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Surfgrass (Phyllospadix torreyi) reproduction: reproductive phenology, resource allocation and male rarity.

Key words: biomechanics; Phyllospadix; seagrass reproduction; sex ratio; surfgrass.

INTRODUCTION

Dioecious plants with sex chromosomes are predicted to have primary sex ratios (i.e., in seeds at the end of parental investment period) of unity due to frequency-dependent natural selection (Fisher 1930, Charnov 1982), yet adult sex ratios in dioecious plants frequently are biased toward one gender (Lloyd and Webb 1977). The degree to which this bias is directly selected for, or reflects ecological processes that change the primary sex ratio, is important to the understanding of demographic processes and the evolution of plant breeding systems (Lloyd 1973, Charlesworth and Charlesworth 1978, Bawa 1980, Thomson and Barrett 1981, Goldman and Willson 1986). Adult plant sex ratios can be biased toward the gender, typically male, that allocates fewer resources to reproduction and thus has more for maintenance, growth, and reproduction where resources are limiting (Lemen 1980, Popp and Reinartz 1988, Armstrong and Irvine 1989, Allen and Antos 1993). Adult plant sex ratios thus might be expected to vary across habitat types, i.e., sexes are segregated spatially (Freeman et al. 1980, Cox 1981, Iglesias and Bell 1989). Spatial segregation of plant genders has been attributed to physiological differences between genders that hypothetically evolved as a result of differential allocation of resources to reproduction (Dawson and Bliss 1989, Dawson and Ehleringer 1993). Proximate causes for skewed adult sex ratios also include differences between genders in age and size effects on reproduction (Gross and Soule 1981, Bullock et al. 1983, Allen and Antos 1993, Thomas and LaFrankie 1993). Finally, environmental determination of gender is another proximate cause of biased sex ratios and spatial segregation of sexes (Freeman et al. 1980, Bierzychudek and Eckhart 1988, Charnov and Dawson 1989).

This study concerns sexual reproduction and sex ratios in surfgrass, Phyllospadix torreyi S. Watson, a marine angiosperm or "seagrass." Little is known about the reproductive ecology of aquatic angiosperms, including sex ratios and factors determining them. Most studies on seagrass reproduction address environmental controls of phenology (e.g., McMillan 1976, 1980, De Cock 1981, Moffler et al. 1981, Phillips et al. 1981, 1983). Although representing a small proportion of angiosperm species, aquatic angiosperms exhibit great taxonomic, reproductive, and ecological diversity useful for comparative studies of plant population biology and evolution (Cox 1988, Barrett et al. 1993).

Phyllospadix spp. are the only seagrasses that grow on rocks in turbulent waters, hence the common name "surfgrass." The genus is restricted to the northern Pacific Ocean where surfgrasses grow in the lower intertidal and shallow subtidal zones (Phillips and Menez 1988). Despite the importance of surfgrass as a dominant, long-lived, persistent species (Turner 1983, 1985, Dethier 1984, Turner and Lucas 1985), little more is known about surfgrass ecology, particularly subtidal aspects (reviewed in Cooper and McRoy 1988). Although this gap is undoubtedly due to the difficulties of working in a turbulent marine environment, the lack of information on surfgrass biology is nevertheless striking for a species that forms a major habitat type within its wide distribution, and is of economic value. For example, in southern California, surfgrass provides a nursery for the valuable California lobster, Panulirus argue, and is susceptible to declining coastal habitat quality (Littler and Murray 1975).

Seedling recruitment is the only well-described aspect of sexual reproduction by surfgrass (Turner 1983, 1985, Turner and Lucas 1985). These studies of Phyllospadix scouleri in Oregon demonstrated that seed recruitment was facilitated by barbs on the seeds that grapple with intertidal red algae. The maximum number of seeds trapped on the substratum ranged from 0 to [approximately equal] 1000 seeds/[m.sup.2] during the dispersal period (September-March) and varied by several orders of magnitude among years. Seed germination was [is greater than] 90% but seedling mortality was equally high, and thus, recruitment of sexually produced progeny was rare. These observations also apparently held for Phyllospadix serrulatus an d Phyllospadix torreyi.

My study attempts to fill the gap in understanding of surfgrass reproductive ecology by focusing on the preseedling stages. Basic information such as relationships of flowering effort to the seed crop, reproductive phenology and variation, and sex ratios is virtually unknown. Because surfgrass is dioecious, as are the majority of seagrass taxa (Pettitt 1984, Cox 1988), fertilization in an aquatic habitat might limit seed production. Dioecy is also of note because, although certain angiosperm families are exclusively dioecious, overall [is less than] 5% of angiosperms surveyed are dioecious (Bawa 1980). Attempts to understand the evolution of dioecy have not included many aquatic taxa. Understanding all stages of sexual reproduction will facilitate subsequent demographic and genetic studies of surfgrass, and provide sorely needed data for comparison to other aquatic angiosperms and algae (Barrett et al. 1993).

Phyllospadix reproductive biology is interesting be cause populations of three species (Phyllospadix scouleri, P. serrulatus, and P. torreyi ) observed from Alaska to California over several years are always female-biased (S. L. Williams, personal observation; Phillips 1979). This strongly female-biased flowering shoot ratio is even more intriguing because typically all ovules become fertilized, despite male rarity. Therefore, in 1990, I began a study of P. torreyi off the coast of California, USA. Here, it was feasible to make subtidal observations on a large surfgrass bed. Upon discovering that the abundance of males increased with water depth, I asked the following questions. (1) Was there a biased sex ratio in the population? (2) Given that surfgrass is diploid and dioecious, was there evidence that surfgrass might violate Fisher's assumptions for a primary sex ratio of 1:1 (was gender environmentally controlled?)? (3) What were the factors contributing to the apparent spatial segregation of the sexes? (4) What were the ecological factors that might control the sex ratio? Although unequal allocation to reproduction is assumed to underlie biased sex ratios in many studies of terrestrial plants, relatively few include the data on sex ratios and their temporal and spatial variation, resource allocation to reproduction, and growth and mortality necessary to evaluate this assumption. This study includes such data, and thus, also represents one of the most comprehensive studies of seagrass reproduction to date.

METHODS

Like all surfgrass species, Phyllospadix torreyi is a diploid clonal plant with several long, thin leaves arranged in shoots along a prostrate rhizome. Vegetative plants are monomorphic; I could not differentiate between genders with confidence until plants were reproductive. Both genders produce long, branched reproductive shoots supporting spikes of flowers, termed "spadices." Pollen is released into the water as clumps of grains [approximately equal] 2 mm long that are dispersed rapidly by water motion (S. L. Williams, personal observation). There are no known animal vectors, and flowers are not showy, lacking sepals and petals. Ovaries contain one ovule each.

Surfgrass reproduction and flowering sex ratio

I studied surfgrass growing intertidally to subtidally in a large bed that stretches [approximately equal] 300 m along the shoreline in the relatively protected lee of a small island (Bird Rock, 33 [degrees] 27' N, 118 [degrees] 29' W, offshore from the Wrigley Marine Science Center of the University of Southern California, Santa Catalina Island, California). After making preliminary observations beginning in March 1990, I censused the gender and density of surfgrass flowering shoots ("rhipidia") in 10 randomly assigned, quadrats (25 x 25 cm) along a 50-m transect tape with haphazardly chosen starting points at 1, 1.5, 3,4.5, 6.1, and 7.6 m water depth, corrected for tidal height. Al though I censused at various times over all seasons from July 1990 to October 1992, I could not always sample all depths, and rough water conditions at the shallowest site frequently prohibited accurate sampling, resulting in missing data. The most complete censuses covered May--August 1991; quantitative winter censuses were minimal. To determine the proportion of shoots that were reproductive, I censused vegetative and flowering shoots at 1, 3, and 6.1 m depth in June 1990 and May 1991, and across all depths in July 1990. Because vegetative shoots were too dense to count in the entire quadrat used for flowering shoot densities, I subsampled vegetative shoots in 100-[cm.sup.2] quadrats haphardly tossed within the larger quadrats. I discontinued counting vegetative shoots thereafter because of time constraints.

For interpretation of statistical independence and results, it is useful to assess whether the quadrats represented different individuals (genets), and thus provide a measure of population structure. Without a genes marker, it is difficult to be certain that a quadrat represented a unique clone, particularly above 3 m water depth where the surfgrass cover was extensive. At depths of [is greater than or equal to] 4.5 m, I often could detect discrete patches of surfgrass that appeared to be clones. These putative clones appeared larger than the quadrat size but [is less than] 1-2 m in diameter, so rarely would they extend to the adjacent random sampling locations. At shallower depths, the quadrat samples could represent several genets. I roughly estimated that 15% of my quadrats represented more than one clone; during the peak reproductive months (May-August, when sexes were obvious), I found females in 5 quadrats of the 33 quadrats that contained males (n = 490 quadrats sampled). Because surfgrass is dioecious, these quadrats obviously contained multiple genets.

I calculated the sex ratio as the total number male per total number female flowering shoots in 10 quadrats at each water depth. Sex ratios at each depth on each census date were compared to an expectation of equal sex ratios with chi-square tests using a Bonferroni correction to the 5% significance level for 45 separate tests. I calculated the mean sex ratio (mean number males per mean number females, n = 10 quadrats) at each water depth, averaged this mean over a maximum of 14 census dates per depth, to compute a linear regression of the mean sex ratio vs. water depth.

To describe the phenology of reproduction, I summarized the stage of reproductive maturation of female flowering shoots over the water depth gradient. Reproductive shoots develop iteratively over several months by growing new branches, each terminating in a spadix or spike of flowers that also develops sequentially over days. The population thus displays an age gradient in floral development within and among spadices and among shoots that I averaged over the clonal hierarchy of flowers within spadices within shoots. In each census quadrat, I haphazardly selected one female flowering shoot, choosing another outside the quadrats when none was available (n = 10 female flowering shoots). In the laboratory, I counted the number of spadices on each flowering shoot and the number of flowers, fruits, and seeds per spadix, noting abortions and grazing damage. I defined the reproductive stage of each spadix as the stage of the majority of the flowers in the spadix, scoring as follows: immature (no ovules visible macroscopically), ovules (ovules visible inside spadix), receptive (stigmas exerted), fruits (recently pollinated ovules and green ripening fruits with a developing seed), seeds (dark brown seed coats visible), dehisced (seeds released, spadix senescent). Typically [is greater than] 75% of the flowers within a spadix were at the same stage. I calculated the mean percent of the spadices on a flowering shoot at each stage of development and averaged over the 10 shoots from each depth. In May 1991, I collected male flowering shoots across the depth gradient and counted the number of spadices and flowers per spadix. Otherwise, I avoided collecting rare males, but noted their development.

Two-way analysis of variance (Model I ANOVA) was performed on (1) female flowering shoot abundance, (2) the number of female spathes per flowering shoot, (3) the number of flowers, fruits, or seeds per flowering shoot, and (4) male flowering shoot abudance over time and depth for June-August 1991. I considered time and depth as fixed effects based on my observations that each summer month represented a different stage in the phenology of surfgrass reproduction (flowers vs. fruits vs. seeds) and because I expected predictable differences among depths due to month as the thermocline developed (Bennington and Thayne 1994). To assess whether the number of female spadices per flowering shoot varied with time during a reproductive episode, one-way ANOVA was performed on counts from a single depth (1.5 m) covering the period from January to September 1991. Variation over depth in the number of (1) male spadices per flowering shoot and (2) anthers per spadix was assessed for May 1991 using one-way ANOVA. Counts (+0.5) were square-root transformed and the transformed data had homogeneous variances for all response variables (Bartlett's test, P [is greater than] 0.05).

I used a 4[Pi] quantum sensor (Model QSI-140, Biospherical Instruments, San Diego, California) to measure light transmission over the surfgrass bed at 1030 local time on 24 July 1990. Six integrations of 30 s each were averaged at each depth; readings taken under clouds were not used. Because the water is very clear around Catalina Island and underwater visibility is rarely [is less than] 10 m horizontal distance, these data are representative of light reduction with water depth (S. L. Williams, personal observation), although the maximum irradiance changes seasonally (R. Carpenter, personal communication).

Pollen counts.--Pollen was counted because it is a component of male reproductive effort, and it might limit female reproductive success, particularly given the observed rarity of males. Also, calculation of a pollen/ovule ratio for surfgrass would allow an interesting comparison to nonaquatic angiosperms.

One spadix with intact mature anthers was sampled from each of six male plants in May 1991. Three anthers were subsampled from each spadix, and one of the paired pollen sacs in each anther was detached and opened under a dissecting microscope to remove the pollen, which is fibrous and several millimetres long. Pollen was placed in a small beaker with 10 mL of deionized water. A few drops of detergent were added to the beaker, which was agitated ultrasonically for 10 min, with periodic mechanical disruption of the pollen mass by a dissecting needle. Pollen was stained by adding some crystals of methylene blue chloride and the volume was brought to 200 mL. Four 1-mL replicates of the diluted sample were counted in a Sedgewick-Rafter cell under a compound microscope and averaged. To calculate pollen dilutions accurately, water volumes were determined as mass at 25 [degrees] C. The pollen grains remaining in the pipette were counted for 16 of the 72 replicates; this error represented (mean [+ or -] 1 SD) 2.2 [+ or -] 1.7% of the total number of grains in the sample.

Reproductive losses to abortions and grazing damage

Surfgrass seedlings are apparently rare (Turner 1983, 1985). In addition to high seedling mortality or prezygotic factors (e.g., limited ovule production, limited males and/or pollen production), this rareness also could be attributable to postzygotic factors such as abortion or herbivory, which I measured as follows.

Using the census data, the mean percent flowering shoots with aborted fruits or seeds was calculated. Not every spadix carried aborted fruits or seeds; I calculated the percent spadices with abortions on each flowering shoot and averaged the percent over flowering shoots with abortions. Similarly, not all fruits or seeds within a spadix were aborted; I calculated the percent of aborted fruits and seeds within a spadix and averaged this over all spadices with abortions. I also summed the number of fruits and seeds aborted on all spadices on a flowering shoot and averaged the sum over all flowering shoots with abortions. I assumed that the maximum potential number of seeds was represented by female reproductive components in June and July 1991, depending on water depth, when I also observed no abortions (see Results). To calculate the potential loss in seed production through abortion, I adjusted the June and July reproductive components for the number of shoots with abortions and the number of abortions per such shoot, using data from August 1991 when abortions were maximal, and expressed the loss as percent maximum potential seed production.

After noticing grazer damage to flowering shoots, I censused herbivorous gastropods on surfgrass within 25 x 25 cm quadrats (n = 42) between 3 and 4.5 m water depth in June 1991. The abundant herbivorous fish, Girella nigricans, was counted along swimming transects 100 m long x 2 m wide in 1 m water depth in April and May 1992 (n = 10 transects). Two divers swam the transect in midmorning or midafternoon and their counts were averaged. The foraging behavior of G. nigricans was observed during 10 additional hours throughout the day during the same time of year.

Over 100 spadices of each gender were collected haphazardly in July 1991 and April 1992 and examined in the laboratory for the percent removed presumably by fishes, based on cleanly cut spadices and by comparison to the average length of a male spadix. Gender differences in grazing damage were tested using loglikelihood tests after a correction for continuity (Wilkinson 1986). Gastropods (Norrisia norrisi, Astrea undosa) were confined in aquaria with male and female spadices to determine the type of damage inflicted.

Resource allocation to reproduction

To evaluate the hypothesis that the sex ratio is biased toward the sex with the lower allocation of resources to reproduction, I estimated resource allocation to reproduction as the biomass of vegetative and flowering shoots, and the carbon and nitrogen content of flowering shoot tissues, and compared these variables between females and males. In early May 1991, I haphazardly collected male and female flowering shoots from distinct clones for biomass determination. Final samples were n = 27 and 34, females and males, respectively, at 1.5 m, n = 19 and 12 at 3 m, n = 27 and 22 at 4.5 m, and n = 27 and 25 at 6.1 m. Differences in biomass were minimized at this time because the majority of th-e females had not begun to develop heavy fruits. I also analyzed leaf shoots from 1.5 m (n = 27 and 29, females and males, respectively), 3 m (n = 10 and 60), 4.5 m (n = 22 and 13), and 6.1 m (n = 44 and 5). Epiphytes were removed by hand, and samples were rinsed briefly in fresh water, dried at 80 [degrees] C, and weighed. Model I ANOVA was performed on the biomass of male vs. female flowering shoots and of vegetative shoots over depth in May 1991.

In early June 1991, I collected flowering shoots (n = 10) of each sex between 4.5 and 6.1 m depth for carbon and nitrogen determinations. I separated samples into (1) spadices, selecting females with stigmas exerted on the majority of flowers and males with mature intact anthers, and (2) the remainder of the flowering shoot biomass (branched stalk). Samples were rinsed briefly in deionized water after removing the few visible epiphytes and wiping with tissues, frozen overnight in acid-cleaned vials, dried at 60 [degrees] C, and ground to a fine powder. Samples were analyzed in an elemental analyzer (Model 2400, Perkin-Elmer, Norwalk, Connecticut) using acetanilide as a standard. Nonparametric Mann-Whitney U tests were used for detecting differences in carbon, nitrogen, and C:N ratios between genders.

Ideally, resource allocation to reproduction should be compared per genes, particularly if there is size dimorphism between genders. Given the difficulties with clone identification I mentioned earlier, I used an indirect approach to estimate the relative resource allocation per clone. First, I measured with calipers the width of the rhizome at the junction of the terminal (youngest) leaf shoot, to estimate plant size "normalized" for age. I selected distinct male and female clones growing within a few metres of each other and across the plant's depth distribution. I also measured the longest leaf on the terminal leaf shoot although rhizome width is a better surrogate for plant size because gender differences could exist in how leaf tips senesce, break, are grazed, or epiphytized. Second, I calculated the areal ratio of the (1) mass of flowering shoots per square metre: total mass of flowering and vegetative shoots per square metre, and (2) density of flowering shoots per square metre: total density of flowering and vegetative shoots per square metre for males vs. females. I used census data from June and July 1990 and the mean biomass data described above. Of a total of 57 census quadrats, I used 22 that were unisex and assumed that a quadrat represented a single clone. Areal ratios for mass include differences in reproductive and vegetative remet densities as well as biomass differences per remet. If females and males are different sizes but allocate relatively equally to reproduction, then the areal ratios should be the same; I tested this with unpaired t tests.

Growth and survival: differences between sexes

Biased sex ratios can result because one gender grows faster, either in response to greater resource acquisition or to reduced resource allocation to reproduction. Seagrass leaf growth is the result of net carbon gain. It is fast, and sensitive to resource availability (Dennison 1987, Dennison et al. 1987, Williams and Ruckelshaus 1993). Rhizome growth is slow enough to require months to measure and for the most part depends on leaf photosynthate (Barbour and Radosevich 1979). Rhizome propagation represents the capacity for the seagrass to occupy space through clonal expansion.

Leaf growth rates.--In June 1991, I measured leaf growth rates. In 32 clones of each sex, I marked 10 leaf shoots in the sheath area with a needle (Williams and Ruckelshaus 1993) and tagged the marked shoots with small strips of aluminum tape wrapped around the base of the shoot. I chose clones along a 50-m section of the bed between 3 and 4.5 m depth where there were enough males to mark. Marked clones of opposite sexes were located within 1-3 m of each other. After 13 d, I harvested the marked leaf shoots to measure leaf elongation rates, summing new growth over leaves within a shoot and averaging elongation rates over all shoots within a clone. Differences in the average leaf growth rates between females and males were analyzed with a t test.

Surfgrass transplants.--Male segregation in deeper portions of the surfgrass bed could be because males could not survive or grow as well as females at shallower depths. To test this hypothesis, I transplanted paired clones of males and females from depths of 6.1-7.6 m to 1 m in June 1991. I removed surfgrass rhizomes with attached leaf shoots with a 0.0165-[m.sup.2] Plexiglas corer and placed them in labelled plastic bags. Males and females were selected from unisex patches separated by no more than 1 m. After collection, leaf shoots were counted (23-87 shoots per clone) and trimmed to 40 cm to minimize leaf breakage. The paired clones were placed 10-15 cm apart in sturdy plastic mesh (1.2-cm mesh size) transplant units by threading leaf shoots between the meshes. Males were marked with cable ties attached to the mesh and both sexes were marked with flagging tape. I transplanted 10 units into the existing bed, avoiding large unvegetated patches and mapping the locations of units and each male and female clone. Transplant units were attached at each corner by stainless steel washers and nuts on bolts cemented with underwater epoxy to the substratum cleared of encrusting biota.

I counted leaf shoots and the area of substratum occupied (number of mesh grids with shoots) in April and August 1992 and March 1993. Many attempts to census the transplants failed because I could not find them in the dense surfgrass canopy or risked damaging them in strong surge.

Strength of rhizome attachment: tenacity measurements.--Surf, surge, and strong tidal currents are important features of the surfgrass habitat. Hydrodynamic forces are a unique feature of marine environments (Denny 1988) that hypothetically could result in spatial segregation of sexes, if gender-based differences in response to these forces exist. Based on results to follow, I initiated a study of surfgrass biomechanics. I measured the tenacity, or the strength of attachment to the substratum measured as the force required for detachment, for males and females. I harnessed 30 leaf shoots at the perimeter of discrete male and female clones (n = 46 each) that grew within a few metres of each other at water depths from 1.5 to 7.1 m. The shoots were wrapped near the rhizome with a cloth towel strip to prevent cutting by the nonextensible string harness. The harness was attached to a spring scale used to weigh game fish (De-Liar, Model 228, Zebco, Tulsa, Oklahoma) that was modified so that the maximum extension of the scale was marked by a bar pushed by a pin attached to the spring. The scale was calibrated with known masses. Harnessed surfgrass was pulled parallel to the substratum to mimic the tensile forces of surge and currents until it detached. If the harness slipped, the measurement was discarded. The recorded mass was multiplied by the acceleration due to gravity (9.81 m/[s.sup.2]) to calculate the force required to remove surfgrass from the substratum. Paired two-sided t tests were used to detect tenacity differences between genders.

RESULTS

Phenology, reproductive components, and sex ratios

Although surfgrass did not occupy 100% of the substratum, it formed a virtually closed canopy down to 4.5 m. The lower depth limit of vegetative and reproductive surfgrass was [approximately equal] 7.6 m where a canopy of the giant kelp Macrocystis pyrifera began. At this depth, surfgrass occurred in scattered patches. Vegetative shoots were much more abundant than flowering shoots, which constituted 24 [+ or -] 21% (mean [+ or -] 1 SD, n = 13 quadrats) of the total shoots during the peak flowering month of June 1990 but dropped to 3.5 [+ or -] 8.1% (n = 44) in July (Fig. 1). In May 1991, flowering shoots composed 2.0 [+ or -] 1.5% (n = 23) of the total shoots. The density of vegetative shoots declined linearly with water depth below 1 m ([r.sup.2] = 0.79).

[Figure 1 ILLUSTRATION OMITTED]

Although both sexes of surfgrass flowered all year long, most reproduction during 1990-1992 occurred between May and August, particularly June and July (Fig. 2). The mean density of flowering shoots during May-August ranged from 20 to 854 shoots/[m.sup.2] and reached a maximum at a depth of 1.5 m. Based on the most complete censuses (June-August 1991), flowering shoot abundance varied significantly from one month to the next and over depth, with a significant interaction (Table 1). By August, flowering shoot density declined at every depth, but the decline was greater for surfgrass above 3 m; thus, deeper surfgrass sustained reproduction longer in the summer.

[Figure 2 ILLUSTRATION OMITTED]

Table 1. Results of analysis of variance (Model 1) over time and water depth for female reproductive ramets. Data (square-root transformed) from June to August 1991 at 1.5, 3, 4.5, 6.1, and 7.6 m (Figs. 2, 5). "Shoot" refers to flowering shoot. "Flowers" include immature, receptive, and fertilized flowers. "Ovules" refer to the average number of ovules per spadix.
    Factor               df    MS         F       P

Flowering shoots
  Month (M)               2   258.8      4.364   0.015
  Depth (D)               4   181.2      3.054   0.019
  M X D                   8   166.9      2.814   0.006
  Error                 134    59.3

Spadices/shoot
  Month (M)               2     0.028    0.192   0.826
  Depth (D)               4     0.585    3.973   0.005
  M X D                   8     0.122    0.828   0.579
  Error                 125     0.147

Flowers/shoot
  Month (M)               1    40.8     10.023   0.002
  Depth (D)               4    16.2      4.053   0.005
  M X D                   4    26.5      6.628   0.000
  Error                  85     4.0

Ovules
  Month (M)               1     0.971    6.093   0.017
  Depth (D)([dagger])     3     0.256    1.608   0.197
  M X D                   3     0.329    2.065   0.115
  Error                  58     0.159


(*) June and July only; seeds dehisced in August.

([dagger]) 7.6 m depth omitted (n = 1 in June).

Because reproductive development of female flowers was basically similar across depths, with deeper surfgrass lagging slightly in reproductive maturation (Fig. 3, June 1991 across all depths), data across the census dates are presented only for 3 m depth (Fig. 4). Female flowering shoots required several months to mature and release seeds, initiating growth in spring but rarely maturing seeds before July. Seeds were most numerous in August, by which time many of the spadices had dehisced. Early flowers and fruits, some in deformed spadices, occurred in January and February but were smaller than those developing in spring.

[Figure 3 and 4 ILLUSTRATION OMITTED]

Because flowering shoots of surfgrass are modular, reproduction by the population is a function of numbers of flowering shoots in the population and spadices per shoot, and flowers, fruits, and seeds per spadix, and a trade-off, for example, between the number of shoots vs. number of spadices per shoot, might occur so that reproductive effort per reproductive remet and within the population remains constant spatially or temporally. Female flowering shoots declined with increasing water depth below 1.5 m and over the summer, and there were no compensating increases in the other reproductive ramets within a flowering shoot (Fig. 5). This decline was primarily due to a reduction in flowering shoots but also a smaller, significant reduction in number spadices per flowering shoot with depth (Table 1). Each shoot had on average four spadices, and the deepest shoots had roughly one less spadix than shallower shoots (Fig. 5). The number of spadices per shoot did not vary throughout the summer (Table 1), nor over the course of a year at 1.5 m (January through September 1991, P = 0.276, df = 6, 54). The average number of mature ovules (fertilized or not) per spadix on a flowering shoot varied between June and July but not across depth (Table 1).1 excluded from this average the spadices that were immature, dehisced, or partially grazed, and the 2-3 youngest ovules within a spadix because they never matured. All flowers on a spadix apparently were fertilized within a few days of each other. With the exception of the youngest ovules, most developed synchronously from stigma exertion through seed release.

[Figure 5 ILLUSTRATION OMITTED]

Throughout the bed, female flowering shoots were much more common than males (Fig. 1). Males were rare above 3 m but increased with depth. The flowering shoot sex ratio was significantly different from 1 at each depth during each sampling date, except for three of a total of 45 depth-date combinations during 14 census dates (P [is less than or equal to] 0.05, Bonferroni corrected). At a given depth-date combination, the sex ratio of male: female flowering shoots ranged from 0 to 1.05, with a population average ([+ or -] 1 SD) of 0.18 [+ or -] 0.28. The mean sex ratio (mean male per mean female flowering shoots) increased linearly with depth (P = 0.002) to a maximum mean of 0.45 at 7.6 m (Fig. 6). This female-biased sex ratio was maintained over yearly reproductive episodes through 1993 (S. L. Williams, personal observation).

[Figure 6 ILLUSTRATION OMITTED]

Male rarity created high variance in male flowering shoot abundance and there was no significant difference in the abundance of male flowering shoots over time or depth during June through August 1991 (Table 2). However, in May 1991 (the most complete collection of males, Fig. 7), the number of spadices per shoot declined significantly with depth (P [is less than] 0.000, df = 1, 36), paralleling the female pattern (see below, Fertilization potential). The mean number of anthers per spadix on a single shoot was constant across depths (P = 0.334, df = 1, 36) and ranged from 16 to 19 anthers (mean [+ or -] 1 SD = 16.8 [+ or -] 1.7).

[Figure 7 ILLUSTRATION OMITTED]

TABLE 2. Results of analysis of variance (Model 1) over summer months and water depth for number of male flowering shoots per square metre. Data (square-root transformed) from June-August 1991 at depths of 1.5, 3, 4.5, and 6.1 m (Fig. 2).
Factor        df       MS        F          P
Month (M)     2      8.572     0.312      0.732
Depth (D)     4     51.972     1.892      0.115
M x D         8     30.246     1.101      0.366
Error       134     27.467




Although distinct clones of each gender were common, they also intermingled and thus, it is unlikely that gender is environmentally determined. This conclusion is supported further with data presented below.

The decline in flowering shoots in winter and over depth paralleled declines in light availability (Fig. 8) and temperature (McFarland and McAlary 1992) and probably underlies the significant time and depth interaction terms in the ANOVAs.

[Figure 8 ILLUSTRATION OMITTED]

Losses of flowers and seeds to mortality and grazing

The potential seed crop of surfgrass was reduced through fruit and seed abortion by only a few percent (Table 3, 1991 data only for brevity). In each year, fruits and seeds showed no mortality until July, with the exception of February 1991. By July, many of the fruits were overgrown with the encrusting bryozoan Membranipora sp., and while some of these epiphytized fruits decomposed, others developed normally. Fruit and seed abortions increased in August when up to 40% of the flowering shoots exhibited evidence of decomposing fruits or seeds (Table 3). These abortions also seemed to increase with water depth, with an average of 0.4 abortions/flowering shoot at 1.5 m water depth and 6 abortions/flowering shoot at 7.6 m. Most of the decomposing fruits and seeds had no evident physical damage. Loss of fruits and seeds to abortion continued into September but reductions in the potential seed crop could not be calculated because most of the seeds had been released and spadices had dehisced. Numbers of abortions per flowering shoot in August 1992 were double the previous year and showed a similar increase with water depth.

TABLE 3. Average seed production and estimated reduction due to fruit and seed mortality across water depth. Seed density was calculated from average flowering shoot density (Fig. 2), average density per shoot (Fig. 5), and average flower density per spadix (Fig. 5). "% shoots aborted" = % of shoots (n = 10) with at least one aborted ovary, fruit, or seed. July abortion density was calculated from average flowering shoot density (Fig. 2) x % shoots aborted x average number of ovules, fruits, and seeds aborted per shoot (data not provided). "% loss in summer 1991" based on maximum seed crops of June and July corrected for maximum abortions in August. Ellipses indicate no data.
                                                    Depth (m)
    Date                        1.5      3.0          4.5
May
  Seeds/[m.sup.2]               9756     2767         2877
  % shoots aborted                 0       0            0
June
  Seeds/[m.sup.2]               4986     12374        9792
  % shoots aborted                 0       0            0
July
  Seeds/[m.sup.2]              11718      4396       10218
  % shoots aborted                 0        20          20
  No.: abortions/[m.sup.2]         0        48          31
  % loss in July                   0         1.1         0.3
August(*)
  % shoots aborted                30        40          40
% loss in summer
  1991                       0.4-0.7    1.2-2.3      1.1-2.3

    Date                        6.1        7.6
May
  Seeds/[m.sup.2]               5421        ...
  % shoots aborted                 0        ...
June
  Seeds/[m.sup.2]                760        334
  % shoots aborted                 0          0
July
  Seeds/[m.sup.2]               4352       2460
  % shoots aborted                 0          0
  No.: abortions/[m.sup.2]         0          0
  % loss in July                   0          0
August(*)
  % shoots aborted                20         40
% loss in summer
  1991                         1.9-2.8      8.0([dagger])


(*) Seed density not available because most seeds had dehisced.

([dagger]) July seed crop only; June seed crop yielded [is greater than] 100% reduction due to delayed development with depth.

Based on mean flowering shoot density, up to [approximately equal] 400 seeds/[m.sup.2] were lost through abortion in August. Assuming that the number of fruits and seeds aborted per flowering shoot in August represented the fate of the peak potential seed production in June or July (before most abortions occurred), abortion reduced seed set by [is less than] 3%, except at 7.6 m (Table 3). This might be extreme for surfgrass at 7.6 m where reproductive development lagged (Fig. 3). Potential fitness was thus highest for individuals living in shallow waters where fecundity is higher and pregermination mortality of offspring was lower. This conclusion assumes that abortions do not select for progeny with higher fitness (Willson and Burley 1983, Lee 1988).

Grazing reduced the seed crop even less than abortion. Estimating this (Table 4) was difficult because typically only one spadix on one flowering shoot per sample was grazed, and most frequently an entire portion of a spadix was clipped by fish, although at times ragged pieces of fruits were missing, similar to the damage a crab can inflict.

TABLE 4. Reduction in female reproduction due to grazing. "Flowering shoots" = % shoots with grazing damage (n = 10); "spadices/shoot" = % spadices grazed per flowering shoot, averaged over grazed flowering shoots; "F + S/spadix" = mean ([+ or -] 1 SD) % fruits and seeds grazed per spadix, averaged over all grazed spadices; "No. (F + S)/ shoot" = no. of fruits and seeds grazed per flowering shoot, averaged over all grazed flowering shoots; "% grazed" = % spadix removed. Fish grazing was assessed as % spadix grazed; grazing by other herbivores as % fruits and seeds within a spadix.
                                   Depth (m)
                           1.5           3.0        4.5   6.1    7.6
June 1991
  Flowering shoots         11             10         0     10      0
  Spadices/shoot           25             25         0     33      0
  F S/spadix              ...             14         0     22      0
  No. (F + S)/shoot       ...              1         0      2      0
  % grazed                 10              0         0    ...      0

July 1991

  Flowering shoots         25             20        22      0     10
  Spadices/shoo       30[+ or -]14   38[+ or -]18   25      0     25
  F + S/spadix             50            ...       ...      0    ...
  No. (F + S)/shoot       ...              7       ...      0    ...
  % grazed                 50            ...       ...      0     20

August 1991

  Flowering shoots         17              0         0      0      0
  Spadices/shoot           25              0         0      0      0
  F + S/spadix            ...              0         0      0      0
  No.(F + S)/shoot          0            ...         0      0      0
  %  grazed                50              0         0      0      0




Males sustained significantly more grazer damage than females (Table 5). Thirteen percent of male spadices were cleanly bitten across the long axis; females showed no evidence of this type of damage. Although the gastropods Norrisia norrisi and juvenile Astrea undosa were abundant on surfgrass (mean [+ or -] 1 SD 9 individuals/[m.sup.2] [+ or -] 14 and 6 individuals/[m.sup.2] [+ or -] 19, respectively, n = 42), they did not cause this type of damage in the laboratory. Instead, the damage was typical of the herbivorous fish Girella nigricans (opaleye), which were abundant in the study area (26 individuals/[m.sub.2] [+ or -] 7, n = 10 transects). Opaleyes ate entire leaf shoots drifting in the water column, and schools of up to 55 individuals would suddenly dive into the canopy and rip surfgrass. I do not know the basis for the selection for rarer male surfgrass; females with fruits or seeds were larger and probably tougher, and males were yellow-colored to my eye. Behavior of herbivores aside, their preference did not cause an effective reduction in the average male fitness.

TABLE 5. Comparison of grazer damage of field-collected male and female spadices by Girella nigricans: numbers of spadices grazed or entire.
                Not               Likelihood
Date          grazed    Grazed      ratio       P
July 1991
  Female       107         0       17.853      0.000
  Male         102        13

April          1992
  Female        105        0       20.604      0.000
  Male          165       22




In summary, surfgrass produced many flowering shoots, flowers, and seeds, and fertilization, seed production and release apparently were not vulnerable life history transitions. Increased male susceptibility to herbivory of reproductive structures did not lower fertilization success in the population, although individual males potentially suffered a loss in fitness.

Sex ratio and fertilization potential

Despite the rarity of males, fertilization apparently was not limited by pollen availability (Table 6). Male flowering shoots typically had at least twice as many spadices and 5-8 more anthers (each with two pollen sacs) per spadix than females had ovules. With an average of 16602 ([+ or -] 1 SD) pollen grains ([+ or -] 2064, n = 6 individuals) in each pollen sac, pollen grains exceeded the number of ovules by five orders of magnitude. Although I do not know the pollen load required for maximum seed set, I never observed an unfertilized ovule within a row of developing or mature fruits on a spadix. Because the surfgrass canopy was so dense and water flow is reduced significantly within seagrass canopies (Fonseca et al. 1982, Eckman 1987, Gambi et al. 1990), I had expected that more seeds would be set on flowering shoots at the edges of patches, but this obviously was irrelevant. These observations indicated that pollen dispersal did not limit fertilization.

TABLE 6. Average ovule (each female flower contains one ovule) and pollen counts for surfgrass in May 1991, from Figs. 2, 5, and 7. "Receptive" indicates stigmas were exerted or ready to exert.
                                             Water depth (m)

                                            1.5          3.0
Female flowers/[m.sup.2]                    9756         2767
Receptive female flowers/[m.sup.2]          2027          539
Male flowers/[m.sup.2]                      5568         1589
Pollen grains/[m.sup.2](*)             184879872     52761156
Average pollen/ovule ratio
in population                              18950        19068

                                            Water depth (m)
                                            4.5          6.1
Female flowers/[m.sup.2]                    2877         5421
Receptive female flowers/[m.sup.2]            58          686
Male flowers/[m.sup.2]                      5058         4096
Pollen grains/[m.sup.2](*)             167945832    136003584
Average pollen/ovule ratio
in population                              58375        25088


(*) Each flower has two anthers with 16 602 [+ or -] 2064 pollen grains/anther, n = 6 males with three anthers averaged per male.

Resource allocation to male and female reproduction

The average mass of flowering shoots of both sexes declined at 6.1 m to [approximately equal] 60% of the maximum mass at 1.5 m (Fig. 9). This result is consistent with the decreasing numbers of vegetative and reproductive shoots over depth and the hypothesis that light limits surfgrass reproduction. The mass of female flowering shoots was on average 25% higher [(is greater than or equal to] 0.1 g) than that of males (Fig. 9), and the average difference among vegetative ramets was similar. Gender and depth differences in mass of both vegetative and reproductive ramets were significant (Table 7); however, the pattern of decreasing mass with depth was not obvious for vegetative ramets, particularly for males. Females had significantly longer leaves than males (mean = 80 vs. 67 cm, longest leaf in a shoot; two-sided t test, P [is less than] 0.024, n = 51 males and 48 females). This length difference could explain the biomass difference, although I noted in the Methods the problems with leaf length as an indicator of plant size.

[Figure 9 ILLUSTRATION OMITTED]

TABLE 7. Results of ANOVA (Model 1) comparing dry mass of female vs. male flowering shoots and leaf shoots over water depth (Fig. 9).
Factor              df    MS        F      P
Flowering shoots
  Gender             1   0.102    6.618   0.011
  Depth              3   0.193   12.503   0.000
  Gender x Depth     3   0.078    5.154   0.002
  Error            185   0.015
Leaf shoots
  Gender             1   0.198   20.236   0.000
  Depth              3   0.115   11.710   0.000
  Gender x Depth     3   0.037    3.772   0.012
  Error            202   0.010




There were no significant differences between males and females in the carbon and nitrogen content or C/N ratio of spadices or the rest of the tissue of the flowering shoots (Table 8). The dry mass of spadices contained on average 3 mol more nitrogen relative to carbon than the rest of the flowering shoot tissue, presumably due to higher nitrogen in pollen and ovules. Spadices represented [approximately equal] 30% of the mass of a flowering shoot.

Table 8. Carbon and nitrogen content (% dry mass) and molar ratios in reproductive tissue from female and male surfgrass and probability levels (P) from Mann-Whitney tests. Mean ([ + or -] 1 SD) values, n = 10 flowering shoots.
                          Spadix
Sex               C                    N
Female   29.66 [+ or -] 2.03   3.27 [+ or -] 0.33
Male     30.31 [+ or -] 2.41   3.29 [+ or -] 0.57
P               0.450                 0.791

                Spadix         Remainder of tissue
                  C/N                    C
Sex       9.08 [+ or -] 0.91   28.92 [+ or -] 2.39
Female    9.38 [+ or -] 1.28   29.98 [+ or -] 3.56
Male            0.520                  0.364
P
                    Remainder of tissue
                 N                       C/N
Sex       2.49 [+ or -]  0.24     11.73 [+ or -] 1.48
Female    2.41 [+ or -]  0.15     12.50 [+ or -] 1.78
Male            0.596                    0.290
P




Although female reproductive shoot densities in the population were obviously higher than males, and the biomass of female vegetative and flowering shoots was significantly greater, other quantitative differences between genders were less obvious, underscoring my inability to sex nonreproductive clones. Rhizome width at the newest leaf shoots (conservative estimate of plant size normalized for age) was not significantly different (P [is less than] 0.588, two-sided t test) between females (mean [+ or -] 1 SD = 3.1 cm [+ or -] 0.63, n = 48) and males (3.1 cm [+ or -] 0.65, n = 51). Although the mean density ([+ or -] 1 SD) of vegetative shoots per 100 [cm.sup.2] quadrat was slightly higher for female than male (65 [+ or -] 30 shoots vs. 58 [+ or -] 46 shoots), this difference was not significant (two sided t test, P [is less than] 0.696, n = 14 females, 8 males).

Assuming these quadrats represented one clone, the two indirect estimates of resource allocation to reproduction relative to genes or to plant size, were not significantly different. The average ([+ or -] 1 SD) ratio of flowering shoot density: total vegetative [+ or -] flowering shoot density per quadrat was 0.122 [+ or -] 0.109 for females and 0.188 [+ or -] 0.116 for males (P [is less than] 0.199). When remet densities were multiplied by per remet masses, the result that the per genes allocation to reproduction was similar between males and females did not change. The average ([+ or -] 1 SD) ratio of flowering shoot mass: total flowering [+ or -] vegetative shoot mass in these quadrats was 0.213 [+ or -] 0.167 for females and 0.343 [+ or -] 0.187 for males (P [is less than] 0.106). Because there were far fewer ovules than pollen (Table 6), the per gamete cost for females was considerably higher per reproductive remet and per genet.

Comparison of male vs. female growth

At depths where males were more abundant (below 3 m), their leaf elongation rates ([+ or -] 1 SD, 2.8 cm [multiplied by] [shoot.sup.-1] [multiplied by] [d.sup.-1] [+ or -] 0.58, n = 32 clones) were not significantly different than females (2.9 cm [multiplied by] [shoot.sup.-1] [multiplied by] [d.sup.-1] [+ or -] 0.46, n = 32, two-sided t test, P = 0.574). Thus, despite higher absolute resource allocation per flowering and vegetative remet, female surfgrass did not forfeit growth of vegetative ramets. A trade-off between reproduction and current growth that could result in a biased sex ratio would have to appear in rhizome propagation, the subject of the transplant experiment below.

Monitoring the longer term growth of surfgrass in the surge zone was frustrating. Three months after transplanting (28 September 1991), 9 of the original 10 transplant units remained. Thereafter, I was unable to monitor the units until spring, when it was obvious that winter surf conditions resulted in the loss of five more. Months later I found several of the units minus plants below 30 m depth.

In the successful transplants, females grew better than males (Fig. 10), despite starting out with equal clone size (see Methods) and leaf shoot density per clone ([+ or -] 1 SD, 63 [+ or -] 29 females vs. 71 [+ or -] 16 males), and presumably rhizome size. Over 22 mo, females nearly doubled the mean ([+ or -] 1 SD) number of leaf shoots and increased by half the mean area of the substratum covered (22 [cm.sup.2] [+ or -] 19, n = 3). The mean ([+ or -] 1 SD)male leaf shoots declined by half as did the area covered (7 [cm.sup.2] [+ or -] 7, n = 3). These differences apparently did not result from interference competition; I did not observe females crowding or overgrowing males. This trend is not statistically defensible because of the small sample size and asymmetrical distribution of the data (mean percent original leaf shoots in August 1992 = 113, median = 84), and unfortunately my other attempts to transplant failed. However, if males continued to decline, there would have been a long-term survival difference between the sexes at shallower depths.

[Figure 10 ILLUSTRATION OMITTED]

All transplanted clones flowered during the subsequent reproductive seasons (between 10 and 14 mo post-transplantation) and there was no adult gender lability. Furthermore, I observed no gender lability in clones I had identified throughout the study area. This evidence suggests that if gender is determined by the environment, it must be canalized early in the life history of surfgrass.

Males are the weaker sex: gender-based differences in tenacity

Drifting clumps of surfgrass with intact shoots and rhizomes were common and indicated that the attachment of rhizome and roots to the substratum was the weakest part of the plant (S. L. Williams, personal observation). The mean ([+ or -] 1 SD) force required to detach 30 shoots from female clones was 78.4 [kg.m.sup.-2] [multiplied by] [s.sup.1] [+ or -] 42.3 (n = 46 clones), compared to 57.4 [+ or -] 27.0 for male clones. This difference was significant (P us less than] 0.002, df = 45); males were more weakly attached to the substratum. Often additional shoots were detached because they were attached to the rhizomes of the ones harnessed and the measured tenacities included this force. No obvious morphological feature was associated with this attachment difference; rhizome size was the same and females had significantly longer leaves, which hypothetically increased the drag on them. There was perhaps a difference in the chemical composition, or quantity, of the "glue" attaching surfgrass to the substratum. Although currently incomplete, complementary laboratory measurements of biomechanics of individual surfgrass tissues have not revealed other notable differences between genders; these data will be reported elsewhere (S. Williams and M. Koehl, unpublished manuscript).

Summary of results

Surfgrass flowered and produced seeds yearly and there was no evidence for differential frequency of flowering between sexes. Gender did not appear to be determined environmentally. Reproductive components (number flowering shoots, number flowers per shoot, biomass) and vegetative shoot density declined with water depth, suggesting light is a limiting resource for growth and reproduction. The flowering shoot ratio was significantly female biased, and males were segregated in deeper habitat. Male rarity, however, did not limit fertilization; the pollen/ovule ratio was high and fertilization was virtually 100%, irrespective of local male density, with few subsequent losses to abortion and herbivore damage. Female clones grew faster and ramets survived better than males in shallow depths. Female vegetative and flowering ramets each contained significantly more biomass than their male counterparts across all water depths, although limited data indicate that biomass allocation to flowering shoots per genes was not different. One mechanism for greater ramification of female clones in shallow waters is that males were more susceptible to dislodgement from the sub-stratum.

DISCUSSION

Sexual reproduction of surfgrass

Surfgrass reproductive effort is considerable; up to a quarter of the shoots invest substantial biomass in flowering ramets (Fig. 1). Fertilization is virtually 100%, despite male rarity, and subsequent losses to abortion or herbivory reduce this maximum possible seed set by only a few percent. Many angiosperms have lower seed set (Bawa 1980, Stephenson 1981, Wiens 1984), particularly other self-incompatible species (Sutherland 1986a). Surfgrass is also unusual in its high average log ([is greater than] 4) of the pollen/ovule ratio (Table 6). This ratio is an order of magnitude higher than the mean ratio (log 3.65) recorded for outcrossing angiosperms, which have high pollen/ovule ratios compared to other breeding systems, and for wind-pollinated grasses (log 2.98) (Cruder 1977). Cruden suggested the pollen/ovule ratio reflects the probability of sufficient pollen transfer for maximum seed set and thus, hypothetically the relative uncertainty of hydrophilous pollination in surfgrass. Certainly, turbulence in the marine environment contributes spatial and temporal unpredictability to reproduction and recruitment at least for animals (Roughgarden et al. 1988, Denny and Shibata 1989, Gaines and Bertness 1993). How such uncertainty influences the evolution of marine plant and algal reproductive systems is unclear. Although beyond the scope of this paper, the combination of hypothetical pollination uncertainty in surfgrass and high seed set might provide an interesting example for assessing thevies on the evolution of plant reproductive systems through experimentation or comparison of pollen/ovule and floral sex ratios and fruit set across taxa (e.g., Sutherland 1986a, b, Campbell and Halama 1993). The study of plant reproduction ecology and evolution should benefit from more aquatic examples (Cox 1988, Lovett Doust and Lovett Doust 1988, Barrett et al. 1993).

Neither pollen availability nor dispersal limit seed production by surfgrass. Up to 10 000 seeds/[m.sup.2] are produced, which, if successfully germinated, could replace virtually every leaf shoot in the population. Although surfgrass germination is apparently high (Turner 1983, Kuo et al. 1990), seedling mortality is even higher (Stewart 1989, Turner 1983). I found only six subtidal seedlings during a systematic search of 350 [m.sup.2] between March and May 1992 and during qualitative observations, although I found seeds in sediments. Thus, seedling recruitment is a particularly vulnerable stage in the surfgrass life history, and should be included as a factor in evolutionary studies of plant reproductive systems. It remains to be determined whether seed predation, similarly to eelgrass (J. R. Fishman and R. J. Orth, personal communication), or seedling mortality limits recruitment relatively more. Because of the reduction in seed production with increasing water depth, there may be demographic or genetic consequences for the population if there is net transport of seeds, which are negatively buoyant, away from the shallow bed. The hydrodynamics of seed dispersal need to be examined in seagrasses (Orth et al. 1994).

Physiological limitations of surfgrass reproduction and seagrass reproduction in general are poorly known. In my study, the decline in vegetative shoots and reproductive effort with increasing water depth is consistent with light limitation of surfgrass growth an reproduction. Light is a major factor controlling seagrass distribution and growth (Drysdale and Barbour 1975, Dennison 1987). Nutrient availability also can influence seagrass reproduction (Short 1983); however, the effect on surfgrass requires further investigation. Nutrient availability in the water column at Bird Rock increases with depth because periodic upwelling deliverscold, nutrient-rich water to coastal southern California (Jackson 1977, Zimmerman and Kremer 1984). Dissolved inorganic nitrogen concentrations are low (<I [micro]mol/L) in surface waters over surfgrass at Bird Rock, even after spring rains expected to deliver nutrient-rich runoff from accumulated guano (S. L. Williams, unpublished data). Nutrient concentrations are likewise low in coastal waters in southern California (Jackson 1977), including within surfgrass beds J. Terrados, personal communication). Based on the observed temperature-nutrient correlation (Jackson 1977, Zimmerman and Kremer 1984), surfgrass below 4.5 m depth should be exposed periodically to higher nutrient concentrations, but the nutrient regime is undoubtedly more complex than predicted by the correlation between temperature and nutrient availability. The actual nutrient flux may vary across depth, but this is not apparent in the absence of water velocity data. Finally, although surfgrass grows on rocks, sediments accumulate in the rhizome mat to various degrees. The sediments could provide a nutrient source for surfgrass roots; this is currently under investigation in my laboratory (J. Terrados and S. L. Williams, unpublished data).

Photoperiod and particularly temperature have been implicated as the major environmental factors controlling seagrass reproductive phenology (e.g., McMillan 1976, Phillips et al. 1983, Durako and Moffler 1987), but the importance of these factors for surfgrass needs to be established under controlled conditions. Certainly, they would co-vary with depth and this could explain why shallow surfgrass completes reproduction earlier than deeper surfgrass.

Female-biased sex ratio

This study addresses the proximate causes of a female-biased sex ratio in surfgrass. The predictable var iation of the flowering sex ratio with water depth suggests that environmental factors control the adult sex ratio in the population, but not through gender determination. T he primary sex ratio (i.e., at the end of the period of parental investment) of surfgrass is virtually impossible to estimate with certainty; the turbulent hydrodynamic environment of surfgrass would be difficult to mimic in long-term culture conditions, and successful crossing and progeny assessment has been achieved for only one seagrass species (Zostera marina; Ruckelshaus 1994). Nonetheless, evidence to suggest that the primary sex ratio is unity includes (1) surfgrass is obligately outcrossing, (2) sex chromosome s were identified equivocally in Phyllospadix torreyi (Stewart and Rudenberg 1980) and unequivocally in the three Japanese species of Phyllospadix (Uchiyama 1993), and (3) adult gender is not environmentally determined (mixed-sex patches, no gender lability in transplants and mapped clones). Even so, an unexplored mechanism for a skewed primary sex ratio in surfgrass could be that female-determining pollen tubes fertilize ovules more frequently than male-determining ones, as in some other angiosperms with female-biased sex ratios (Lloyd 1974). If this occurs in surfgrass, ecological factors as described here would further skew the primary sex ratio.

Although determination of the primary sex ratio is important for considerations of whether the sex ratio is adaptive, i.e., selected for, it is also important to consider subsequent ecological modifications of sex ratios. For example, biased adult sex ratios can have pro-found implications for the genetic effective population size or neighborhood area (Levin 1978). An unequal sex ratio in a reproducing population acts to reduce the effective population size, which has theoretical consequences for the rate of loss of genetic diversity through genetic drift (Lance and Barrowclough 1987).

Sex ratio biases in some angiosperms result from variations in the frequency and size dependence of flowering (Gross and Soule 1981, Bullock et al. 1983, Allen and Antos 1993, Thomas and LaFrankie 1993), but not in surfgrass (Table 1). Such variations are typically associated with male biases, and they usually reflect a greater reproductive cost for females, so that females reproduce only in "good" resource years. I observed no gender-based variation in reproductive effort between years, despite occurrence of a major El Nino event in 1990-1991 (McFarland and McAlary 1992). El Nino occurrences likely represent the most severe oceanographic disturbances in southern California, and they have striking ecological effects on marine organisms (Tegner and Dayton 1987). The El Nino event of 1990-1991 changed the temperature profiles around Catalina Island (surface sea temperatures reached above 21 [degrees] C compared to [is less than] 20 [degrees] C in non El Nino years). Because nutrient availability is strongly correlated with temperature (Zimmerman and Kremer 1984), the event probably changed the nutrient, and perhaps the light, regimes at the study site. Although the event resulted in loss of giant kelp (Macrocystis pyrifera) at my site, there was no change in the degree of female bias in the surfgrass population.

Although the age structure of the surfgrass population is unknown, differences between genders in time of first reproduction are also unlikely to explain the biased sex ratio. Because recruitment from seeds is a rare event, most of the clones in the bed should be relatively old. Certainly, the majority of distinct clones flowered and a quarter of all ramets flowered. Gender differences in a minimum clone size required for reproduction are also unlikely to cause a sex ratio bias; the size of the transplanted clones was small but males and females flowered with as few as 24 leaf shoots (compare density to Fig. 1).

A female-biased sex ratio in surfgrass apparently results from greater ramification of female clones. Empirical studies have supported the theory that sex ratios should be biased toward the gender that allocates fewer resources to reproduction, and thus has more available for survival and growth where resources are limiting, particularly in relatively long-lived plants (e.g., Lloyd 1973, Waser 1984, Allen and Antos 1993, Thomas and LaFrankie 1993). Although Sakai and Burris (1985) reported that the expected reduction in female clonal growth and increased mortality associated with higher resource allocation to reproduction was not supported in clones of trembling aspen, the sex ratio was presumed to be unity or male biased. For surfgrass, there is no convincing evidence that females allocate fewer resources to reproduction than males. Greater female vegetative propagation could be the result of larger plant size or other vegetative differences, although such differences are too subtle to use for field identificaton of sexes. Rhizome width was not different, nor were leaf shoot densities in census quadrats and transplants. One uncertainty in my estimate of resource allocation to reproduction relative to plant size is that rhizome and root biomass might differ and not be correlated directly with rhizome width; however, this difference is unapparent. Differences in leaf mass could be due to size differences unrelated to resource allocation (e.g., breakage, herbivory); certainly, leaf growth rates were not different between genders. Thus, there was no obvious cost in terms of vegetative growth, or advantage in terms of size, for females to allocate more biomass per reproductive remet or per gamete. The mean biomass allocation to flowering shoots (relative to total biomass) was slightly but not statistically higher for male genets. If this difference is biologically significant, it implies that subtle differences in resource allocation between genders can have large effects on population sex ratios. More detailed physiological data are required to evaluate this hypothesis. If the chlorophyll-containing flowering ramets are self-sufficient in resource acquisition through photosynthesis and nutrient uptake, this resource-limited reproduction hypothesis would be negated. Certainly, the decline with increasing water depth in reproductive ramets and flowering shoot biomass of both sexes, and also the absolute decline in the number of female flowering ramets, suggest that light is limiting to reproduction, particularly female.

Resource limitation and greater allocation of resources to reproduction cannot, however, explain why there is an increase in the absolute number of male flowering ramets with depth. A proximate explanation for male rarity and lower male survivorship and clonal growth in shallow waters is that males are more weakly attached to the substratum than females. Hydrodynamic forces on surfgrass appear to be greatest in shallow waters. A manifestation of this difference is the relative ease of completing a surfgrass census at 5 m vs. 1 m water depth. Although water flow data are incomplete for the study site, average water velocities in the intertidal zone are 50-100 cm/s, slowing by half at -1 to -2 m water depth at high tide (R. Carpenter and C. Robles, personal communication). Surfgrass leaves in 1-2 m water depth often are completely extended during a wave period and thus, experience the full tensile force of wave surge, while leaves deeper in the bed do not become fully extended, except in strong tidal currents (S. L. Williams, personal observation). Males, weakly attached to the substratum, should have higher mortality from hydrodynamic forces than females, and males should survive best in calmer, deeper waters. Hydrodynamic-induced male mortality provides a hypothesis for the female-biased sex ratio in the face of apparently equal allocation to reproduction. Also, once females ramified extensively in shallow waters, recruitment of either gender perhaps is difficult under the dense canopy and the bias would be reinforced. An alternative hypothesis is that there is a gender difference in germination requirements, so that most males would germinate best in conditions in deeper waters. There is no apparent dimorphism in seed morphology and thus, both sexes hypothetically have similar transport characteristics. In any case, net transport of seeds away from shallow regions would confer increased fitness for males, unlike females.

Losses of flowering ramets due to hydrodynamic forces would not be adaptive for females because they must support developing seeds over the several months required for maturation and release. Individual male ramets, in contrast, mature and release pollen over a much shorter time period. Why males would not evolve similar strong attachment to the substratum is puzzling. Weak attachment might facilitate pollen dispersal through drifting of flowering shoots. Male and female flowering shoots are neutrally buoyant and commonly drift and entangle in the bed. This hypothesis is tenuous, though, because it requires that pollen would remain viable in a drifting shoot and that the gain in male fitness via drifting shoots would be substantial relative to pollen dispersal from attached shoots, which have sequential development of spadices. Males in deeper water depths might have a pollen dispersal advantage, depending on water flow. Obviously, data are needed on pollen dispersal, frequency of detachment and subsequent viability of flowering shoots, and residence times within the bed under natural hydrodynamic conditions.

Unfortunately, few data are available on seagrass sex ratios, despite the notable high occurrence of dioecy within the taxa. The female-biased sex ratio observed at my study site occurs at least intertidally in Phyllospadix torreyi, P. serrulatus, and P. scouleri along the Pacific coast of North America (S. L. Williams, personal observation) and in the Japanese species (Uchiyama 1993). Les (1988) interpolated sex ratio data for seven seagrass species, including two surfgrass species. Unfortunately, generalizations about sex ratio bias in seagrasses cannot be made because the limited data rarely account for seasonal or site variations. For example, male and female biases have been reported from short-term surveys of Thalassia testudinum (turtlegrass), a long-lived, dioecious, tropical species (Grey and Moffler 1978, Durako and MoMer 1985a, Cox and Tomlinson 1988), but a more comprehensive study revealed that the ratio varies between male and female bias temporally and spatially in Florida (Durako and MoMer 1985b, 1987). Limited spatial segregation also occurs in Thalassia, with females more common at the edge of beds (Durako and MoMer 1985b). Although Cox and Tomlinson (1988) observed a male-biased sex ratio over only 3 d in a Caribbean turtlegrass bed, they were able to conclude that the bias was not due to greater temporal variability in male flowering, based on an examination of distinct flowering scars left on perennial leaf short shoots.

Life history characteristics and breeding systems of aquatic angiosperms, and not their habitat, appear to determine the genetic structure of their populations (Barrett et al. 1993), as has been concluded for terrestrial a ngiosperms (Hamrick and Godt 1990). Yet, the details of the influence of gene flow, local selection, and sex ratio biases on the genetic structure and demography of aquatic angiosperms remain to be investigated. In surfgrass, gender segregation according to water depth implies that paternal gene flow is predominately in the onshore direction, where female fitness components are highest but male fitness components of survival, growth, and reproduction are lowest. At this level, hydrodynamics appear to influence both female and male fitness; pollen dispersal is not limiting to female reproductive success and male mortality is increased in turbulent shallow waters. Turbulent water motion characterizes many aquatic habitats, and it has led to a unique pattern of gender bias in surfgrass.

ACKNOWLEDGMENTS

I thank the following for risking motion sickness while diving in surfgrass: R. Espinoza, Dr. T. Klinger, B. Nyden, E. Takahashi, Dr. J. Terrados, A. Whitmer. For laboratory assistance, I thank H. Carpenter, N. Eckrich, R. Espinoza, B. Nyden, and S. Tibbitts. I am indebted to Dr. T. Klinger for helping design effective transplant units and stimulating discussion. Drs. Klinger, S. Cohen, and D. Reed provided insightful comments on manuscript drafts. S. Shaffer counted pollen, after perfecting the method. B. Nyden shared his data on opaleye herbivory. Dr. M. Koehl initiated me in the study of biomechanics, enabling the test of the cherished hypothesis of weaker males. R Ewanchuk modified the spring scales and assisted in tenacity measurements. Dr. R. Carpenter provided his inimitable field camaraderie. The director, Dr. W. McFarland, and staff of the Catalina Marine Science Center (now Wrigley M.S.C.) greatly facilitated this research, and McFarland provided temperature records. I thank Dr. R. Orth, and an anonymous reviewer for their critical evaluation of the submitted manuscript. Editor D. Marshall made a significant contribution to this study by suggesting I address resource allocation relative to genes and plant size, in addition to other useful clarification. The research was supported by Research, Scholarship, & Creative Activity and Grant-in-Aid faculty awards and by the College of Sciences, San Diego State University. This is a contribution from the Ocean Studies Institute, California State University System and ffom the Wrigley Marine Science Center.

(1) Manuscript received 18 January 1994; revised 29 September 1994; accepted 14 October 1994; final version received 14 November 1994.

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Susan L. Williams Department of Biology, San Diego State University, San Diego, California 92182-4614 USA
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