Ecology, 80(6), 1999, pp. 2085±2101 ᭧ 1999 by the Ecological Society of America

MUTUALISM AND CORAL PERSISTENCE: THE ROLE OF HERBIVORE RESISTANCE TO ALGAL CHEMICAL DEFENSE

JOHN J. STACHOWICZ1 AND MARK E. HAY2 University of North Carolina at Chapel Hill, Institute of Marine Science, 3431 Arendell Street, Morehead City, North Carolina 28557 USA

Abstract. Because seaweeds uncontrolled by herbivores can overgrow and kill corals, competition can exclude corals from temperate latitudes where herbivores generally fail to control seaweed biomass. In this study, we show that the coral Oculina arbuscula persists on reefs in temperate North Carolina where seaweeds are common by harboring the om- nivorous crab Mithrax forceps, which removes seaweeds and invertebrates growing on or near the coral. In the ®eld, corals from which crabs are experimentally removed develop a dense cover of epibionts, exhibiting reduced growth and increased mortality relative to corals with crabs, which remain epibiont-free. This crab is unusual in that it readily con- sumes all local seaweeds in laboratory choice assays and is not deterred by chemical defenses that suppress feeding by local ®shes, sea urchins, and other crabs. This allows Mithrax to defend corals from overgrowth by chemically noxious seaweeds like Dictyota and Sargassum that are avoided by most local herbivores. However, further ®eld manip- ulations under reduced light conditions demonstrate that the outcome of the crab±coral interaction is context-dependent: crabs only bene®t corals in well-lit areas where seaweeds are abundant. Field observations and tethering experiments show that, by living in asso- ciation with Oculina, Mithrax gains a refuge from predation. Additionally, crabs grow faster when associated with live corals than with structurally equivalent dead corals, apparently because they are able to consume lipid-rich coral mucus. This mucus provides a dietary supplement that may help corals attract and retain low-mobility symbionts such as Mithrax, securing for the coral long-term and predictable protection against competitors. Structurally complex but competitively inferior organisms, like some corals and coralline algae, provide the biogenic habitat complexity upon which many other species depend. Because these sessile organisms may be dependent on symbionts to remove superior com- petitors, mutualisms can play an important, but currently underappreciated, role in struc- turing marine communities where biotic interactions are intense. In this study, the mutualism between Oculina and Mithrax promotes the persistence of both species in habitats from which they might otherwise be excluded by competition and predation. Key words: associational escape; chemical defense; competition; context-dependent interactions; coral; crab; Mithrax; mutualism; Oculina; predation; seaweed; temperate reef.

INTRODUCTION diversity (Hacker and Gaines 1997). In contrast to this Recent experimental investigations of positive in- growing appreciation for the role of these one-way pos- teractions such as commensalism and facilitation dem- itive interactions in structuring ecological communi- onstrate that they are predictable forces capable of ties, mutualisms are still regularly portrayed as little shaping community structure and composition (Bert- more than natural history curiosities (but see Regal ness and Callaway 1994, Bertness and Leonard 1997, 1977, Vance 1978, Witman 1987). Thus, despite an Callaway and Walker 1997, Holmgren et al. 1997). In impressive amount of amassed information about some habitats with extreme physical (Bertness and Hacker mutualisms and their direct consequences for the par- 1994) or biotic (Atsatt and O'Dowd 1976, Hay 1986, ticipants (see reviews by Boucher et al. 1982, Addicott Littler et al. 1986, P®ster and Hay 1988, Stachowicz 1984, Boucher 1985, Bronstein 1994), there is still little and Hay 1996) stresses, species resistant to these stress- rigorous empirical evidence for the broader role of mu- es modify the local environment, allowing the persis- tualism in ecological communities. tence of less tolerant species and enhancing species Tropical reef-building corals and their endosym- biotic dino¯agellates are one of the most often cited Manuscript received 2 March 1998; revised 3 August 1998; examples of the importance of mutualism to commu- accepted 11 August 1998. nity structure and function. This association provides 1 Present address: University of Connecticut, Department reef corals with the bulk of their dietary requirements of Marine Sciences, 1084 Shennecossett Road, Groton, Con- necticut 06340 USA. E-mail: [email protected] (Muscatine and Porter 1977, Davies 1991), enhancing 2 Present address: School of Biology, Georgia Institute of calci®cation rates and reef accretion. Other less-obvi- Technology, Atlanta, Georgia 30332-0230 USA. ous, but critically important, mutualisms between cor- 2085 2086 JOHN J. STACHOWICZ AND MARK E. HAY Ecology, Vol. 80, No. 6 als or calci®ed seaweeds (coralline algae) and mobile morphology that provides shelter for a species-rich epi- invertebrates have been reported; in these interactions, fauna. Over 300 species of invertebrates are known to low-mobility invertebrates gain food or shelter from live among the branches of Oculina colonies, and al- the host, while enhancing host ®tness by discouraging though only a few are obligate coral dwellers, many predators (Glynn 1983, 1987) or removing competitors more are reported to complete much of their life cycle (Steneck 1982, Coen 1988, Littler et al. 1995, Sta- within the coral (McCloskey 1970). In this paper, we chowicz and Hay 1996). Such studies have rarely ad- investigate the possibility that the success of Oculina dressed the broader implications of these associations, on temperate reefs is derived from its ability to harbor but where they have, these mutualisms have been symbiotic herbivorous crabs that mediate competition shown to facilitate the production of biogenic structure with encroaching seaweeds and invertebrates. (Littler et al. 1995), which can have important com- Using ®eld, mesocosm, and laboratory manipula- munity and ecosystem level consequences (Lawton and tions, we demonstrate a mutually bene®cial association Jones 1995, Jones et al. 1997). between Oculina and the majid crab Mithrax forceps Positive interactions between corals and herbivores that is similar to some ant-plant mutualisms in terres- are at least partially responsible for the restriction of trial environments (e.g., Janzen 1966, 1969, review in most corals to tropical environments (Johannes et al. Beattie 1985). The coral provides the crab with dietary 1983, Miller 1998). Although temperature may play an supplements and shelter from predators while the crab indirect role, many temperate and subarctic habitats defends the coral from overgrowth by encroaching support corals (Cerame-Vivas and Gray 1966, Squires competitors, thus enhancing coral growth and survi- and Keyes 1967, Jacques et al. 1983, Schumaker and vorship. We also experimentally examine how variation Zibrowius 1985, Ruppert and Fox 1988), and some in external environmental conditions affects the out- tropical species occur where temperatures decline to come of this interaction, highlighting the context-de- 10ЊC or lower for certain months of the year (MacIntyre pendent nature of mutualistic interactions. Our results and Pilkey 1969, Ruppert and Fox 1988). Intolerance suggest that this type of protective mutualism has pop- to cold is, therefore, not an insurmountable physical ulation and community implications that extend beyond barrier. In well-lit habitats, corals are slow growing the participant species. The crab directly alters the local relative to seaweeds, and the persistence of coral reefs benthic community, enhancing the growth and survival appears to be tightly linked to the high abundance of of its host and ensuring the persistence of the diverse herbivores that prevent seaweed overgrowth of corals host-associated community by increasing the produc- (Miller 1998). When herbivorous ®shes or sea urchins tion of biogenic structure. are naturally or experimentally removed from tropical reefs, seaweed biomass increases dramatically and cor- METHODS als are smothered (Lewis 1986, Hughes 1989, 1994). Study sites and organisms In contrast, on temperate reefs, herbivorous ®shes are less abundant than in the tropics and algal standing Field experiments were performed at Radio Island stock is typically much higher (Horn 1989, Choat 1991, Jetty near Beaufort, North Carolina, USA (34Њ42Ј N, Ebeling and Hixon 1991). On the temperate reefs in- 76Њ41Ј W). This rock jetty runs from just subsurface vestigated here, herbivorous ®shes and urchins alter to 9 m depth, and ®eld experiments were deployed at the species composition of the algal community 2.0 and 6.0 m. Although the jetty is man-made, its ¯ora through selective removal of preferred species, but they and fauna are similar to that of natural rock ledges do not diminish total seaweed biomass (Miller and Hay along the North Carolina coast (Richardson 1978, Link 1996) and are thus unlikely to mediate coral±algal com- 1980, Peckol 1982, see Results). In the summer and petition (see reviews in Lubchenco and Gaines 1981, fall, the shallow, well-lit portion of the jetty is domi- Horn 1989). The dependence of corals on positive in- nated by brown seaweeds like Sargassum, Padina, and teractions with herbivores may thus help explain why Dictyota, whereas the deeper portions are dominated corals are generally uncommon in temperate latitudes by colonial invertebrates, including the scleractinian and why coral abundance is inversely correlated with coral Oculina arbuscula, the upright bryozoan Bugula algal abundance among habitats in temperate regions neritina, the hydroid Eudendrium carneum, several (Miller and Hay 1996, Miller 1998). species of tunicates, and a few sponges. Abundant om- In contrast to this general latitudinal pattern, the cor- nivorous ®shes include the spottail pin®sh Diplodus al Oculina arbuscula does co-occur with seaweeds on holbrooki, the pin®sh Lagodon rhomboides, and the natural and arti®cial reefs in North Carolina. Although sheepshead Archosargus probatocephalus. The pred- it forms much denser aggregations in poorly lit habitats atory black sea bass Centropristis striata is also abun- where seaweeds are rare or absent, Oculina is a com- dant. In the winter and spring, colder temperatures in- mon member of many North Carolina reef communities duce an offshore migration of most ®shes and reduce (McCloskey 1970, Peckol and Searles 1984, Miller and activity of resident urchins (Arbacia punctulata), shift- Hay 1996). Oculina is also the only species of coral ing community dominance toward more palatable red in this region with a structurally complex branching and green seaweeds and an increased abundance of September 1999 MUTUALISM AND CORAL PERSISTENCE 2087

¯eshy invertebrates (Hay 1986, Hay and Sutherland harvesting excessive amounts of coral, we also re- 1988). corded crab abundance in corals at the two nearshore Oculina arbuscula is a branching, scleractinian coral rocky outcrops mentioned previously. Using a small endemic to North and South Carolina. Oculina growing metal rod, we probed the recesses of each coral in a in sunlit waters possess symbiotic zooxanthellae, but 20 ϫ 1 m belt transect at each site, counting the number this relationship is facultative. In dark habitats, colo- and species of crabs present. Most individuals could nies are azooxanthellate, yet continue to grow (Miller be identi®ed to species, but xanthid crabs were grouped 1995). A diverse invertebrate fauna hosted by the coral together because distinctions among some of the lo- includes the majid crab Mithrax forceps (McCloskey cally occurring species in this family require micro- 1970). This crab occurs from Cape Hatteras, North Car- scopic examination or dissection. olina south through Florida and the Caribbean to Brazil on rocky shores and reefs from the intertidal to a depth Field experiments of 90 m (Williams 1984). Mithrax has been found as- Because Mithrax forceps was the most abundant crab sociated with various species of sponges and branching living on Oculina, and other crabs of the genus con- corals, as well as intertidally on oyster shells, and its sume seaweeds (Coen 1988, Stachowicz and Hay geographic range extends well south of that of Oculina, 1996), we reasoned that it might be capable of medi- so association with this coral is not obligate. Little is ating competition between corals and encroaching sea- known of the ecology or feeding habits of M. forceps, weeds. To evaluate this hypothesis, we performed two although other crabs in the genus are herbivorous and ®eld experiments monitoring fouling and growth of enter into facultative associations with corals and cal- corals in the presence and absence of crabs. In the ®rst ci®ed seaweeds (Coen 1988, Stachowicz and Hay manipulation, metal stakes were driven into a sandy 1996). To avoid biasing the results of ®eld experiments area immediately adjacent to Radio Island Jetty at a through excessive disturbance, crabs and corals for all depth of 2 m, and one coral was fastened to each stake ®eld, mesocosm, and laboratory experiments were col- 0.75 m above the bottom. We term this the ``fouling lected at a depth of 9 m from the deck of the Liberty experiment'' because it evaluated whether these crabs Ship, a large sunken ship ϳ10 km from Radio Island affected coral growth by reducing the load of fouling (34Њ41Ј10Љ N, 76Њ43Ј30Љ W). organisms recruiting to, and growing directly on, the coral. In the second experiment, corals were attached Field surveys to concrete blocks placed on the jetty. We term this the We assessed which seaweeds might compete with ``encroachment experiment'' because it examined Oculina in the ®eld by determining the species with whether crabs affected coral growth by mediating in- which it commonly co-occurs on a variety of natural teractions with encroaching benthic organisms growing and arti®cial hard substrate communities. Three types on the blocks as well as those growing directly on the of sites were sampled, including an inshore rock jetty coral. (Radio Island Jetty, 3 m deep), two nearshore natural In the fouling experiment, performed from Septem- rock ledges (10 km from shore, 17 m deep), and ®ve ber 1994 to May 1995, we fastened a single coral (mean offshore outcrops (40 km from shore, 27 m deep). The size ϭ 229 g) to each of 20 stakes, then placed a single natural reefs consisted of rock ledges with a vertical Mithrax forceps on 10 of the corals, and left the other relief of ϳ3 m. The ¯ora and fauna at these natural 10 vacant. At the end of the experiment we removed reefs are generally similar to that described previously all epibionts from the coral, sorted them into gross for Radio Island (see Methods: Study sites), with the taxonomic categories, and dried them in an oven at exception that the offshore sites have greater proximity 65ЊC for 48 h, before weighing to the nearest milligram. to the warm waters of the Gulf Stream, and thus support After removal of epibionts, corals were reweighed to an increased number of tropical species. To determine measure growth. Because corals are modular organ- patterns of abundance of sessile organisms, a 50 ϫ 50 isms, and growth involves the production of new mod- cm quadrat ®tted with a mono®lament grid of 100 ran- ules (polyps), growth can be considered a direct mea- dom points was placed at 3-m intervals along a hap- sure of ®tness (Buss 1985). We analyzed crab-occupied hazardly located transect at each site. The plant or an- and unoccupied corals for differences in epibiont load imal under each point was identi®ed and recorded, as and growth rate using an unpaired t test. Because some was the total number of coral colonies within each corals were lost due to storms, and some crabs dis- quadrat. appeared from their corals during the experiment, our We determined the composition of the decapod crab ®nal sample size for analysis was six corals with crabs community associated with Oculina by examining hap- and eight without crabs. hazardly selected coral heads from several North Car- In the encroachment experiment, which ran from Au- olina sites. We removed individual corals from two gust to November 1996, we transplanted 30 pairs of separate locations at the Liberty Ship, sealed them in corals to Radio Island Jetty where they were grown on plastic bags underwater, and returned them to the lab- ¯at cement blocks (39 ϫ 19 ϫ 4 cm) for 102 d. Each oratory for examination. To broaden our survey without block with a coral was af®xed to a 39 ϫ 19 ϫ 19 cm 2088 JOHN J. STACHOWICZ AND MARK E. HAY Ecology, Vol. 80, No. 6 cinderblock sunk 8 cm into the sand between rocks of brown algae Padina gymnospora, Dictyota menstru- the jetty. Blocks were arranged in pairs within 1 m of alis, Dictyota ciliolata, and Sargassum ®lipendula, and each other, and pairs of blocks were spaced by at least the red algae Hypnea musciformis, Chondria dasy- 2 m. Within a pair, a crab was added to one block but phylla, and Gracilaria tikvahiae. We placed each crab not the other. Half of the pairs were placed at 2.0 m (N ϭ 22) in a separate 0.5-L bowl with four 1 cm depth (shallow site; N ϭ 15 pairs) and half were placed diameter holes to allow for ¯ow-through seawater. Each at 6.0 m (deep site; N ϭ 15 pairs). The blocks to which bowl with a crab held a 200±250 mg piece of all eight the corals were attached had been placed in the ®eld seaweed species. As a control for changes in seaweed at the shallow and deep sites for 10 wk prior to the mass unrelated to herbivory, 22 identical bowls without start of the experiment to allow a natural fouling com- crabs contained same-sized pieces of the same species munity to develop. At least once a week throughout of seaweed. Within each replicate pair of bowls, treat- the course of the experiment, each coral was checked ment and control pieces of algae were taken from the for crabs; missing crabs were replaced and new colo- same algal thallus. After 33 h, each seaweed was blot- nizers were removed to maintain treatments and con- ted dry with a paper towel and reweighed. trols. Mean retention of crabs was 80% between mon- To calculate net mass loss for each algal species due itoring intervals (see Results). We thus avoided using to crab feeding in the choice assays, we corrected for cages to maintain treatments, eliminating potential ar- mass changes unrelated to herbivory using the formula, tifacts associated with reduced ¯ow, light, and abun- [Ti ϫ (Cf/Ci)] Ϫ Tf, where Ti and Tf are the initial and dance of large consumers. ®nal masses of the seaweed portion in the container To monitor the effect of crabs on the benthic com- with a crab and Ci and Cf are the initial and ®nal masses munity, we recorded the percent cover of benthic or- of the seaweed portion in the paired control. Because ganisms on each block every 4 wk using a metal frame the amount of each species consumed may depend on the size and shape of the block that was ®tted with a other available choices (i.e., the factors are not inde- mono®lament grid of 100 points. We placed the frame pendent; cf. Peterson and Renaud 1989), we analyzed over a block and recorded the seaweed or invertebrate choice data using the nonparametric Friedman's test species beneath each point; unoccupied points were (see Alldredge and Ratti 1986, 1992, Roa 1992). We recorded as bare substrate. After 102 d in the ®eld, used the same methods to assess the feeding prefer- corals were collected, cleaned, and reweighed, and the ences of the majid crab Libinia dubia (N ϭ 19), and benthic community growing on the blocks was har- the xanthid crab Panopeus herbstii (N ϭ 18) to see if vested. Prior to removal of the community, each block they could also function as effective cleaners of Ocu- was divided into three equal-sized sections: the middle lina. third of the block immediately adjacent to the coral, As a contrast for our crab assays, we determined and the outer third on each side. The outer thirds were feeding preferences of larger omnivores that commonly pooled and contrasted with the middle third to deter- co-occur with the crabs: the sea urchin Arbacia punc- mine if the crabs' impact on community biomass was tulata and the pin®sh Lagodon rhomboides. Urchin as- restricted to the area adjacent to the coral. Because we says were conducted in a similar manner to the crab were not interested in interactions among times of sam- assays, except in larger containers (1.4 L) with larger pling, we analyzed percent cover data separately for pieces of seaweed (700±800 mg). Ulva could not be each sampling date using a two-factor ANOVA with used in the urchin assay because it was not available depth and crab presence as ®xed factors. We adjusted in suf®cient quantities. We tested pin®sh feeding pref- ␣ for these tests using the Bonferroni correction (␣ϭ erences by offering a choice of seaweeds to 12 indi- 0.01) to avoid in¯ating our Type I error rate due to vidual ®sh isolated in separate ¯ow-through aquaria. nonindependence of cover measurements across time. A 40-L aquarium was divided in half by a piece of Coral growth was also analyzed by two-way ANOVA cloth mesh (0.5 cm diameter), and a pin®sh was placed with ®xed factors. Community biomass (dry mass per in one of the two halves. We placed 200±250 mg pieces square centimeter) was analyzed separately for shallow of each of the eight seaweeds between the strands of 0.25 m long pieces of weighted polypropylene rope, and deep sites using ANOVA with position on the block and placed a rope in the half of each aquarium holding and crab presence as ®xed factors. Post hoc compari- a pin®sh. As a control for changes in algal mass un- sons for each ANOVA, where appropriate, were made related to herbivory, we placed equivalent ropes, with using Ryan's Q test (Day and Quinn 1989). pieces of the same species of algae, in the half of each Whole-plant feeding assays aquarium that did not have a pin®sh. Changes in mass due to herbivory were calculated and differences be- To determine if Mithrax forceps readily consumed tween species analyzed using the methods outlined for seaweeds that co-occurred with Oculina, we offered the crab assay. individual crabs a simultaneous choice of eight com- mon seaweeds in laboratory experiments. Each of these Assays with prey chemical extracts seaweeds occurs in shallow waters of North Carolina To test whether feeding preferences observed in in the early summer: the green alga Ulva rigida, the whole-plant assays were related to plant secondary September 1999 MUTUALISM AND CORAL PERSISTENCE 2089 chemistry, we fed crabs (Mithrax and Panopeus) and vores did not feed or ate all of both foods between urchins (Arbacia) arti®cial foods containing the lipo- monitoring intervals, then that replicate was excluded philic crude extract of each algal species using a meth- from analysis because it provided no information on od modi®ed from Hay et al. (1994). Extracts of each relative palatability of the foods. The effect of extracts alga were obtained by grinding a known fresh volume on feeding was analyzed using a paired t test. of each species in a blender with 2:1 dichloromethane : methanol. Solids were ®ltered and solvents removed Predation on crabs in the ®eld by rotary evaporation. Water soluble materials in this To determine if association with Oculina reduced extract were removed via ethyl acetate/water partition predation on Mithrax, we tethered crabs at Radio Island and discarded. We did not test the water soluble portion Jetty either with or without access to a coral. Fifteen of the extract for deterrent effects on feeding because cm long tethers of mono®lament ®shing line were af- (1) the herbivores fed slowly, and water soluble ma- ®xed to crab carapaces using super glue according to terials would likely have leached from the arti®cial methods in Stachowicz and Hay (1996). The free end food before the completion of the assay, thereby com- of the tether was tied to galvanized nail, which was promising the results of these tests; and (2) previous driven into the substrate. Crabs with and without access assays of lipophilic and water soluble extracts from to a coral were paired within 0.5 m of each other; marine algae in this region have indicated that feeding separate pairs were spaced by at least 2 m. Each tether is commonly affected by the lipophilic extract, but rare- was checked after 1 and 24 h to see if crabs were still ly by the water soluble extract (Bolser and Hay 1996). present. We analyzed these data using Fisher's exact The arti®cial food was made by freeze-drying the test. Although these crabs are mobile, their typical de- palatable alga Ulva, grinding it to a ®ne powder, mixing fensive response is not to ¯ee, but rather to remain it in an agar base, and forming the mixture onto a strip motionless and hold tightly to the substrate (J. Sta- of window screen. The screen provided a matrix to hold chowicz, unpublished data and observations); thus we the food, as well as an internal grid that allowed us to believe that tethering is an acceptable method for test- quantify the amount eaten by counting squares from ing the refuge hypothesis. which the food had been removed (Hay et al. 1998: As an additional test of the refuge bene®ts of the Fig. 2). To make the food, we mixed 2.0 g of dry Ulva coral at a different site, and to ensure that our results in 5 mL of distilled water with 0.36 g of agar dissolved from the previous experiment were not artifacts of the in 13 mL of boiling distilled water. This recipe yields tethering process (Peterson and Black 1994), we placed 20 mL of arti®cial food with a water content of 90%, untethered crabs at the Liberty Ship either with or with- similar to that of the seaweeds being tested (J. Sta- out access to a coral, and observed them over a 2-h chowicz, unpublished data). Algal extracts were added period. Each pair of crabs (one with and one without to the food volumetrically by dissolving the lipophilic access to a coral placed 1 m apart) was observed by a crude extract from 20 mL of seaweed in anhydrous scuba diver from a distance of 2 m for ϳ15 min or ether, and adding this solution to the 2 g of dry Ulva until the crabs had been consumed. We recorded the powder in a small ¯ask. Enough ether was added to length of time from placement of a crab until its con- cover the powder with liquid. The solvent was then sumption, as well as the species of the predator. After removed by rotary evaporation, resulting in a uniform 15 min, the location of surviving crabs was marked to coating of the extract on the algal particles. Control allow them to be relocated; crabs were marked with a foods were treated identically, but without the addition small drop of super glue to allow us to distinguish them of extract to the ether. We also tested the effect of from other crabs in the ®eld. Two hours after initial lipophilic extracts from several invertebrates (Oculina placement, we rechecked any crabs that had survived arbuscula, Eudendrium carneum, and Bugula neritina) the initial 15-min period. We analyzed for differences on feeding by Mithrax by incorporating these extracts in the frequency of consumption of crabs with and into an arti®cial food comprised of freeze-dried com- without access to a coral using Fisher's exact test. mercial ®sh food using the same procedure outlined for the seaweed chemical extract assays. For a detailed Nutritional bene®ts to the crab description of the preparation of arti®cial foods, see To determine if crabs use factors other than protec- Hay et al. (1994, 1998). tion from predators in selecting a habitat, we offered The sections of window screen holding the arti®cial individual Mithrax a choice between associating with foods with and without extracts were cut into pieces a live or a dead coral of similar size and structural measuring 10 ϫ 10 squares, and offered together to complexity. Tissue was stripped from the ``dead'' coral individual animals in ¯ow-through containers. Exper- using a high-pressure jet of fresh water; we then rinsed iments were monitored regularly, and feeding was al- each coral in fresh water, and placed them in running lowed to continue until either (1) over 50% of either seawater for 24 h. In a 10-L tub, we placed equal-mass the treatment or control food was eaten; or (2) the heads of live and dead corals (means Ϯ 1 SE, live ϭ termination of the experiment (for replicates with low 211.8 Ϯ 13.25 g, dead ϭ 211.1 Ϯ 10.14 g; N ϭ 20, P rates of feeding, usually after 12±24 h). If the herbi- ϭ 0.967, paired t test). Thus, the two choices were 2090 JOHN J. STACHOWICZ AND MARK E. HAY Ecology, Vol. 80, No. 6 equivalent with the exception of the presence of live coral tissue. We placed a single crab in the center of the tub, equally distant from the live and dead coral, and monitored its habitat choice after 0.25, 12, 18, and 24 h. We analyzed crab distribution on live and dead corals (N ϭ 20) at each time interval using a G test. To determine if crabs might be feeding on mucus or other materials from the surface of the corals, we dyed live Oculina (N ϭ 7) by holding them for 10 min in baths of ®ltered seawater containing 0.57 g/L of neutral red. Seven control corals (unstained) were held in equivalent baths of ®ltered seawater without neutral red. Corals were rinsed brie¯y in fresh seawater to remove unbound dye and placed individually into ¯ow- through containers, each with a single crab. Crabs were allowed to feed on stained or unstained corals for 24 h, and we then analyzed crab feces for the presence of the stain. Crab feces were collected from each con- tainer, weighed, and extracted with 2.5 mL acetone. Extracts were ®ltered through a plug of glass wool to remove solids, then solvents were removed using a slow stream of N2 gas. The dry extract was then dis- solved in 2.5 mL distilled water and absorbance mea- sured at 530 nm (the wavelength of maximum absorp- tion for neutral red) in a Spectronic 21D spectropho- tometer (Spectronic Instruments, Incorporated, Roch- ester, New York). The relative absorbance of fecal extract from crabs on stained vs. unstained corals was compared using an unpaired t test. We also made direct FIG. 1. Coral and seaweed abundance. Bars represent observations of crab behavior on live corals at night mean percent cover of seaweed or number of corals per 0.25- with video cameras under red light, which did not in- m2 plot. Error bars represent 1 SE. Nearshore reefs are natural terfere with their nocturnal behavior (white light hardbottom sites 17 m deep and 10 km from shore; offshore caused them to hide). reefs are 27 m deep and 40 km from shore (see Table 1). To assess whether access to live corals affected crab growth, we raised individual crabs in 1500-L outdoor mesocosms for 6 wk on both live and dead corals. was determined to allow us to pair the crabs on the Un®ltered seawater from nearby Bogue Sound entered live and dead corals within a replicate by initial size the mesocosms through a wave generator that produced and sex. Cage sides and tops were cleaned weekly to water movement conditions similar to those encoun- prevent excessive fouling and sediment accumulation, tered in the ®eld. Because these tanks were located but corals and cage ¯oors were not scrubbed; rather, outside and used un®ltered seawater, physical condi- they were allowed to develop an epibiotic community tions in the mesocosms were similar to, and varied on which the crabs could feed. Thus, crabs on dead with, conditions in the ®eld. Within each mesocosm, corals were not starved, and this experiment tested individual crabs were raised in 39 ϫ 19 ϫ 24 cm rect- whether crabs derive a greater nutritional bene®t from angular vexar cages (0.5 cm mesh) each of which con- the coral than they obtain from the natural fouling com- tained a ¯at concrete slab on which was placed either munity. We compared changes in wet mass and cara- a live or a dead coral (N ϭ 13 for live and dead corals). pace width for crabs grown on live vs. dead corals using Using a LICOR LI-193SA light meter attached to a LI- a paired t test, with separate analyses for males and 1000 data logger (LICOR, Lincoln, Nebraska), we de- females due to the large difference we found in growth termined that the vexar used in making the cages rate between sexes. screens out 50% of ambient light. We further reduced RESULTS the level of incident light to 25% of surface irradiance by placing an additional sheet of vexar across the entire Field surveys mesocosm. This reduced light levels inside the cages Corals were common at a depth of3moncoastal below the maximum levels that may naturally be en- rock jetties and at 17 m on nearshore reefs where water countered by corals and crabs under typical ®eld con- was turbid, but were rarer on offshore reefs at 27 m ditions. Prior to the experiment, crabs were weighed where water was clear (Fig. 1). Oculina was the only (blotted wet mass), measured (carapace width), and sex coral recorded in any of the quadrats. The seaweed September 1999 MUTUALISM AND CORAL PERSISTENCE 2091

TABLE 1. Composition of decapod crab fauna on Oculina arbuscula in North Carolina.

Depth Mithrax Mithrax Petrolisthes Site Location N (m) forceps pleuracanthus galathinius Xanthidae Liberty Ship 1 34Њ41Ј10Љ N, 76Њ43Ј29Љ W 24 9 1.42 (0.195) 0 (0) 1.25 (0.367) 0.333 (0.177) Liberty Ship 2 34Њ41Ј10Љ N, 76Њ43Ј30Љ W 50 9 0.760 (0.110) 0.061 (0.031) 0.500 (0.115) 0.260 (0.080) Inshore Reef 1 34Њ06Ј05Љ N, 77Њ45Ј02Љ W 58 17 0.400 (0.088) 0.086 (0.037) 0 (0) 0 (0) Inshore Reef 2 34Њ05Ј29Љ N, 77Њ40Ј30Љ W 81 17 0.321 (0.058) 0 (0) 0 (0) 0 (0) Offshore Reef 34Њ01Ј06Љ N, 77Њ36Ј00Љ W 8 27 0.500 (0.189) 0 (0) 0 (0) 0 (0) Note: Values are mean number of crabs per coral; standard errors are given in parentheses.

community at all sites was dominated by brown algae. At sites where corals were most abundant, Sargassum was the dominant seaweed, with Dictyota and Padina also being common (Fig. 1). Surveys of the abundance of crabs in Oculina heads from three offshore sites in North Carolina indicated that Mithrax forceps was the most common crab on these corals (Table 1). This crab occurred at densities between 0.32 and 1.42 crabs per coral. The other majid found in our surveys (Mithrax pleuracanthus) was far less common, occurring at a maximum density of one crab per 10 corals at the 10-km reef. Neither the lone porcellanid species found in our samples (Petrolisthes galathinius) nor the xan- thids occurred as commonly as Mithrax forceps. Ad- ditionally, although the xanthid and porcellanid crabs were common at the two locations on the Liberty Ship, they occupied no corals on the three natural reefs that we sampled (Table 1).

Field manipulations In the fouling experiment, corals occupied by Mith- rax forceps grew 10 times faster than unoccupied col- onies (P ϭ 0.008, Fig. 2A) and accumulated only one- seventh of the fouling organisms (P ϭ 0.0002, Fig. 2B). Seaweeds (primarily Codium and Ectocarpus) formed a small component of the overgrowth on corals without crabs during this fall±spring experiment; most overgrowth was due to invertebrates, particularly co- lonial and solitary ascidians (Botryllus, Styela), sea anemones (Aiptasia), and barnacles (Balanus spp.). Corals without crabs did not show a change in mass (i.e., growth) that was signi®cantly different from zero (P ϭ 0.409, one sample t test). Given the large dif- ference in the abundance of fouling organisms on corals with and without crabs, we expected greater coral mor- tality among colonies without crabs, so we used a one- tailed Fisher's exact test to evaluate this hypothesis. Corals without crabs did exhibit greater mortality (Fig. 2C, P ϭ 0.051), as three of the eight coral colonies without a crab experienced total mortality and three sustained partial mortality (i.e., areas of the coral where FIG. 2. Fouling experiment (September±May): (A) living polyps had been killed), whereas only one of the growth (% change in wet mass/mo); (B) fouling (dry mass six corals with crabs exhibited even partial mortality. of epibionts as a percentage of host wet mass); and (C) mor- In shallow, well-lit habitats where algae dominate, tality of corals with and without Mithrax forceps. In panels Mithrax was especially important in defending corals (A) and (B), values are means, error bars represent 1 SE, and statistical analysis is by unpaired t test. In panel (C), analysis from algal overgrowth (Figs. 3±5). In the encroachment is by Fisher's exact test. experiment, Mithrax enhanced coral growth and de- 2092 JOHN J. STACHOWICZ AND MARK E. HAY Ecology, Vol. 80, No. 6

FIG. 3. Total percent cover (mean Ϯ 1 SE) of all organisms on blocks from the encroachment experiment (August± November, 1996). Results of separate ANOVAs for each date are given on the ®gure. N for the ®rst sampling date was 15; N for all remaining dates was 14. Letters indicate signi®cant (P Ͻ 0.05) among-treatment differences in cover at that time period. The arrow beneath the x-axis indicates the occurrence of Hurricane Fran. creased the biomass and cover of the benthic com- there was a nonsigni®cant trend toward a decrease in munity surrounding corals on the shallow, but not the community cover on blocks with crabs at the shallow deeper blocks. After just 20 d, crabs had depressed total site, and by late October (day 76) this effect was sta- cover of organisms (community cover), relative to con- tistically signi®cant (see Fig. 3). Because of the hur- trols, on the shallow blocks, while there was never a ricane-generated disturbance, our data may underesti- difference between corals with and without crabs on mate the normal cumulative impact of these crabs at the deep blocks (␣ϭ0.05, Fig. 3). This was not a the shallow site. function of differential retention of crabs because site Crabs appeared to be indiscriminate removers of ®delity did not differ between the shallow and deep fouling organisms; although they signi®cantly reduced location, as 79.4 Ϯ 3.7 and 76.2 Ϯ 5.2% of crabs placed the total cover of benthic organisms, they had no effect on corals were still present each time corals were on species composition. There were no signi®cant dif- checked at the shallow and deep sites, respectively ferences in the relative cover (percentage of total cover) (7±10 d intervals, N ϭ 11 different determinations dur- of any species between crab and no-crab treatments for ing this experiment; P ϭ 0.609, paired t test). At every a given date and sampling depth (paired t tests, P Ͼ sampling period where data could be taken at both 0.05, Fig. 4). Shallow blocks were consistently dom- depths, there was an interaction between depth and inated by the brown seaweeds Dictyota menstrualis and treatment, re¯ecting the fact that crabs depressed total Sargassum ®lipendula, with occasional red algae in the cover in shallow water (P Ͻ 0.05) and slightly en- hanced it in deeper water (nonsigni®cant trend, P Ͼ understory (Hypnea and Chondria). During one sam- 0.05, Fig. 3). The large decrease in percent cover on pling period, the red alga Spyridia hypnoides was found the shallow blocks both with and without crabs around loosely snagged onto several corals, apparently via de- day 30 was associated with Hurricane Fran. Rough seas tachment and drift of adult algal fronds. A shift from during this period removed much of the benthic com- a Dictyota-dominated to a Sargassum-dominated com- munity from the substrate both on the blocks and on munity occurred between day 10 and 40 (Fig. 4), as- the surrounding reef, and destroyed one replicate at sociated with both decreasing water temperatures and each depth. Additionally, immediately following the the occurrence of the hurricane. The arborescent bryo- storm the water remained turbid for several weeks, zoan Bugula neritina also increased in abundance later probably slowing algal growth and interrupting the crab in the season. Seaweeds rarely grew at the deep site, treatment effect for ϳ1 mo. By early October (day 53) where the blocks were consistently dominated by a low September 1999 MUTUALISM AND CORAL PERSISTENCE 2093

FIG. 4. Relative cover (mean Ϯ 1 SE) of dominant species or groups on blocks in the encroachment experiment. Paired t tests between blocks with and without crabs at each depth for each date indicated no signi®cant effects of crabs on relative cover of seaweeds or invertebrates. Sample sizes are as in Fig. 3. absolute cover of Bugula and the hydroid Eudendrium depth P ϭ 0.001, interaction P ϭ 0.232; see Fig. 5C carneum. for post hoc tests at ␣ϭ0.05). Thus crabs signi®cantly At the shallow site, crab impact on community cover bene®ted corals only at shallow depths where seaweeds was localized to areas immediately around the coral. occur (Fig. 4) and total cover is high (Fig. 3). Crabs reduced total community dry mass and there was reduced dry mass in the middle of the blocks compared Feeding preference assays to the outer portions (P ϭ 0.013 and 0.005, respec- In assays with whole seaweeds, Mithrax was a less tively), but there was no signi®cant interaction between discriminating feeder than the pin®sh Lagodon rhom- these factors (P ϭ 0.190, Fig. 5A). Although we may boides, the urchin Arbacia punctulata, or the crabs have had insuf®cient power to detect a signi®cant in- Panopeus herbstii and Libinia dubia (Fig. 6). Mithrax teraction between crab presence and location on the preferred Dictyota menstrualis over most other species, block in the full ANOVA, total community dry mass but this crab consumed large amounts of all species on blocks with crabs was three times greater on the with minimal distinction among species (Fig. 6C). In outer portions of the blocks than in the middle (Fig. contrast, the ®sh, urchin, and other crabs strongly 5A, Ryan's Q test, P Ͻ 0.05), whereas community bio- avoided brown seaweeds, and consumed primarily red mass did not differ between the middle and the outer and green seaweeds such as Ulva, Hypnea, Gracilaria, portions of blocks without crabs. On the deep blocks, and Chondria. Pin®sh preferred Hypnea, but also con- neither crab presence nor location on the block affected sumed signi®cant amounts of Ulva and Chondria (Fig. community biomass, and there was no interaction be- 6A). Urchins consumed Gracilaria, Hypnea, and Chon- tween these factors (P ϭ 0.372, 0.132, and 0.406, re- dria in large amounts (Fig. 6D). Other than Mithrax, spectively; two-way ANOVA, Fig. 5B). Apparently, in only Libinia dubia consumed signi®cant quantities of shallow waters dominated by seaweeds the feeding ac- any brown seaweeds, eating Padina at levels not sig- tivities of these crabs result in a halo of decreased ni®cantly different from Chondria (Fig. 6B). However, biomass immediately surrounding their host; this effect both Libinia and Panopeus strongly avoided consum- is not apparent in deeper waters where seaweeds are ing Sargassum and both species of Dictyota (Fig. 6B rare and benthic invertebrates more common (Figs. 4 and E). Thus Mithrax was the only species that readily and 5). Correspondingly, in shallow water corals with consumed the wide variety of brown seaweeds that crabs grew 65% more than corals without crabs, while commonly co-occur with Oculina (Fig. 1). there was no detectable effect of crabs on coral growth The proximate mechanism for the broad diet of Mith- at the deep site (two-way ANOVA: crab P ϭ 0.023, rax appears to be its resistance to chemical deterrents 2094 JOHN J. STACHOWICZ AND MARK E. HAY Ecology, Vol. 80, No. 6

species on the blocks with corals and on nearshore reefs (Dictyota, Sargassum) are chemically defended from grazers other than Mithrax. Bene®ts to the crab from associating with Oculina Crabs tethered directly to the jetty at Radio Island were more likely to be consumed than crabs tethered near corals both after 1 and 24 h (Fig. 8, P ϭ 0.0001 and 0.008, respectively), indicating that the association reduces predation on the crab. Similarly, in our teth- erless experiment at the Liberty Ship, crabs without access to a coral were more likely to be consumed than those with access to a coral after both 15 min and 2 h (Fig. 8, P Ͻ 0.0001). Our observations of these non- tethered crabs indicated that they often survived for several minutes in the open by remaining motionless, but as soon as they moved, they were attacked and rapidly consumed. The mean survival time of the 11 untethered crabs placed outside corals that were even- tually consumed was 3 min 7 s (3:07). Two crabs with- out access to a coral were not observed to be consumed by ®shes; one reached the shelter of a coral in 1:01, and the other was not consumed after being in the open for 16:41, but was missing when we checked the point of its release after 2 h. All of the crabs placed on a coral remained intact after 2 h. The black sea bass (Centropristis striata) was the primary consumer of untethered crabs at the Liberty Ship (10 of 11 acts of predation observed); spottail pin®sh (Diplodus hol- brooki) were also frequently observed attacking crabs, and on one occasion consuming them. When given a choice between live and dead Oculina heads, crabs initially did not discriminate between the two (P ϭ 0.527), but gradually moved to live corals such that after 12, 18, and 24 h, more of the crabs FIG. 5. Effects of Mithrax forceps on community biomass occupied live corals than dead corals (Fig. 9, P Յ and coral growth at the end of the encroachment experiment. 0.001). In mesocosm experiments, crabs grew faster on Community biomass is given as dry mass per cm2 (mean ϩ live corals than on dead corals, but this effect was sex 1 SE) for (A) shallow and (B) deep sites. Analyses were by two-factor ANOVA with position on block (middle vs. outer dependent. When measured as change in carapace portion) and crab presence as ®xed factors with N ϭ 14 for width or as change in wet mass, female Mithrax grew each treatment combination. (C) coral growth is expressed as faster on live than on dead corals (Fig. 10, paired t the total percentage change in wet mass over the course of tests P ϭ 0.010 and P ϭ 0.029), while males grew the experiment (mean ϩ 1 SE). Analysis was by two-factor ANOVA with depth and crab presence as ®xed factors and equally well on live and dead corals (P ϭ 0.421 and N ϭ 14. Different lowercase letters above histogram bars P ϭ 0.818). within a panel indicate signi®cant differences (P Ͻ 0.05). This increased growth rate among crabs on live cor- als may be due to supplemental nutrition obtained by consuming coral mucus. Both male and female crabs produced by these seaweeds. None of the extracts tested observed at night under red light repeatedly scraped signi®cantly deterred feeding by Mithrax (P Ͼ 0.05), and plucked at the surface of the coral with their chelae, and the extract of Padina actually stimulated feeding then brought the chelae to their mouth and moved their (Fig. 7A, paired t test, P ϭ 0.0003). In contrast, Pan- maxillipeds as they do while feeding, yet we observed opeus was signi®cantly deterred by extracts from both no obvious damage to the corals as a result of these Dictyota species (Fig. 7B), and there was a nonsignif- activities. Crabs of both sexes placed on corals stained icant trend (P ϭ 0.080) for deterrence in the extract of with neutral red produced dark red feces within 24 h. Padina. Similarly, four of the six extracts tested (D. The relative absorbance of extract from these feces at menstrualis, D. ciliolata, Sargassum, and Hypnea) sig- 530 nm was 0.625 Ϯ 0.129 while that from feces of ni®cantly deterred feeding by sea urchins (P Ͻ 0.05, crabs on unstained corals was 0.046 Ϯ 0.008 (means paired t test, Fig. 7C). Thus, several of the dominant Ϯ 1 SE; N ϭ 7; P ϭ 0.001, unpaired t test). There was September 1999 MUTUALISM AND CORAL PERSISTENCE 2095

FIG. 6. Multi-choice feeding assays. Amount consumed over the duration of the assay (mean ϩ 1 SE) for (A) the pin®sh Lagodon rhomboides; (B) the spider crab Libinia dubia; (C) Mithrax forceps; (D) the sea urchin Arbacia punctulata; and (E) the mud crab Panopeus herbstii. Analyses were by Friedman's test. Within each panel, histogram bars that do not share a lowercase letter indicate signi®cant differences between means (P Ͻ 0.05). no difference in the dry mass of feces produced by croaching seaweeds (Figs. 3 and 5A). Seaweeds or in- crabs on stained and unstained corals (P ϭ 0.774, un- vertebrates compete with corals by shading or direct paired t test) so differences in absorbance were not overgrowth (Jacques et al. 1983, Miller 1995), by al- caused by increased feeding on stained corals. Rec- lelopathy (de Nys et al. 1991), and/or by physically ognition of Oculina and initiation of scraping behavior abrading the coral (Coyer et al. 1993). Thus their re- may be chemically cued, as lipophilic crude extracts moval by crabs results in increased coral growth and from Oculina stimulated feeding by Mithrax (P ϭ survivorship (Figs. 2A, C, and 5C). Because Oculina 0.030, Fig. 11). This stimulation was not simply a con- derives the bulk of its nutrition from photosynthetic sequence of the additional nutrition found in the li- symbionts (Miller 1995), shading may have a greater pophilic extracts of all animals because extracts from impact than reduced heterotrophy, although there is Eudendrium carneum and Bugula neritina deterred, evidence for both exploitative and interference com- rather than stimulated, crab feeding (Fig. 11; P ϭ petition between Oculina and seaweeds (Miller and 0.002, and P Ͻ 0.0001, respectively). Hay 1996). In well-lit habitats, corals are slow-growing relative DISCUSSION to ¯eshy macroalgae and are thus susceptible to being The mutualistic interaction between Mithrax forceps overgrown where herbivory is insuf®cient to reduce and Oculina arbuscula may have signi®cant conse- the abundance of seaweeds (Lewis 1986, Hughes 1989, quences for the population biology of the species in- 1994). On North Carolina reefs, grazing by ®shes and volved and for benthic community structure in general. urchins can alter seaweed species composition, but These crabs protect their host from competition by re- does not reduce total biomass, so these herbivores are moving fouling epibiota (Fig. 2B) and clearing en- ineffective at facilitating coral growth (Miller and Hay 2096 JOHN J. STACHOWICZ AND MARK E. HAY Ecology, Vol. 80, No. 6

and Dictyota species, are the most common plants co- occurring with Oculina on both natural and arti®cial reefs (Fig. 1), and are thus critical targets for removal by potential mutualists. We could not directly test whether local crabs other than Mithrax forceps could prevent overgrowth of corals in the ®eld because in- dividuals of these species would not remain on corals for longer than one day. However, because only Mith- rax readily consumes the chemically noxious seaweeds that co-occur with Oculina, it alone appears capable of adequately mediating competition between Oculina and seaweeds in the ®eld. Refuge from predation rather than nutrition appears to be the most important selective factor driving crabs into this association. Although there may be potential problems with tethering experiments (cf. Peterson and Black 1994), experiments with and without tethers in two different sites bracketing the range of coral and crab densities in the ®eld both support the conclusion that crabs gain a refuge from predation by associating with Oculina. Although crabs derive additional nutri- tional bene®ts from associating with live Oculina, only gradually over a 12±24 h period did individual Mithrax express a preference for live corals, suggesting that this choice was made only once predation risk was deter- mined to be low. That a refuge from predation may drive habitat selection by Mithrax would not be sur- prising, given that predation pressure on small herbi- vores is often intense. Predation refuges may com- monly drive the formation of associations with chem- ically or morphologically defended plants or animals (see reviews in Hay 1992, 1997). We suggest that es- cape from predation may have driven the initiation of this association as a fairly loose interaction, while the more specialized trophic component (Fig. 10) and chemically mediated stimulation of feeding (Fig. 11) may have arisen later. The production of dietary sup- plements may help attract and retain facultative sym- bionts such as Mithrax, securing long-term protection against encroaching competitors for the coral. The increased growth of female crabs on live corals is likely derived from ingesting coral mucus, which is FIG. 7. Effects of seaweed chemical extracts on feeding commonly rich in lipids and other high-energy organic by (A) Mithrax forceps; (B) Panopeus herbstii; and (C) Ar- compounds (Coles and Strathmann 1973, Benson and bacia punctulata. Analyses were by paired t test, and N is given at the base of each pair of bars. Arrows pointing up Muscatine 1974, Ducklow and Mitchell 1979). Many indicate that an extract signi®cantly stimulated feeding, and coral-associated crustaceans, including several from arrows pointing down indicate that an extract signi®cantly Oculina arbuscula, are known to use coral mucus as a deterred feeding (P Ͻ 0.05). food source (Knudsen 1967, McCloskey 1970, Castro 1976). The coral Pocillopora damicornis produces fat bodies held within its polyps that are consumed by 1996). In contrast, Mithrax reduces local community mutualistic crabs in the genus Trapezia (Stimson 1990). biomass (Fig. 5A), but causes no change in species Although we did not look for them in Oculina, lipid composition (Fig. 4). This is likely because Mithrax droplets occur in the mucus of many corals and may exhibits little selectivity in food choice, consuming a be bound in vesicles (Crossland et al. 1980) allowing wide variety of seaweeds including those avoided by, for easy harvest and use by mutualists. The frequently and chemically defended from, other herbivores (Figs. observed plucking behavior of Mithrax on live Oculina 6 and 7; also see Hay et al. 1987, 1988, Cronin and suggests that this coral may produce similar rewards Hay 1996). These brown algae, particularly Sargassum to attract and retain mutualists, just as numerous ter- September 1999 MUTUALISM AND CORAL PERSISTENCE 2097

FIG. 8. Predation on Mithrax forceps with vs. without access to a coral. The assay at Radio Island Jetty used crabs on mono®lament tethers, whereas the assay at the Liberty Ship used un- tethered crabs observed directly by divers. Analysis was by Fisher's exact test. N is given at the base of each pair of bars.

restrial plants produce food rewards for their ant mu- males (Jormalainen and Toumi 1989, Merilaita and Jor- tualists (e.g., Janzen 1966, reviewed by Beattie 1985). malainen 1997). Thus there may be increased selection The potential caloric value of coral mucus and fat bod- for female Mithrax to take advantage of host-associated ies relative to seaweeds suggests that these could pro- nutritional supplements. vide good dietary supplements to herbivores like Mith- rax. Community consequences of protective mutualisms We could ®nd no previous reports of differential use On temperate reefs, where grazing rates are low and of coral products by male and female symbionts, and seaweed biomass is high (Gaines and Lubchenco 1982, it is unclear why male Mithrax did not bene®t from Hatcher and Rimmer 1985, Horn 1989, Ebeling and mucus consumption in our experiments. Although the Hixon 1991), most corals are restricted to habitats small number of male crabs used in the crab growth where seaweeds cannot grow (Miller 1998). Although experiment reduced our power to detect potential dif- 12 species of corals are known to occur in coastal North ferences in growth between males from live and dead Carolina and the adjacent waters on the continental corals, there does not appear to be any trend in the data shelf, most are restricted to deep or turbid water (Cer- that might become more apparent with increased rep- ame-Vivas and Gray 1966, MacIntyre and Pilkey 1969, lication (Fig. 10). One possible explanation for the Ruppert and Fox 1988), and only Oculina arbuscula male±female difference is that male crustaceans are commonly co-occurs with seaweeds on natural hard- generally more mobile than females, which tend to bottom reefs (McCloskey 1970, Peckol and Searles spend more time sheltering and less time foraging than 1984; Fig. 1). Oculina is also the only one of these species with a branching morphology capable of pro- tecting herbivorous symbionts like Mithrax; the other species are small tube corals (Cladocora coespidosa), encrusting or mounding corals (Siderastrea radians, Siderastrea siderea, Astrangia danae, Solenastrea hy- ades), or solitary cup corals (Bathycyathus maculatus, Dasmosmilia lymani, Monomyces fragilis, Paracyathus de®lipii). The branching morphology of Oculina and its ability to shelter herbivorous crabs like Mithrax may account for its persistence and success in seaweed- dominated temperate areas. Structurally complex organisms like branching cor- als and coralline algae may commonly harbor protec- tive symbionts that appear to suppress competitors and extend host ranges into more biologically stressful en- vironments (see e.g., Glynn 1987, Coen 1988, Littler FIG. 9. Habitat choice between live and dead Oculina arbuscula by Mithrax forceps over a 24-h period. Statistical et al. 1995, Stachowicz and Hay 1996). Additionally, analyses of the proportion on live vs. dead corals at each time several other studies have demonstrated community- period were performed using a G test (N ϭ 20 for each test). level effects of mutualisms involving structurally com- 2098 JOHN J. STACHOWICZ AND MARK E. HAY Ecology, Vol. 80, No. 6

weed community are highly localized around the host coral, Mithrax creates small patches of intense, non- selective, grazing superimposed on the background of selective grazing by more mobile herbivores like ®shes and urchins. On a landscape level, the combined effect of both types of grazing should result in a mosaic of patches with high and low algal density. Such increases in patchiness and local habitat diversity can have im- portant consequences for species diversity at both the local and regional scale (Abele 1974, Heck and Wet- stone 1977, Hay 1985, 1986, Stoner and Lewis 1985, Harrison 1997). Additionally, local reductions in plant density may alter the nature of inter- and intraspeci®c interactions among seaweeds (Schiel 1985, Paine 1990, Steneck et al. 1991), reduce the density of seaweed- associated invertebrates (Stoner and Lewis 1985, Dean and Connell 1987), and decrease the abundance and recruitment of reef ®shes (Anderson 1994, Carr 1994, Levin and Hay 1996). Thus, although the impact of small, nonselective grazers may be spatially restricted, this type of grazing clearly merits consideration in models of herbivore impact on community dynamics and local ecosystem function. Spatial and temporal variability in mutualisms Conceptual models have suggested that certain types of positive interactions will be most common where physical conditions are harsh or consumer pressure is high (Bertness and Callaway 1994). This dependence on physical or biotic conditions outside the association, which are likely to vary over time and space, makes these interactions particularly subject to variability in outcome (see e.g., Holmgren et al. 1997). Similarly, FIG. 10. Growth (mean ϩ 1 SE)ofMithrax forceps on Addicott (1984) was among the ®rst to draw attention live and dead Oculina arbuscula. Statistical contrasts of to the idea that mutualisms may be particularly im- growth were made separately for male and female crabs using paired t tests on change in (A) carapace width and (B) wet portant in areas of biotic or abiotic stress. As such, mass. N is given at the base of each pair of bars. mutualisms may exhibit even greater context depen- dency than other positive interactions because multiple stresses must be present for the interaction to be re- plex organisms in the marine environment (e.g., Vance 1978, Witman 1987, Littler et al. 1995), so this type of mutualism may be more important than is currently appreciated. These structurally complex organisms provide protective habitat for a diverse suite of organ- isms. Individual Oculina heads have been reported to support as many as 161 species, and a total of 309 species from taxa as diverse as cnidarians, mollusks, crustaceans, tunicates, and ®shes have been recorded living on, or in, the coral (McCloskey 1970). Most of these species are not found in the surrounding reef habitat, suggesting that without the corals they could become locally extinct (McCloskey 1970). By increas- ing host growth rates and/or survivorship, mutualists such as Mithrax facilitate the production and mainte- nance of biogenic structure and may therefore function as keystone species within this assemblage of host- FIG. 11. Effects of invertebrate chemical extracts on feed- associated organisms. ing by Mithrax forceps. Statistical analyses were by paired t Because the effects of Mithrax on the benthic sea- test. N is given at the base of each pair of bars. September 1999 MUTUALISM AND CORAL PERSISTENCE 2099 ciprocally positive. For example, in the encroachment interspeci®c competitors may be common where this experiment, community cover was low on the deep kind of competition is particularly intense. Continued blocks (Fig. 3) and dominated by species chemically focus on patterns of spatial and temporal variation in defended from Mithrax (Figs. 4 and 11). As a result, the outcomes of these interactions should yield a clear- Mithrax had no signi®cant impact on community cover er picture of the conditions under which mutualisms or coral growth at this depth. However, because many are (and are not) likely to play important roles in struc- of the invertebrates that co-occur with Oculina in turbid turing ecological communities. waters also grow slowly or are susceptible to con- sumption by large, mobile predators like ®shes or ur- ACKNOWLEDGMENTS chins (Sutherland 1974, Karlson 1978), symbiotic me- This investigation was funded by the National Science diation of competition may be less critical for coral Foundation through grant OCE no. 95-29784 to M. Hay and a predoctoral fellowship to J. Stachowicz, and through a Uni- growth and survival in poorly lit waters. Under these versity of North Carolina Graduate School Dissertation Fel- conditions, the interaction is best regarded as com- lowship to J. Stachowicz. Assistance underwater and in the mensal because the crab does not affect the coral, but lab throughout this study was cheerfully provided by S. Bul- continues to use it for protection from predators and lard, G. Cetrulo, E. Cruz-Rivera, M. Deal, Z. Feldman, C. presumably continues to acquire food from the coral Kicklighter, N. Lindquist, G. Safrit, and E. Sotka. Comments by M. Bertness, B. Menge, R. Peet, C. Peterson, and an anon- (although this has not been tested under low-light con- ymous reviewer improved previous drafts of the manuscript. ditions that may restrict the coral's ability to produce We are indebted to M. Miller for providing algal cover data energetic rewards for the crab). from North Carolina offshore reefs and H. Paerl for use of Despite the lack of a crab effect on coral growth and the light meter. community cover during the summer at the inverte- LITERATURE CITED brate-dominated deep site, Mithrax mediated coral Abele, L. G. 1974. Species diversity of decapod crustaceans competition with invertebrates under some circum- in marine habitats. Ecology 55:156±161. stances (Fig. 2). The abundance of the tunicates and Addicott, J. H. 1984. Mutualistic interactions in population anemones that overgrew Oculina without crabs in the and community processes. Pages 437±455 in P. W. Price, fouling experiment is controlled, to some extent, by C. N. Slobodchikoff, and W. S. Gaud, editors. A new ecol- ®shes and urchins in the summer (Karlson 1978), but ogy: novel approaches to interactive systems. Wiley Inter- science, New York, New York, USA. these predators migrate offshore or become inactive Alldredge, J. R., and J. T. Ratti. 1986. 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