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Dispersal in Kelps: Factors Affecting Spore Swimming and CompetencyAuthor(s): Daniel C. Reed, Charles D. Amsler and Alfred W. EbelingReviewed work(s):Source: Ecology, Vol. 73, No. 5 (Oct., 1992), pp. 1577-1585Published by: Ecological Society of AmericaStable URL: http://www.jstor.org/stable/1940011 .Accessed: 08/10/2012 17:08

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Ecology,, 73(5), 1992, pp. 1577-1585 ? 1992 by the Ecological Society of America

DISPERSAL IN KELPS: FACTORS AFFECTING SPORE SWIMMING AND COMPETENCY'

DANIEL C. REED,2 CHARLES D. AMSLER,2'3 AND ALFRED W. EBELING Coastal Research Center, Marine Science Institute, University of California,

Santa Barbara, California 93106 USA

Abstract. The distance over which propagules can successfully colonize new sites depends on processes that increase the time they remain competent while being dispersed. As do feeding larvae, algal spores can contribute to their own nutrition (via photosynthesis) during dispersal. We explored the dispersal potential of the kelps Macrocystis pyrifera and Ptervgophora californica in laboratory experiments by examining (1) how long their spores can swim, (2) the contribution of energy derived from photosynthesis to spore swimming duration, and (3) the ability of spores to germinate and attach after they stop swimming. Results indicate that under photosynthetically saturating irradiance no spores of either species can swim longer than 120 h; < 10% of the spores were still swimming after 72 h. When placed in the dark, spores did not swim longer than 72 h; < 10% remained swimming after 48 h. More importantly, spores did not die after they stopped swimming; most germinated in the water column and retained their capacity to produce viable sporophyte recruits. The ability of spores to attach after they stopped swimming differed between the two species; settlement density declined in Macrocystis and increased in Pterygophora. Thus, the viable planktonic stage of these algae is not necessarily restricted to the spore but may include later life history stages. These results provide biological evidence that the spores and germlings of these kelps can remain competent in the plankton for extended periods of time, which is consistent with our previous findings that their dispersal can occur over greater distances than previously thought possible.

Key words: algae; competency; dispersal; kelp; Macrocystis; pyrifera; photosynthesis; plankto- trophic; propagule; Pterygophora californica; spore; swimming duration.

INTRODUCTION

The dispersal of propagules is of fundamental biological importance in restoring populations, maintain- ing species distributions, and promoting genetic diversity. Except perhaps for animals with relatively large larvae and short planktonic lives (Olson 1985, Young 1986, Davis and Butler 1989, Stoner 1990), direct mea- surements of dispersal for most marine organisms with planktonic propagules have not been obtained. In general, spores and larvae of most benthic marine organisms are small and difficult to identify, much less follow in an environment as vast and diverse as the pelagic ocean. Consequently, indirect methods are generally used to estimate the dispersal potential of most species with planktonic propagules (Keough 1989). Among these methods is that of estimating the usual length of time that spores or larvae remain competent (i.e., have the potential to settle and grow) in the plankton.

Competency can be prolonged through processes that either decrease the amount of metabolic energy ex-

' Manuscript received 13 May 1991; revised 25 October 1991; accepted 29 October 1991.

2 Contributed equally to this work. 3Present address: Department of Microbiology and Im-

munology (m/c 790), University of Illinois, P.O. Box 6998, Chicago, Illinois 60680 USA.

pended by a propagule or increase the amount of metabolic energy available to a propagule during its dispersal phase. For example, seed dispersal in many higher plants can be extended in both space and time if seeds undergo dormancy, a mechanism for energy conser- vation. Alternatively, the larvae of many marine animals remain competent in the plankton for weeks if they continue feeding. Although spores of most macroalgae appear to be quite short lived (reviewed in Hoffmann 1987, Santelices 1990), their dispersal has been likened to that of wind-dispersed seeds of higher plants (Hoffmann and Ugarte 1985, Hoffmann 1987, Reed et al. 1988). However, a more appropriate analog for the dispersal of marine algal spores may be plank- totrophic larvae of many benthic marine invertebrates (Amsler and Neushul 1991). As do feeding larvae, planktonic spores of at least some algae have been shown to contribute to their own nutrition (via photosynthesis) during dispersal (Kain 1964, Amsler and Neushul 1991). Although spores and larvae are trans- ported primarily by ocean currents, they may indirectly influence the distances they are dispersed by adjusting their position in the water column with photo-, geo-, or chemotactic behavior (algae: Kylin 1918, 1933, Suto 1950, Christie and Evans 1962, Muller et al. 1987, Reed et al. 1988, Amsler and Neushul 1989; larvae: reviewed in Thorson 1964, Crisp 1974). As with many

1578 DANIEL C. REED ET AL. Ecology, Vol. 73, No. 5

larvae (e.g., Knight-Jones and Crisp 1953, Crisp 1974, Jensen and Morse 1984, Raimondi 1988) chemicals may also stimulate settlement in actively swimming spores (Thomas and Allsopp 1983, Dillon et al. 1989, Amsler and Neushul 1990), thereby increasing their probability of settling in a "safe site" (sensu Harper et al. 1965).

Numerous observations provide evidence that many seaweeds can disperse over distances of hundreds to thousands of kilometres (reviewed in van den Hoek 1987, Santelices 1990, Neushul et al., in press). It has been argued that such long-distance dispersal occurs via detached plants or plant fragments that release spores or gametes after being set adrift. Colonization resulting from the dispersal of spores has been docu- mented over distances of at least 35 km (Amsler and Searles 1980), suggesting that at least some algae have spores that can remain competent for prolonged periods. Much of the evidence indicates that small ephemeral opportunistic algae have larger dispersal shadows than larger, longer lived species (e.g., Amsler and Searles 1980, Reed et al. 1988), with some excep- tions (Hoffmann and Ugarte 1985).

Kelps (Order Laminariales) are large, mostly long- lived, brown algae, which are prominent in temperate reef communities throughout the world. Their ability to disperse is critical because many species occur in highly disturbed habitats and have unstable population structures due to frequent local extinctions and recolonizations (Leighton et al. 1966, Barrales and Lobban 1975, Cowen et al. 1982, Foster 1982, Dayton and Tegner 1984, Dean et al. 1984, Dayton 1985a, Ebeling et al. 1985, Harrold and Reed 1985, Miller 1985, John- son and Mann 1988). Numerous reviews (e.g., Dayton 1985b, Schiel and Foster 1986, van den Hoek 1987, Santelices 1990) have suggested that effective spore dispersal in kelps is limited to a few metres and that recolonizations result from spores being released from drifting fertile plants (a narrow interpretation of An- derson and North 1966). Events of relatively dense, uniform recruitment, however, have been observed at several kilometres away from stands of fertile adults (Chapman 1981, Druehl 1981, Davis et al. 1982, Ebel- ing et al. 1985, Reed et al. 1988, Ambrose et al., in press). The uniform distribution of recruits over relatively large areas reported in these studies suggests that such widespread recolonizations probably result from the uniform dispersal of spores rather than the hap- hazard drifting of fertile plants (see arguments in Reed et al. 1988). Dispersal over these relatively long distances may require that spores remain competent in the plankton for extended periods. The biological mechanisms that allow for the prolonged competency of planktonic spores, however, are poorly understood.

To date, relatively little is known about the length of time kelp spores can swim and whether or not their ability to settle depends on motility. Kain (1964) reported that only relatively few spores of Laminaria

hyperborea (Gunn.) Foslie could swim longer than 20 h; however, there was no mention of the ability of spores to attach after they stopped swimming. Hoff- mann and Camus (1989) found that spores of Lessonia nigrescens Bory were still able to germinate after 4 d in suspension. Yet, as in the previous study, their experiments were done in small containers at spore densities much greater than those found in nature, and high spore densities can inhibit spore swimming (cf. Amsler and Neushul 1990).

In the present study, we used laboratory experiments to examine three questions pertaining to swimming and competency in spores of the kelps Macrocystis pyrifera and Pterygophora californica, two species for which widespread dispersal over at least several kilometres has been observed (Davis et al. 1982, Ebeling et al. 1985, Reed et al. 1988, Ambrose et al., in press): (1) How long can spores swim? (2) How is swimming duration influenced by spore photosynthesis? and (3) Is a spore still able to germinate and attach after it stops swimming? Our experiments were designed to closely mimic the natural environment of a planktonic spore and to test the hypothesis that spore photosynthesis extends dispersal by prolonging the competency of spores in the plankton.

MATERIALS AND METHODS

Spores were obtained from fertile sporophylls taken from Macrocystis in May and June 1990 and Ptery- gophora in February and March 1990 near Goleta Point or at Naples Reef in Santa Barbara County, California, USA (34025' N, 119057' W), using the methods de- scribed by Amsler and Neushul (1989) and Reed et al. (1991). A different batch of spores was used for each replicate of each treatment for both species. In each case, newly released spores were diluted to a density of 200 spores/mL in a large translucent tank containing 190 L of filtered seawater. This density was high enough for spores to be observed but low enough that spore motility was unaffected by contact with other spores (only 2 x 10-6% of the volume of the tank was occupied by-spores).

Swimming duration and attachment ability were ex- amined using three different photoperiod regimes: 14 h light followed by 10 h dark (14:10), 10 h light followed by 14 h dark (10: 14), and constant dark (00:24). The 14: 10 and 10: 14 daylengths approximate the sea- sonal extremes in Santa Barbara. Photosynthetically active photon flux density during lighted periods ranged from 85 to 140 klmol m2 s- ', which is photosynthetically saturating but not photoinhibiting for spores of both Macrocvstis and Pterygophora (Amsler and Neu- shul 1991). Thus, experiments were done over a range of quantum doses that encompassed the minimum and maximum photosynthetic potential of the spores in nature.

For each replicate trial of species and daylength, the percentage of spores swimming and the density of spores

October 1992 SPORE SWIMMING AND COMPETENCY IN KELPS 1579

remaining in suspension were determined from water samples withdrawn from the tank at 12- or 24-h in- tervals up to 144 h. Samples were fixed immediately in 5% formalin, and a known volume was concentrated onto a 0.4 Am Nucleopore filter and transferred to a glass microscope slide using the filter-transfer-freeze technique (Hewes and Holm-Hansen 1983). The density of spores that remained in suspension was estimated by counting the number of preserved spores in 15 0.048 mm- or 0.028 mm2 regularly arranged fields using a light microscope. To estimate the percentage of spores that had remained swimming at the end of each sample period, we recorded the shape of first 50 spores encountered in a haphazardly oriented transect on each slide. Spores of Macrocystis and Pterygophora change from pear shaped to spherical as they lose or withdraw their flagella when they stop swimming. Therefore, transferred spores were counted as swimming if they appeared pear shaped. Because the percentage of spores that were initially swimming at the time of release varied slightly among different batches of spores, the percent of spores swimming at the end of a sample period was expressed as a percentage of the initial value.

Two replicate pairs of horizontal and vertical slides were suspended along the sides of the culture tank and were used to examine how the attachment ability of spores varied over time. Slides were suspended for 24 h, beginning at 0, 72, 96, and 120 h after spore release (only at 0 h in the 00:24 treatment) after which they were removed and fixed in 5% formalin seawater. Any loose or weakly attached spores or germlings were removed by a stream of water from a squirt-bottle. At- tachment was estimated from the density of settled spores (or germlings) determined from five 0.74 x 22 mm transects regularly spaced across the width of each slide. Settlement densities were standardized to the initial density of spores in suspension (densities are reported as the number of settled spores or germlings per square centimetre per 100 spores per millilitre initially in suspension).

The effects of daylength and species on the time it took for all spores of Macrocystis and Pterygophora to stop swimming or on the percent still swimming at different times after spore release were determined in two-way ANOVAs with daylength and species as fixed factors; in these analyses, the response variable "pro- portion swimming" was transformed to arcsin x to meet the assumption of homoscedasticity (Zar 1974).

The effects of species, daylength, spore batch, time after release, and substrate orientation on the ability of spores to attach were determined in partially nested ANOVAs (see Winer 1971 for example), with species, daylength, time after release, and substrate orientation as fixed factors, and settlement density as the response variable. Three replicate trials, each using a unique batch of spores, were done for each combination of species and daylength. Each trial included all combi-

nations of time after release and substrate orientation. Thus, batch was considered a random factor and was nested within species and daylength. Since settlement in the dark treatment (00:24) was assessed only after 24 h, two separate nested ANOVAs were done: one (with species, daylength, batch, and orientation factors) for settlement only at 24 h after spore release and using all three levels of daylength (14:10, 10:14, 00:24) and the other (adding "time after release" to the other four factors) for settlement at different times after spores were released using only the two daylength levels that had lighted periods (14:10, 10:14). In both ANOVAs, settlement was transformed to log (x + 0.1) to meet the assumption of homoscedasticity. Differences among means within fixed factors were assessed using Ryan- Einot-Gabriel-Welsch multiple-range test (SAS 1985).

RESULTS

The duration of spore swimming was affected significantly by daylength (F2 2 = 18.38, P = .0002), which reflects the total quantum dose received by the spores. In constant dark (00:24), the rate at which spores stopped swimming increased sharply at 48 h, and spores were never observed swimming after 60 h (Fig. 1). In contrast, swimming in the two treatments with lighted periods (14:10, 10:14) declined steadily over time, and swimming spores were observed up to 120 h after release (P < .05. Ryan-Einot-Gabriel-Welsch multiple- range test). Swimming duration did not differ between the two species (Fig. 1; F.2 = 0.26, P = .62), nor was there any species x daylength interaction (F2 12 0.26, P = .77).

Although neither species nor daylength affected the percent of spores that remained swimming for the first 36 h after spore release (Fig. 1; in all cases P - .10), daylength had a marginal effect on spore swimming at 48 h, when only 7% of the spores placed in constant dark remained swimming, compared to 13-1 9% in treatments with light periods (F2 12 = 3.9 1, P = .049). Such differences among daylength treatments increased over time as the percent of swimming spores declined (Fig. 1).

Spores did not necessarily die after they stopped swimming, as most germinated in suspension and be- gan to grow. Germination was not light dependent; spores showed similar patterns of germination in constant dark and lighted daylength treatments. Newly developing germination tubes were apparent in 60- 70% of nonmotile spores of Macrocystis and Ptery- gophora just 12 h after release (Fig. 2a, b), and in 90- 95% of the spores at 120 h (Fig. 2c, d). When placed in culture, planktonic germlings of Macrocystis and Pterygophora that settled on slides during the 120-144 h sample period (see following for explanation of the attachment of germlings) became fertile and produced sporophytes within 2 wk, indicating that planktonic germlings are competent propagules capable of pro- ducing viable recruits.


100 Ol~~~~____0 4:1 0, L: D

Pterygophora Al 0:14, L:D M

.---- Macrocystis E00:24, L:D

10

0 -

, I , I I , . ,

I

0 24 48 72 96 120 144

TIME AFTER RELEASE (h) FIG. 1. The percentage of Macrocystis and Pterygophora spores swimming as a function of time after spore release for

three different levels of daylength. Data are means ? 1 SE. n = 3 replicate trials using different batches of spores. Note logarithmic vertical scale.

Substrate orientation had a dramatic effect on the ability of spores to attach during the first 24 h (Table 1). Settlement densities on the paired slides placed hor- izontally were much higher than those on vertical slides (Fig. 3). This pattern suggests that spores may prefer to settle on horizontal surfaces, since most spores were still motile during this time period and not sinking passively (Fig. 1). In contrast to spore germination, spore settlement was affected by light (Table 1); the overall density of settled spores during the first 24 h was significantly lower in constant dark (00:24) than in the daylength treatment with the longest light period

(Fig. 3). The two species had similar settlement patterns except that Pterygophora showed proportionally greater preference for settlement on horizontal slides than did Macrocystis (Fig. 3, see species x orientation interaction in Table 1). Settlement also varied among individuals from different batches of spores (Table 1).

Greater settlement on horizontal slides was consis- tently observed for both species over time following spore release. The species-specific difference in settlement rate varied with time after release (see species x time interaction in Table 2). Settlement density of Macrocystis was significantly higher during the first 24

a g p i ms ; G-'<'5 9 9

o ~~~~~~~~~~~~~~~g t ns gs

es

Ms

gs ~es

FIG. 2. The morphology of planktonic germlings (camera lucida drawings). (a) Macrocystis 12 h, (b) Pterygophora 12 h, (c) Macrocystis 120 h, (d) Pterygophora 120 h. ms = motile spore, ns = non-motile spore, gs = germinated spore, es = empty spore cell, gt = germ tube, gp = gametophyte. Scale bars = 10 Atm.


500 - C~j E U Macrocystis

D Pterygophora 400-

0 CL)

300-

200 -

wI 100

-LJ

V HV HV H

00:24 10:14 14:10

DAYLENGTH (h light h dark)

FIG. 3. The effects of daylength and substrate orientation (V = vertical, H = horizontal) on spore settlement density in .lacroclystis and Ptervgophora during the first 24 h after spore release.

h after release (when most spores were still swimming) than during periods beginning at -72 h when the vast majority of spores had stopped swimming, regardless of substrate orientation (Fig. 4a, b; P < .05 for both horizontal and vertical, Ryan-Einot-Gabriel-Welsch multiple-range test). In contrast, settlement density of Ptcrt'gophora on horizontal slides increased markedly after 24 h in later sampling periods (Fig. 4a; P < .05 Ryan-Einot-Gabriel-Welsch multiple-range test). The effect of time after release on settlement also varied with substrate orientation (see time x orientation interaction in Table 2); in contrast to horizontal slides, the settlement density of Pterl'gophora on vertically positioned slides was relatively constant over time (Fig. 4b). There was a marginal effect of spore batch on settlement density but no effect of daylength (i.e., set-

TABLE 1. The effects of species (Macroc vistis, Pterygophora), daylength (14:10. 10:14, 00:24), replicate trial using a unique batch of spores (=batch), and substrate orientation (=orien; vertical, horizontal) on settlement density [log(density + 0. 1)] for the first 24 h after spore release. Batch(Species x Daylength) indicates Batch was nested within the Species x Daylength interaction.

Source of variation df MS F P

Species 1 0.7978 2.57 .1352 Daylength 2 1.5307 4.92 .0275 Batch(Species

x Daylength) 12 0.3109 2.40 .0092 Orien 1 12.0593 93.21 .0001 Species x Daylength 2 0.0682 0.22 .8062 Species x Orien 1 1.0043 7.55 .0157 Daylength x Orien 2 0.1338 1.01 .3907 Orien x Batch(Species

x Daylength) 14 0.1330 1.03 .4327 Residual 95 0.1294

element was similar in the 10:14 and 14:10 daylength treatments) (Table 2).

DISCUSSION

The distance over which viable propagules are dispersed depends on how long they remain competent to settle while in the plankton (Dana 1975, Hoffmann 1987, Richmond 1987, Keough 1989). Characteristics of algal spores that increase this period, therefore, should increase their potential as effective dispersal agents. One such characteristic is the ability of spores to pho- tosynthesize and contribute to their own energy needs. Contrary to previous belief (Santelices 1990) the spores of several species of kelps including Macrocystis and Ptervgophora have recently been shown to maintain photosynthetic rates that can compensate for respira- tion during swimming (Amsler and Neushul 1991). Our results are consistent with this finding and also indicate that spores of Macrocystis and Ptervgophora swim longer in the light than in the dark (Fig. 1).

The daylength treatments used in this study repre- sented conditions of maximum and minimum photosynthetic potential for Macrocvstis and Ptervgophora spores. Daylength effects on spore swimming, however, were not noticeable until 48 h after release when, even under the most optimal light conditions, the percent- ages of MacrocYstis and Ptervgophora spores still swimming were only 13 and 19%, respectively (Fig. 1). Thus, the extent to which the swimming duration of spores in nature is effectively influenced by variation in light is questionable. Nonetheless, the importance of ade- quate light levels should not be underestimated in de- termining the success of a spore as a viable propagule. The carbon content of Macrocvstis and PterYgophora spores has been shown to increase z30% during 12 h


900 a. Horizontal

800

700 cli E

0 a) 600

500

Pterygophora _ 400

z 1{ Macrocystis w a300 |----

Z A W 200

w I 100

W/ * ------A------- 0 ~ ~ ~~~~~~~~I I

0-24 72-96 96-120 120-144

100 H ices b. Vertical

0 - - - - -4 --- - - - - - 0-24 72-96 96-120 120-144

TIME AFTER RELEASE (h)

FIG. 4. The effects of substrate orientation, (a) horizontal or (b) vertical, on spore settlement density in Macrocystis and Pterygophora as a function of time after spore release. Means + I SE are shown.

of photosynthetically saturating irradiance (Amsler and Neushul 1991), while neutral lipid reserves of recently settled Macrocystis spores were depleted more rapidly in the dark than at near saturating irradiance (M. A. Brzezinski et al., unpublished manuscript). Since competition among newly settled spores of these kelps can be intense (Reed 1990, Reed et al. 1991), any advantage to early growth and development of a recently germinated spore may enhance its chances for eventual recruitment. Therefore, increased irradiance is un- doubtedly beneficial because spores are able to fuel their own energy requirements via photosynthesis, thereby conserving reserves of maternal carbon for subsequent growth and development.

The beneficial effects of autotrophic nutrition to planktonic viability may not be limited to algal spores. Planula larvae from a wide diversity of cnidarians contain endosymbiotic dinoflagellates (=zooxanthellae) (Trench 1987), and recent information suggests that autotrophic nutrition derived from zooxanthellae in- creases the duration of larval competency (Richmond 1987). Morse and Morse 1991) found that larvae of the scleractinian coral Agaricia humilis (a species whose larvae contain zooxanthellae) remained competent and retained their ability to respond to a specific exogenous settlement cue after 30 d when maintained under dim light in the absence of food. Competency was extended to 60 d in subsequent experiments but was greatly re-

duced in similar experiments when larvae were placed in the dark (D. Morse, personal communication). Auto- trophic endosymbionts contribute substantially to larval nutrition, and in general, species whose planulae contain zooxanthellae remain competent longer (and thus disperse farther) than those species whose planulae lack zooxanthellae (Richmond 1989, Richmond and Hunter 1990).

Perhaps more important than the contribution of spore photosynthesis to the capacity of kelps to disperse, is the likelihood that spores do not die once they stop swimming but instead germinate in the water column and continue to grow. A similar phenomenon was observed in the spores of Laminaria hyperborea (Kain 1964). Thus the competent planktonic stage in these kelps is not necessarily confined to a motile spore, but may be extended to other microscopic stages as well. Extended dispersal of this kind has been suggested as the mechanism by which kelp colonizes offshore gas platforms in the North Sea (Moss et al. 1981). Such prolonged competency in the plankton may not be common to all kelps, however. Hoffmann and Camus ( 1989) made no mention of spores of the kelp Lessonia nigrescens germinating in suspension when maintained in small dishes; they found that germination declined by 70% (relative to newly released spores) after spores had been in suspension for 5 d.

The value of dispersal is not only in the distance of transport but also in the quality of the microsite in which the propagule is deposited (Fenner 1985). There- in lies the value of spore motility. Although spore motility probably has little effect on the distance over which kelp spores are dispersed (Suto 1950, Reed et al. 1988), it may greatly enhance the spore's ability to find a high-quality microsite on which to settle. Swim-

TABLE 2. The effects of species (Macrocystis, Pterygophora), daylength (14:10, 10:14), replicate trial using a unique batch of spores (=batch), time after release (0-24, 72-96, 96-120, 120-144 h), and substrate orientation (=orien; vertical, horizontal) on settlement density [log(density + 0.1)]. Batch(Species x Daylength) indicates Batch was nested within the Species x Daylength interaction.

Source of variation df MS F P

Species 1 83.8566 219.90 .0001 Daylength 2 0.0070 0.02 .8951 Batch(Species

x Daylength) 8 0.3831 1.93 .0553 Time 3 9.8664 49.77 .0001 Orien 1 121.7608 93.21 .0001 Species x Daylength 2 0.0173 0.05 .8369 Species x Time 3 12.4644 42.97 .0001 Species x Orien 1 0.0057 0.02 .8944 Daylength x Time 3 0.5705 1.97 .1447 Daylength x Orien 2 0.0017 0.01 .9417 Time x Orien 3 5.0837 25.65 .0001 Time x Batch(Species

x Daylength) 25 0.2901 1.46 .0755 Orien x Batch(Species

x Daylength) 9 0.3057 1.54 .1330 Residual 95 0.1982


ming spores of Macrocystis and Pterygophora exhibit chemotaxis towards nutrients that not only stimulate settlement but also promote growth and development following germination (Amsler and Neushul 1989, 1990). Hence, factors that prolong the swimming stage of spore development may increase the chances of successful settlement and recruitment, because a motile spore is better able to select a favorable microsite than is a nonmotile, planktonic germling.

The ability of microscopic life history stages of kelp to attach or stick to a substrate, once encountered, is essential to settlement and eventual sporophyte recruitment. We observed distinct differences in the abil- ities of Macrocystis and Pterygophora to attach to glass slides after having germinated (Fig. 4). Although a decrease in the settlement rate of Macrocystis propagules onto vertically placed slides over time is expected (since passively sinking germlings are less likely to contact and adhere to a vertical surface than are actively swimming spores), a concomitant decrease onto horizontal slides (Fig. 4a) indicates that the ability of the propagules to attach drastically declines after they have germinated. Similarly, Suto (1950) found that the attachment ability of the spores of several species of algae declined over time. In contrast, settlement densities of Pterygophora significantly increased on horizontal slides (Fig. 4a) and remained constant on vertical slides (Fig. 4b) during periods after the vast majority of spores had germinated. This indicates that compared to those of Macrocystis, Pterygophora germlings remain relatively "sticky" to the extent that they readily attach even after germinating in the plankton. The increase in settlement on horizontal slides by nonswimming Pterygophora germlings is probably due to necessity, not design. Like motile spores of other macroalgae, actively swimming kelp spores can "choose" whether or not to settle and can terminate the settlement process after contacting a surface (Amsler and Neushul 1990). In contrast, a nonmotile germling has no "choice"; it invariably at- taches to a surface upon contact, providing it is "sticky."

The relative "stickiness" of planktonic germlings may or may not be advantageous, depending on the circum- stances. The ability of a propagule of a sessile benthic organism such as kelp to quickly adhere to the bottom upon contact should facilitate the species' successful recruitment in a turbulent nearshore environment. Thus, the potential for "sticky" planktonic germlings of Pterygophora to settle after an extended period of dispersal may be much greater than for nonsticky germlings of Macrocystis, which can only weakly attach to substrates upon contact. On the other hand, a sticky propagule is more likely to adhere to objects in the water column along the way. This could alter its (1) sinking rate, (2) risk to predation, (3) ability to attach to the bottom, (4) exposure to light and nutrients, and thereby affect its chances for successful recruitment.

In conclusion, our laboratory results provide evidence that the spores and germlings of Macrocystis and

Pterygophora can remain competent in the plankton for extended periods of time. These data are consistent with our previous findings that dispersal of these kelps in the field can occur over distances much greater than previously thought (Ebeling et al. 1985, Reed et al. 1988). Although conditions that allow for such long- distance dispersal may occur episodically, they probably are not rare. Storms that generate enough turbu- lence to keep spores suspended in the water column for further transport by prevailing currents occur during most years. Propagule characteristics that prolong their competency and/or enhance their ability to adhere to a suitable surface once deposited interact to promote dispersal over longer distances (Keough 1989, Richmond 1989). This increased potential for dispersal, in turn, enables kelp populations to persist in highly disturbed habitats because it provides a means by which local populations can become re-established following local extinction. This would tend to allow the geographic range of the species to be maintained, and its genetic diversity (and consequently its pheno- typic adaptability to future disturbances) to be con- served.

AcKNOWLEDGMENTS

We thank M. Bertness, M. Carr, J. Connell, C. Gotshalk, T. Farrell, M. Ilan, A. Morse, D. Morse, M. Neushul, P. Raimondi, and R. Trench for their insightful comments and ideas and C. Ebeling for assistance in the laboratory. This material is based on support by the National Science Foun- dation under grant number OCE88-3393 1.

LITERATURE CITED

Ambrose, R. F., J. M. Engle, J. A. Coyer, and B. V. Nelson. In press. Changes in urchin and kelp densities at Anacapa Island, California. In F. G. Hochberg, editor. Recent ad- vances in California islands research. Proceedings of the Third California Islands Symposium. Santa Barbara Mu- seum of Natural History, Santa Barbara, California, USA.

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