Maintenance of a balanced, shifting boundary between the seagrass Phyllospadix and algal turf

Aquatic Botany, 33 (1989) 223-241

223

Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands

M A I N T E N A N C E OF A B A L A N C E D , S H I F T I N G B O U N D A R Y BETWEEN THE SEAGRASS P H Y L L O S P A D I X AND ALGAL TURF

JOAN G. STEWART

A-002, Scripps Institution of Oceanography, University of California, La Jolla, CA 92093 (U.S.A.) (Accepted for publication 23 November 1988)

ABSTRACT Stewart, J.G., 1989. Maintenance of a balanced, shifting boundary between the seagrass PhyUospadix and algal turf. Aquat. Bot., 33: 223-241. A dense mat of algal turf covers much of the rocky mid-intertidalsubstrate on beaches in southern California. Beds of Phyllospadix dominate the lower part of the intertidal zone. The study was designed to identify processes that result in this distribution pattern. To evaluate the role of direct plant/plant interactions, changes in the position of the border were measured in undisturbed vegetation and in clearings between two dominant taxa, P. torreyi S. Watson and CoraUinapinnatifolia (Manza) Daws. Recovery of the substrate in clearings within the bed was monitored. Growth rates for prostrate and erect portions of each of the taxa were determined. To assess the effect of environmental factors on each of the two vegetation forms intact clumps were reciprocally transplanted, leaves were removed experimentally under several conditions, and leaf length and density, seasonally and in different habitats, were compared. Analysis of biomass data showed that longer leaves are restricted to wetter habitats. Leaves turned brown when exposed to air, indicating that shoreward extension of the Phyllospadix beds is constrained by physical factors. When the rhizome mat was removed from rocks, CoraUina regenerated and within several months its turf covered the area. Rhizomes slowly regrew into turf, unimpeded by algal thalli or the layer of sand that often buries rhizomes and basal portions of thalli. Corallina and PhyUospadix share certain morphological and life history properties that are adaptive to seasonal weather patterns and the effects of sand movement on these intertidal platform beaches; each has distinct advantages on short or longer time scales within the boundary zone where one form replaces the other at a discrete border.

INTRODUCTION

Zonation patterns for intertidal plants are often explained both in terms of the effects of conditions that limit distributions of individual species, and as consequences of competition between species. On rocky beaches the abundances of many species follow gradients from high on the beach, where at-

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© 1989 Elsevier Science Publishers B.V.

224

tached organisms frequently are exposed to drying for many hours during a tidal cycle, into shallow subtidal sites where they always are submerged. Chapman (1973) reviewed studies of marine algae and suggested that biological interactions, rather than physiological tolerance limits, are of prime importance in establishing clearly demarcated zones in intertidal regions. Pielou ( 1974 ) included seaweeds in a model that invoked competitive interactions to explain transition zones. More recent field work has demonstrated that where upper limits for algae in the intertidal region are regulated by relative tolerances to physical factors, mechanisms often are unclear (Schonbeck and Norton, 1978, 1980; Lubchenco, 1980; Kastendiek, 1982). Experimental studies on rocky intertidal shores showed how the lower limit of a barnacle was regulated by interspecific competition for space and then suggested that lower distributions for many other intertidal species also might be determined mainly by biotic factors (Connell, 1961). The importance of predation and competition in setting lower distributional limits was recently discussed by Lubchenco (1980). Populations of PhyUospadix torreyi S. Watson and P. scouleri W. Hooker form extensive beds across low intertidal and shallow subtidal rocky beaches from southern Canada to Mexico. Many of the algal species (Stewart, 1982) that compose the turf on rocks above mean lower low water (MLLW) (0 datum), also grow as discrete clumps under the PhyUospadix canopy (Stewart and Myers, 1980), but as dominant forms PhyUospadix and turf do not intermingle and the boundary between them is discrete. Flattened rhizomes attach by short unbranched roots; the horizontal intertwined branches trap sediment and are buried much of the year. The contrast between bright green leaves and the dull brownish color of the shoreward algal mat delineates distinct zones. Turner (1985) and Turner and Lucas (1985) have recently shown that three species of PhyUospadix play similar roles in communities on the open coast of Oregon where their persistence stability, despite slow recovery following disturbance, is explained mainly by high preemptive ability; other organisms do not invade established beds. Dethier (1984) identified P. scouleri as one of six dominant taxa in intertidal pools on the coast of Washington; when abundant (monopolizing 20-50% of an individual pool), potential competitors do not settle or survive. This paper describes natural events and manipulative investigations in the region where seagrass beds and algal turf meet. Certain distinctive morphological properties of the two dominant taxa are similar (e.g. prostrate vegetative perennial growth, sand-trapping erect branches), suggesting that direct interactions might determine small-scale distributional limits. On a broader scale, the restriction of PhyUospadix to wetter, lower habitats implicated exposure as a regulating mechanism. Experiments were planned to examine possible competitive interactions between P. torreyi and algal turf and to evaluate whether and how physical factors might influence the distributions of these plants.

225

Accordingly, two hypotheses were considered: ( 1 ) competition between Phyllospadix and CoraUina-anchoredalgal turf near M L L W limits the seaward extension of t u r f as a dominant cover on horizontal rock platforms; (2) zonation patterns that separate Phyllospadix into lower intertidal habitats and Corallina turf into higher areas are indices of the responses of the two species to exposure. STUDY SITE AND METHODS

Site The study area consists of a broad gently sloping wave-cut intertidal bench as much as 60 m wide on the west side of Pt. Loma at approximately 32 ° 40' N, 117°14'W in San Diego County, southern California. Throughout the year algal turf, anchored predominantly by two species of CoraUina, covers most rock surfaces in the mid- to low-intertidal region and binds a layer of sand into the mat during summer months of relatively quiet water. Phyllospadix torreyi beds extend seaward from the low-intertidal into the shallow subtidal zone. Above the border zone where the two vegetation forms meet, Phyllospadix grows in surge channels, pools or shallow depressions that on low tides drain more slowly than the higher surrounding rock surfaces that are algae covered (Fig. 1). In February 1983, eyebolts were embedded in marine epoxy within the area 50m TO SHORE

. ......~/..:

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Fig. 1. Study site. • -- permanent reference point. Diagonal lines indicate PhyUospadix in the main bed seaward below Corallina-anchored turf, in channels, a small shallow pool, and in four isolated patches surrounded by algae. The upper limit of intertidal rocks is about 50 m shoreward. 1, 2 and 3 mark extensions of PhyUospadix that grew in slightly lower depressions into algal turf. E-18 and E-20, and A-D mark positions of clipping experiments.

226 shown in Fig. 1. All monitored quadrats were relocated by measurements from these permanent reference points.

Change in borderposition Changes in the extent of canopy cover were assessed by comparing photographs of fixed quadrats around eyebolts 1, 2 and 3 (Fig. 1 ). Additional data were obtained by measuring distances from reference eyebolts to marginal shoots and by tracing the shoreward perimeter of the canopy above eyebolts.

Leaf damage experiments (a) Water temperature. A laboratory experiment compared effects of different water temperatures on leaf color. In February, 24 leaves, 50-90 cm long from a single clump, were placed in each of five 1-1 jars which were aligned on a temperature gradient plate so as to maintain water temperatures at 15, 16, 20, 24 and 28°C. Filtered seawater was changed and leaves were rinsed at 4day intervals. (b) Canopy removal in isolated patches. All leaves were cut 2-3 cm above the rhizome mat in four areas approximately 2-4 m 2 in size where Phyllospadix grew surrounded by turf (A-D in Fig. 1); in late May, July and November of 1983 for A, late July and November of 1983 for B, and in late July 1984 for C and D. Patch A, with an area of ~ 2.5 m 2, included a pool about 1 m 2 that held water during most low tide periods, while all the other clipped areas were exposed to air on most minus tides. (c) Canopy removal within the bed. Near E-18 and E-20 (Fig. 1) 6 (in December) and 15 (in January-April) 0.06-m 2 quadrats were clipped. Regrowth or loss of canopy and rhizome mat were monitored. In both sets of experiments undisturbed nearby canopy was observed as a control. (d) Hypophyte census. Abundances of field-identifiable algae attached to rhizomes or substrate under the Phyllospadix canopy were recorded prior to, and following, leaf clipping in the four patches, A-D, described in (b) above. Similar data were collected, at times shown in Fig. 6, from three areas where changes in the position of the boundary (1,2,3 in Fig. 1 ) were measured. I use the term "hypophyte" to describe the position of the algae, distinct from epiphytes.

Phyllospadix/turf interactions (a) Transplants. From near the border where the two forms meet, slabs of the mudstone substrate with attached rhizomes and leaves, and pieces with intact algal turf were removed, and either reattached reciprocally or returned to the same habitat as controls for the treatment. (b) Clearings between the two forms. In May 1983 bare rock was exposed

227 experimentally by scraping vegetation from quadrats along the upper margin of Phyllospadix beds adjacent to turf. During the following winter naturally occurring events exposed new patches of bare rock within the upper portions of the Phyllospadix bed and enlarged or obliterated the outlines of most experimental quadrats. Numerous of these "natural experiments" were then mapped and monitored to follow changes on the newly exposed surfaces.

Comparison of growth rates (a) Phyllospadix rhizomes. Elongation rates for rhizomes were calculated from measurements of 29 individually tagged tips whenever they were temporarily unburied. Growth of another set of 22 rhizomes was followed by measuring the distance between a reference eyebolt and emerging new apical shoots above the sand. (b) PhyUospadix leaves. Approximate rates for regrowth of clipped leaves and for growth of leaves from new shoots were determined in patches A-D and in the 21 quadrats of E-18 and E-20. When newly tagged rhizomes could be relocated after 2-4 weeks, leaves in new distal shoots were measured. (c) Erect axes of CoraUina. Active uptake of Alizarin red dye (Andrake and Johansen, 1980) into the dividing cells of the apical meristems of erect thalli of C. pinnatifolia (Manza) Daws. was the basis for two sets of in situ growth estimates. (d) Crust expansion was estimated from successive tracings in quadrats within the turf zone during winter months when the rock was free from sediment.

Biomass data Samples of Phyllospadix, collected as detailed in Table 1, provided indices of plant growth that combined shoot density and leaf length. Rhizome mat with attached leaves from a 0.06-m e quadrat was washed, leaves were cut 50 and 20 cm above the shoot base, then the basal 20-cm portion of the leaves was cut from rhizomes. Subsamples were dried for 15-18 h at 105-115 ° C for dry weight data, with ash-free biomass determined after heating at 550°C for 12 h. Significant differences among habitats and seasons for each of four variables were found with an ANOVA test following a test for normality. Pairs of means were then compared with a Student-Neumann-Keuls test to identify those data sets that differed significantly from one another. Use of the same data for multiple tests can increase the probability of a type-one error; an approximation of the actual P value is ~ 0.024, rather than 0.001, statistically not significant in this case. Corallina-anchored algal turf was similarly sampled, dried and weighed.

228 TABLE 1 Means and SD for four variables, in seven sets ofPhyUospadix biomass samples. 25 × 25 cm Quadrat size= (0.0625m 2) ~n=33

Biomass dry wt. Leaf dry wt. % rhizome % leaves > 20 cm

(1)

(2)

(3)

(4)

(5)

(6)

(7)

High-dry

High-wet

April border

May border

Nov. border

July border

Low

42 ± 21 9 +_7 80 ±10 0

119 ± 63 46 ±25 62 ±8 25 ±16

47 ± 18 13 ±5.4 74.2 +3.8 15.2 ±7.6

84.4 ± 12.9 32.4 ±4.6 61 _+8.6 20.8 ±8.3

92.8 ± 23.9 31.0 ±5.1 65.4 _+8.2 44.2 _+3.8

100.6 ± 55.2 68.6 ±23.1 42.6 ±8.8 54.6 _+9.9

152.3 ± 18.4 68.6 ±10.7 54.6 _+7.6 57 ±1.7

( 1 ) Feb., July, mid-intertidal rocks, exposed by most low tides, n = 4. (2) Feb., July, mid-intertidal pools, never completely emerged, n = 6. (3- 6 ) near upper margin of main bed, ± 0.5 m, each n = 5; (3) after 6 months of daytime low tides; (4) after 4-6 weeks without daytime exposure; (5) after 1 month of daytime low tides with prior 6 months without daytime emergence; (6) after 4 months without daytime emergence. (7) Feb., lower portion of intertidal bed, seldom and briefly exposed, n=3. Dry wt. is expressed as g 0.06 m -2. RESULTS

Changes in border position The shoreward margin of the PhyUospadix bed was observed from March 1983 to December 1986; a representative summary of changes recorded in photographs of one of the fixed 1-m e quadrats is diagrammed in Fig. 2. By the end of the period 50-70% of the originally dense cover of Phyllospadix had been lost in small increments, and the upper edge had receded by up to 1 m. The greatest rate of loss occurred between May and November of 1984 when 24-40 cm were lost from sides and shoreward edges. A mechanism to explain this loss was the washing away of sediment from rhizome branches during winter storms with the resultant exposure of chunks of black mat, much of it loosely or unattached to rock substrate. Very low midday tides between November and February exposed mid- to lower intertidal vegetation for 4-6 h on as many as five successive days each month. Under these conditions leaves turned brown to straw color after 1-2 weeks, and became detached and entangled into snarled knots which also incorporated drift algal debris (Fig. 3A). These masses presumably contributed to drag and removal of exposed rhizomes during storms. White coralline crusts and chiton holes {Fig. 4) were exposed by the removal of rhizomes.

229

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S

Fig. 2. Changes in the surface covered by Phyllospadix rhizomes within shoreward 1 m2 of El. Increments were lost throughout winter storm seasons and regrowth was recorded intermittently. The figure, drawn from photographs, shows changes over three years.

Damage to leaves Leaves in pools high on the beach (high-wet habitats) remained bright green and long (often > 50 cm) despite summer water temperatures over 25°C. Leaves exposed to air nearby (high-dry habitats) became bleached and never exceeded 20 cm in length. In a laboratory test, leaves were apparently undamaged (no discoloration) following immersion at temperatures up to 28°C for one week. Clipping experiments (Fig. 5) indicated that leaves recover (elongate) less where they are exposed on low tides (A-H, B,C,D) than when submerged in a pool ( A - P ) . The difference between exposed and unexposed habitats is most marked when leaves are cut in November just prior to the period of midday very low tides. In the shallow pool ( A - P ) the canopy regenerated at the same rate and to the same extent in three successive treatments. In A - H , B,C and D, initial regrowth of short leaves was succeeded by gradual reduction of the number of shoots and leaves and the surface was algae-covered three years later. In the clipped quadrats of E-18 and E-20 that were surrounded by an undisturbed canopy, more and longer new leaves developed in those clipped quadrats where the flow of outgoing tides strewed leaves from the surrounding canopy over the clipped area than in those that were left relatively uncovered during low tides. In this uppermost portion of the main bed, new shoots were sparse

230

Fig. 3. (A) Clumpof short-leafedP. torreyi,algaldebris entangledwith distal leaves. (B) Clumps of PhyUospadixcollectedon same day from less exposed (left) to more exposed (right) habitats. Metre stick indicates relative length of leaves. Note similar rhizome density on all samples. and leaves short; e.g. mean dry leaf biomass for six quadrats initially clipped in December was 36.8 _ 5.2 g, while after 5 months, second clippings averaged only 3.53 + 3.1 g per quadrat. Protection of new shoots by adjacent uncut canopy is a function of their distance from the edge of the bed, the length of nearby leaves, and the direction of flow during retreating tides.

Leaf removal and hypophytes At the beginning of the study, 37 algal taxa were identified under the canopy in 9 fixed m 2 quadrats in the boundary zone. Both the number of species and their abundances decreased over succeeding months as Phyllospadix decreased in cover and density until only 13 species and few occurrences were recorded in J a n u a r y 1986 (Fig. 6).

231

I 0

I P

I 4

I 6crn

Fig. 4. Spots of white CoraUinacrust (white areas) and empty chiton holes (black areas) exposed on rock surface (stippled surface) followingloss of rhizome mat within upper portion of Phyllospadix bed (diagonal lines). The larger chiton holes are 3-4 cm long (drawn fromphotograph). In clipping experiments most of the associated hypophytes either disappeared or became bleached within four weeks except where depressions in the surface provided standing water on low tides. Algae were found only in trace am ount s a t t a c hed to rhizomes in Phyllospadix biomass samples and the dry wt. ranged between 0 and 21.0 g 0.06 m -2. Wi t hi n

232 6C o

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Low Midday Tides

Low Midday Tides

Fig. 5. Regrowth of canopy following clipping of isolated patches of PhyUospadix surrounded by algal turf, May 1983-Dec. 1986. Patch A included a small pool A (P) ( ~ 1 m 2) that held water during low tide periods while other clippings were exposed to air on most minus tides (AH, B, C, D). 40

7O /~

IQ

% Occurrences

I

60 u) 0 0 e-

0 0

0

'

3O

50

_e o 0 O.

40

-20

30 20

, 10

, 20

10 30

0

month Fig. 6. Decrease in the number of species found in E 1-3 after canopy became thinner and leaves were damaged during months of daytime low tides between April 1983 and January 1986.

each of six sets of n=5 collections, means varied from 0.04 g where three of five very low intertidal samples contained no algae, to 9.9 g _+7.1 (SD) dry wt.

P hyllospadix/turf interactions Three of the transplants of Phyllospadix to areas shoreward from the main bed where turf was the dominant cover lasted nearly 12 months. Leaves in these clumps gradually became shorter and less dense but new shoots developed during the first few months after transplanting, and in one instance several bore pistillate flowers. Green leaves completely disappeared during the months when low tides coincided with warm dry midday hours. No recovery was observed during the following months. W h e n intact algal turf was moved into the area covered by Phyllospadix, Corallina persisted and developed new erect thalli as long as the reattached rock remained in place.

233 Because natural events subsequently swamped the original experimental design, voiding attempts to replicate same-sized quadrats in either space or time, the results of clearing rock on the margin and within the bed are reported from representative examples. All exposed rock surfaces followed the same sequences. On surfaces naturally cleared by the removal of PhyUospadix rhizomes during storms, up to approximately 51% of the newly exposed bare rock was spotted with white coralline crust (Fig. 4) that often became pink and produced erect algal axes within 2-4 weeks. Small thalli of ephemeral algal taxa developed in succeeding weeks while crusts and erect axes of corallines continued to grow. In one quadrat where a sequence of tracings was obtained, after two months nearly 40% of the surface was occupied by erect CoraUina thalli that were mostly less than 5 mm high; 15 months later uniform 2-4-cm high CoraUina-anchored turf had replaced Phyllospadix. In another quadrat, the crust changed from white to pink in 17 days and erect axes were 2 mm high in 33 days. Erect algal thalli grew from crusts that were newly exposed in the last year of the study in portions of the site known to have been covered by Phyllospadix for at least the preceding three years. Wherever removal of rhizomes exposed rock, algal thalli developed over the surfaces, Corallina became increasingly abundant in percentage cover, and after 1-3 years algal turf replaced the earlier PhyUospadix cover. Actively growing yellow-green (as opposed to black, presumably dead) rhizomes that were exposed and marked during winter months for growth rate estimates were observed later to grow into undisturbed turf, apparently unimpeded by the mesh of algal thalli or the layer of sand. Roots developing from these advancing rhizome apices were frequently not attached to underlying rock. Horizontal elongation of buried rhizomes continued under the sediment trapped by algal thalli throughout the summer.

Growth rates Rhizome elongation rates averaged 2.8-7.0 mm week-1 at different seasons and in different portions of the site. More rapid growth, to 14.7 mm week- 1 was measured during 4 months of mid-winter to spring. Rhizomes rarely grew upwards or downwards on steeply sloping surfaces, and none crossed narrow gaps or cracks in horizontal surfaces. Growth rates for leaves in clipped patches were higher for short periods initially (to 1.0 cm d a y - 1in July) and lower over longer periods, suggesting either that a period of rapid elongation from the basal meristem is followed by a period of slower or no growth, or that loss from the leaf tip keeps pace with growth from the leaf meristem after a certain length is reached. Most rates ranged between 0.10 and 0.50 cm day -1. In pools, always-submerged leaves regrew to 30 cm in 2 months. Erect axes of Corallinapinnatifolia grew at a maximum rate of 1.5 mm week- 1

234 in experiments based on uptake of Alizarin red dye. After I month, the average elongation for 24 axes was 0.83 mm week-1. Erect axes newly initiated from crusts grew at a maximum rate of 1 mm week-1 over 4-6 weeks. Calculated growth estimates of ~ 1 mm week-1 for crust margins are suggested by the limited data available.

Biomass The differences in mean values for entire-sample biomass dry wt. were correlated with the a m o u n t of daytime exposure (Table 1 ), related both to seasonal differences at the same level (3-6, Table 1) and differences between position on the beach (1,2,7). Variance within and among sets of samples was large and statistically significant differences (Table 2) were found only between low (7) and high-dry (1), and between low (7) and April border (3) collections. Comparisons of the percentage rhizome, the total leaf wt. and the percentage of leaf mass in > 20 cm subsamples together show t h a t leaves are longer and heavier in habitats less exposed to air. July border (6) samples represented growth during several months with little daytime exposure and did not differ from low samples (7) in total leaf wt. (S, Table 2). These two (6,7) contained significantly larger amounts of leaf t h a n any of the more exposed samples. The high-wet (2) leaves were significantly heavier and longer t h a n high-dry (1), and longer t h a n April border leaves. The high-wet (2) plants and those in the May border (4) mat were intermediate in percentage rhizome. Longest leaves were found in November and July border (5,6) and low (7) samples and statistically these three collections were similar (L, Table 2). F o r > 50 cm length leaf subsamples, November border (5) averaged 2.2 g quadrat -1, high-wet (2) 5.4 g quadrat -1, while July border (6) had 16.8 g TABLE2 Comparisons (with Student-Neumann-Keuls test) between pairs of means for four variables, from samples described in Table 1. Those which differsignificantly(P < 0.001 ) are identified

1 2 3 4 5 6 7

1

2

3

4

5

6

7

x

SRL x

x

RL

L L L L x

SRL RL SRL SRL SR x

BSRL L BSRL S L S

x

x

B = (total) biomass; S = sum of leaf dry weight; R = per cent rhizome; L =per cent leaves in > 20 cm length subsample.

235 quadrat- 1 and low (7) 19.0 g quadrat- 1. None of the leaves in other samples exceeded 50 cm, and in high-dry (1), all leaves were less than 20 cm long. Ash-free dry weights were proportional to dry weights, showing no independent variability. Mean leaf organic (ash-free) dry wt. for all samples combined was 76.8 _+4.3% of the total dry wt.; for rhizomes, 70.5 + 4.4%; the highest value for organic wt. 0.06 m -e sample was 152.8 g. Biomass of Phyllospadix is potentially more than 3 times that of turf, on the basis of calculated ash-free dry wt. data: 136-2445 g m -2 compared with 176-720 g m -2 for CoraUina in turf. Samples from flowering patches included up to 73 reproductive shoots in 0.06 m e, with an average dry wt. of 5.6 g. DISCUSSION

Role of environmental constraints Between November and March, biweekly low tides occur midday and weather is often warm, sunny and dry. Occasionally during these months east winds bring relative humidity down to as low as 8% on hot days. As an example of conditions during these months, between 14 January and 9 April 1984 there were 50 days when minus tides exposed upper portions of the Phyllospadix beds to clear daytime skies. Spring and summer lowest tides occur at night or early morning hours when fog often provides additional protection from drying. The mixed semidiurnal tidal regime is regular and predictable seasonally and from year to year. Long, > 50 cm, leaves that remained bright green occurred only where the plants were seldom or never emerged. Plants with shorter leaves that often were brown or straw colored grew on the upper margins of the bed or in isolated patches above the boundary zone. Leaves in transplanted clumps became brown and died under conditions drier than where surfgrass was the dominant form. Biomass data collected across gradients of high to low on the beach (Tables 1 and 2 and illustrated in Fig. 3b), and analyzed to compare wet with dry habitats in a high zone and seasonal changes in the mid-intertidal, document that leaves are longer when seldom or never emerged. Clipping experiments suggest that there is limited regrowth potential when leaves near the upper margin of the main bed or in isolated patches at higher levels are severely damaged. Repeatedly it was observed that during periods when low tides exposed shoreward or higher areas of PhyUospadix to warm dry air, leaves became discolored and broken, while leaves in pools, channels or seaward did not. Information reported here supports the hypothesis that weather during these critical periods damages exposed leaves, effectively "limiting the rate of dry matter production". It is during this same season that storm surf unburies, breaks and removes rhizome mat, "causing partial or total destruction (of bi-

236 omass)". As thus defined by Grime's (1979) model for plant distributions, stress and disturbance determine the upper limit ofPhyllospadix torreyi growth in this site. It is unlikely that warmer water temperatures alone cause much of the damage, as plants in high isolated pools remained bright green as long as they were covered with water despite increases in water temperature during low tides to > 25 ° C. Leaves in 1-1 jars showed little difference when maintained for several weeks at 15-28 ° C, a range of water temperatures naturally encountered in high pools. McMillan and Phillips (1981) found that in the laboratory P. torreyi survived at 21°C as well as at 14-16°C. In the field in northern California, Drysdale and Barbour (1975) concluded that although leaf growth of Phyllospadix (stated to be P. torreyi but reported by Barbour and Radosevich (1979) to have been P. scouleri) was somewhat less at temperatures above 14 ° C, the magnitude of decline indicated a relatively broad tolerance range. Harrison (1982) concluded that the vertical distributions of two intertidal Zostera species are restricted by tolerance of exposure to air. Leaf discoloration indicates damage both to photosynthetic organelles and to tissue that transports oxygen to buried organs. In Zostera, where root-rhizome respiration is supported primarily by shoot photosynthesis via transport of 02 from leaves to rhizomes (Smith et al., 1984), damage or loss of leaves affects growth, perhaps viability, of buried tissues. Barbour and Radosevich (1979) found that most of the 14C taken into intact PhyUospadix plants was absorbed, fixed and accumulated by leaves, with much less absorbed by rhizomes and roots. Their study also showed that photosynthesis in leaves exposed to air was 10% or less of estimated gross photosynthesis for immersed leaves. C. McMillan's experience (personal communication, 1985) growing seagrasses in aquaria convinced him that PhyUospadix uses its root system largely for attachment, and that leaves are crucial for nutrient uptake, thereby differing from Zostera (Penhale and Thayer, 1980) where uptake from sediment is an important nutritive process. Many cells around the central cylinder in P. torreyi rhizomes stain for starch (J.G. Stewart, personal observation, 1985 ). The growth of flowering stalks in transplanted clumps may have drawn on underground reserves at a time when leaves were discolored. Regrowth of new leaves following successive clippings presumably also utilized photosynthate stored in rhizomes. Continuing low productivity in the more often exposed habitats, if inadequate to support recovery following one or several periods of leaf loss, would account for the disappearance of most non-submerged high isolated patches. The physical conformation of the beach - broad, nearly flat - allows accumulation and seasonal movement of sediment that is trapped among rhizomes or a layer of algae. J. Kuo (personal communication, 1985) has demonstrated

237 with SEM the presence of root hairs with adherent sand grains on Phyllospadix, a means by which the rhizomes can bind and become enmeshed within sand. Sand deters settlement of seedlings (making vegetative propagation critical) or algal spores that might otherwise compete for substrate, and excludes or keeps in low abundances most invertebrates. For many months wet sand keeps rhizomes and the developing leaf-shoots damp. The prevalence of broad gently sloping benches in the lower intertidal and shallow subtidal regions coupled with predictable sand deposition appears to favor dominance of dense, consolidated beds of PhyUospadix in such localities (cf. Turner, 1985 ). Algal species that co-occur with PhyUospadix, with the exception of a few small leaf epiphytes, are attached to substrate or to rhizomes and basal axes are buried for most of the year. Most are red algae, taxa with apical meristems that remain above the sand. The calcified axes of the very abundant coralline taxa and the fibrous sheaths of PhyUospadix provide protection from abrasion. Many of the hypophytes of the boundary region were the same taxa that occur on coralline turf as epiphytes or as opportunistic colonizers on newly exposed surfaces. Thus, the difference between the epiphyte assemblage associated with turf and the hypophyte flora in adjacent regions of surfgrass beds is more one of relative abundances than species composition. Those species that occur only rarely in boundary-zone turf but that are often abundant and common under nearby PhyUospadix can be treated as obligate understory species (Dayton, 1975).

Role of biological interactions Competition in the form of direct plant-plant interactions between Phyllospadix and CoraUina-anchored algal turf was demonstrated, with each of the dominant taxa "winning" on different temporal scales in terms of percentage cover in a boundary zone. When waves uncover, break and remove rhizomes, the shoreward margin of the bed recedes; up to 1 m year- 1 seaward shift was documented in the present study. Loss of PhyUospadix cover both on the upper margin of the bed and in patches within the canopy is immediately followed by slow growth of erect Corallina thalli from persistent crusts or newly settled spores. Evidence that PhyUospadix, in turn, usurps and holds space previously covered by Corallina consists of finding crusts on rocks that had been buried for several years beneath rhizomes, and of observing rhizomes growing into and through intact turf. Calculated with 10 mm week-1 as a reasonable estimate of potential rhizome growth, a single rhizome could elongate a distance of i m in 2 years. Lateral growth of crustose thalli that rely on contact with the rock for attachment does not compete with growth of rhizomes that overgrow the thin algal layer. Workers elsewhere have described PhyUospadix as a competitive dominant. Dethier (1984) states that P. scouleri appears invulnerable to competitive re-

238 placement, having found no evidence that other organisms in that system can appropriate space from the species. In Oregon, once P. scouleri was established, it was similarly successful in resisting removal by wave action or invading organisms (Turner, 1985). In my study, following the 1982-1983 storm season when loss of rhizome mat increased the amount of space and light available in the beds near and below MLLW, the only plant or animal species, other than CoraUina, that even briefly became abundant in the clearings were ubiquitous ephemeral algae. PhyUospadix in different situations has been shown to replace Egregia (Black, 1974), Gastroclonium (Hodgson, 1980) or the several species in tide pools reported by Dethier (1984). To survive and compete in this system, perennial plants must be able to both regain and retain primary substrate. For CoraUina pinnatifolia, slow but opportunistic erect regenerative growth from prostrate crusts appears to outweigh advantages of short-range dispersal by means of spores. Regrowth from pre-existing prostrate thalli allows CoraUina species to successfully compete with other common opportunistic taxa ( Ulva, Colpomenia) which also attach to CoraUina axes and therefore do not depend on bare rock. The differing capacity for production, implicit in comparisons between angiosperms and coralline algae, constitutes a form of exploitative competition, in the sense that greater size entails greater utilization of resources. As discussed by Grime ( 1979 ), relative productivity becomes important only under conditions of low stress and low disturbance, requirements met only intermittently in this midto low-intertidal zone. Here, the proportion of space occupied is a more relevant way of assessing resource utilization. Along the border, competitive processes apparently reverse occupancy of space within a narrow band; above and below this shifting boundary zone, turf and PhyUospadix, respectively, monopolize space. Disparate sizes of both prostrate and erect parts of each plant seem adaptive under different conditions. Greater size of erect Phyllospadix plants becomes a disadvantage if this contributes to loss of mat. The depth of the rhizome mat, 1 to several cm compared with crusts less than 1 mm thick, confers an advantage in terms of interference, while the trapping of sand within intertwined rhizome branches forms a solid layer that blocks attachment or invasion by macroorganisms requiring contact with rock. The thinness of the closely adherent Corallina crust allows it to persist where a thicker, obtrusive layer is scraped or loosened. Submerged PhyUospadix leaves fill the water column, forming a partial barrier to settlement and growth of other organisms. The greater biomass of rhizomes, compared with prostrate crusts of algae, allows them to push through turf and cover substrate even when the roots do not reach the rock beneath algal thalli. Crusts that remain viable beneath Phyllospadix possess the advantage of long-term persistence and are impervious to wave disturbance as PhyUospadix is not. Dethier (1984) found that erect CoraUina

239 increased following loss of Phyllospadix, and because bases are not removed, "total destruction of populations is practically impossible". Phyllospadix reproduction Seed production by PhyUospadix is seasonal insofar as flowering regularly begins mid- to late February, and flowers and fruits are found into mid-summer. Certain portions of the bed produced only male or only female flowers whereas other portions remained vegetative. In three years, I found two seedlings attached to axes of CoraUina thalli in turf (where one would expect to find them; Gibbs, 1902) above the shoreward margin of PhyUospadix beds. Growth of such seedlings is assumed to produce the isolated patches that occur within the turf zone. Patches C and D (Fig. 1) developed within dense algal turf between 1980 and 1983, and establishment from seedlings is the only plausible explanation. By March 1984 rhizomes had spread nearly 1 m in one direction and total cover was ~ 0.05 m 2. These two patches have now reverted to algal turf, following rhizome disappearance and regeneration of Corallina from residual crusts after leaves were clipped. In a sample collected from an area of relatively dense pistillate flower shoots, 11% of the total shoot dry wt. consisted of fertile spathes, compared with 42 % for Zostera marina L. (also perennial) and 92% for Z. americana den Hartog ( = Z. japonica Aschers. & Graebn. ), an annual species (Harrison, 1982). Large areas of the bed remain vegetative, with no reproduction observed from year to year. Low reproductive effort and effective vegetative propagation by means of horizontally growing rhizomes appear to characterize species of Phyllospadix here and in Oregon (Turner, 1985).

Balanced shifts in the surfgrass-algal turf boundary I propose that there are periods of many years when Phyllospadix can (re)grow shoreward and consolidate the upper limit of the bed near MLLW. Occasionally there are years such as 1982-1984 when seasons of severe winter storms coupled with extreme damage during daytime low tide cycles result in the loss of seagrass along the upper limit of the bed, with subsequent development of algal turf. If such years were followed by considerably longer periods of more benign conditions, PhyUospadix could recover this surface. In the summer of 1987, green leaves were again dense in the upper 1-2 m of the extensions 1, 2 and 3 of Fig. 1 and the shoreward margin of rhizome development, recognized by new shoots above the sand, had moved back toward the original level. This suggests that disturbance during the 1982-1984 winters was relatively high, and supports the hypothesis that reversals on this scale indeed occur. Chiton depressions under buried rhizomes are additional evidence that in the past there have been intervals when the substrate was at least partially bare of

240

sand-trapping vegetation. Piper ( 1984 ) suggests that sand accumulation (depth and duration) sets the lower limit to the distribution of intertidal chitons on these beaches. This would exclude them from Phyllospadix mats as well as from well-developed dense algal turf. Alternating development of surfgrass and algal turf on the same surface could account for the appearance and disappearance of chitons; the holes that persist in the well-cemented mudstone-shale substrate will increase in number and size over the years. Various processes in this intertidal system effect changes on different scales: 24 h (for sand deposition or removal; Stewart, 1983); 5-14 days (bleaching of coralline thalli and discoloration of PhyUospadix blades); 2-6 weeks (breaking and loss of blades and of rhizome mat); months (regeneration of erect axes from Corallina crusts and rhizome elongation); seasonal variation in abundances of associated taxa; potential annual changes of about a meter in the position of the border between the forms; 3-5 years for the growth of isolated patches of Phyllospadix from seedlings that attached within the turf-dominated zone. ! predict, however, that over periods of many years the border zone will remain balanced near MLLW. The shifts in relative abundances of the two dominant taxa, CoraUina (that anchors the algal mat) and PhyUospadix, are mediated in turn by physical factors and competitive interactions. The presence of one or the other of these two vegetation forms provides the structure for two distinct intertidal assemblages. ACKNOWLEDGEMENTS

J. Kuo and C. McMillan accompanied me to the site during visits to San Diego and generously shared their experiences with PhyUospadix biology. W. Dennison, T. Turner and P.K. Dayton read and discussed drafts of the manuscript, greatly improving the organization. Suggestions from anonymous reviewers are appreciated. The research was supported by National Science Foundation grant OCE 8213965.

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