Matthew Perl ABSTRACT Spore packets from Smithora naiadum (Anderson) Hollenberg were shown to settle preferentially on its natural host Phyllospadix torreyi (S. Wats.) over several other natural and artificial substrates. Flourescein dye was introduced to both intact and rhizome-severed basal portions of Phyllospadix blades but showed little translocation beyond point of entry. This dispelled the possibility of distant translocation of nutrients through Phyllospadix and into its epiphytes. An attempt to qualitatively determine if Smithora receives biochemical communicants from its seagrass host yielded no such products. A possible procedure for approaching the question was developed though. A possible circadian variation in photosynthetic rate in the red alga Smithora was demonstrated. INTRODUCTION The red alga Smithora naiadum has been only described growing on two closely-related seagrasses, Phyllospadix torreyi and Zostera marina L. (Hollenberg, 1959). Harlin (1973a) reported culturing immature Smithora on a synthetic seagrass, "Olefern," but reproductive maturity was reached on natural hosts alone (Harlin, 1973b). Harlin (1973b) further demonstrated the movement of labelled carbon from seagrass host to Smithora epiphyte in culture. Possibly the red alga receives some nutrients or a biochemical developmental cue from its host. This "messenger" might well be derived from the host's photo- synthetic process. Sugars have been found to be passed Matthew Perl from autotroph to parasite (Smith, et al, 1969). Other plants have been demonstrated to leach photosynthetic products, some of which are subsequently reabsorbed (Tukey, 1970; Tukey & Mechlenburg, 1964). Brown algae actually absorb sugars from their environment which are later processed by the plant (Drew, 1969). Penhale and Smith (1977) found that Zostera released photosynthates into surrounding water and suggested that these products might be used for nutrition by the adjacent epiphytic community. Electronmicroscopy has shown there are no cytoplasmic connections between the laminae of the host seagrass and the rhizoids of the alga (McBride & Cole, 1969). Seagrass release, followed by algal reabsorbtion, presents itself as a candidate for the Smithora-Phyllospadix association. My investigations were aimed at helping to explain the alga's host specificity through nutritional requirements. In addition other experiments were also directed towards clarifying the symbiosis. Spore settling studies followed substrate preferences of the loosed marginal sori (spore packets). Daily tests were conducted to see if the algal sori preferentially land on their natural hosts or if random chance alone dictates where the spore bundles settle. Dye movement in the seagrass was examined as a possible indicator of nutrient flow between host and epi- phyte. Final experiments measured photosynthetic activity of the red alga over 24 hour periods to further describe Smithora itself. Circadian cycles, demonstrated in innu- merable plant and animal species, have received sparse attention in the algae until recently. Daily variation in photosynthetic capacity for a red alga Iridaea flaccida Matthew Perl reaches a maximum near noon, when available light also peaks (Harris, 1978). A daily cycle was shown for Ulva lactuca, and seasonal variations above and beyond the daily one were also discovered (Mishkind, et al, 1979). SPORE SETTLING am MATERIALS AND METHODS A special frame was built from 1 by 2 redwood with central horizontal strips to sandwich the substrates under examination (Figure 1). Phyllospadix, another sea plant Gracilaria, and a land plant of the cat-tail family Typha sp. were the organic substrates chosen. Rubber and glass were also tested. The substrates were prepared as thin strips to resemble the Smithora's natural hosts. Yellow flags attached to vertical posts facilitated location of the apparatus during high tides. The frame was freshly prepared with the substrates each morning for four consecutive days. Phyllospadix was cleaned of all epiphytes before being inserted; other substrates were examined to remove any blotches which might later be confused with algal spores. Four strips of each substrate served as replicates for each trial. The frame was tied to stakes in the lower intertidal such that it would remain submerged for all but the lowest tides. The tie stakes were planted adjacent to densely Smithora-covered Phyllospadix to insure availability of algal sori. The apparatus remained in the field for 24 hour inter- vals. At the time of collection it was removed from the stakes and brought into the lab where spore packets could Matthew Perl be counted. Each substrate strip was examined with a hand lens, and a record was made of the number of packets which had settled on it. The strips were then cleaned or replaced before the frame was returned to the field. 1 RESUDI Figure 2 shows the results of four runs. The Phyllospadix had a far greater number of spores land and attach than other substrates tested. The figures vary from one day to the next but are consistent for each day. All figures are lower estimates because spores which had landed on other spores could not be resolved. During the study it was observed that spore packets will wash off most substrates on which they settled except Phyllospadix. SION This experiment showed a marked spore preference for attachment to Smithora's natural host (Phyllospadix) over several other substrates, whether natural or synthetic. This phenomenon may be a derivative of the obligate rela- tionship between the seagrass and the alga. Smithora may be bound by some sticky, mucus-like substance on the Phyllospadix. Extracts of the seagrass, coated on glass rods, could be used to test this possibility. The frame received exposure to a full range of tides during the experiment. Some mornings the apparatus lay fully exposed. At other times it was submerged beneath three feet of water. These widely variable circumstances serve to substantiate results obtained rather than to com- plicate them. The data represents full exposure to tide fluctuations. These are the conditions under which sori will encounter their host seagrass as well as other substrates. Matthew Perl While settling data from one day to the next may not be compared quantitatively, the relative magnitudes of settling within each trial, a qualitative demonstration of host binding preference, stands up consistently. Thus I may say that in the ocean the spores tend to attach to Phyllo- spadix rather than to an old bottle or stray Gracilaria strand. That Smithora has a much greater binding rate to its host makes for a survival rate higher than chance landings alone. If there is a real physiological requirement, provided by seagrasses, for Smithora to mature, then a distinct preference for spores to settle on that host is a tremendous reproductive advantage. Particularly in the marine environment, where continual water motion is a rule, a true binding capacity of symbiote for its host is beneficial. NUTRIENT TRANSLOCATION The possibility that nutrients are absorbed through the roots of Phyllospadix and move up through the rhizome structure into the blades, as a prerequisite for transfer directly to the epiphytes, was examined. TR TERIALS AND M THODS A patch of the seagrass, lightly colonized, was uprooted and rinsed in seawater to remove debris and detritus from the intact root-rhizome system. Large blades of Smithora which might interfere with dye position determination were cut from the seagrass's laminae. The plants were divided into two similar clumps for parallel studies. One half had roots and rhizomes severed near the proximal portion of their sheathes; the other clump remained uncut. Through- Matthew Perl out the procedure the plants were submerged in ambient seawater. The basal ends of both seagrass portions were inserted into a concentrated flourescein-seawater solution (Figure 3). The blades were put into plain seawater. Tissue was draped over the air-exposed sections to prevent drying out and to prevent the dye from carrying from one vessel to the other across the Phyllospadix's surface. The plants were kept in the dye for four hours. Previous dry runs had shown longer exposures (up to 24 hours) to have negligible effect on the results of the experiment. The plant was exposed to light of intensity 13 pEin/m/s for the duration of the experiment. The baths varied in temperature from 17°C to 21°c. After the set interval the plants were removed from the apparatus and immediately washed in fresh water to remove dye from their exterior. They were then laid out on moist paper in a dark room. The plants were sectioned into 5 cm. lengths to prevent further dye movement and to simplify subsequent measurements. An ultraviolet lamp (UVSL 25 Mineralight) was used to determine the longitudinal distance the dye had penetrated each Phyllospadix blade. Also, the total length of each blade was measured. Finally a notation was made as to whether a particular blade was intact (designated normal) or had been torn at its distal end (broken). SULTS Table I summarizes the results of the simulated nutrient movement. Little translocation of dye beyond the surface of the flourescein solution was observed for normal blades. Matthew Perl The liquid in the dyeing vessel was 12 cm. deep; these blades had a mean dyed distance of 13 cm., both for sections with and without root structures. Broken strands of Phyllospadix (torn at the distal leaf tip) showed much greater dye transfer. In the sample clump which retained its root complex the dye moved an average of 23 cm. beyond the surface of the coloring solution. Most notable were the strands severed at both ends. These laminae moved the dye an average of 12 cm. or 98% of the average total length of all blades. ISCUSSION While many marine plants have been described that absorb nutrients through their root systems (McRoy & Goering, 1974), this mode of action is apparently not significant for Phyllospadix. Experiments on closely-related Zostera showed good uptake of, but minor subsequent movement of either "CO or 3P through the root-rhizome system (Penhale & Thayer. 1980). The absence of flourescein movement beyond the surface of the dye suggests that Phyllospadix used an alternate method of nutrient absorption as well. One might expect some residual level of root uptake since seagrasses are submerged vascular plants. However, it seems that as the sea permits the entire plant to be bathed in a nutrient broth, absorption via the entire leaf surface is a more efficient and effective way for the seagrass to "feed." Nutrient translocation after absorption by the root system would be minimized, as observed. The results of the dye movement studies cannot be considered absolutely conclusive. The flourescein molecule is larger than many inorganic nutrients like nitrogen and phosphorous. These smaller molecules may be more easily absorbed by the Matthew Perl roots. Experiments indicate otherwise however, showing negligible 'C uptake by roots or rhizomes when compared "C absorbed through the leaves (Barbour & Radosevich, 1979). Lateral sections of dyed Phyllospadix showed the dye tended to travel by way of three air canals of the lamina, probably by diffusion. These canals extend the length of the leaf and may play a role in gas transport in the plant. These tubes are sealed at the tip. When blades were severed at both ends they acted as siphons. Water was observed to move from a high reservoir to a lowerone via the blades. This activity explains the near complete transfer of dye through the broken, root-severed laminae. Most likely though this activity doesn't reflect on any life-preserving function in the real world. LEACHATE ANALYSIS An experiment was run to isolate and identify carbo- hydrates released by Phyllospadix into surrounding water. Later experiments would be aimed at demonstrating uptake of these sugars by the epiphytic community, if these nutrients could be located. THODS MATERIALS AND ! A portion of Phyllospadix was uprooted and transferred with seawater into the lab. The plant was rinsed in fresh water to remove microorganisms; all visible epiphytes were removed. The plant was inserted into the apparatus shown in Figure 4. The collection container into which the seagrass ran was called "active;" the other, "control." Each contained 900 ml. of 0.22 um filtered "Instant Ocean.' Matthew Perl The leaching experiment was conducted for five days. Water in the two collection vessels was continuously agitated by magnetic stirrers. The plant was exposed to 125 pEin/m/s on a light-dark cycle which approximated the normal daylight. Air-exposed seagrass parts were wrapped in plastic to reduce desiccation. The baths were kept at about 11 C. At the end of the experimental period the two collection solutions were filtered to remove all debris; centrifuged samples from each vessel showed no particulate impurities, so 600 ml. of fluid was poured off of each one. In a control experiment both active and control were spotted on paper chromatograms to check for the presence of carbohydrates. The solvent system used was n-butanol/ethanol/water (40:11:19); ammoniacal silver nitrate was sprayed on finished chromatograms to reveal any sugars (Benson, et al, 1950; Heftmann, 1967). For the final run the control aliquot was refrigerated while the active sample was lyophilized. The dried salts from the active chamber were then stored in a desiccator while the control was freeze-dried. Drying of both samples took five days. The next step in the analysis involved separating minute amounts of photosynthates presumably released by the seagrass from the large mass of sea salts to allow concentration of the organic fraction. Carbohydrates and inorganic salts share similar solubilities in most solvents, complicating separation. A trimethysilyl (TMS) ether formation promised to be the easiest to prepare and the most stable (Hammarstrand, 1968; Szymanski, 1968; Holligan & Drew, 1971). Derivative preparation involved replacing the sugars' hydroxy groups 10 Matthew Perl hydrogens with TMS groups. The appropriate reagent Sigma Sil-A (Sigma Chemical Co.) is a mixture of trimethylchlorosilane, hexamethyldisilazane, and pyridine (1:3:9). To each dry salt sample (active and control) 5 ml. of TMS reagent was added under nitrogen, following the directions supplied with the reagent. The major obstacle at this point was that the instructions recommended O.1 ml. reagent be used for each 1 mg. of sample. Because the reactant sugars were in a mixture with sea salts, it was impossible to know beforehand the concentration of sugars in each sample. Thus an anticipated excess of reagent was used. After two hours the reaction mixture was placed in 10 ml. of pesticide-grade hexane and vigorously shaken. The hexane would dissolve the sugars-turned-ethers; inorganic salts are insoluble in hexane. The solution was decanted to isolate organic fractions from salts. The liquid was placed on dry ice and taken to Stanford's main campus. The next morning 10 ul aliquots of the hexane-soluble components of both active and control solutions were to be gas chromatographed. LTS Paper chromatograms from the dry run developed poorly. Only random splotches appeared on them. The gas chromatogram of the active sample leachate derivative showed no peaks beyond those of standard background noise. The control was not processed because of the poor showing of the primary sample and because of the prohibitive cost of G.C. analysis. DISCUSSION Harlin's data suggest that there is some type of biochemical Matthew Perl communication between host and epiphyte of the Smithora- Phyllospadix complex (Harlin, 1973b). The preceding experiment supposed the most likely candidates for such a transfer would be carbohydrates. The primary suspects (fructose. sucrose, and an unidentified trisaccharide) were described by Drew data as the major free sugars of Phyllospadix leaves (Phillips & McRoy, 1980). I was unable to demonstrate that these or any other sugars are leached by the seagrass. This result most certainly doesn't serve to discount the hypothesis of a chemical messenger, nor does it discount sugars' involvement. If present, sugars may have been in minute concentrations, undetectable by the procedure which was followed. The TMS reagent could have been absorbed by the much greater mass of salts present in the mixture. Reagent concentration may have been diluted beyond reactive and detectable levels. Time constraints prevented repetition of this experiment. Should the general procedure be repeated, a more effective method should be sought for separating the salts from the suspected leachates. Radioactive carbon labelling also presents itself as a useful tool for identifying the leachates. Labelled compounds could be followed closely during many phases of the separation and analysis. Aside from sugars. other organic products are possible candidates for passing from seagrass to Smithora. These may serve as nutrients for epiphytes or in the capacity of hormone-like signals for induction of algal maturation. The identification of such transferred leachates should be actively pursued; this effort would contribute much towards elucidating the precise nature of the Smithora-Phyllospadix association. Matthew Perl 12 CYCLIC VARIATION IN SMITHORA PHOTOSYNTI STIC POTENTIAL The photosynthetic capacity of the red alga was monitored over two 24 hour periods. The results were correlated with natural light availability and tides. Possible relations between the data and the symbiosis under consideration were proposed. MA ERIALS AND METHODS The first half of this experiment consisted of the per- iodic collection of heavily colonized Phyllospadix at four hour intervals for a 24 hour period. Sections of Smithora were removed, and the alga's photosynthetic capacity at that particular time was measured. The second half of the exper- iment was conducted two days later and differed in that a large amount of epiphytized seagrass was collected at one time (6:30 A.M.). Again the photosynthetic activity of the alga was monitored at four hour intervals for one day. Smithora not being tested at a particular time was kept intact on its host in seawater at 12°0 with a light-dark regime to match the natural diurnal one. Photosynthetic rates of the epiphyte were measured on a Gilson Differential Respirometer. Slices 1.2 cm in area were made of Smithora blades. Six such sections were placed in each reaction vessel with 6 ml. of filtered seawater. 0.75 ml. of 0.035 M KHCO,/0.065 M NaHCO, buffer solution was placed in the flasks' sidearms to maintain a constant pressure of CO gas. Five replicates were run for each time period. along with a dark control (flask prepared as above but covered with black plastic) and a plain seawater control. Respirometer vessels were equilibrated for 30 minutes prior to each run. The respirometer bath was held at ambient Matthew Perl 13 ocean temperature of 12°0; shaking speed was 3. Lights for photosynthesis were partially shielded by mesh screens to exaggerate periodic fluctuations in the potentials; intensity was 60 pEin/m/s. Net change in oxygen within each reaction vessel was measured at fifteen minute intervals for approximately two and a half hours. The runs were stopped after two successive readings showed significantly reduced gas production as compared to earlier measurements. Mean oxygen production as ul/15 min. was calculated for each replicate. A single mean value was obtained for each time interval (6:00 A.M.. 10:00 A.M., 2:00 P.M., etc.). These numbers are plotted in Figure 5 along with daily light-dark cycle and tidal cycle for comparison. ESULT Smithora showed a pronounced, regular variation in photosynthetic capacity over 24 hour periods. The alga produced oxygen at a maximum rate in early morning. The rate drops during daylight hours and then climbs again during the night. There was a 25% difference between maximum and minimum production rates in the first trial (samples collected from the field for each time run). An overall change of 10% was observed for the second run (algal collection kept in controlled conditions for the duration of the experiment). Controls showed negligible changes in gas within their vessels, never producing nor consuming more than 1 ul of gas during any 15 minute period. Because of this insignificant rate as compared to those measured for Smithora in light, the controls were discontinued for the latter half of the second run. They do not appear on Figure 5. No measurement was made Matthew Perl between the hours of 5:00 P.M. and 12:30 A.M. on the first run because extreme high tide and darkness prohibited collection of samples. TTTSSION Drset There should be no surprise to find a daily rhythm in the photosynthetic capacity of the red alga. Insufficient data are available to call this particular rhythm circadian, but circadian rhythms have been demonstrated in many plants (as mentioned in the introduction). When plotted in con- junction with tidal and daylight cycles though, the variations take on an interesting perspective. The highest rates of gas production match times when the tides are lowest. As mean tide level climbs, the photosynthetic capacity declines. This phenomenon may be related to the position of Smithora on its seagrass host. The alga is found on distal portions of Phyllospadix. At high tide periods both host and epiphyte tend to lay well below the water's surface. During low tide Phyllospadix is often exposed to the air. However, epiphytic Smithora, because of its position on the host, usually floats just on the surface. Only during extreme low tides is Smithora ever exposed to air. While floating at the surface during low tides, the alga receives a maximum amount of light. It would be sound biological strategy for the alga to peak in its photosynthetic potential at these times. This is just what I observed. Finally, as the available sunlight declines during the day, the photosynthetic activity of Smithora drops also, preserving production energy for better conditions. The conclusions drawn above should be read with care. Photosynthetic measurements are tremendously variable. In 15 Matthew Perl order to standardize measurements, equal area sections of the alga were required. These could only be taken from the blades of Smithora. Presumably these structures possess the major photosynthetic apparatus in the mature algal specimens. Additionally, the procedure required that the largest blades of the alga be used. This may have biased my results to some extent. Finally, the season of the year could have a critical influence on the capacity for production of photosynthetic metabolites. One might expect higher rates would be measured in the Spring and Fall than in other seasons. The importance of these considerations (portion of plant used, age of samples, season) has been recently demonstrated by Littler and Arnold (1980) and deserves to be kept in mind whenever data on photosynthetic production is considered. SUMMARY I have attempted to demonstrate a few physiological implications of the symbiosis between the epiphyte Smithora The naiadum and its natural host Phyllospadix torreyi. information which I have presented includes: 1. The spore bundles of the algae show a settling preference for the host over several other organic and inorganic substrates. This would be important for host location and to insure survival of the species. 2. A dye was absorbed through the roots and rhizomes of the seagrass but showed negligible rates of translocation. This information leads one to conclude that nutrients are more likely taken up by all surfaces of the plant and used mainly where they are absorbed. 3. Carbohydrates may be leached out by the seagrass and Matthew Perl 16 subsequently taken up by the surrounding epiphytic community. However, I was unable to demonstrate either phenomenon. 4. The red alga Smithora shows a definite rhythm in its photosynthetic capacity which may be important in explaining its presence and position on the host Phyllospadix. ACKNOWLEDGMENTS My sincere thanks go to the entire faculty and staff at H.M.S. for their friendship and support this quarter. These fine people bring to Hopkins a warm, receptive stimulating climate for research and learning. Special thanks go to three people for guiding me along through the quarter. Dr. Robin Burnett, Dr.-to-be Celia Smith, and Dr. Isabella Abbott provided me with inspiration and insight. And in the end I have to thank Kimberly too, for she kept my spirit buoyed as it bobbed up and down with the tides. Matthew Perl 17 LITERATURE CITED Barbour, M.G. and Radosevich, S.R., 1979. 0 Uptake by the marine angiosperm Phyllospadix scouleri. Amer. J. Bot. 66(3): 301-306. Benson, A.A., Bassham, J.A., Calvin, M., Goodale, T.C.. Haas, V.A. and Stepka, W., 1950. The path of carbon in photosynthesis. J. Amer. Chem. Soc. 72(4): 1710-1719. Drew, E.A., 1969. Uptake and metabolism of exogenously supplied sugars by brown algae. New Phytol. 68: 35-13. Hammarstrand, K., 1968. Gas chromatographic analysis of carbohydrates. Varian Aerograph, Walnut Creek, 6 pp. Harlin, M., 1973a. "Obligate" algal epiphyte: Smithora naiadum grows on a synthetic substrate. J. Phycol. 9: 230-232. -1973b. Transfer of products between epiphytic marine algae and host plants. J. Phycol. 9: 243-248. Harris, J., 1976. Endogenous circadian rhythmicity of photosynthesis in the marine alga Iridaea flaccida (Rhodophyta) of the central California coast. Unpublished paper on file at Hopkins Marine Station, Pacific Grove. CA. Heftmann, E., 1967. Chromatography. Van Nostrand Reinhold Company, New York, 851 pp. Hollenberg, G.J., 1959. Smithora, an interesting new algal genus in the Erythropeltidaceae. Pacific Naturalist, 1(8): 3-11. Holligan, P.A. and Drew, E.A., 1971. Routine analysis by gas-liquid chromatography of soluble carbohydrates in extracts of plant tissues. New Phytol. 70: 271-297. Matthew Perl 18 Littler, M. and Arnold, K., 1980. Sources of variability in macroalgal productivity: sampling and interpretation. problems. Aq. Bot. 8: 111-156. McBride, D. and Cole, K., 1969. Ultrastructural characteristics of the vegetative cell of Smithora naiadum (Rhodophyta). Phycologia 8: 177-186. McRoy, C. and Goering, J., 1974. Nutrient transfer between seagrass Zostera marina and its epiphytes. Nature 218(5444): 173-174. Mishkind, M., Mauzerall, D., Beale, S.I., 1979. Diurnal variation in situ of photosynthetic capacity in Ulva is caused by a dark reaction. Plant Physiol., 64: 896-899, Penhale, P. and Smith, Jr., W., 1977. Excretion of dissolved organic carbon by eelgrass (Zostera marina) and its epiphytes. Limnol. and Ocean. 22(3): 4oo-407. Penhale, P. and Thayer, G., 1980. Uptake and transfer of carbon and phosphorous by eelgrass Zostera marina and its epiphytes. J. Exp. Mar. Biol. Ecol. 12(2): 113-123. Phillips, R.C. and McRoy, C.P., 1980. Handbook of seagrass biology: an ecosystem perspective. Garland STPM Press, New York, 353 pp. Smith, D., Muscatine, L., and Lewis, D., 1969. Carbohydrate movement from autotroph to heterotroph in parasitic and mutualistic symbiosis. Biol. Rev. 14: 17-90. Szymanski, H.A, 1968. Biomedical applications of gas chromatography, Plenum Press, New York, 198 pp. Tukey, Jr., H.B., 1970. The leaching of substances from plants. Ann. Rev. Pl. Phys. 21: 305-324. Tukey, Jr., H.B. and Mechlenburg, R.A., 1964. Leaching of metabolites from foliage and subsequent reabsorbtion and : 737 ichate in plants. Am. J. Bot. Matthew Perl 7 30 CM V 38 CM —a SUBSTRATES —— 0 TET 0 TIE LINE I —— — 19 Matthew Perl 40 30 20 10 40 30 5 20 E 10 g 40 § 30 20 10 40 30 20 10 37 16 35 26 12 DAY 1 DAY 2 DAY 3 DAY 4 —0- SUBSTRATE 20 FIG 2 Matthew Perl 21 12CM FIG 3 Matthew Perl G 22 A V SIDE VIEW 4 H O E N TOP VIEW FIG 4 Matthew Perl 2 L 0 e— 8 e TIDE HEIGHT (FT) e —0— e e 1 — OooO SAIONIN SI/GHATOAS 0 SaSIHOHDIN 23 J0 0 o 10 o Matthew Perl Root Condition Intact: Severed: Table I DYE MOVEMENT STUDY Ti Distance Dye Moved S X(cm) s f 13 3.1 36 Normal 35 11.5 12 Broken Normal 13 2.3 33 Broken 42 8.4 10 % Length w/ Dye S 20% 6.3 36 66% 22.2 12 23% 3.8 33 98% 3.3 10 0 Matthew Perl TABLES lable 1. Dye Movement Study.