevations, even though a comparison of photosynthetic rates indicates that this alga could outgrow algae in subtidal areas. When several individuals of P. perforata were found at a very low tidal elevation, these thalli had low photosynthetic rates and pathogens present in tissues. It seems that pathogens of P. perforata are abundant in seawater (Goff and Glasgow 1980), and that too little air-drying eliminates this disease-susceptible alga from subtidal areas (Smith and Berry unpublished work).

Significance of temperature tolerance to algal distributions Temperature of seawater is hypothesized to be a major factor influencing distributions of algae into different biogeographic regions (Druehl 1982). To test the role of tempera-

ture tolerance for latidudinal distributions of marine algae, we calculated the distribution for four species based on known ranges (Table 2), and compared latitudinal distributions with photosynthetic tolerance of temperatures extremes (Fig. 4 B). Reasons for the correlation between temperature tolerance and latitudinal range are not fully clear, but the result suggests that physiological adaptations to temperature may play a role in determining latitudinal ranges of species. Additionally, the tidal elevation at which intertidal species are distributed appears to change with latitude (Colinvaux 1966). That report report may explain why G. coulteri has not been collected in waters as cold as it appears to be able to tolerate; this alga may have been overlooked if it was growing in shallow subtidal areas. The cold temperature tolerance of this alga was not included in the regression analysis of Fig. 4B. A great deal more work is needed to define the relationship between temperature and latitudinal distribution. Tolerance of high temperatures by intertidal algae does not appear to be an important influence for tidal distributions of marine algae, even though during low tide exposures, high tidal species may heat to temperature twice those of low tidal species (Glynn 1965; Smith 1984b). The greatest increases in tissue temperature for intertidal algae generally occur when individuals are drying while exposed during low tides (Glynn 1965; Smith 1984b). For dehydration tolerant bryophytes, an increased tolerance to high temperatures is latently expressed when tissues are dehydrated (Norr 1974); similar responses may be found for many intertidal marine algae.

Conclusions

Results presented here show marked correspondence bet w e e n photosynthetic tolerance to environmental stresses by marine algae and the distributions of these species. While we cannot discount the potential importance of biological factors as influences on species distributions, these results support the hypothesis that environmental factors influence photosynthesis, and ultimately, distributional patterns of marine algae along intertidal and latitudinal gradients.

Acknowledgments. This work is a result of research sponsored in part by NOAA, National Sea Grant College Program, Department of Commerce, under grant number NA 80A-D-00120, through the California Sea Grant College Program, and in part by the California State Resources Agency, project numbers R/A -34, -49, and R/F --58. The US Government is authorized to reproduce and distribute for governmental purposes. The first author would like to also acknowledge generous support and encouragement from Dr. Isabella A. Abbott, the Wilkinson Foundation, the Carnegie Institution of Washington, Department of Plant Biology, and the Miller Institute for Basic Research in Science, University of California, Berkeley. Comments on several drafts from W Briggs, E Gantt, C Pringle, R Robichaux, J West and anonymous reviewers greatly improved the manuscript.

References

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Received December 4, 1985