EFFECTS OF BOTTOM RELIEF AND FISH ...

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urchin grazing, unfouled sections of adult kelp plants were similarly exposed. ...... City of Escondido, City of Oceanside, Encina Water Pollution Control Facility,.
BULLETIN OF MARINE SCIENCE, 55(2-3): 631-644. 1994

EFFECTS OF BOTTOM RELIEF AND FISH GRAZING ON THE DENSITY OF THE GIANT KELp, MACROCYSTIS M. L. Patton, C. F. Valle and R. S. Grove ABSTRACT A series of SCUBA surveys of subtidal reefs in the mainland Southern California Bight were used to relate the density of giant kelp (Macrocystis), kelp-grazing fish, kelp-fouling organisms, and sea urchins to bottom relief. On natural and artificial reefs, adult giant kelp plants were more common on low-relief substrates, i.e., on hard substrates lying less than I m above the surrounding sand. Conversely, juvenile kelp, kelp-fouling organisms, and kelpgrazing fish were more common on high-relief substrates. There was no statistically significant relationship between the density of sea urchins and bottom relief. The effects of fish grazing, but not the effects of abrasion and sea urchin grazing, are probably much greater on kelp plants that are partially encrusted with fouling organisms. To study fish grazing, fouled sections of adult kelp plants were exposed on high and low relief. To study abrasion and sea urchin grazing, unfouled sections of adult kelp plants were similarly exposed. On both artificial and natural reefs, fouled sections of kelp plants lost significantly more tissue on high relief; unfouled sections did not. The results indicated that the relationship of giant kelp density to bottom relief was produced by differences in fish grazing which were, in turn, produced by the higher densities of kelp-grazing fish or kelp-fouling organisms on high relief. The data did not suggest that the relationship between kelp density and bottom relief was produced by abrasion, sea urchin grazing, or kelp recruitment. Finally, the data suggest that a reef intended to support giant kelp should be designed to minimize bottom relief and the number of shelter crevices suitable for kelp-grazing fish,

Giant kelp, Macrocystis, is a large and abundant canopy-forming algae which grows in extensive, and densely inhabited, beds throughout the subtidal Southern California Bight (North, 1991). The environmental factors controlling the density of this algae have been extensively studied (North, 1971; Dayton, 1985; Foster and Schiel, 1985), but there have been few studies of the relationship between giant kelp and bottom relief. We felt that kelp density was probably

affected by

bottom relief, because bottom relief has a strong effect on the densities of many other subtidal organisms (Pequegnat, 1964; Patton and Harman, 1983, 1986; Patton et a!., 1985). Moreover, if kelp density was related to bottom relief, an understanding of this relationship would be essential to the design of artificial reefs intended to support kelp beds. During a 1979 baseline study of the mainland Southern California Bight, we noticed that giant kelp tended to be more dense and more persistent on low-relief substrates than on high-relief substrates. This observation, which we confirmed with more localized studies, was interesting because it was counter-intuitive. Both sediment scour (North, 1971; Dayton, 1985) and dim light (Dayton et aI., 1984; Dayton, 1985) are harmful to giant kelp. Since there is more suspended sediment present near low relief (Cook and Gorsline, 1972; Patton and Harman, 1983), giant kelp should be relatively less dense on low relief. We studied the effect of fish grazing on giant kelp because fish grazing has produced low algae densities on high-relief substrates in the tropics (Hay, 1981a, 1981b) and because fish grazing has frustrated several attempts to transplant kelp to both artificial (Carlisle et a!., 1964; Turner et a!., 1969; Carter et aI., 19R5) and natural (North and Hubbs, 1968) substrates in the Southern California BigLl. Also, several relatively large, abundant fish that graze on algae, halfmoon (Medialuna 631

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californiensis), opaleye (Girella nigricans), garibaldi (Hypsypops rubicunda), and sheephead (Semicossyphus pulcher) (Limbaugh, 1964; Quast, 1968; North and

Hubbs, 1968; MEC, 1991), are usually more common in high-relief areas of both natural (Pequegnat, 1964; Patton et aI., 1985) and artificial (Jessee et aI., 1985; MEC, 1991) reefs, We also studied kelp fouling because most kelp-grazing fish prefer fouled plants (Limbaugh, 1964; Bernstein and lung, 1979; Dixon et aI., 1981) and, therefore, differences in fish grazing could be produced by differences in the density of fouling organisms. We expected fouling organisms to be more dense at reef crests because water motion is faster and more turbulent at reef crests (Pequegnat, 1964; Patton and Harman, 1983) and because some fouling organisms are more likely to settle out in such conditions (Bernstein and lung, 1979; Dixon et aI., 1981). We also examined other factors that affect kelp density and might, therefore, affect the relationship between kelp density and bottom relief: sea urchin grazing (Ebeling et aI., 1985; Lawrence, 1975), abrasion (Carter et aI., 1985), kelp recruitment (Reed et aI., 1988; Reed, 1991), and fish grazing on unfouled juvenile kelp plants (Harris et aI., 1984), In these studies, we used data from the baseline study and from more intensive and localized studies. We examined the relationship between bottom relief and the densities of adult kelp plants, juvenile kelp plants, kelp-grazing fish, sea urchins, and fouling organisms. We used single, fouled kelp blades to measure the grazing rates of fish. Because fish usually do not feed heavily on unfouled mature kelp plants (Bernstein and lung, 1979; Dixon et aI., 1981; Harris et aI., 1984), we were able to use the unfouled tips of mature kelp fronds to measure the effects of abrasion and sea urchin grazing. The results suggested that giant kelp is uncommon on high relief because kelp is more heavily grazed or more heavily fouled in high-relief areas. The data did not suggest that the relationship between kelp density and bottom relief was produced by abrasion, sea urchin grazing, or kelp recruitment. METHODS

Baseline Study.- The density of kelp, like most of the phenomena ecologists study (Quinn and Dunam, 1983), is affected by a large number of factors (Dayton, 1985), In the baseline study, therefore, we examined a large number of sites so that the variation due to factors other than bottom relief would "average out." The effects of bottom relief were therefore compared with the variation in kelp density due to "chance" which was not entirely physical randomness but included " .. , the contributions of the large number of deterministic effects not included in the model." (Quinn and Dunham, 1983). "Relief" was defined as elevation of the substrate above thc plain of sand covering most of the southern California subtidal sea floor (Dennis, 1974), We used this definition because the amount of suspended sediment impinging a hard substrate is probably inversely related to its elevation above a sand bottom (Cook and Gorsline, 1972; Patton and Harman, 1983), and sediment movements have profound effects on giant kelp (North, 197 J; Dayton, 1985) and other organisms (Limbaugh, 1955; Moore, 1977). Earlier work (Patton and Harman, 1983, 1986; Patton et a!., 1985) indicated that organism densities change little with bottom relief when bottom relief is greater than 1.5 m, so bottom reliefs greater than 1.5 m were represented as 1.5 m, We studied 24 different sites in the southern half of the Southern California Bight during 1979 (Fig, 1), Giant kelp and sea urchins were counted with belt transects. Usually, two I m x 30 m transects were taken at each site on each of two sample dates, Transect locations were haphazard; they were taken at the point where the divers first reached the bottom, Divers counted the number of sea urchins and the number of Macrocystis stipes that were longer than 2 m. Usually, divers also made five measurements of the elevation of the transect above deep, level sand. Roughly half of the sites lay at depths of 6 m and half at 15 m, Fish densities were measured at the same sites, Usually two free swim samples were taken on each of two sample dates, Pelagic and suprabenthie ("reef") fish were counted with a straight free swim wherein the diver swam 1 m above the bottom at a speed of about 12 m·min ) and counted all the fish he saw, Swim distance was controlled by limiting swim time, Swimming speed, periodically

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Figure I. Study sites. Black dots mark the locations of the baseline study sites; most dots represent two sites. Triangles mark the location of the sites of intensive studies: Barge Rock, and Oceanside Artificial Reef (OAR), the Pendleton Artificial Reef (PAR), and the Topanga Artificial Reef (TAR).

calibrated, tended to remain constant. Since the diver looks both ways, the area searched was twice the product of the visibility distance and the swim distance; this area was held constant at 700 m2• Visibility was the average of four measurements of the distance at which a white globe with a diameter of 20 cm disappeared as a result of turbidity or kelp interference. The globe was suspended I m above the bottom. Sampling was done when visibility was greater than 4 m, i.e., largely during the clearwater summer-fall season. This technique was designed to measure between-site differences in the densities of fish species. It does not measure absolute densities because, even under the same conditions, different species are visible from different distances. Intensive Studies.-Four sites were used: Barge Rock, the Oceanside Artificial Reef (OAR), the Pendleton Artificial Reef (PAR), and the Topanga Artificial Reef (TAR) (Table I). All lie 0.5 to 1.0 nautical miles offshore and all, at the time of the study, supported kelp beds. Barge Rock is composed of large (> I m) natural boulders and bedrock; OAR, PAR, and TAR are composed of quarry rock. Most studies were done at Barge Rock and OAR, but since fronts of feeding urchins and terrestrial runoff largely removed kelp from Barge Rock and OAR before our studies were completed, some

Table I. Characteristics of reefs used for intensive studies

SITE

BASE DEPTH (m)

CREST DEPTH (m)

Barge Rock OAR PAR TAR

15 13 13 8.5

10 10 8.5 6

DIMENSIONS (m)

15 X 15 X 15 X 40 X

25 24 30 130

YEAR CONS1RUCIED Natural

1987 1980 1987

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BULLETIN OF MARINE SCIENCE, VOL. 55, NO. 2-3, 1994

measurements were made on PAR and TAR. Most measurements were made in the first 4 months of 1991. To relate kelp density and bottom relief on these sites, each diver measured the depth at the base of each holdfast and the depth at the adjacent sand, Holdfast elevation was defined as the difference between the holdfast depth and the depth at the sand. To ensure the holdfasts were selected haphazardly, each diver measured the elevation of the first holdfast encountered and then determined the bearing between the first holdfast and its nearest neighbor, He then swam 10 m along this bearing, measured the elevation of the holdfast lying closest to the end of this swim, and repeated the process, To measure the mean elevation of the reef, divers measured the depth at haphazard points on the reef and compared these depths with the mean depth at the sand, Each diver measured the depth at the sand at the point where he first reached the reef, then swam across the reef stopping at random points to measure the depth of the rock substrate, When he reached the sand-rock interface on the other side of the reef, he measured the depth at the sand, swam a random number of meters along the sand-rock interface, and then crossed the reef again, "Random" numbers were obtained from a random number table, To measure the effect of fish grazing on fouled kelp, we used single blades that were 30 to 80% covered with fouling organisms (mainly Membranipora). Cable ties were used to fasten the kelp blades to sea fans (Muricea calijornica), short algae, or stalked tunicates. Ten blades, spaced I to 2 m apart, were used in each experiment. They were placed within 1 m (vertical distance) of the reef crest or on the flat bottom 10 to 15 m away from the reef base, After exposure, the blades were weighed and the number of scars from fish grazing (Quast, 1968) were counted, In this and subsequent experiments, blade fouling was measured with a plastic grating of 225 mm2 squares with intersections that were I mm wide. Grating and blade were placed on a light table and the intersections touching fouling organisms were counted and expressed as a percent of the number of intersections touching the blade. Since plants growing close to the reef crests had few blades, the fouling of kelp "floats" or pneumatocysts was measured, Kelp plants were chosen in the same way they were chosen when holdfast depth was measured. A frond was then selected at random, and a pneumatocyst growing about 0,5 m above the holdfast was removed, Random numbers were again obtained from a random number table, Reef crest samples were taken within I m (vertical distance) of the reef crest; reef base samples were taken within 0,5 m (vertical distance) and 10 m (horizontal distance) of the reef base, After the floats were cut and flattened, float fouling was measured in the same way that blade fouling was measured except that the grid had 6.25 mm2 squares with intersections that were 0,5 mm wide, Since the measurement of pneumatocyst fouling was used as a surrogate for the measurement of blade fouling, it was necessary to examine the correlation between blade fouling and pneumatocyst fouling using measurements made on intact blades that were heavily or lightly fouled, To measure the effect of bottom relief on abrasion and sea urchin grazing, tips of unfouled adult fronds were exposed on reef crests and reef bases in the same way as the fouled blades were exposed. Frond tips were one meter long, After exposure, tips were weighed and the number of scars from fish grazing (Quast, 1968) were counted, Laboratory measurements of sea urchin grazing were made in two lO-gallon aquaria. Aquaria were aerated, supplied with a trickle of fresh water, and all fecal material and detritus was removed daily. Four Strongylocentrotus franciscanus were placed in each aquarium and starved for 2 days, Five fouled kelp blades were placed in one aquarium and five unfouled blades were placed in the other; before the experiment was started, all blades were trimmed to a wet weight of 7.0 gm. Fouled blades were 35 to 36% covered with fouling organisms; unfouled blades were 0 to ] % covered with fouling organisms. Kelp remaining after 24 h was removed, blotted dry, and weighed. The urchins were then starved again for 2 days and fouled blades were introduced into the aquaria that previously held unfouled blades and vice versa, The experiment was repeated twice using the same urchins, To measure the density of juvenile kelp, the divers used 0.125 m2 quadrats placed haphazardly on the reef. The first measurement was made at the point where the diver first reached the reef. The diver then determined the bearing between the two nearest sea fans. He then swam 4 m along this bearing, measured density again, and repeated the process. Divers counted the number of juvenile kelp plants between 5 and 20 cm long. Reef crest samples were taken within I m (vertical distance) of the reef crest. Reef base samples were taken within 0,5 m (vertical distance) and 10 m (horizontal distance) of the reef base. This technique was also used to determine the proportion of abraded or bitten juvenile kelp plants. Prior to ANOV A and t-tests, data were tested for heteroscedasticity and measurements of proportion were subjected to an angular transformation (arcsin of the square root of the proportion) (Sokal and Rohlf, 1969).

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Figure 2. Macrocystis density vs. bottom relief. Bottom relief defined as the average elevation in meters of the substrate above the sand. Each point represents the average of two to four 30-m2 transects taken on a single baseline study site (See Fig. ]).

RESULTS

Baseline Study.-On natural reefs, giant kelp density was significantly greater on low-relief substrates (Fig. 2). The results of an ANOV A, based on regression analysis, indicated that the negative relationship between kelp stipe density and bottom relief was significant (F = 8.121, P = 0.020). It was striking that kelp density was zero on all high-relief sites. The results of ANOV As, based on regression analyses, indicated that the densities of several kelp-grazing fish were significantly greater on high-relief sites. This was true of H. rubicunda (F = 22.67, P < 0.00 I), M. californiensis (F = 8.15, P = 0.009), and S. pulcher (F = 18.01, P < 0.001) (Fig. 3). The densities of G. nigricans, however, were not significantly greater on high relief (F = 3.03, P = 0.085) (Fig. 3). Sea urchin densities were not significantly greater on high-relief sites, either (Fig. 4). This was true for both S. franciscanus (F = 2.37, P = 0.11) and S. purpuratus (F = 0.03, P = 0.87). Intensive Studies.-A frequency distribution of holdfast elevation on the Pendleton artificial reef (PAR) and the Topanga artificial reef (TAR) (Fig. 5) clearly indicated that kelp grew more densely close to the sand. A few holdfasts had negative elevations; they were growing on rocks lying in small depressions in the sand. Mean holdfast elevation was significantly lower than mean hard substrate elevation at both Pendleton (t = 14.5, P < 0.00l) and Topanga (t = 6.5, P < 0.001). Kelp appeared to grow most densely at an elevation of 0.2 m. The examination of videotape taken at Barge Rock and the Oceanside artificial reef (OAR) indicated that kelp grew most densely at the bases of these reefs, also. To measure fish grazing, fouled kelp blades were exposed at Barge Rock and the Oceanside Artificial Reef for 4 to 8 days. The results of one-way ANOV As indicated that fish grazing was heavier at reef crests than at reef bases at both Barge Rock (F = 12.6, P = 0.0013) and OAR (F = 16.8, P = 0.003) (Fig. 6A). Hypsypops rubicunda, M. californiensis, and S. pulcher were observed grazing on the blades. The hemispherical scars left by fish grazing were common; the average blade had about three obvious scars. Necessarily, the blades exposed on reef crests lay in shallower water than the

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BULLETIN OF MARINE ScrENCE. VOL. 55. NO. 2-3. 1994

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Figure 5. Frequency distribution of the elevation of kelp holdfasts above the base of the Pendleton Artificial Reef (PAR) and the Topanga Artificial Reef (TAR). Arrow indicates the mean elevation of the rock substrate above the base of the artificial reef.

the effects of bottom relief on fish grazing with the effects of depth on fish grazing. Since differences in fish grazing could be produced by differences in fouling, we measured the density of fouling organisms on kelp pneumatocysts at Barge Rock and, because all kelp temporarily disappeared from OAR following heavy terrestrial runoff, at the Pendleton Artificial Reef (Fig. 7). The results indicated that the pneumatocysts taken from reef crests were more heavily fouled than those taken from reef bases. This was true at both Barge Rock (t = 3.21, P = 0.007) and PAR (t = 6.08, P < 0.001). Pneumatocyst fouling probably reflects blade fouling because, in a sample of intact blades collected from PAR, the regression of blade fouling on pneumatocyst fouling was statisticaJly significant (F = 11.37, P = 0.04) (Fig. 8). To separate the effects of abrasion and sea urchin grazing from fish grazing, we repeated the grazing experiment using the unfouled tips of adult fronds instead of single fouled blades. During the 6 to 9 days the fronds were exposed, there was at least one day of heavy surf. The results of one-way ANOVAs indicated that bottom relief had no effect on tissue loss at either Barge Rock (F = 0.085, P = 0.771) or OAR (F = 0.313, P = 0.579) (Fig. 9). These results suggest that abrasion and sea urchin grazing did not change with bottom relief. These results

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