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i Oecologia (1996) 105:377-387 0 &ringer-Verlag 1996 - John J. Stachowicz Mark E. Hay Facultative mutualism between an herbivorous crab and a coralline alga: advantages of eating noxious seaweeds Received: 1 May 1995/ Accepted: 1 1 September 1995 Abstract Because encrusting coralline algae rely -on herbivory or low light levels to prevent being overgrown by competitively superior fleshy algae, corallines are relatively rare in shallow areas with low rates of herbivory. In contrast to this general trend, the branching coralline alga Neogoniolithon stricturn occurs primarily in shallow seagrass beds and along the margins of shallow reef flats where herbivory on macrophytes is low. This alga apparently persists in these habitats by providing refuge to the herbivorous crab Mithrax sculptus at mean densities of 1 crab per 75 g of algal wet mass. When crabs were removed from some host corallines,, hosts without crabs supported 9 times the epiphytic growth of hosts with crabs after only 30 days. Crabs without access to a coralline alga were rapidly consumed by reef fishes, while most of those tethered near a host alga survived. These results suggest that the crabs clean their algal host of fouling seaweeds and associate with the host to minimize predation. However, to effectively clean the host, the crab must consume the wide array of macroalgae that commonly co-occur with coralline algae in these habitats, including chemically defended species in the genera Halimeda, Dictyota, and Laurencia. Crabs did readily consume these seaweeds, which were avoided by, and are chemically defended from, herbivorous fishes. Even though crabs readily consumed both Halimeda and Dictyota in whole-plant feeding assays, chemical extracts from these species significantly reduced crab feeding, suggesting that factors other than secondary chemistry (e.g., food value, protein, energy content), may determine whole-plant palatability. Having the ability to use a wide variety of foods, and choosing the most profitable rather than the least defended foods, would diminish foraging time. increase site fidelity, and allow the crab to J.J. Stachowicz . M.E. Hay University of North Carolina at Chapel Hill. Institute of Marine Sciences. 3431 Arendell St.. Morehead City NC 28557 USA, Phone: 919-726-6841, Fax: 919-726-2426. Internet: [email protected] (J. Stachowicz) [email protected] (M. Hay) function mutualistically with the host alga. Despite the obvious benefit of associating with N. stricturn, M. sculptus did not prefer it over other habitats offering a structurally similar refuge, suggesting that these crabs are not N . stricturn specialists, but rather occupy multiple habitats that provide protection from predators. Structurally complex organisms like N. stricturn may commonly suppress competitors by harboring protective symbionts like M. sculptus. It is possible that diffuse coevolution has occurred between these two groups; however, this seems unlikely because both herbivore and host appear to respond most strongly to selective pressures from predators and competitors outside this association. Key words Algal chemical defenses . Competition. Fouling . Mutualism . Plant-herbivore interaction Introduction Trade-offs between competitive ability and resistance to herbivores are well known for plants in both marine (Lubchenco and Gaines 1981; Hay 1985; Lewis 1986; Estes and Steinberg 1988) and terrestrial (Cates and Orians 1975; Connell and Slatyer 1977; Crawley 1989) systems. Herbivore-resistant plants in low-herbivory environments are often at a competitive disadvantage and may be susceptible to overgrowth by superior competitors that are vulnerable to herbivores (Hay 1981a, 1984a, 1985; Gaines and Lubchenco 1982; Steneck 1982; Carpenter 1986; Lewis 1986; Sousa and Connell 1992). When this overgrowth is epiphytic, it can harm the host plant by: (1) reducing growth through shading and competition for nutrients (Orth and van Montfrans 1984; Brawley 1992; Williams and Seed 1992), (2) increasing drag on the plant, leading to a greater possibility of dislodgment or breakage by physical forces (Sousa 1979; D' Antonio 1985), or (3) increasing the probability that the host will be consumed by large herbivores if it is overgrown by more palatable epiphytes (Wahl and Hay 1995). 378 * OECOLOGIA 105 (1996) 0 Springer-Verlag Large herbivores like fishes and sea urchins are known to have a considerable impact on marine algal communities (e.g., Hay 1981a, 1984a; Lewis 1986; Carpenter 1986), but small, less apparent grazers like amphipods, dipteran larvae, and gastropods can also alter community composition by removing fast-growing, grazersusceptible plants and epiphytes, allowing dominance by competitively inferior, grazer-resistant species (Sousa 1979; Brawley and Adey 1981; Dethier 1981; Robles and Cubit 1981; Lubchenco 1983; McBrien et al. 1983; Steneck et al. 1991). In marine systems, predation pressure is commonly high on these small grazers and can select for specialization on chemically defended plants in order to reduce encounters with, and susceptibility to, predators (Hay et al. 1989, 1990a,b; Duffy and Hay 1991a,b, 1994; reviewed in Hay 1992; Hay and Steinberg 1992). However, using a plant as both food and shelter imposes constraints on the amount of food available for consumption. If an herbivore eats too much of its host, its shelter may be compromised. Herbivores that associate with particular plants for shelter may be forced to reduce feeding on host tissue in order to maintain the integrity of the shelter. This might be accomplished by: (1) foraging away from the shelter when predators are less active, (2) lowering metabolic rates, (3) evolving alternative energy sources such as sequestered chloroplasts (Hay et al. 1989), or (4) consuming primarily epiphytes. When an herbivore restricts feeding to epiphytes, a mutualistic interaction between the host-plant and the herbivore could arise if alternative means of removing overgrowth, such as shedding of surficial cells (Moss 1982; Masaki et al. 1984; Johnson and Mann 1986) or production of allelopathic chemicals (Sieburth and Conover 1965; Schmitt et al. 1995), are not completely effective. Coralline algae are slow-growing (Littler and Arnold 1982), heavily calcified macroalgae that may be rapidly overgrown by epiphytes and other fleshy algae in the absence of herbivores (e.g., Littler and Doty 1975; Wanders 1977; Steneck 1982, 1986; Hay and Taylor 1985). These calcified algae are major components of coral reefs where herbivory is intense (Hay 1981b, 1991; Lewis 1986; Carpenter 1986; Steneck 1986), but their relative cover is generally low in habitats such as reef flats, seagrass beds, and damselfish temtories that serve as spatial escapes from intense herbivory (Hay 1985, 1991). In contrast to this general pattern, the coralline alga Neogoniolithon stricturn (Foslie) Setchell and Mason (as Goniolithon strictum in Taylor 1960) thrives on portions of shallow reef flats and in tropical grass bed habitats where herbivory is relatively low (Ogden et al. 1973; Hay 1984a,b; 1985). How N . stricturn is able to avoid overgrowth by foulers and rapidly growing macroalgae in such a low herbivory environment is unknown. Although sloughing of surficial cells by some corallines has been interpreted as an anti-fouling trait, Keats et al. (1994) have recently cast doubt on the general effectiveness of sloughing in removing overgrowth. In contrast to this possible physiological mechanism, the herbivorous crab Mithrar sculptus Lamarck. which commonly lives among the branches of N. stn'cfum,might clean its host of epiphytes much as ants remove competing plants from near their Acacia hosts (Janzen 1966). Previous work has demonstrated that these crabs keep small corals free of seaweed overgrowth (Coen 1988a). Whether these crabs can serve as effective cleaners of N. stricrum would depend, in part, on whether they can consume the wide range of seaweeds, including several chemically defended species in the genera Dictyotu, Hulimeda, and Laurencia (reviewed by Hay 1991; Paul 1992), which commonly overgrow corallines in habitats where herbivory is reduced (Hay and Taylor 1985; Lewis 1986; Momson 1988). Many studies describing apparently mutualistic associations demonstrate a tangible benefit to the host, but fail to provide direct evidence for a reciprocal benefit to the associate (Cushman and Beattie 1991). In this study, we show that not only does M. sculptus protect its host by preventing overgrowth by other seaweeds, but that the crab also benefits from the association by reduced predation. Despite the reciprocal benefits involved, this relationship is not obligate, and we argue that even diffuse coevolution (sensu Fox 1981) between coralline algae and small grazers that remove foulers is unlikely in this case, because the crab and coralline alga respond primarily to selective pressures from predators and competitors outside the association (Vermeij 1983, 1994). Methods Study site and organisms This research was conducted on several patch reef and grass bed habitats.on the seaward side of Key Largo, Florida, United States during July and August 1993 and July 1994. Coralline algae and crabs for all experiments were collected in < I m of water in a grass bed on the south and east sides of Rodriguez Key, Florida. Other algae for feeding assays were collected from a nearby mixed stand of the seagrass Thalussiu restudinurn Koenig and numerous species of algae in 1.O m of water. The crab Mithrax sculprus is a member of the family Majidae, and is commonly found from the Bahamas and Miami throughout the Caribbean to Abrolhos Islands, Brazil (Rathbun 1925). The species occurs intertidally, under rocks at low tide, and to a depth of 55 m on grass, sand, shell, or mud bottoms (Rathbun 1925; Powers 1977). Males are generally larger than females (Hartnoll 1965), but no differences in feeding preferences among sexes or crabs of different sizes have been observed (Coen 1988b). Individuals used in this study ranged from 0.40 g to 2.00 g in wet weight and 8.2 m m to 15.6 mm in carapace width. Neogoniolithon stricturn (hereafter referred to as Neogoniolirhon) is a branching crustose (i.e., not articulated) coralline alga that commonly grows in shallow water in coral reef and grass bed habitats throughout the Caribbean (Taylor 1960; Littler et al. 1981). Although the branching morphology of this species is variable (e.g., Bosence 1985), the spaces between branches are usually large enough to provide a habitat for a diverse community of invertebrates including sessile (ascidians, sponges) and mobile @tomatopods. decapod crabs) groups. Crab abundance To determine the density of crabs on Neogoniolirhon, we haphazardly collected 40 separate clusters of Neogoniolirhon from a shal- OECOLOGIA 105 (1996) 0 Springer-Verlag low (<I m) grass bed near Rodriguez Key, and placed each individually in plastic bags underwater. These were returned to the laboratory where each was inspected carefully for crabs. We recorded the wet mass of each clump and the number of Mithrar occupying it. 379 (Gmelin) Montagne. Despite a recent revision of the taxonomy of the genus Dicfyota (Hornig et al. 1992), we were not able to unambiguously assign the Diczyota to a specific species. Dasya and Padina were in limited supply and were used only in the choice assay with crabs. Because stress can affect algal palatability to herbivores (Renaud et al. 1990; Cronin and Hay in press), we minimized algal stress by placing the algae in coolers with fresh sea Fouling experiment water for transport to the lab, sorting and holding the algae in flow-through seawater tanks upon arrival (within 0.5 h of collecWe tested whether Mithrax prevents seaweed overgrowth of Neo- tion), and beginning all assays within 6 h of collection. goniofithon by removing crabs from some algal clusters and comTo determine the relative dietary preferences,of Mithrax, we paring the mass of epiphytes on algal hosts without crabs to the placed one crab in each of 20 separate 1.4-1 bowls, each of which mass of epiphytes on control clusters with crabs. We constructed a held a 60-80 mg piece of all seven seaweed species collected (i.e., floating rack that held forty 1.4-1 containers, each with four 1.2- a choice assay). As a control for changes in seaweed mass unrefatcm-diameter holes equally spaced along the wall of each container ed to herbivory, 20 bowls without crabs contained pieces of the to allow lateral exchange of water with the environment. This rack same species of seaweed. Within each replicate, treatment and was anchored in a grass bedalgal flat (1 .O m deep at low tide) on control pieces of algae were taken from the same algal thallus to the seaward side of Key Largo. The rack was deployed such that provide an accurate estimate of changes in algal mass due to facthe top of each container floated at the sea surface, and the bogom tors unrelated to the activities of the crab. After 48 h of grazing, (where the crab and coralline alga were) was 15 cm below the sur- each piece of alga was reweighed, and changes in mass of treatface. Wave action provided water movement through the holes in ment algae were compared to changes in their paired control porthe containers. We placed in each container a 70-100 g cluster of tions using a paired two-tailed t-test. Neogoniolithon that was determined by visual examination to be To determine the willingness of crabs to consume the various free of epibionts (this approximated the mean-sized cluster on seaweeds when no alternative choice was available (i.e., a nowhich we found one crab). We placed one crab in each of 20 hap- choice assay), we conducted Mithrax feeding assays in which each hazardly selected containers (the other 20 containers served as crab was offered only one species of alga. Pieces of five species of controls), and covered all containers with a 0.4 cm mesh to pre- algae (Dictyota sp., Halimeda sirnufans, and the three Luurencia vent loss of the crabs. There was no significant difference in the species) between 1.00 and 2.00 g wet weight with appropriate initial weight of the Neogoniolithon clusters with and without controls were offered to Mithrax as described previously, with the crabs (two-tailed t-test, equal variances; P = 0.8137) and treatment exception that each crab had access to only one species of alga. and control replicates were interspersed randomly in the rack. There were eight replicates for each seaweed species, and assays After 30 days, the contents of each container were removed, for all five seaweeds ran simultaneously for 48 h. We tested for sealed in individual plastic bags with seawater, and transported to significant differences in mass change in grazed versus control althe laboratory for quantification of epiphyte mass. We were able to gae for each species using the Mann-Whitney U-test. remove some of the epiphytic growth from Neogoniolithon by imTo calculate net mass loss due to crab feeding for each algal mersing each cluster in sea water and shaking vigorously for 15 s. species in the choice and no-choice assays, we corrected for Some remaining epiphytes were removed using a jet of sea water changes in mass unrelated to herbivory using the formula, from a squirt bottle (volume used = 200 ml per cluster). However, [Tix (CdC,)]- T,, where Tiand T, are the initial and final masses thorough removal of epiphytes could only be achieved by breaking of the seaweed portion in the container with a crab, and Ciand C, the cluster into pieces and manually removing them. Basal por- are the initial and final masses of the seaweed portion in the paired tions of some epiphytes remained on the more fouled host-plants control container. Preliminary data indicated that there was no reeven after cleaning. This, combined with the slow growth rate of lationship between the size of the crab and the amount of algae coralline algae in general (Adey and McKibbin 1970; Adey and consumed (see also Coen 1988b), so results are reported as milliVassar 1975; Littler and Arnold 1982; Steneck 1986), prevented us grams of alga consumed per 48 h. Data from no-choice assays from obtaining reliable estimates of coralline growth in mass over were analyzed by one-way ANOVA, but choice assays cannot be this 30-day period. For this reason, we compared only the mass of analyzed this way due to the non-independence of treatments (see epiphytes, not growth rates of Neogoniolithon, between treat- Peterson and Renaud 1989). We therefore analyzed choice data usments. ing the non-parametric Friedman’s two-way test on ranked data, The water containing the epiphytes removed from Neogoniofi- which allows for dependence among treatments, provided that rhon was filtered in a 0.5-mm nitex sieve to remove larger epi- each replicate is independent (Conover 1980; Coen 1988b). phytes, and again in a 0.2-mm nitex sieve to separate smaller epi- Among-species comparisons were made using Friedman’s multiphyte fragments. Seagrass and other obvious drift items, such as ple comparisons test (Conover 1980) with Sidak’s correction (Sobits of plastic, were removed from the filtered material, and the kal and Rohlf 1981). Preferences of reef fishes for the seaweeds used in the nomass of epiphytes dried in an oven at 65°C for 30 h, then weighed to the nearest 1 mg. To standardize the mass of epiphytes for hosts choice crab feeding assay were determined by offering all five of different size, the data were expressed as dry mass of epiphytes species to a natural assemblage of reef fishes in the field. .We as a percentage of host wet mass. To achieve homoscedasticity of placed a 5-cm-long piece of each seiweed species between the variances, the data were arcsine transformed before performing strands of a 0.5-m-long piece of biided polypropylene rope statistical analysis by an unpaired two-tailed t-test. (n = 23), and fastened these ropes at a depth of 2-3 m on Pickles Reef, near Key Largo. Grazing by reef fishes was allowed to proceed for 1.5 h, and then each species on each rope was recorded as Whole-plant palatability to crabs and fishes either still present or totally consumed (see Hay 1984a; Paul and Hay 1986 for more details of this method). Among-species differTo assess the potential of M. sculptus to be an effective cleaner of ences in the frequency of total consumption were determined by Neogoniolithon we used both choice and no-choice assays to de- contingency table analysis using the G-statistic with Sidak’s cortermine the crab’s feeding preferences for macroalgae that com- rection for multiple comparisons. monly co-occur with Neogoniolithon. We collected seven of the most abundant species growing subtidally at the site of the fouling experiment: the calcareous green alga Hulimeda simuluns Howe: Effects of algal extracts on crab feedine the lightly calcified brown alga Pudina gymnosporu (Keutzing) Sonder, and another brown alga in the genus Diccora; and the red To determine how seaweed chemical defenses might affect herbialgae Laurenciu pupiffosa (C. Agardh) Greville, L. intricatu Lam- vory, Iipophilic crude extracts of each alga were obtained by ouroux, L. poitei (Lamouroux) Howe, and Dasyu baillouviuna gnnding a known fresh volume of each species in a blender i n 2 1 380 OECOLOGIA 105 (1996) Q Springer-Verlag dichloromethane (DCM):methanol (MeOH). Solids were filtered then placed a single droplet of glue on the back of the carapace. and solvents removed by rotary evaporation. Water soluble materi- We allowed the drop to sit for about 30 s to gel, then placed the als in this extract were removed via dichloromethane/water parti- end of the monofilament line into the glue, and held it in place for tion and discarded. We did not test the water-soluble portion of the 30 s to allow the glue to set. The crabs were then paired by size extract for deterrent effects on crab feeding because (1) the crabs and each pair put in a small container full of seawater and covered feed slowly, and water-soluble materials would likely leach out of with a lid for transport. One crab of each pair was tethered such the artificial food before the completion of the assay, thereby com- that it had access to a cluster of Neogoniolirhon that we had placed promising the results of these tests; and (2) previous assays of li- on the reef, and the other was tethered within 50 cm of the first, pophilic and water soluble extracts from tropical marine algae but without access to a Neogoniolithon cluster. We monitored both have indicated that deterrent activity is common in the lipophilic crabs for the first few minutes of the experiment to be sure that the extract, but rare in the water soluble extract (Bolser and Hay, in tether was holding, and then checked again after 0.5 and 5 h, repress). cording the presence or absence of the crabs in each treatment. To qualitatively determine the presence of lipid soluble sec- The frequency of consumption of crabs tethered in the open was ondary metabolites in each seaweed species, we examined the compared to that of those tethered near Neogoniolithon by Fisher’s contents of each crude lipophilic extract by thin layer chromatog- exact test. raphy (TLC). TLC plates spotted with the lipophilic extracts of each species were developed using three different solvent sequences: (1) 100% hexane only, which allowed us to optimally resolve Substrate choice the least polar metabolites in the extract; (2) 100% hexane followed by 1:l hexane/ether, which allowed us to clearly view com- To determine if Mithrax sculptus preferred Neogoniolithon over pounds of intermediate polarity, and (3) 100% hexane followed by other habitats, we placed crabs in 1.4-1 round bowls (one crab per 1:l hexane/ether and then 100% ether, to resolve the more polar bowl) with two substrates having approximately equal surface area compounds in the lipophilic extract. Developed plates were (visually estimated). One of the two substrates in every trial was a sprayed with 50% sulfuric acid, then heated with a hot-air gun. piece of Neogoniolithon judged visually to be free of large epiThis caused both primary and secondary metabolites to be con- bionts. Alternative substrates were (1) a piece of Halimeda sp. verted to colored decomposition products for easy visualization of ( n = 14; a mix of H. monile and H. incrassuta); (2) dead fragments separated compounds. Additionally, the color after acid charring of the coral Porites sp. encrusted with a filamentous brown algae ( n = 16); or (3) N. strictum encrusted with ascidians (n = 30). Each can be characteristic of certain types of compounds. To test if feeding preferences observed in whole-plant assays substrate was placed haphazardly within the container and the two were related to plant secondary chemistry, we fed crabs artificial choices were placed far enough apart (not touching) to allow us to foods incorporating the lipophilic crude extract of each algal spe- unambiguously determine to which substrate the crab moved. cies using a method modified from Hay et al. (1994). The artifi- We waited between 0.5 and 2 h to allow the crabs to choose becial food was made of freeze-dried, powdered Ulva (a green alga tween the habitats, and then recorded which habitat housed the palatable to many herbivores) mixed in an agar base, and formed crab in each replicate. For each pair of substrate types, the obonto a strip of window screen. The screen provided a matrix to served frequency of habitat selection was compared to that expecthold the food, as well as a grid that allowed us to quantify the ed if there were no significant preference between substrates using amount of food removed by the herbivore by counting empty a G-test. squares (see Fig. 1 in Hay et al. 1994). Algal secondary metabolites were added to the food by dissolving the lipophilic crude extract from 2.0 g of seaweed in anhydrous ether, and adding this solution to 2.0 g of dry Ulva powder in a small flask. Enough Results ether was added to cover the powder with liquid. The solvent was then removed by rotary evaporation, resulting in a uniform coat- Crab density and fouling experiment ing of the extract on the algal particles. Control foods were treated identically, but without the addition of extract to the ether. For more detailed description of the preparation of the artificial food, M. sculptus was the dominant mobile organism associated with Neoguniolirhon at our study site, although seversee Hay et al. (1994). The sections of window screen holding the artificial foods with al other crabs, stomatopod shrimp, and small fishes were and without seaweed extract were cut into pieces measuring also present at much lower frequencies. Of the 40 Neo10 x 10 squares, and offered together to individual crabs in 1.0 1 goniolithon clusters examined, 30 contained at least one dishes containing fresh seawater. Experiments were monitored regularly, and feeding was allowed to continue until either (1) over Mithrax sculptus, and the mean mass of alga per crab 50% of either the treatment or control food was eaten; or (2) the was 75.1 g. termination of the experiment (for replicates with low rates of After 30 days in the field, clusters of Neogoniolithon feeding - usually after 12-24 h). If the herbivores did not feed or without crabs were covered with filamentous algae, and ate all of both foods between monitoring intervals, then that replicate was excluded from analysis because it provided no informa- were pale in color, while clusters with crabs appeared tion on relative palatability of the foods. The mean difference be- free of epiphytes and were pink in color. Crabs were tween the number of treatment and control squares eaten for each missing from seven of the containers that initially held species was analyzed by a two-tailed paired sample t-test. crabs, so these were excluded from the analysis. NeoCrab susceptibility to predation To determine if Neogoniolithon could provide a refuge from predation for Mirhrax, we tethered crabs both within reach of Neogoniolithon clusters and in the open on a patch reef 3-4 m deep at Dry RocksAVhite Banks near Key Largo. We tied a 10-12 cm length of 0.18-mm-diameter monofilament line to a 10-cm-long galvanized nail and affixed the other end of the line to the center of the carapace of the crab using Duro Quick Gel no-run super glue (Loctite Corp.). We blotted the crab dry with a paper towel, goniolithon clusters without crabs sepported a mass of epiphytes 9 times greater than clusters with crabs (Fig. 1, P < 0.0001, two-tailed t-test). Whole-plant palatability All species of algae exposed to crab grazing showed greater mass loss than controls for both choice ( P < 0.05, two-tailed t-test, n = 20) and no-choice assays ( P < 0.05, OECOLOGIA 105 (1996) 0 Springer-Verlag P < .o001 h 38 1 P<.ooo1 1m-I A d0-l P N=23 3 1 Mithrax absent Mithrax present Fig. 1 Dry mass of fouling organisms (mean 2 ISE) as a percentage of host wet mass on Neogoniolithon clusters with and without resident crabs after 30 days in the field. Analysis by two-tailed ttest; n is given at the base of each bar Mann-Whitney U-test, n = 8 for each species), indicating that crabs fed on all species of algae (Figs. 2B,C). When offered a choice between all seven species of algae, crabs showed relatively few significant preferences among algal foods (Fig. 2B). Dasya baillouviana was eaten less than the four species that were most preferred and Laurencia papillosa was eaten significantly less than two of the more heavily consumed species (Fig. 2B, P < 0.05, Friedman’s multiple comparisons test with Sidak’s correction). Thus, in the choice assay, there was no significant preference expressed between the following potential foods: Padina gymnospora, L. poitei, Halimeda sirnulam, L. intricara, or Dictyota sp. In the no-choice assay, feeding differed significantly among the various foods (Fig. 2C, P = 0.0039, one-way ANOVA), but this effect was produced solely by L. papillosa being consumed more than Dictyota, Halimeda, L. poitei, or L. intricata [Fig. 2C, P < 0.05, Fisher’s protected least squares difference (PLSD)]. These last four species did not differ from each other in either choice or no-choice assays. L. papillosa was an intermediate to low preference species in the choice assay, yet consumed at high rates in the no-choice assay, possibly indicating compensatory feeding on L. papillosa when alternate foods are unavailable. Parrotfishes (Scaridae) and surgeonfishes (Acanthuridae) were commonly observed feeding on the algae that we transplanted onto Pickles Reef, and these fishes fed selectively (Fig. 2A, P < 0.0001, G-test). L. papillosa and L. intricata were most preferred, L. poitei was of intermediate preference, and Dictyota sp. and Halimeda simulans were low preference foods (Fig. 2A; P < 0.05; pairwise G-tests, holding the significance level constant at 0.05 using Sidak’s correction). Feeding preferences clearly differed between crabs and fishes, as there is no significant correlation between the feeding preference ranks of crabs and fishes, when both were given a choice of algal foods (Kendall rank correlation tau = -0.400; P = 0.3272; n = 5). Fig. 2A-C Comparison of feeding preferences of reef fishes and the crab, Mithrax sculptus. A Frequency of total consumption of algae exposed to a natural assemblage of reef fishes at Pickles Reef, Florida. Analysis by G-test with Sidak’s correction for multiple comparisons (k0.05).B Wet mass of tissue consumed by crabs (corrected for autogenous changes unrelated to herbivory, see Methods) for 7 species of seaweed offered simultaneously for a 48 h period (mean 2 ISE). Analysis by Friedman’s rank test (P<O.OOO I), and multiple comparisons made using Friedman’s multiple comparison test with Sidak’s correction (P<0.05). Initial masses of all pieces of algae were between 60 and 80 mg wet weight. C Wet mass of tissue consumed by crabs (corrected for autogenous changes unrelated to herbivory, see Methods) for 5 species of seaweed offered separately for a 48-h period (mean f ISE). Analysis by one-way ANOVA, followed by Fisher’s PLSD at P<0.05. Initial masses of all pieces of algae were between 1 .OO and 2.00 g wet weight Crude extract feeding assays TLC indicated that L. papillosa lacked secondary metabolites, but that all other algae contained several lipophilic secondary metabolites. Dictyota sp. and L. intricata were most chemically rich, each containing at least five obvious (producing large, brightly colored spots on the TLC plate) secondary metabolites. Both Halimeda simulans and L. poitei contained one or two obvious secondary metabolites and several that were less apparent (produc- OECOLOGIA 105 (1996) Q Springer-Verlag tmatment tethered in Neogonidithon controi P < .oO01 0.5 tethered intheopen P =.0062 5.0 Hours since tethering Fig.3 Number of squares of artificial foods consumed by crabs Fig.4 Number of crabs consumed by reef fishes when tethered (mean k ISE). Treatment is artificial food with seaweed extract; with or without access to Neogoniolithon clusters (total number of control is artificial food without extract (see Methods). Analysis crabs of each treatment = 11). Analysis by Fisher's exact test by paired sample r-test (twetailed); n is given at the base of each pair of bars ing less distinct or smaller spots on the TLC plate). The genus Dicryoru has recently undergone taxonomic revision (Hornig et al. 1992), so prior reports of secondary chemistry in Dicfyora by species may be confused. However, the genus Dicfyota is, in general, very rich in secondary chemistry, including several diterpene alcohols (Faulkner 1993, and references cited therein) which are known to inhibit feeding by various herbivores (Hay and Fenical 1992). L. inrricuru is known to contain many non-polar secondary metabolites, but the bioactivity of these compounds has not been reported (Faulkner 1986, 1991, 1993). Many species of Hulimedu, including H. simuluns, produce the secondary metabolites halimedatrial and halimedatetraacetate in significant quantities; both of these compounds deter feeding by reef fishes (Paul and Fenical 1983; Hay et al. 1988; Paul and Van Alstyne 1992). L. poirei contains several secondary metabolites including poitediol, dactyol and poitediene, but the bioactivity of these compounds has not been reported (Faulkner 1984, 1986). No secondary metabolites have been reported from L. pupillosu (Faulkner 1993, and references cited therein). Four of the five species tested contain obvious secondary metabolites, but only the extracts of Dictyotu sp. and H . simuluns significantly deterred feeding by Mithrax (Fig. 3; P = 0.0406 for Dictyotu and P = 0.0497 for Hulimedu; two-tailed r-tests). Fig. 5 Percent of crabs choosing Neogoniolithon versus an alternative habitat. Analysis by G-test; n is given at the base of each pair of bars In laboratory assays, crabs showed no preference between Neogoniolirhon that was free of fouling organisms and Neogoniolirhon partially overgrown by ascidians (Fig. 5, P = 0.1201, G-test). Crabs also showed no preference between clean Neogoniolithon clusters and Porires fragments (Fig. 5, P = 0.4795, G-test). However, a strong preference for Neogoniolifhon over Halimedu was observed (Fig. 5, P < O.OOO1, G-test), despite the fact that Hulimeda was a high-preference food (Fig. 2B), suggesting that food may not be the most important factor in habitat selection. Tethering experiment and habitat choice Discussion Crabs tethered near Neogoniolithon clusters were preyed upon significantly less than crabs tethered in the open after both 0.5 and 5 h (Fig. 4;P < 0.0001 and P = 0.0062, respectively; Fisher's exact test). We observed blueheaded wrasse (Thalassoma bifasciutum) and gray angelfish (Pomucanrhus arcarus) attacking crabs that were tethered in the open. Herbivores are most often thought of as the natural enemies of plants, but there are situations where grazers can benefit the plants they associate with or consume. Some of the more common examples involve an increase in propagule release or settlement due to feeding on reproductive tissue that survives gut passage (Santelices OECOLOGIA 105 (1996) 0 Springer-Verlag . 1992). As an example, the amphipod Hyale media feeds preferentially on the mature cystocarpic tissue of the red alga Irideaea laminarioides resulting in an increase in spore release over ungrazed plants (Buschmann and Santelices 1987). Settlement of algal spores to the bottom is enhanced by spore incorporation into herbivore fecal material after ingestion (Santelices and Ugarte 1987), which may increase growth and development of the spore by providing a nutrient rich microenvironment (Santelices 1992). This same process can also enhance dispersal of algal propagules (Buschmann and Vergara 1993), much as fruit and seed predation by mobile animals can increase seed dispersal if seeds survive gut passage (review by Janzen 1983). Removal of plant biomass may increase the productivity of surviving plants and plant portions in terrestrial (McNaughton 1983, 1985; Paige and Whitham 1987), freshwater (Flint and Goldman 1975; Porter 1976; Lamberti and Resh 1983) and marine (Carpenter 1981, 1986; Klumpp et al. 1987) environments, especially at intermediate grazing intensities. In most of these cases, the increased production is thought to result from decreased self-shading or increased nutrient availability from herbivore excretions. However, the longterm effects of herbivory are poorly understood, and short-term increases in productivity may be achieved by depletion of reserves or reduced reproductive output (Belsky 1987). Grazing that has some positive effects may also involve a cost to the plant due to a loss of tissue, but where herbivores feed primarily on epiphytes the host plant may suffer little, if any, direct damage from associated grazers (Brawley and Adey 1981; Brawley 1992; Duffy 1990). Additionally, even if herbivores do directly graze a host plant, the overall effect on the host can be positive if the herbivore does even greater damage to nearby competitors of the host (Steneck et al. 1991). Small amounts of epiphytic growth can have beneficial effects on host plant growth by minimizing photoinhibition in shallow waters (Norton and Benson 1983). However, most of the effects of epiphytes on host plant growth and survivorship are negative (Sousa 1979; Orth and van Montfrans 1984; DAntonio 1985; Brawley 1992; Williams and Seed 1992; Wahl and Hay 1995). Following the removal of grazing crabs from Neogoniolithon, epiphytes completely covered the surface of the host plant, shading it from light. Such overgrowth of coralline algae frequently results in mortality (Littler and Doty 1975; Steneck 1982, 1986) or at minimum a competitive supression of growth (Steneck et al. 1991). Coralline algae are slow-growing (Adey and McKibbin 1970; Adey and Vassar 1975; Littler and Arnold 1982; Steneck 1986) and highIy resistant to herbivory (Steneck 1986, 1992), but may be rapidly overgrown in the absence of herbivores (e.g., Paine and Vadas 1969; Littler and Doty 1975; Wanders 1977; Brock 1979; Steneck 1982; Hay and Taylor 1985). Thus, in environments like seagrass beds where herbivory on seaweeds is relatively low (Ogden et al. 1973; Hay 1984a,b), corallines are competitively disadvantaged relative to faster-grow- 383 ing fleshy species. This appears to be true for Neogoniolifhon, as clusters isolated from grazing for only 30 days developed a heavy coating of epiphytes (Fig. 1). By harboring herbivorous crabs, Neogon!olithon increases localized, grazing pressure, potentially tipping the competitive balance in its favor. However, because Neogoniolithon commonly grows in sedimentary environments where it may be subject to frequent burial, it may also be able to tolerate some degree of shading without fatal consequences. These crabs can be effective cleaners of Neogoniolithon because they readily consume a wide ,range of seaweeds (Fig. 2B), including species that are defended from other grazers by secondary metabolites [e. g., Halimeah, Dictyota, and some species of Laurencia (Hay et al. 1987; Hay 1991; Paul 1992)l. Fishes consumed almost no Halimeda or Dictyotu in whole-plant assays (Fig. 2A), and, correspondingly, the extracts or pure secondary metabolites from these algae have been repeatedly shown to deter feeding by reef fishes (reviewed by Hay 1991; Paul 1992). Interestingly, extracts from Dictyora and Halimeda deterred Mithrax feeding (Fig. 3) even though Mithrax readily consumed both species in wholeplant assays (Fig. 2B,C). Several hypotheses might explain this apparent incongruity between Mithrax feeding in the whole-plant assays (Fig. 2B,C) and the effects of algal extracts on feeding (Fig. 3). First, food nutritional quality can interact with chemical defenses to determine the overall acceptability of a food to reef consumers like fishes and urchins (Duffy and Paul 1992; Hay et al. 1994). Nutritional quality might be even more important for less mobile grazers such as crabs. Small crustacean herbivores are highly susceptible to predation, so their foraging time and prey choices can be much more constrained than are those of fishes (Duffy and Hay 1991b, 1994). Thus, crabs might need to bias their dietary choices in favor of those foods that are high in value (protein, essential nutrients, energy), and be less constrained by secondary metabolite content. As a possible example, Laurenciu papillosa was among the lower-preference species in choice assays (Fig. 2B), but its extract did not deter crab feeding (Fig. 3) and in no-choice assays Mithrax consumed twice as much L. papillosa as any other species offered (Fig. 2C). Coupled with the findings that L. papillosa has high water content and low energy content relative to other seaweeds (Coen 1988b), these patterns suggest that Mithrax may avoid L. papillosa when more valuable species are available (Fig. 2B), but can compensate for its low value by increased feeding where alternative foods are unavailable (Fig. 2C). Herbivorous fishes, in contrast, prefer L. pupillosu over most other species offered in choice assays (Fig. 2A), possibly because it was the only seaweed species without secondary metabolites, and secondary metabolites from Hulimedu, Dictyota and other Laurencia spp. are known to deter feeding by reef fishes (Hay 1991; Paul 1992). Although these crabs appear to exhibit compensatory feeding in the laboratory (Fig. 2C), this could be constrained in the 384 0E C 0L 0 GIA 105 ( 1996) 0 Springer-Verlag field if increased foraging time involved increased risk of predation. Under these conditions, crabs that tolerate seaweed secondary metabolites may be advantaged if doing so allows them to consume more valuable foods and reduce the predation risk associated with increased foraging. The differences in palatability between a whole plant and its chemical extract could also be resolved if crabs can deactivate plant chemical defense mechanisms before they take effect. This might occur in the same way that proteins in the saliva of mule deer bind tannins, eliminating their digestibility reducing effects (Robbins et al. 1987). As a possible example, Mithrax might circumvent the defenses of Hulimeda by deactivating the mechanism that converts the less-deterrent secondary metabolite halimedatetraacetateto the more-deterrent halimedatrial upon crushing of plant tissue (Paul and Van Alstyne 1992). When Hulirnedu is extracted by the method used in this study, the conversion to the more deterrent compound takes place during the extraction, and thus would preclude the crab from interfering with this reaction. Regardless of the reason, M. sculptus consumes a wide range of algae and appears to use factors other than plant chemical defenses in choosing food, suggesting that it could prevent chemically defended seaweeds from overgrowing Neogoniolithon. Despite reciprocal benefits between the crab and coralline alga, Mithrax is not a specialist on Neogoniolithon, and it is unlikely that the relationship is coevolved. Habitat architecture, including spatial complexity, shape, and color, is known to play an important role in habitat selection by small crustaceans such as amphipods (Hacker and Steneck 1990) and shrimps (Hacker and Madin 1991). Habitat choice for Mithrax also appears to be based on the physical structure of the habitat and the degree of protection it affords from predators, as the crab chooses with equal frequency several substrates that provide a similar structural refuge (Fig. 5). M. sculptus is also commonly associated with the branching coral Porites, where it removes encroaching seaweeds (Coen 1988a). Similarly, Neogoniolithon is known to harbor another herbivorous crab species (M. coryphe) that appears to exhibit similar food choice patterns to M. sculptus (J. Stachowicz and M. Hay, personal observation), and may also serve a cleaning function. Association with a structurally complex sessile organism provides a refuge from predation for Mithrax, as crabs which were given access to Neogoniolithon clusters were far more likely to survive than crabs on exposed substrate (Fig. 4). Gut analyses of tropical fishes (Randall 1967) showed that 22 species of fishes in 13 families contained crab parts identified as belonging to Mithrax species, so predation by a wide variety of fishes is likely to be a major source of mortality for these crustaceans in tropical habitats. Many other crustaceans experience high predation pressure from predatory and omnivorous reef fishes (Randall 1967), and both crabs (Hay et al. 1989, 1990b) and amphipods (Hay et al. 1990a; Duffy and Hay 1991b, 1994) reduce encounter rates with predators and increase survivorship by associating with seaweeds that are unpalatable to fishes. Mutually beneficial plant-animal relationships have previously been documented in both marine (Steneck 1982; Branch et al. 1992) and terrestrial (Janzen 1966; O’Dowd and Wilson 1991; Cushman and Beattie 1991) environments. An herbivore of low mobility that cannot easily relocate may be likely to develop a close association with its host (Steneck 1982, 1992), especially when that herbivore uses the host as an important refuge from predation (Duffy and Hay 1991a,b, 1994; reviewed in Hay and Steinberg 1992). In these cases, the herbivore may be expected to minimize damage to the host plant in order to preserve its host’s value as a refuge. Such relationships may be most common when the host provides a spatial refuge from potential predators, but is in an environment where it competes poorly with other sessile organisms, thus providing an ample food source for resident herbivores through epiphytes and encroaching competitors. Predation pressure rather than feeding specialization appears to drive crustaceans to seek these associations with herbivore-resistant seaweeds (Hay 1992; Hay and Steinberg 1992; Duffy and Hay 1994). Because of their susceptibility to predation, crabs and other small herbivores may be unable to spend as much time foraging as larger, more mobile, or better defended, herbivores such as fishes or urchins. Crabs may, therefore, need to choose the most profitable foods rather than the least defended ones. These feeding preferences may be driven by predator avoidance strategies, but they coincidentally benefit the host alga by removing both palatable and chemically defended competitors. It is doubtful that Neogoniolithon has evolved in response to selective pressure by M. sculptus, as coralline algae evolved present morphologies well before the advent of modem herbivores (Steneck 1992), and other small herbivores (e.g., other crabs, chitons, amphipods, etc.) may also be capable of removing epiphytes from Neogoniolithun. While it is possible that diffuse coevolution (Fox 1981) between small herbivorous crustaceans and branched coralline algae has occurred to enhance the relationship initiated by chance, this appears unlikely because the participants in this association do not appear to be responding to selective pressure from each other, but to pressure from predators or competitors outside the association (Vermeij 1983). Acknowledgements This investigation was supported by NSF grant OCE 92-02847 to M. E. Hay, and NOAA grants NA88AAD-UR004 and NA36RU0060 (to N. Lindqllist and M. E. Hay) through the UNCWMURC lab at Key Largo, Florida. J. 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