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Oecologia Springer-Verldg

Oecologia (Berlin) (1985) 65 591-598

1985

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Competition between herbivorous fishes and urchins on Caribbean reefs Mark E. Hay' and Phillip R. Taylor

' University of North Carolina at Chapel Hill, Institute of Marine Sciences, Morehead City, N C 28557, USA Division of Science and Mathematics, College of the Virgin Islands, St Thomas, US \'I 00801, USA

Summary. When the common sea urchin Diadema nntillaritm was removed from a 50 m strip of reef in St. Thomas, US Virgin Islands, cover of upright algae and the grazing rates and densities of herbivorous parrotfish and surgeonfish increased significantly within 11-16 weeks when compared to immediately adjacent control areas. Sixteen months after removal, Diadema had recovered to 70% of original density, abundance of upright algae no longer differed between removal and control areas, and the abundance and grazing activity of herbivorous fish in the removal was approaching equivalence with control areas. On a patch reef in St. Croix that had been cleared of Diadema 10-1 1 years earlier (Ogden et al. 1973b), urchins had recovered to only 50-60% of original density. This reef still showed significantly higher rates of grazing by fish and a significantly greater density of parrotfish and surgeonfish than a nearby control reef where Diadema densities had not been altered. These results indicate that high Diadema densities (7-12/mZ for this study) may suppress the densities of herbivorous fish on Caribbean reefs.

Most experimental investigations of competition between mobile organisms concentrate on interactions between closely related species (see references in Connell 1983 or Schoener 1983) that are assumed to require similar resources. However, completely unrelated organisms may also have largely overlapping resource requirements that result in intense interspecific competition. As an example, granivorous ants and rodents are important competitors for seeds in desert habitats (Brown and Davidson 1977; Brown et al. 1979; Davidson et al. 2980) despite their great differences in morphology, physiology, mobility and behavior. A recent investigation in tropical seagrass beds has been unable to document strong competitive interactions between two species of herbivorous sea urchins (Keller 1983), yet interference competition between other sea urchin species or between a territorial damselfish and a herbivorous sea urchin can be pronounced on some patch reefs (Williams 1981). In this study we investigate the effects of the sea urchin Diadema antillarum on the local density and feeding activity of herbivorous parrotfish and surgeonfish. Reef fish are generally thought to be space limited rather than food limited (Sale 1977, 1978, 1980; Smith 1978) but recent tests have been unable to substantiate this hypothesis (Robertson and Sheldon 1979; Robertson et al. 1981). Sev-

era1 observations suggest that food availability has a significant impact on the biology of herbivorous reef fishes. Three examples are as follows. Firstly, herbivorous fish that usually feed on algae of low caloric value consume, and further digest, the feces of fish that usually eat algae of higher caloric value; the reverse interaction does not occur (Robertson 1982; Bailey and Robertson 1982). Secondly, for territorial herbivorous fish, defense is directed primarily against other herbivorous species (Low 1971) or egg predators and the intensity of defense is correlated with the impact of the intruding species on food supply (Ebersole 1977) and with the similarity of diets between the invader and the territorial species (Myrberg and Thresher 1974; Thresher 1976a, b). Thirdly, mass death ofjuvenile herbivorous fish from apparent starvation has been reported on one occasion (Tsuda and Brian 1973). If food availability affects reef fish either directly (i.e., is a limiting resource) or indirectly (i.e., by lowering foraging time and thus increasing the time available for mating, detecting predators, etc.), then herbivorous urchins may negatively affect fish abundance by over exploitation of algal resources. We suggest that once urchins become abundant on shallow Caribbean reefs, they can severely deplete algal populations and reduce the density of herbivorous fish. The potential competitive relationship between Diadema and herbivorous fish, such as parrotfish and surgeonfish, has been suggested by earlier studies (Ogden 1976) but remains untested. Study sites

An urchin removal experiment was conducted in Brewer's Bay, St. Thomas, U.S. Virgin Islands. The reef at this location runs from the surface to a depth of 2-3 m where a halo of bare sand separates it from the nearby seagrass bed (Thalassia testudinum). Most of the reef is composed of beach rock covered by encrusting coralline algae; small stands of the corals Acropora palmata and Millepora spp. also cover a limited area. Topographic complexity, species diversity and coral cover a13 low relative to most other Caribbean reefs. The sea urchin Diadema antillarum is abundant (7-10/mZ) on subtidal portions of the reef. Herbivorous fish are found throughout the area but abundance appears to be low compared to other reefs on St. Thomas that have greater topographic complexity. Experiments also were conducted in Knight Bay, St. Croix, U.S.V.I., on the same patch reefs used by Ogden et al. (1973a, b) and Sammarco et al. (1974) for earlier stu-

dies on urchin gr2zing. As part of these studies, all Diadema had been removed from one patch reef in April of 1972, a similar sized patch reef located 150 m from the removal patch reef \bas not manipulated and served as a control. The reefs are about 50 m in diameter, isolated within a seagrass bed, and lack much of the topographlc complexity that characterizes the bank barrier reef 250-350 m to the north There are a febt colonies of the branching coral Acroporn yalrnntn around the edge of the control patch reef, but a large portion of both reefs is covered by a coralline algal pavement that has little topographic complexity. To control, to some extent, for the structural differences In topographic complexity between the two patch reefs, all experiments were conducted within the coralline pavement area of each reef. Urchin density In these coralline pavement areas is higher on the control (9-12/m2) than on the removal patch reef (4-7/mz). A more detailed description of these patch reefs can be found in Ogden et al. (l973a, b). Methods

The study site on St. Thomas consisted of a 150 m long section of uniform reef that was divided into three S 0 m long sections. Width of these sections, between the shore and the grass bed, varied with reef configuration but ranged from 25-47 m. All Diadema in the center section ( ~ 8 , 0 0 0 ) were killed by crushing with an iron bar. Removals were carried out between 30 January and 13 February 1982. Urchin density in the removal area was held below 0.2 Diadema/m2 by periodic removals until September 1982; after this time, urchins were allowed to reinvade from the adjacent control areas. The SO m sections of reef on each side of the removal area served as controls. Before removal of urchins from the center section, Diadema density was measured by flipping a 1.0 m 2 quadrat along S randomly located transects within each 50 m section of reef. All Diademu were counted regardless of size. The transects were oriented perpendicular to shore, started a t a depth of about 0.5 m and run to the inner edge of the halo at a depth of 2-3 m. Because of variations among transects in the slope and extent of hard substrate, the number of quadrats assessed in each control or removal area varied from 57 to 97. Urchin counts were made just before removal and again on 21 May 1983 (9 months after reinvasion of the removal area started). On the patch reefs at St. Croix, urchin densities were measured in a similar fashion but counts were taken only in the coralline pavement area of each reef. Counts were made on 19 March 1982 (20-21 quadrats on each reef) and on 31 May 1983 (160 quadrats on each reef). Cover of benthic organisms in the control and removal areas o n St. Thomas was measured 11 weeks, 30 weeks, and 74 weeks after Diadema removal. One hundred 5 mm holes were punched in a 50 cm x 30 cm vinyl quadrat. The holes were arranged in a stratified random array by placing 5 holes within each of 20 equal sized subsections. To measure cover, the quadrat was draped over randomly located sections of the reef to determine the type of organism found beneath the center of each hole. Organisms were grouped into the following categories: crustose algae (almost exclusively encrusting corallines), filamentous algae (e.g. Cfadophora, Ceramium), larger algae (e.g. Dictyota, Laurencia), and sessile benthic invertebrates (e.g. corals and sponges).

At each sampling period, 10-14 quadrats were assessed in the removal area and in each control area. Dates for benthic monitoring were 30 April and 9-13 September 1982 and 10 June 1983. Grazing activity of herbivorous fish in control and removal areas on both St. Thomas and St. Croix was monitored using transplanted sections of the seagrass Thnlassin testzrdinum as a bioassay (see Hay et al. 1983; Hay 1984). Hay (1984) lists several limitations of this method. Additionally, recent field observations (Lewis 1984: M. Hay and J. Trendall work in progress) have shown that almost all loss of Thalassia transplants is due to grazing by parrotfish (Scaridae) despite surgeonfish (Acanthuridae) being common in the area. The Thalassia bioassay thus measures primarily grazing by some of the common parrotfish. In order to control for the differences in urchin grazing between the removal and control areas, all blades showing any evidence of urchin grazing were excluded from the analyses. Thus, we measured the percentage of available Thalassia (i.e., not eaten by urchins) that was eaten by fish. This allowed us to assess differences in fish grazing without the confounding problem of our experimentally induced changes in urchin grazing. An exception to this could occur if a n urchin ate most of a Thalassiu blade but the remainder was consumed by a fish, thereby removing the evidence of urchin grazing. This would have resulted in artificially high rates of fish grazing in the control areas. Since this situation appeared to be very uncommon and would bias against our hypothesis, we d o not consider this a significant limitation. During 1982, 6 determinations of fish grazing in the removal and control areas were made on St. Thomas and 6 on St. Croix. We conducted these determinations at several different times of day to make sure that our measurements were not biased by unusual feeding patterns that might occur only within one time period. Approximately one year later, 2 additional measurements were made on St. Croix and 5 on St. Thomas. All comparisons between Diudema-removal and control areas were paired in time. Number of Thalassia blades transplanted into each area at each time was 19-30 for St. Thomas and 20-45 for St. Croix. Determinations of grazing on St. Croix were conducted between 17 and 22 April 1982 and 31 May and 1 June 1983; determinations on St. Thomas were conducted between 24 and 26 April 1982 and 25 and 27 May 1983. Between 31 May and 8 June 1982 and 5 and 6 June 1983, direct counts of herbivorous fish were made in the removal and control areas on St. Thomas. Counts of parrotfish (Scaridae) and surgeonfish (Acanthuridae) were made by slowly swimming 50 m long transects through each area. The sampling area was standardized by staying over areas that were 1.S-3 m deep and looking down and slightly forward. This resulted in a transect width of approximately 3 m. All individuals of each category of fish were counted regardless of size. Counts in 1982 were made between 1400 and 1600 h ; counts in 1983 were made between 0900 and 1500 h. All counts were grouped in t h e (i.e., within the course of only a few minutes a count was made in one control area, the removal area, and then the second control area). Sample size equaled 18 counts for each area in 1982 and 16 counts for each area in 1983. Fish counts in St. Croix were not made in 1982. In June 1983, 8 counts (consisting of 3 transects per count) were made on the control reef and 8 on the removal reef in St. Croix. Counts were paired in time, were conducted only on the similar pave-

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ment areas ofieach reef, and were made in transects that were 20 m long and 3 m mide.

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Before removal in early February of 1982, Dindemn densities in the 3 study areas on St. Thomas were as follows (mean *95% confidence intervals/m2): control area A = 10.0 1.2 ( N = 89), removal area = 7.1 1.O (N=97), control area B=7.2+1.4 (N=64). Nine months after reinvasion of Diadema started, densities were: control area A = 7.2+ 1.3 (N=57), removal area=5.0f0.8 ( N = 6 8 ) ; control area B = 8 . 9 f l . l (N=91). The density in the removal area was significantly lower than in either control area (P