ELSEVIER Journal of Experimental Marine Biology and Ecology

191 (1995) 83-99

JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY

Sea urchin cavitation of giant kelp (Macrocystis pyrifera C. Agardh) holdfasts and its effects on kelp mortality

across a large California forest

M.J. Tegner*, P.K. Dayton, P.B. Edwards, K.L. Riser

Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093-0201, USA

Received 20 September 1994; revision received 21 February 1995; accepted 15 March 1995

Abstract

Sea urchins, Strongylocentrotus franciscanus (A. Agassiz) and especially S. purpuratus (Stimpson) sheltering in holdfasts of giant kelp, Macrocystis pyrifera, feed on haptera, eventually creating cavitation damage that leads to structural failure of the holdfast when the plants are stressed by large waves. Periodically giant kelp plants on permanent transects in a large Southern California forest were categorized for their degree of urchin infestation and cavitation damage, and subsequent survival followed for 5 yr. Plants with a high degree of urchin damage had significantly higher rates of mortality than plants with little damage during several assessment periods. There was a decreasing gradient in the degree of urchin damage and importance of cavitation from the deep (18 m), outer edge of the Point Loma forest, through the center (15 m), to the inner (12 m) edge of the forest which paralleled urchin abundance and recruitment rates. This gradient acts to reduce the impact of the gradient of giant kelp mortality caused by storms, which is much greater in shallow water and decreases seaward.

Keywords: Herbivory; Holdfast; Kelp; Macrocystis; Sea urchin

1. Introduction

Well known for their grazing impacts, sea urchins play an important ecological role in benthic macrophyte communities generally and in temperate zone kelp forests in particular (reviewed by Lawrence, 1975; Harrold & Pearse, 1987). In forests of giant kelp (Macrocystis pyrifera), benthic herbivores including echinoids

* Corresponding author.

0022-0981/95/$09.50 0 1995 Elsevier Science B.V. All rights reserved

SSDI 0022-0981(95)00053-4

84 M.J. Tegner et al. I J. Exp. Mar. Biol. Ecol. 191 (199.5) 83-99

are normally sustained by drift kelp, fragments carried along the bottom by currents and surge. When drift becomes limiting, sea urchins may aggregate and attack attached plants (Dean et al., 1984; Ebeling et al., 1985; Harrold & Reed, 1985; Tegner & Dayton, 1991; Dayton et al., 1992). The best known and most destructive grazing, termed “frontal attack”, by Leighton (1971), occurs when grazing is concentrated on structures at the apex of the giant kelp holdfast: sporophylls, primary stipe, and base of the secondary stipes. Stipe damage leads to breakage and the release of most of the plant biomass. Because of the buoyancy provided by the pneumatocysts, most of this biomass is lost to the local benthic community. When sea urchins are abundant, such grazing can lead to large areas of barren grounds (reviewed by Lawrence, 1975; Harrold & Pearse, 1987). A less obvious mode of sea urchin grazing is “cavitation” (Leighton, 1971). Urchins sheltering in the holdfast feed on hapteral tissue, eventually excavating enough of the holdfast to lead to structural failure when the plants are stressed by storm waves. In contrast with frontal attack on the holdfast apex or primary stipe, entire plants including a large proportion of the holdfast are frequently dislodged by large swells as a result of cavitation. Unlike other forms of mortality, the role of cavitation in Mucrocystis population dynamics has not previously been docu- mented.

Macrocystis plants can live to 7 yr in Southern California (Rosenthal et al., 1974) although a more realistic life expectancy is 4-5 yr (Dayton et al., 1984, 1992). The main sources of giant kelp mortality in the Point Loma kelp forest near San Diego include storm-dislodgement followed by entanglement of attached Mucrocystis, and, in some cases, frontal-attack grazing by sea urchins (Dayton et al., 1984). Young plants (less than 2 yr old) with small holdfasts are weakly attached and more easily ripped off the substratum (Norton et al., 1982). In the Point Loma kelp forest, 2- and 3-yr-old Mucrocystis survive better than do other ages (Dayton et al., 1984). The attachment of older plants gradually deteriorates as the center of the holdfast dies due to sedimentation and shading (Ghelardi, 1971); this plus their greater biomass (and thus increased drag) makes older plants more susceptible to storm waves.

The Point Loma kelp forest is large enough to encompass gradients in important factors such as depth, light, nutrients, wave energy, currents, planktonic propagule supply, and epifauna. To understand the role of these gradients on the population dynamics of kelps and benthic macroinvertebrates, especially sea urchins, long term study sites were established in various areas of the kelp forest (Dayton et al., 1984, 1992). An important example of such a gradient is storm mortality of giant kelp which increases with decreasing depth; in fact the inner edge of the Macrocysfis forest appears to be set by the height of breaking waves (Seymour et al., 1989). Recruitment and abundance of the the important echinoids, the commercially-harvested red [Strongylocentrotus franciscanus (A. Agassiz)] and the smaller purple [S. purpurutus (Stimpson)] sea urchin, are both significantly greater along the outer edge of the Point Loma forest (Tegner & Dayton, 1981, 1991). This gradient in urchin recruitment may play an important role in the life history of Mucrocystis in deeper water.

M.J. Tegner et al. I J. Exp. Mar. Biol. Ecoi. 191 (1995) 83-99 85

In this study we evaluate the effects of sea urchin cavitation on Macrocystis mortality patterns in terms of giant kelp and sea urchin demographics across the depth gradient of the Point Loma kelp forest. Holdfast dete~oratio~ is a major part of the normal aging process in these kelps; here we seek to determine the potential role of sea urchin cavitation in giant kelp age structure and how it varies spatially.

2. Materials and methods

The Point Loma kelp forest, generally about 8-10 km long by 1 km wide, is located on a broad, mudstone-sandstone terrace offshore of San Diego, CA (32” 42’ N; 117” I@ W). Permanent stations have been used for long-term population studies (Tegner & Dayton, 1981, 1991; Dayton et al. 1984, 1992). There are four parallel 25 m transects at 18, 15, and 12 m oriented perpendicular to shore in the center of the forest where kelps have been mapped quarterly since 1983. Sea urchins have been censused annually along the lines, and sea urchin recruitment rates assessed twice a year during this period. Additional observations are reported from experimental sites at 21,15, and 8 m, also in the center of the Point Loma forest; on average, the five sites are each about 250 m apart.

Kelps are mapped within 2 m to each side of each line, so that a total of 400 m2 is surveyed per site. All Macrocystis with at least four stipes are mapped and stipes counted. The maps are updated quarterly to evaluate recruitment, surviv- orship, and growth of individual plants. Maximum densities are not recorded because initial densities of newly recruited adults (defined as four or more stipes, Dayton et al., 1992) are often so dense that the sampling itself would cause mortalities from diver entanglement. Holdfast volume is calculated from in situ measurements of height and two basal diameters, assuming the shape to be an elliptical cone (Ghelardi, 1971).

To determine the effect of sea urchin damage to holdfasts on giant kelp survivorship, a rating system was devised (Table 1) and added to the quarterly mapping once or twice a year. In undamaged plants, the categories are based on

Table 1

Rating scheme for assessing the degree of sea urchin infestation/cavitation damage in Mucrocystis pyrifera holdfasts

Rating Description

0 No visible urchins, no damage 1 Less than four urchins, no damage 2 More than four urchins, no damage 3 Minor (<25%) cavitation. urchins present 4 Major (25-50%) cavitation, urchins present 5 More than half of the holdfast gone, urchins present

The number of urchins indicates how many animals could be observed by a diver using a light without disrupting the holdfast.

86 M.J. Tegner et al. I J. Exp. Mar. Biol. Ecol. 191 (19Y5) 8_7-99

the number of urchins visible to a diver using a light but not disrupting the holdfast in any way. Once cavitation damage occurs, the ratings are based on the degree of holdfast damage and the presence of urchins, as assessing the number of urchins in the interior of the holdfast is problematic. Generally, individual plants scored in the same or higher categories as they increased in age, but some scores decreased. To some degree this reflects the subjectivity of the categorization and variation among divers. Occasionally, however, mapped holdfasts were able to cover cavitation damage with new haptera during optimal conditions for growth; it is likely that urchins remained inside these holdfasts. In 1989-1990, ratings were conducted at 18 and 15 m only (no urchins were observed in holdfasts at 12 m) and, due to the high kelp densities, on a limited number of randomly selected plants per site. From 1991 through spring 1994, all plants on the permanent transects at all three depths were categorized for the degree of urchin infestation. G tests, functionally similar to chi-square tests (Sokal & Rohlf, 1969) were used to compare the numbers of live and dead plants in each category of holdfast damage with expected values calculated from the prior assessment. The null hypothesis for these tests is that the distribution of mortalities among categories of urchin damage is proportional to the number of plants in each category, i.e. that mortality is independent of prior urchin infestation. Because of the multiple testing problem for the 1991-1994 data set and the lack of independence among these serial comparison periods (i.e. the same plants may appear in all or some comparisons), probability values are distorted by some uncertain amount and given for reference purposes only.

Experimental clearings (20 X 20 m) were established at 21,15, and 8 m in winter 1989 for successional studies; all the plants in each clearing were of uniform age. Giant kelp plants were tagged for growth studies and rated for degree of urchin infestation beginning in December 1990 and quarterly thereafter.

Sea urchin recruitment was assessed from size-frequency distributions gener- ated twice yearly, during spring and fall. A 1 mz frame was haphazardly placed over aggregations of urchins away from the transects at each site; all rocks were overturned to search for urchins. We attempted to measure 100 individuals of each species. As purple urchins greatly outnumbered red urchins at 12 m, additional 1 m2 samples of only the latter species were searched to obtain an adequate sample size. Test diameter was measured to the nearest mm with vernier calipers. Urchins smaller than 10 mm were counted but are not quantitatively sampled by this method (Tegner & Dayton, 1981, 1991).

We define recruitment rate as that portion of the population of red urchins up to 35 mm and purple urchins to 25 mm test diameter at each site (Tegner & Dayton, 1991). Sea urchin density is highly variable among sites at Point Loma, in part due to differences in habitat structure where the size-frequency distributions are taken, although density has remained fairly constant within most sites during the last decade (see Results). Thus, it would be misleading to compare recruit- ment rates in terms of density in the size-frequency distributions among the sites. Similarly because of high variability in the habitats where the urchin aggregations are sampled, the results from the m* samples are pooled and one value of percent

M.J. Tegner et al. / J. Exp. Mar. Biol. Ecol. 191 (1995) 83-99 87

recruitment is calculated per sampling period per site. Kruskal-Wallis tests were conducted to determine whether there were significant differences in urchin recruitment among sites, and differences among sites were analyzed with Student- Newman-Keuls tests.

In addition to the sea urchin recruitment and size frequency estimates discussed above, urchin densities on the permanent transects were determined annually during spring. Urchins which could be seen with the use of a light but without disrupting animals or the substrate were counted in 10 quadrats (5 X 2 m) along the permanent lines. This procedure misses most small individuals.

3. Results

3.1. Macrocystis populations

Because Macrocystis mortality is strongly age specific (Dayton et al., 1984), it is important to consider the age structure of the study populations. The Point Loma kelp forest was subjected to a massive storm in January 1988 that caused almost complete mortality of MQc~ocy~t~~ (Seymour et al., 1989; Dayton et al., 1992); the few survivors were mostly in deeper water (Fig. 1). Subsequent optimal growth conditions led to large cohorts which dominated the study period of 1989 through spring 1994. At each site, these giant kelp plants fell into three or four different cohorts which recruited as adults over periods of 7 to 11 months. maximum density of adults was observed in winter 1989 at 15 m, summer 1989 at 18 m, and

1.2 1

1988 1989 1990 1991 1992 1993 1994 1995

Fig. 1. The density of adult (defined as four or more stipes, Dayton et al., 1992) Macrocystis pyrifera at

three sites in the center of the Point Loma kelp forest, 1988 through spring 1994.

88 M.J. Tegner et at. I J. Exp. Mar. Bid. Ecol. 191 (fW.5) SF99

fall 1989 at 12 m. The delay in the appearance of adults at 12 m was caused by a post-storm bloom of Desmarestiu Zigulata (Lightfoot) (Dayton et al., 1992). Thus, average plant age at each site was very similar for most of this period. As the 198911990 Mucrocystis cohorts declined in density, the first significant new recruitment was observed in 1994 at 12 and 15 m.

3.2. Holdfast damage and Macrocystis demography

During fall 1989, sea urchins and Macrocystis holdfast cavitation were conspicu- ous in older plants which had survived the 1988 storm, especially at 18 m. Generally plants with less than six stipes had no urchins, plants with six to 10 stipes typically had a few small purple urchins, and very large plants had cavitation damage, many (up to 65) purple urchins, and one or two red urchins. At 12 m where only three Macrocystis survived the 1988 storm and the degree of urchin infestation is generally lower, no urchins were detected in giant kelp holdfasts until 1992 (Fig. 2).

There were several storms and 10 days with maximum significant wave heights between 2 m and 3 m between 12/l/90 and 5/30/91. This provided the opportunity to test the role of sea urchin damage to holdfasts in giant kelp survivorship under non-severe winter wave conditions (see Seymour et al., 1989). The average category of urchin damage of Macrocystis holdfasts in fall 1990 was more than four times higher at 18 m than 15 m. G test comparisons of the numbers of live and dead plants by categories of damage in July 1991 indicated that mortality was not independent of the prior degree of urchin infestation at 18 m (Table 2). The average prior rating of urchin infestation of the dead plants at 18 m was two categories higher than the average prior rating of the survivors. At 15 m, the average prior rating of mortalities was again higher than that of survivors and the total mortality was higher, but the G statistic was not significant, suggesting a reduced influence of urchin cavitation. At 12 m, where there was no evidence of urchin infestation of holdfasts in either 1990 or 1991 and few 1988 storm survivors, 26% of the 110 plants mapped the previous fall died during this period; this is comparable to other mild winters (see Seymour et al., 1989).

We also compared the mortality of Macrocystis in the experimental clearings at 21,15, and 8 m over the winter of 1991 (Table 2). In contrast with the mixed age stands on the permanent transects, the plants in the clearings were of uniform age: 26, 27, and 28 months in December 1990 at 21, 15, and 8 m, respectively. Again, the degree of urchin damage in the holdfasts decreased with decreasing depth, and the average prior urchin ratings of surviving kelps were lower than those of mortalities. There were a few urchins observed in holdfasts at 8 m, however. The distribution of live plants among urchin categories in July 1991 was not in- dependent of the fall 1990 degree of urchin infestation at 15 m.

Standing stocks of Macrocystis plants on the permanent transects by category of sea urchin damage and subsequent mortalities by category for the period of summer 1991 through spring 1994 are shown in Fig. 2. The differences among sites are readily apparent and there is a strong gradation in the degree of urchin

M.J. Tegner et ai. I 1. Exp. Mar. Biol. Ecol. 191 (1995) 83-99 89

Fig. 2. (A) Standing stocks of Macrocysris pyrifera by category of sea urchin infestation for 18, 15, and 12 m, 1991-1994. (B) Mortality of Macrocystis within each category of urchin infestation/damage

assessed subsequent to the observations in (A).

90 M.J. Tegner et al. I .I. Exp. Mar. Bid. Ed. 191 (199.5) 83-99

Table 2 Impact of the winter 1991 storms on Mucrocystis pyrifera categorized hy degree of sea urchin

infestation in fall 1990 and after reevaluation in July 1991

Site

(m)

Total

mortality

(%)

Average

rating, Fall

1990

Average

rating of

survivors,

July 1991

Average

rating of

mortalities

G test result:

probability

(A) Permanent sites (N = 67 at 18 m and 24 at 15 m)

18 19 1 .I3 1.32 3.46 0.005 i < 0.001 p 1.5 29 0.38 0.06 1.14 0.1 <p<o.25

(B) Experimental clearings at 21, 15, and 8 m (30 tagged plants per site)

21 26 2.6 2.3 3.8 0.25 < < 0.5 p 15 25 1.5 2.3 3.8 0.025 < < 0.05 p

8 67 1.0 0 0.3 0.75 < < 0.90 p

G tests compared the numbers of live and dead plants in each category in 1991 to test the hypothesis

that mortality is independent of the prior degree of urchin infestation.

damage from deep to shallow water. The 18 m site consistently has the lowest proportion of plants in category zero (no sea urchins or damage visible), and the highest proportion of plants in the full range of higher categories. Relative to 18 and 12 m, the 15 m site is intermediate in terms of the proportion of plants in category zero and in higher categories, although the latter increase with time. At 12 m, all of the plants are in the zero category for the first two assessments, and the majority remain without evidence of urchin damage to holdfasts throughout this period. Comparing category frequency distributions of live plants with the mortality within each rating group, it is apparent that most of the mortalities at 18 and 15 m are in higher category plants. The 12 m site has the highest proportion of mortalities in the zero category, although the few plants that did become infested with urchins suffered substantial losses.

TO test the hypothesis that mortality is independent of prior urchin infestation/ damage, G tests were used to examine the numbers of live and dead plants according to their degree of urchin infestation during the previous assessment. The results (Table 3) illustrate large differences among the three sites. The consistently high values of the G statistic at 15 and especially 18 m suggest that mortality is disproportionately higher among plants previously associated with higher categories of urchin damage. In contrast, all but the last G value at 12 m were very low, indicating that mortalities were evenly distributed, regardless of prior urchin densities. The higher G value for the last period does, however, suggest some urchin-mediated mortality and raises the question of what would happen to this population over a longer time period. As is clear from Fig. 1, however, 12 m was again dominated by newly recruited Mucrocystis in May 1994; there were only nine plants (representing 8% of the total number of adults present) from the 1989/1990 cohorts remaining.

Plants tracked from the initial categorization in fall 1989 through spring 1994 illustrate survivorship as a function of original urchin rating (Fig. 3). Of the 106

M.J. Tegner et al. I J. Exp. Mar. Biol. Ecol. 191 (1995) 83-99 91

Table 3

Comparison of the sea urchin damage category-frequency of live and dead Macrocystis pyrifera at 18,

15, and 12 m from July 1991 through May/June 1994 (see Fig. 2)

Period G value Probability

(A) 18 m

l/92 vs. 7191 12.48 0.025 < 0.05 <p 8/92 vs. l/92 9.42 0.05 < 0.10 <p 6193 vs. 8192 11.28 0.025 < < 0.05 p 10193 vs. 6193 10.66 0.05 < 0.10 <p 5194 vs. 10193 14.18 0.01 < 0.025 <p

(B) 15 m

l/92 vs. 7191 10.74 0.05 < 0.10 <p 8192 vs. l/92 12.26 0.025 <p < 0.05

6193 vs. 8192 23.38 p < 0.001

10193 vs. 6193 7.38 0.10<p<0.25

5194 vs. 10193 4.22 0.50 <p < 0.75

(C) 12 m

l/92 vs. 7191 *

8192 vs. 1192 *

6193 vs. 8192 1.04 0.95 <p i 0.975

10193 vs. 6193 0.22 0.995 <p < 0.999

5194 vs. 10193 8.84 0.10 <p <c 0.25

G tests compare the numbers of live and dead plants in each category to test the hypothesis that

mortality is independent of the degree of prior urchin infestation. Because of the multiple testing

problem and lack of independence among comparison periods, probability values are given for

reference purposes only.

* For these dates, all plants, both live and dead, were in category 0.

Mucrocystis originally rated at 18 m, those in high damage categories four and five died within l-2.5 yr, while categories zero, one, two, and three have declined at fairly gradual and similar rates with approximately lo-30% of the plants still alive in April 1994. At 15 m, only the plants originally rated as zeros remained alive in spring 1994; the category four and five plants died during the first year, and categories one and three were intermediate (there were no category two plants in 1989 at this site).

Finally, we return to the relationship between sea urchin infestation and Macrocystis aging; is the degree of urchin damage simply a function of holdfast volume and thus age? Comparisons of holdfast volume with the number of visible urchins in fall 1989, when there was a mixture of pre- and post-storm kelp cohorts, suggested a linear relationship between number of urchins and holdfast volume, and that the relationship was stronger at 18 m (data not shown). However, that relationship between number of urchins and holdfast volume did not continue. We compared the categories of the 1989/90 cohorts in August 1992 and May 1994, and found no differences in ages among the full range of categories at all three permanent transect depths (data not shown). The clearing experiments, where holdfast volume and rating were assessed quarterly on plants of uniform age, also suggest a lack of dependence of urchin damage category on holdfast volume (Fig.

M.J. Tegner et al. I .I. Exp. Mar. Biol. Ecol. 191 (1995) 8.3-99

n A. 18m Central

-0 67

100 -1 15

-2 6

x 80 -3 3

.E -4 4

2 2 60

t; 40

z

z 20 a

0 r

1989 1990 1991 1992 1993 1994

”

B. 15m Central -0 49

100 -1 13

-3 3

5 80 -4 2

.? -5 2

2

cz

60

0 r

1999 1990 1991 1992 1993 1994

Fig. 3. Survivorship of Macrocystis pyrifera plants through time as a function of category of urchin

infestation/damage in fall 1989 at 18 and 15 m.

4). Holdfast volume increased gradually with age of the plants in the 16 months from June 1990 through October 1991. Over the same time period, the urchin rating stayed fairly constant at 21 m, increased slightly at 15 m, and decreased to zero at 8 m. Decreases in average rating could be caused by either the loss of high rated individuals or increases in holdfast growth. At any rate, while larger holdfasts obviously have more space for, and have had more time to accumulate sea urchins, the degree of urchin damage is not a simple function of plant age.

3.3. Sea urchin demographics

The importance of sea urchin cavitation as a source of Macrocystis mortality appears to be related to variation in recruitment and abundance patterns of these grazers across the kelp forest. In a previous study of the microhabitats of juvenile (here defined as s 20 mm test diameter) sea urchins at Point Loma, about 7% of small red urchins and 20% of juvenile purple urchins were found in Macrocysfis

M.J. Tegner et al. i J. Exp. Mar. Biol. Ecol. 191 (1995) 83-99 93

A. 21m Clearing

30 a t

25 : 2.5

20 2.0

15 1.5

- ~asl~~~ 10 --+- Rating 1.0

0-j 1 . . , . . . . , . . . . .

24 30 36 42

6. 15m Clearing = - 30 3.0

$ 26 2.5

3 2o 2.0

15 1.5

';i (II 10 1.0

% 5;

z! ~.....,.....,.....,

0.5

0 0.0

24 30 36 42

C. 8m CIearing

303

24 30 36 42 Age MW

Fig. 4. Average holdfast volume and cavitation rating of Macrocystis pyrifera in the experimental clearings at 21, 15, and 8 m from June 1990 through October 1991.

holdfasts (Tegner & Dayton, 1977). These data and the occasional appearance of a number of small urchins within a narrow size range in holdfasts suggests that they may be sea urchin recruitment sites, especially important for purple urchins, and thus particularly germane to the issue of Mucr~cystis cavitation. From 1983 through 1987, recruitment rates of both urchin species were significantly higher along the outside edge of the Point Loma kelp forest and there was consistently less recruitment within the bed (Tegner & Dayton, 1991). When the 1983 through spring 1994 data set (Fig. 5) was tested, recruitment rates again varied highly

94 M.J. Tegner et al. I J. Exp. Mar. Bid. Ed. 191 (199-T) X3-99

A. Stronqylocentrotus purouratus

80 V lI3m Central 70 - 15m Central 60 --+-- 12m Central

50

40

30

20

10

0

1983198419851986198719881989199019911992199319941995

B. Stronavlocentrotus franciscanus

100

90

80 - lfrr Cenlral

70 - 15m Central

60 An - 12m Central

50

40

30

20

10

0

1983198419851986198719881989199019911992199319941995

Fig. 5. Recruitment of Strongylocentrotus franciscanus and S. purpuratus at 1X, 15, and 12 m in the

center of the Point Loma kelp forest, 1983 through 1994. See Materials and methods for details.

significantly among sites (p = 0.006 for purple urchins, p < 0.001 for red urchins). Student-Newman-Keuls tests indicated which sites had significantly different recruitment rates (Table 4). For red urchins, there was a decrease in recruitment rate with decreasing depth, and all three sites were significantly different from one another. The same trend was observed for purple urchins, although recruitment

Table 4

Mean percent recruitment of Strongylocentrotus franciscanus and S. purpuratus from 1983-1994 at

sites in rank order

S. franciscanus: 18m

20.13

15 m 12 m 9.05 3.24

S. purpuratus: 18m

13.56

15 m 12m

8.38 4.39

Lines connect values which are not significantly different.

M.J. Tegner et al. i J. Exp. Mar. Bid. Ed. 191 (19!25) 83-99 95

rates at 15 and 12 m were not significantly different. In smaller kelp forests without this strong gradient of urchin recruitment rates, gradients in cavitation- induced mortality of giant kelp are likely to be reduced or absent.

In addition to variation across the depth gradient at Point Loma, sea urchin recruitment exhibited considerable interannual variability (Fig. 5). At both 18 and 15 m there were peaks in recruitment of both red and purple urchins, in 1986 at 18 m and in 1988 at 15 m.

Sea urchin densities along the permanent transects from 1983-1994 are shown in Fig. 6. Densities of the intensively-exploited red urchins (e.g. Tegner, 1989; Tegner and Dayton, 1991) are about an order of magnitude lower overall than purple urchin densities, and very low at 15 and 12 m. Purple urchin densities show a consistent pattern with highest abundance at 18 m, intermediate numbers at 15 m, and fewest individuals at 12 m, which is probably related to recruitment rates. Both species showed an increase in numbers at all depths in 1991 which has since declined.

A. Stronavlocentrotus Durmratus

v 1 Bm Central Et- - 15m Central

- 12mCentral

6-

1@8319841985198619871@6Q198919@01991199219931@@41995

B.

1.0 -

Stronavlocentrotus franciscanus

- 18rn Cenlral

---t 15m Central

0.0t

198319841985198619671@66198919901@@119921@@31@941995

Fig. 6. Density of Strongylocentrotus franciscanus and S. purpuratus at 18, 15, and 12 m in the center of

the Point Loma kelp forest, 1983 through 1994. See Materials and methods for details.

96 M.J. Tegner et al. 1 J. Exp. Mar. Biol. Ecol. lY1 (19Y5) 83-99

4. Discussion

Macrocystis holdfasts increase in size by the addition of haptera to the outside of the initial structure. In young plants virtually all the haptera are living, but as the holdfast grows, the central haptera begin to die; eventually only a thin outer layer of hapteral tissue remains alive in large holdfasts. Ghelardi (1971), based on analyses of two size ranges of holdfasts, suggested that the thickness of the living portion remained nearly constant during the life of the plant. This characteristic growth pattern of iVucrocystis holdfasts appears to govern the maximum size that giant kelp plants can attain in a given wave climate. Following the arguments of Denny et al. (1985) and Gaylord et al. (1994) wave swept organisms encounter forces associated with both the velocity and the acceleration of the surrounding water. The forces of lift and drag associated with water velocity are proportional to the area of attachment and may remain relatively independent of an organism’s size. Accelerational force, however, scales with the volume of the organism, and thus increases faster for a given growth increment than does the ability to remain attached to the substrate. This argument would predict that larger giant kelp plants have a much higher risk of mortality due to breakage or dislodgment. In fact, the total observed mortality rate of Macrocysris in the Point Loma kelp forest during three winters in the 1980s was predicted remarkably well by acceleration forces for the outer edge of the kelp forest calculated from nearby wave data (Seymour et al., 1989).

Macrocysris holdfasts support a very diverse community. Ghelardi (1971) listed more than 150 species, including many grazers that potentially contribute to holdfast failure. In particular, the kelp gribble (Limnoria algarum), a boring isopod, accelerates the decay of older haptera near the center of the holdfast by hollowing them out (Jones, 1971). Nevertheless, major holdfast damage such as tunnels and large cavities was generally of a scale appropriate for the sea urchins found inside. While we do not discount the activities of the smaller grazers, the significantly greater mortality of plants with a high level of urchin infestation observed several times during this study suggests that sea urchin cavitation plays an important role in Macrocystis population dynamics. Koehl & Wainwright (1977) demonstrated the role of flaws induced by sea urchin grazing on stipes of Nereocystis luetkeana in structural failure of this kelp under conditions of high drag; 51% of the solitary beach-cast plants they examined had urchin grazing marks at the break point. Similarly, Black (1972) studied grazing of the limpet Notoacmea insessa on the stipes of the kelp Egregia menziesii; grazing scars were a major site of frond breakage.

The role of urchin cavitation in kelp mortality was strongest at 18 m, but also appeared to be significantly important at 15 m during some time periods. Sea urchin recruitment and abundance, presumably the driving forces in cavitation, were both highest at 18 m and decreased with decreasing depth. Even at 12 m, it is clear from Fig. 2B that there was high mortality of plants with an urchin infestation rating of three or four. The lack of significance in the G tests was

M.J. Tegner et al. I J. Exp. Mar. Biol. Ecol. 191 (1995) 83-99 97

probably due to the large number of holdfasts that had little or no evidence of urchin infestation.

It is not surprising that Macrocystis mortalities did not correspond directly with the degree of holdfast damage during each assessment period. There is consider- able seasonal and interannual variability in the wave climate and wind direction; storms with winds out of the south which stretch the canopy shoreward appear to increase the probability of holdfast or stipe bundle failure due to wave loading (Seymour et al., 1989). Drag forces are affected by the timing of storms relative to kelp harvesting; with 50% or more of the total giant kelp biomass in unharvested, mature plants found in the upper 1 m of the water column (North et al., 1982) there is a large difference in drag between harvested and unharvested canopies subject to breaking waves. Furthermore, entanglement by storm-dislodged drif- ters, the major source of Mucrocysfis mortality at Point Loma, is highly patchy and has a variable effect depending on plant age. Entanglements effectively cull young (less than 2 yr) and old (more than 4 yr) plants, while 2- to 4-yr olds have more robust holdfasts (Dayton et al., 1984). Thus, there may be substantial loss of young plants despite little or no urchin infestation. The outcome of any grazing event such as holdfast cavitation is dependent on the relative rates of grazing and plant growth. There was substantial interannual variabililty in temperature during the period of 1989 through 1994; 1989 and 1990 were colder than normal (Dayton et al., 1992) and 1992 was much warmer than average. Given the strong inverse relationship between temperature and nitrate availability (Jackson, 1977; Gerard, 1982; Zimmerman and Kremer, 1984) these temperature records indicate major interannual differences in kelp growth potential. Finally, there is interannual variation in sea urchin recruitment rates, which may have an effect on temporal variation in the degree of holdfast infestation and cavitation. The low to zero urchin recruitment rates observed at Point Loma sites during the very strong 1982-1984 El Nirio, for example, suggest the importance of large scale oceanog- raphic processes to interannual variability (Tegner & Dayton, 1991).

Storm-induced mortality of Mucrocystis increases with decreasing depth (Seymour et al., 1989; Dayton et al., 1992). The role of sea urchin cavitation decreased with decreasing depth in this study, and thus may act to reduce the gradient in Mucrocystis mortality with depth; i.e. if there was no urchin cavitation in deeper water, the plants at 18 m might have even higher survival. Dayton et al. (1984) noted that drifting holdfasts caused a higher percentage of mortality per encounter with attached giant kelp plants at 18 m than at 15 m at Point Loma, and speculated that this might be due to deeper plants being older and more vulnerable. The results of this study suggest that plants at 18 m are more vulnerable due to a higher degree of holdfast infestation by sea urchins.

It should be noted that the urchin cavitation patterns across depths described here for the large Point Loma kelp forest may be different in small forests of giant kelp if urchin recruitment shows an edge effect. Indeed the spatial scale of a forest influences many factors affecting the survival of kelps such as susceptibility to grazing by fishes and to storm dislodgement as surrounding plants appear to be

98 M.J. Tegner et al. I J. Exp. Mar. Biol. Ecol. 191 (1995) X3-99

able to dampen the effects of severe water motion (e.g. North & Hubbs, 1968; Seymour et al., 1989).

Acknowledgements

We thank E. Venrick for her patient help with statistics, L. Hall for assistance in the field, and L. Basch, D. Green, R. Rowley, E. Vetter and an anonymous reviewer for their comments on the manuscript. This research was funded by the National Science Foundation.

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