MARINE ECOLOGY PROGRESS SERIES Published November 3 Mar Ecol Prog Ser

Reduced mobility is associated with compensatory feeding and increased diet breadth of marine crabs

John J. Stachowicz*, Mark Hay8*

University of North Carolina at Chapel Hill, Institute of Marine Sciences. Morehead City, North Carolina 28557. USA

ABSTRACT: Direct effects of predation have been widely recognized as important in affecting prey population dynamics and evolution. However, less attention has been devoted to the consequences of indirect effects of predators on prey behavior. For example, to avoid predation many animals restrict their activities to physical refugia and adopt low-mobility Mestyles, yet the consequences of these anti- predator behaviors for foraging and diet selection are relatively unknown. In this study we examine the relationships between mobility, feeding preferences, and compensatory feeding for 3 species of marine decapod crabs feeding on seaweeds in North Carolina, USA. Low mobility and high site fidellty of crabs were associated with a broad, non-selective diet and compensatory feeding. The majid Mithrax forceps exhibited the lowest mobility, highest site fidelity, and least selective diet of the 3 species, whereas another majid Libinia dubia was intermehate in both rnobllity and selectivity, and the xanthid Panopeus herbstii had the greatest mobility and narrowest diet. Of these 3 crabs, only M. forceps com- pensated for low food quality by increasing consumption rates in single food-species feeding assays. This may be because M. forceps is resistant to (or tolerant of) seaweed chemical defenses, while other crab species are not. The ability to consume, and presumably subsist on, a wide variety of potential foods including those defended from more mobile consumers may facilitate a low-mobllity lifestyle, allowing the crab to minimize movement and reduce exposure to predators. Low mob~lityand high site- fidelity may thus facilitate the formation and use of associational refuges with sessile benthic organisms that are resistant to predators; these associations can have important community and ecosystem-wide consequences.

KEYWORDS: Associational refuge. Compensatory feedlng . Crabs . Diet breadth. Mobility

INTRODUCTION organisms adopt sedentary lifestyles in refuges from predation (e.g. Steneck 1982, Coen 1988a, Hay et al. Predation pressure on small marine invertebrates 1989, Duffy & Hay 1994, Littler et al. 1995, Stachowicz like crabs, amphipods and gastropods may be intense & Hay 1996, 1999a). Because predation pressure in and can limit the distribution and abundance of these some habitats may be predictably high, and because animals in the field (Randall 1967, van Dolah 1978, the cost of gathering information about predation risk Nelson 1979, Stoner 1979, Heck & Wilson 1987, Duffy may be great, some animals spend the bulk of their & Hay 1994, Stachowicz & Hay 1996). However, in lives in these refuges (Sih 1987), potentially limiting addition to the direct effects of consumption, predators the kinds and numbers of available foods to which they may indirectly affect prey population dynamics and have access. To ensure an adequate and reliable food evolution by selecting for anti-predator behaviors such supply, some consumers specialize on one type of food as decreased mobility. Many otherwise mobile marine (often an alga) and live directly on it, using it as both food and shelter (Hay et al. 1989, 1990a,b, Pennings Present addresses: 1990, Faulkner 1992). However, this lifestyle may not 'Univers~tyof Connecticut, Department of Marine Sciences, be feasible for animals that have high consumption 1084 Shennecossett Rd., Groton, Connecticut 06340, USA. E-mail: [email protected] rates which preclude specialization on an individual "School of Biology, Georgia Institute of Technology, Atlanta, plant or that are too large for an alga to provide ade- Georgia 30332-0230, USA quate shelter (e.g. Pennings 1990). As a consequence,

O Inter-Research 1999 Resale of full article not permitted 170 Mar Ecol Prog Ser 188: 169-178, 1999

larger grazers (such as many decapod crabs) that have 28 mm. Crab nomenclature and ecological background low mobility may be driven to adopt a broader diet to is from Williams (1984) unless otherwise noted. M. for- decrease foraging time and minimize the risk of preda- ceps lives on rocky shores and reefs and is commonly tion. Thus, these species may be better able to con- found associated with corals and sponges from Brazil sume whatever foods are nearby, including those with to North Carolina. In North Carolina, this crab occurs morphological or chemical defenses. primarily in a mutualistic association with the coral There is some evidence for a relationship between Oculina arbuscula. The crab consumes coral competi- mobility and resistance to seaweed chemical defenses tors such as seaweeds and sessile invertebrates, and among marine animals. Many small, low-mobility the coral provides the crab with shelter from predators amphipods, polychaetes, ascoglossan gastropods and and with dietary supplements (Stachowicz & Hay crabs readily consume seaweeds that produce noxious 1999a). L. dubia 1s found on most types of bottom in chemicals which deter feeding by larger, mobile graz- sounds and saltier estuaries from southern New Eng- ers like fishes and urchins (Hay et al. 1987, 1988, 1989, land to southern Texas, and also in the Bahamas and 1990a,b, Stachowicz & Hay 1996, 1999a). Limited eni- Cuba. Juveniles often decorate their carapace with pirical evidence suggests that this pattern may be gen- seaweeds or invertebrates, presumably as camouflage eralizable to closely-related, similar-sized species that against predation. In the southeastern US, L. dubia differ in mobility. Among amphipods, for example, selectively decorates with the chemically defended low-mobility species are more tolerant of seaweed brown alga Dictyota menstrualis when this alga is chemical defenses than higher-mobility species (Duffy available. In so doing, it behaviorally sequesters the & Hay 1994), and are also better able to substitute food defensive chemistry of this plant for use against its own quantity for quality (Cruz-Kivera & Hay 2000). How- enemies (Stachowicz & Hay 199913). P. herbstii is one of ever, the robustness and generality of this relationship the more colnmon estuarine crabs in North and South for other groups of marine consumers remains un- Carolina, found wherever the bottom is muddy or cov- tested. Additionally, the relationship between mobility, ered with shells or stones. The species is common selectivity (or breadth of the potential diet) and the intertidally to 22 m depth th.roughout its range from ability to engage in compensatory feeding has not Boston, MA to Santa Catarina, Brazil. For all 3 species, been tested using naturally occurring foods. Such in- individuals in the size ranges we used readily consume vestigations may provide insight regarding the barri- macroalgae as we1.l as animal material in the labora- ers to, and constraints on, the evolution of low-mobility tory (Stachowicz & Hay 1999a, and unpubl. data). lifestyles among marine consumers. Unlike terrestrial consumers, there are very few In thi.s study, we examined the relationship between marine organisms that can be considered strictly her- mobility and food choice by 3 species of marine deca- bivorous (Karlson 1978, Darcy 1985, Horn 1989), and pod crabs feeding on CO-occurring seaweeds in North most crabs are probably best considered omnivorous. Carolina: the majid crabs Mithrax forceps and Libinia Majid and grapsid crabs that are generally regarded as dubia, and the xanthid Panopeus herbstii. We asked 'herbivorous' have diets comprised of as much as 50% the following questions: (1) Are there differences in animal material (Hines 1982, Kennish 1996, Lohrer & mobility among crab species? (2) Are low-mobility spe- Whitlatch 1997), and 'carnivores' such as the blue crab, cies better able to adjust their feeding rate on sea- Callinectes sapidus consume significant amounts of weeds based on organic content (i.e. do they exhibit plant material (Laughlin 1982). Crabs in the genus compensatory feeding?) and (3)Are low-mobility crabs Mithrax have been reported to be largely herbivorous less selective and do they have a broader algal diet (Coen 1988a,b, Stachowicz & Hay 1996), but they will than those with greater mobility? readily consume animal material (Winfree & Weinstein 1990, J Stachowicz unpubl. data) and actually grow best on an omnivorous diet (Wilber & Wilber 1989, Sta- METHODS chowicz & Hay 1999a). Similarly, the diet of Libinia in the field has been described as 'predominantly her- Study organisms. We used 3 decapod, brachyuran bivorous with carnivorous tendencies' on the basis of crabs of similar size: the majid crabs Mithrax forceps studies that show that most individuals have guts with and Libinia dubia, and the xanthid crab Panopeus more plant than animal material (Ropes 1987). Al- herbstii. We selected these species based on their though adult Panopeus herbstii are often considered abundance and ease of collection near our study sites carnivores, much of the evidence for this comes from in North Carolina (USA).lndividuals used were repre- laboratory or controlled f~eldstudies that demonstrate sentative of sizes found in the habitats where experi- these crabs can be voracious predators of commercially ments were performed: M. forceps: 13 to 25 mm cara- important bivalves (e.g. Lee & Kneib 1994, Micheli pace width; L, dubia: 9 to 23 mm; and P. herbstii: 12 to 1997 and references cited therein). Gut contents of Stachowicz & Hay:Mobility and diet breadth of marine crabs 171

field-captured individuals that are similar in size to Each release point was marked with the tag number those used in our experiments show that xanthids of the crab to allow determination of distance traveled (including members of the genus Panopeus) are omni- from capture to release. After 48 h, we intensively sur- vorous in the field and frequently consume macroalgae veyed the area within a 5.0 m radius of the release and other plant material when they inhabit areas point either by hand at low tide (oyster bar, shallow where it is abundant (Knudsen 1960, Gore et al. 1995, grassbed), or by SCUBA (Oculina heads) to determine Greenway 1995). Futhermore, direct observations of P. (1) the number of individuals of each species that were herbstii show that these crabs do consume macroalgae still located at the release point (site fidelity), and in the field (Reames & Williams 1983). On balance, (2) for those crabs we were able to locate, each crab's most evidence suggests that the crabs we used are distance from the release point (mobility). Site fidelity opportunistic omnivores. The proportion of animal ver- was analyzed by contingency table analysis (chi- sus plant material in the diet appears to be set, at least square) comparing the frequency of individuals of in part, by availability. each species at several distance intervals from the Crab mobility. We examined the movement patterns release point:

offered a simultaneous choice among the green alga, Previously we found that seaweeds that were low- Ulva rigida, the brown algae Dictyota menstrualis, Dic- preference food items for the crab Mithrax sculptus in tyota ciliolata, Padina gymnospora, and Saryassum fil- the Florida Keys (USA) were consumed at the highest ipendula, and the red algae Chondria dasyphylla, rates when no alternative foods were available (Sta- Gracilaria tikvahiae, and Hypnea musciformis. Sepa- chowicz & Hay 1996), and we speculated that this was rate assays measured consumption rates of these same due to compensatory feeding. We hypothesized that seaweeds when no alternative foods were available; differences in internal anatomy among seaweed spe- we also measured feeding in these no-choice assays on cies resulted in differences in the water content and Gracilaria verrucosa. We placed each crab in a sepa- corresponding differences in the am0un.t of organic rate 0.5 l bowl that had four 1 cm-diameter holes to material ingested per unit of alga consumed. Thus, allow for flow-through seawater. For choice assays, foods of low organic content appeared to be avoided each bowl with a crab held a 200 to 250 mg piece of by this crab when alternatives were available, but each algal species. For no-choice assays, each bowl were consumed at high rates when alternatives were with a crab held a 500 to 600 mg piece of 1 of the 9 sea- unavailable in order to meet intake requirements. We weed species. Sample sizes were 10 to 16 crabs of each evaluated this hypothesis more rigorously for Mithrax species for the choice assays, and 7 to 15 crabs of each forceps, Libinia dubia and Panopeus lierbstii feeding species per algal species for the no-choice assays. As a on seaweeds from North Carolina by comparing feed- control for changes in seaweed mass unrelated to her- ing rates in choice and no-choice assays with the per- bivory, ~denticalbowls without crabs contained equiv- cent organic content (ash-free dry mass / wet mass) of alent pieces of the same individual seaweed. These each algal species. We used organic content for our bowls were paired spatially in our seawater tables. measure of food quality because it allowed us to evalu- Assays were begun in the late afternoon and termi- ate the generality of our previous results by quantify- nated 2 mornings later so that each assay lasted 40 h; ing the amount of plant material consumed per unit this duration and timing has been found to be suffi- wet mass of food. No measure of the quality of algal di- cient to measure consumption rates and relative pref- ets has been consistently correlated with consumer erences of crabs feeding on seaweeds (Stachowicz & preference or performance, including protein and total Hay 1996, 1999a,b). At the end of each assay, each nitrogen (Carefoot 1967, Nicotri 1980, Robertson & Lu- seaweed piece was blotted dry with a paper towel and cas 1983, Duffy & Hay 1991, Cronin & Hay 1996a), so reweighed. To calculate net mass loss for each algal we did not measure these factors. While the presence species due to crab feeding, we corrected for mass of noxious chemicals does consistently affect feeding changes unrelated to herbivory using the formula by many marine consumers (review in Hay 1996), here [T,X (C,/C,)]- Tl , where T, and Tl were the initial and we tested whether consumers can compensate despite final masses of the seaweed portion in the container the presence of possible chemical defenses. with a crab and C, and C, were the initial and final Ash-free dry mass (AFDM) per unit wet mass masses of the seaweed portion in the paired control. (organic content) was obtained for each algal species To provide a qualitative assessment of the relative offered in no-choice assays. Wet mass was obtained by preferences expressed by the 3 crabs, we analyzed the weighing a piece of the alga after it had been blotted results of choice assays using the non-parametric Fried- dry with a paper towel. AFDM was calculated as the man test. Additionally, as a quantitative measure of the difference between the dry mass of that same piece of selectivity of each crab species, we used an index of diet alga (after drying in an oven at 65°C for 48 h) and the breadth (B)derived by Levins (1968): B= (l/xp?), where ash mass (after combusting at 500°C for 24 h). Deter- piis the fraction of the total diet mass represented by mination~of organic content were made for 5 individ- item i. An index of 1.0 indicates that consumers are ual plants of each species. The strength of the associa- highly selective and a single prey type comprises the tion between the mean organic content of each algal entire diet, whereas the maximum value of the index species and the mean amount of that alga consumed in occurs at Nwhen each species is represented equally in the no-choice assays by each crab species was as- the diet and N is the total number of choices available sessed using Spearman's rank correlation procedure. (N= 8 for our experiments). Differences in diet breadth among crab species were assessed using a l-way ANOVA, and post-hoc tests were made using the Tukey- RESULTS Kramer method. Differences among algal species in organic content and consumption rate in no-choice Crab mobility assays were also assessed using l-way ANOVA. Data were transformed where necessary prior to analysis to Mithrax forceps exhibited the greatest site fidelity meet the assumptions of ANOVA. and lowest mobility of the species tested. In the contin- Stachowicz & Hay: Mobility and diet breadth of marine crabs 173

gency table analysis, M. forceps exhibited Distance from release to recapture point slocrn greater site fidelity than either Libinia dubia or 10-loocm Panopeus herbstii (Fig. lA, x2= 28.5 and 31.0, 100-500cm respectively; p < 0.0001 for both), as 16 of the 18 not relocated within 500 M. forceps were relocated within 10 cm of the point of release 48 h later. Because no individuals of L. dubia or P. herbstii were relocated within 10 cm of the release point, we combined the

seaweeds tested (Fig. 4, l-way ANOVAs with Tukey- Kramer multiple comparisons at a = 0.05). However, both L. dubia and P. herbstii consumed large amounts of Ulva, the seaweed with the highest organic content, while M. forceps consumed this plant the least (Fig. 4). Additionally, L. dubia and P. herbslu' avoided con- suming Dictyota ciliolata or Dictyota rnenstrualis, and P. herbstii also avoided consuming Sargassum or Chon- dria (Fig. 4).Thus there was a significant negatlve cor- relation between the organic content of a glven sea- M~thrax Libinia Panopeus weed and the amount of that seaweed consumed in a no-choice assay for M. forceps (p = 0.009, Fig. 5A), but Fig 3 Levins' (1968) index of diet breadth of each crab as assessed by multi-choice lab expenments (see 'Methods' for details). A completely non-selective crab that consumed all a species of seaweed equally would have an index value of 8, Mlfhrax forceps whereas a crab that fed exclus~velyon a single species would N=15 have an Index value of l. Thus, larger index values indicate a broader (less selective) diet. Statistics are by 1-way ANOVA wth significant differences among species indicated by dif- ferent letters above each bar (Tukey-Kramer multiple com- pansons procedure p < 0 05)

.. .. not for P. herbstii (p = 0.332, Fig. 5B) or L. dubia (p = 0.368. Fig. 5C) Only M. forceps. the crab with the lowest mobility and highest site fidelity appears to con- sistently compensate for the low organic content of a seaweed by consuming greater quantities.

DISCUSSION

Our results suggest that low mobility among manne crabs is associated with compensatory feed~ngand a broad seaweed diet with little selection among species (Table 1). Although there may be negative impacts on growth and f~tnessassociated with chronic consump- tion of low quality diets (Cruz-Rivera & Hay 2000), L~biniadubia N = 16 Mithrax forceps can at least behaviorally compensate for the low nutntional value of some seaweeds by increasing consumption rates when confined with these species (Fig. 5). M. forceps can compensate be- cause it readily consumed all of the seaweeds offered in no-choice assays whereas Libinia dubia and Pano- peus herbstu consistently avoided consuming most

Table 1 Summary of mobihty and diet charactenstics for Mithrax forceps, L~bin~aduhla. and Panopeus herbstu

M. forceps L. dubla P. herbstu I Fig. 2. Selection of seaweeds as food by (A) M~thraxforceps. Mobhty Low Moderate Moderatehgh (B) Panopeus herhstii, and (C) L~binld dubla Crabs were Compensatory feedmg Yes No No offered a simultaneous choice of 8 species of seaweed and Algal dlet breadth Broad Interme&ate Narrow were allowed to feed for 40 h. Statut~calanalysis is by the Resistant to non-pardmetrir Friedman's test; different letters over each chemical defense?" Yes No2 No bar inhcdte differences in amount consumed (p < 0 05, see I dfrom Stachowicz & Hay (1999a) 'Results' for details) Stachowicz & Hay: Mobility and diet breadth of marine crabs 175

species of brown algae (Figs. 2 & 4). In this regard, selected red and green algae and generally avoid both L. dubia and P. herbstii behave similarly to local brown algae altogether (Hay et al. 1987, 1988, Stacho- species of fishes and sea urchins considered to be her- wicz & Hay 1999a). bivorous or omnivorous, as these species consume only Avoidance of brown algae by many grazers appears to be related to chemical defenses produced by these seaweeds (Hay et al. 1987, 1988, Cronin & Hay 1996b, _ Seaweed organic content Stachowicz & Hay 1999a). Extracts from Dictyota men- struaLis and Dictyota ciliolata deter feeding by Pano- peus herbstu but not by Mithrax forceps (Stachowicz & Hay 1999a). Although the effects of seaweed defensive chemistry on Libinia dubia are unknown, this crab avoided consuming these chemically-rich algae (Fig. 2) even when no other choices were available (Fig. 4). This suggests that these algae may be chemically de- fended from L. dubia. Thus, low mobility is also associ- ated with resistance to chemical defenses. The ability

Mithrax forceps rs=-0.921 p = 0.009

Panopeus herbstii

Panopeus hertstn r, = -0.343 D = 0.332

Libinia dubia rs=-0.318 p = 0.368

Fig. 4. (A) Organic content and consumption of seaweeds by Ash-freedry mass / wet mass (B) Mithrax forceps, (C)Libinia dubia and (D) Panopeus herb- stii. Sample sizes for each crab-seaweed combination range Fig. 5. Feeding rate versus seaweed organic content for from 7 to 15. Statistical analysis of feeding rate for each crab (A) Mithrax forceps, (B)Libinia dubia and (C)Panopeus herb- and seaweed organic concentration is by l -way ANOVA with stii. Data points are means rl SE. Correlation between the significant differences among seaweed species indicated by seaweed consumption rates for each crab species and the different letters above each bar (Tukey-Kramer multiple com- organic content of that seaweed species was assessed by the parisons procedure p < 0.05) Spearman rank procedure. p-values are given on each figure 176 Mar Ecol Prog Ser 188: 169-178, 1999

of M. forceps to exhibit true compensation may be a Reduced mobility decreases predation risk in a wide consequence of its resistance to, or tolerance of, sea- variety of animals (e.g. Sih 1987, Duffy & Hay 1994); weed defensive metabolites. This may be a common however, reduced mobility also limits the prey choices feature of low-mobility grazers, as reduced mobility available for consumption, limiting the animal to near- among amphipods is also associated with tolerance of by foods. Thus, a low mobility species like Mithrax seaweed secondary metabolites (Duffy & Hay 1994) forceps, which is too large to inhabit the plants it con- and compensatory feeding on artificial foods (Cruz- sumes, has a broad, low-selectivity diet (Fig. 2A) and Rivera & Hay 2000). can compensate for low food quality by increasing Additional measures of nutritional quality, such as intake (Figs. 4 & 5A). Having these diet characteristics protein content, do not appear to help further explain may further reduce the amount of movement required preferences and consumption rates among these crabs. to meet dietary needs, and decrease predation risk by For example, protein concentrations are twice as high maximizing the amount of time the crab can spend in Dictyota menstrualis as they are in Hypnea and near a refuge. This low-selectivity diet gives these Chondria (Duffy & Hay 1991),yet Mithrax forceps con- crabs the potential to locally reduce seaweed biomass, sumed all 3 of these species at equal rates in no-choice whereas more selective grazers typically alter only the assays (Fig. 4). The low rates of feeding by Libinia species composition of the algal community (Miller & dubia on higher-protein brown algae such as Sargas- Hay 1996). Because of their low mobility, the feeding sum and D, rnenstrualis relative to algae with lower activities of these animals are concentrated around protein content like Chondria and Hypnea (Duffy & their shelter. When this shelter is comprised of a living Hay 1991) in no-choice assays (Fig. 4) might be con- organism such as a coral or calcified seaweed, low- strued as compensatory feeding in response to pro- mobility consumers may benefit their host by removing tein concentrations. However, these brown algae are epiphytes or encroaching competitors (Coen 1988a, strongly avoided when these crabs are provided with Littler et al. 1995, Stachowicz & Hay 1996, 1999a). alternative algae (Fig. 2), suggesting that low feeding Interestingly, the refuge that is derived from the rates in no-choice assays are due to the chemical camouflage behavior typical of decorator crabs (Wick- unpalatability of these species rather than satiation. As sten 1980, Stachowicz & Hay 1999b) may facilitate in several previous studies (Carefoot 1967, Nicotri increased mobility because the 'shelter' is portable. Al- 1980, Robertson & Lucas 1983, Duffy & Hay 1991, though decorator crabs move slowly to avoid detection, Cronin & Hay 1996a), we saw no consistent correlation even the small increase in mobility observed in Libinia between nitrogen or protein levels and consumer pref- dubia relative to Mithrax forceps (Fig. 1) may permit erences among, or feeding rates on, marine algae. this crab to encounter a greater diversity of prey more We are confident in our field-based mobility estimates, reliably, and safely, facilitating the observed increase because (l) they assess mobility and site fidelity of these in selectivity in seaweed consumption (Figs. 2 & 3). crabs in their natural environment; and (2) they are consistent with previous reports of high site-fidelity in Mithrax species (Hazlett & Rittschof 1975), and lower Caveats and conclusions site-fidelity in Panopeus herbstij (Lee & Kneib 1994). However, our data only point out an association between Although all 3 crabs we used are brachyuran crabs, mobility and diet parameters and do not demonstrate the splitting of the majid family from the rest of the causation. Male and female crabs of many species have brachyurans is apparently ancient, and subfamilial different mobilities that are related to mating behaviors phylogenetic relationships within the majidae are (Wirtz & Diesel 1983, Lindberg & Stanton 1989, Lindberg unclear (Rice 1983). Thus, in our study, as in much et al. 1990), but these cannot explain the differences we of comparative biology, it is difficult to determine observed in mobility between species. The high site- whether present traits are a consequence of current fidelity observed in some crabs is tied to brooding or selection pressures or are relics of ancient splitting guarding of juvenile stages (Diesel 1989, Diesel & Horst events. However, given that the relationship between 1995) or mates (Lindberg & Stanton 1989). Conversely, low mobility, compensatory feeding and consumer re- high adult mobility and low site-fidelity may be required sistance to algal chemical defenses appears to hold for species that migrate among habitats, as do semi- among species within a family (majidae), as well as terrestrial crabs that live on dry land but release larvae between families (majid vs. xanthid), and that our directly into the sea (Diesel & Schuh 1998 and references results are consistent with previous comparisons (Hay cited therein). Regardless of what ultimately determines et al. 1987, 1988, Duffy & Hay 1994, Cruz-Rivera & Hay mobility, it seems likely that any constraints placed 2000), this association appears to be robust. on patterns of movement could profoundly influence Any trait that facilitates reduced mobility can be of feeding behavior and risk of predation. considerable advantage to marine invertebrates in- Stachowicz & Hay: Mobility a1 nd diet breadth of marine crabs 177

habiting shallow water coastal communities where Darcy GH (1985) Synopsis of biological data on the pinfish, predation is intense, because it allows them to maxi- Lagodon rhomboides (Pisces: Sparidae). NOAA Tech Rep, mize the amount of time they spend in refuges. In Nat Mar Fish Serv Circ 19 Dean RL, Connell JH (1987) Marine invertebrates in algal many cases these predator refuges are sessile plants or succession. I1 Tests of hypotheses to explain changes animals that physically or chemically exclude larger in diversity with succession. J Exp Mar Biol Ecol 109: omnivores that prey on small invertebrates like crabs 217-247 (Coen 1988a, Hay 1992, Hay & Fenical 1996, Stachow- Diesel R (1989) Parental care in an unusual environment: Metopaulias depressus (Decapoda,Grapsidae), a crab that icz & Hay 1996, 1999a,b). The broad diet of these lives in epiphytic brorneliads. Anim Behav 38:561-575 low-mobility animals has important system-wide con- Diesel R,Horst D (1995) Breeding in a snail shell. ecology and sequences, because it allows these consumers to facili- biology of the Jamaican montane crab Sesarrna jarvisi tate the growth and survival of their hosts, which are (Decapoda: Grapsidae). J Crustac Biol 15:179-95 often important producers of biogenic habitat for a Diesel R,Schuh M (1998) Effects of salinity and starvation on larval development of the crabs Armases ncardi and A. variety of species (Littler et al. 1995, Stachowicz & Hay roberti (Decapoda: Grapsidae) from Jamaica with notes on 1999a). In addition, the activities of these grazers can the biology and ecology of adults. J Crustacean Biol 18: create mosaics of algal density and productivity 423-436 (Branch et al. 1992, Stachowicz & Hay 1999a), which Duffy JE. Hay ME (1991) Food and shelter as determinants of food choice by an herbivorous marine amphipod. Ecology can directly alter the outcome of competitive interac- 72:1286-1298 tions among seaweeds (Bertness & Leonard 1997) and Duffy JE. Hay ME (1994) Herbivore resistance to seaweed decrease recruitment of fishes and invertebrates (Dean chemical defense: the roles of mobility and predator risk. & Connell 1987, Levin & Hay 1996). Thus, although Ecology 75:1304-1319 the impact of small, non-selective grazers may be spa- Faulkner DJ (1992) Chemical defenses of marine rnollusks. In: Paul VJ (ed) Ecological roles of marine natural products. tially limited, this type of grazing clearly merits con- Comstock, Ithaca, New York, p 119-164 sideration in models of grazer impact on ecosystem Gore RH, Sotto LE, Becker LJ (1995) Community composition, dynamics. stability. and trophic partitioning in decapod crustaceans inhabiting some subtropical sabellarid worm reefs. Stud- ies on decapod crustaceans from the Indian River region of Acknowledgements. The work was supported by the National Florida. Bull Mar Sci 28:221-248 Science Foundation through NSF grant OCE 95-29784 to Greenway M (1995) Trophic relahonships within a Jamaican M.H. and a doctoral fellowship to J.J.S., and by a dissertation seagrass meadow and the role of the echinoid Lytechinus fellowship from the Graduate School of the University of vanegatus (Lamarck). Bull Mar Sci 56719-736 North Carohna at Chapel Hill to J.J.S. We thank J. Pawlik for Hay ME (1992) The role of seaweed chemical defenses in editorial assistance and 3 anonymous reviewers for comments the evolution of feeding specialization and in the media- on a previous draft of the manuscript. tion of complex interactions. In: Paul VJ (ed) Ecological roles of marine natural products. Comstock, Ithaca, NY, p 93-118 LITERATURE CITED Hay ME (1996) Marine chemical ecology: what's known and what's next? 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Editorial responsibility: Joseph PawLik (Contributing Editor), Submjtted: December 28, 1998; Accepted: June 9, 1999 Wihnington, North Carolina, USA Proofs received from author@): October 25, 1999