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AMER. ZOOL., 32:370-381 (1992) Herbivory in Crabs: Adaptations and Ecological Considerations1 DONNA L. WOLCOTT AND NANCY J. O'CONNOR Department of Marine, Earth, and Atmospheric Sciences, North Carolina State University, Raleigh, North Carolina 29695-8208 SYNOPSIS. Plant material is the major source of nutrition for many species of crabs in both marine and terrestrial habitats. Physical and chemical characteristics of plants can lead to difficulties in harvesting and ingestion, to low digestability, unpalatability and toxicity, and to deficiencies in specific nutrients, especially nitrogen, vitamins and fatty acids. We describe the range of herbivory in crabs, as well as the anatomical, physiological and behavioral adaptations that enhance nutrient acquisition from plant material. We assess the impact of herbivory by crabs on plant communities, and highlight topics for further research. Herbivory is a common phenomenon in crabs. In fact, a significant amount of nutrition may be provided by plant consumption even in species that are considered carnivorous (Warner, 1977). Some crabs clearly obtain most of their nutrition from plants (Table 1), but herbivory occurs also in species that are carnivorous, such as the voracious predator, Callinectes sapidus (Alexander, 1986; Laughlin, 1982). Conversely, field observations of crabs whose main diet is plants reveal opportunistic consumption of animal material, through both predation and scavenging. Whatever its proportion of the diet, plant material presents nutritional challenges for consumers. This review attempts to point out the unique aspects of consuming plants, and the diversity of cellular, physiological, morphological, and behavioral adaptations that enhance the acquisition of nutrients from plants. The impact of crab herbivory in various plant communities is assessed, and gaps in the current knowledge about crab herbivory are highlighted. and terrestrial habitats (Table 1). As a consequence, crabs consume a tremendous variety of plant material (Table 1) and practice many modes of herbivory. Suspension feeding is largely confined to the anomurans, whose foliose mouth parts are more suited for creating the water currents from which planktonic prey are captured and sorted (Warner, 1977). Deposit feeders, e.g., Uca species, consume a mixture of benthic microalgae and detritus. In shallow aquatic systems, crabs graze microalgae that grow on the sediment surface and that can be responsible for more productivity than the vascular plants in the system (Sullivan and Moncreiss, 1988). They also consume small detrital particles largely derived from plants (review, Bowen, 1987). Crabs eat macroalgae on tropical coral reefs (Coen, 1988a, b) and on temperate rocky shores (Sousa, 1979; Hines, 1982). A few species utilize living vascular plants. Of those feeding on seagrasses, at least one, Nectocarcinus integrifrons, appears to derive substantial nutrition from the grass itself, in addition to that from the epiphytes present (Klumpp and Nichols, 1983). The terrestrial crab GecarEXAMPLES OF PLANTS AND HABITATS cinus lateralis consumes substantial amounts UTILIZED BY HERBIVOROUS CRABS of grass in Bermuda (Wolcott and Wolcott, Herbivorous crabs are found in many 1984). Crabs that eat living mangrove leaves phylogenetic groups, and in both aquatic are found only in the genus Aratus (Hartnoil, 1988), although a host of terrestrial 1 From the Symposium on The Compleat Crab pre- species subsist on mangrove litter. Curisented at the Annual Meeting of the American Society ously, there are no Aratus in the Indo-Pacific, of Zoologists, 27-30 December 1990, at San Antonio, the region with the most extensive and Texas. 370 371 HERBIVORY IN CRABS TABLE 1. Examples of plant material consumed by crabs. Plant material eaten Phytoplankton Benthic microalgae and detritus Macroalgae Vascular plants Foliage Seeds and fruits Crab Reference Gaetice depressus (Grapsidae) Petrolisthes cinctipes (Porcellanidae) Uca spp. (Ocypodidae) Scopimera injlata (Ocypodidae) Grapsus tenuicrustatus (Grapsidae)" Caphyra rotundifrons (Portunidae) Mithrax sculptus (Majidae) Microphrys bicornutus (Majidae) Pugettia producta (Majidae)" Pachygrapsus crassipes (Grapsidae) Nectocarcinus integrifrons (Portunidae)' Sesarma reticulatum (Grapsidae)" Chasmagnathus convexus (Grapsidae)d Aratus pisonii (Grapsidae)' Birgus latro (Anomura, Coenobitidae)f Coenobita compressus (Coenobitidae) Cardisoma carnifex (Gecarcinidae) Neosarmatium smithi (Grapsidae) Leaf litter Gecarcoidea natalis (Gecarcinidae)8 Chiromanthes onychophorum (Grapsidae)' Sesarma erythrodactyla (Grapsidae)' Cardisoma guanhumi (Gecarcinidae)' Depledge, 1989 Hartman and Hartman, 1977 Crane, 1975; Montague, 1980 Zimmer-Faust, 19876 Alexander, 1979 n&yetai, 1989 Coen, 1988a KilarandLou, 1986 Hines, 1982 Sousa, 1979 Klumpp and Nichols, 1983 Seiple, 1981 Nakasone et ai, 1983 Beever et al, 1979; Wilson, 1989 Vogel and Kent, 1971; Alexander, 1979 Kurta, 1982 Lee, 1985 Giddins et al, 1986; Smith, 1987; Neilsone/a/., 1989 O'Dowd and Lake, 1989 Malley, 1978; Lee, 1989 Camilleri, 1989 Henning, 1975; Wolcott and Wolcott, 1987 • Blue-green algae; b kelp; c seagrasses;d marshgrasses;' mangroves;' coconut;«rainforest. diverse mangrove systems, and a comparably rich fauna of terrestrial and semi-terrestrial crabs (Malley, 1978;Hartnoll, 1988). POSITIVE ASPECTS OF USING PLANTS AS FOOD Herbivory has both positive and negative aspects for the herbivore. Benefits include the greater mass and predictable availability of plant vs. animal prey, and the reduced risk of predation that crabs may experience while foraging in vegetated habitats. NEGATIVE ASPECTS OF EATING PLANTS Physical defenses of plants against herbivory Plants have evolved a diverse arsenal of physical defenses against herbivores (Howe and Westley, 1988; Duffy and Hay, 1990). Adaptations include structural modifications that make plants difficult to harvest, process and digest. The presence of lignin makes plants rubbery or tough, protecting plants against smaller predators. Hardness caused by calcification or by the presence of silica reduces harvestability and causes excessive wear on chelae, mandibles and especially the teeth of the gastric mill (Coen, 1987). Undigestibility of plants The same compounds that make harvesting and grinding difficult increase the bulk of undigestible material that must be processed by the digestive system (Howe and Westley, 1988). Even cellulose, the major structural component of cell walls, is largely undigestible. As a further deterrent to predation, plants elaborate various concentrations of chemicals, such as tannins and phenolics, that interfere with digestion (Mattson, 1980). As a result, much of the carbon and nitrogen that is present in plants is not available to the herbivore. In crabs, nitrogen assimilation on an herbivorous diet may be 30% lower than on an animal diet (Wolcott and Wolcott, 1984). 372 D. L. WOLCOTT AND N. J. O'CONNOR Plants as an inadequate source of nitrogen and other nutrients Nitrogen is a limiting nutrient for many herbivorous animals (Mattson, 1980), including the herbivorous crabs studied to date (Wolcott and Wolcott, 1984, 1987; O'Connor, 1990), due to low nitrogen content and low nitrogen assimilation efficiencies. Plants usually contain an unfavorably high carbon to nitrogen ratio. In leaf litter, the ratio may exceed what is considered nutritional over 10 fold (Giddins et al, 1986), and nitrogen may constitute less than 1% of the dry weight, as compared to 714% in animal tissue (Mattson, 1980). Nitrogen is a limiting nutrient for the semi-terrestrial herbivorous crab, Cardisoma guanhumi, when its diet consists of an abundance of its natural plant foods. Supplementing the plant diet with protein results in enhanced growth (Wolcott and Wolcott, 1987). Growth is also greater in Gecarcinus lateralis when its natural plant diet is supplemented with high-quality plant material (Wolcott and Wolcott, 1984). Both Uca pugnax and U. pugilator adults experience enhanced growth when offered highnitrogen foods, either alone or added to the sediments on which they feed (O'Connor, 1990). Plants are poor sources of essential amino acids, vitamins, and sterols, compared to animal tissue. In vascular plants, polyunsaturated fatty acids are also scarce (Phillips, 1984). has evolved in crabs to maximize the return from a diet of plants. Although descriptive studies of herbivory in crabs are becoming more numerous, few specifically address the current hypotheses in plant-herbivore ecology (but see Coen, 1988*; Hay et al., 1989) or physiology (Giddins et al., 1986). Because herbivorous crabs occupy both aquatic and terrestrial habitats and eat most types of plant material, they should be excellent organisms with which to test theories of optimal herbivore strategies developed in terrestrial systems. Morphological adaptations Morphological specializations that characterize herbivorous crabs include spoonshaped or spatulate chelae for harvesting plants (Coen, 1987), modified mouth parts, robust gastric mill teeth for processing fibrous plant material (Coen, 1987; Warner, 1977), and increases in foregut volume to process larger volumes of low nutrient food (Wolcott and Wolcott, 1984). Mouth parts.—In deposit-feeding crabs, extensive modifications of the mouthparts and buccal cavity serve to create water currents that minimize the amount of nonnutritive inorganic material that is ingested. Small, organically rich particles are directed to the mouth, while heavier particles, whose nutrient value is usually inferior, are rejected (reviews, Warner, 1977; Lopez and Levinton, 1987). In ocypodids, additional enrichment of the organic fraction is accomplished by scraping the organic material from larger Chemical defenses of plants particles using specially modified setae on against herbivory the second maxillipeds. In various fiddler To reduce herbivory, plants synthesize crab species, the number of these spooncompounds that are either unpalatable or tipped setae correlates with the typical partoxic to consumers, including those which ticle size of the sediment processed (Miller, interfere with digestion. These compounds 1961). Gastric mill.—Early studies found no often are concentrated in the parts of plants in which the most nutrients are invested. obvious correlation between the type of diet Consequently, nutrients and chemical and the morphology of the gastric mill defenses frequently covary within an indi- (review, Dall and Moriarty, 1983), but this vidual plant (Mooney and Gulmon, 1982; may have been confounded by analyzing Kilar and Lou, 1986; Duffy and Hay, 1990). species whose diets are too general for morphological specialization to have evolved. ADAPTATIONS OF CRABS TO CIRCUMVENT Especially robust gastric mills occur in two THE SHORTCOMINGS OF HERBIVORY highly herbivorous species that consume An integrated suite of morphological, very tough mangrove leaves, Aratus pisonii physiological and behavioral adaptations (Warner, 1977) and Neosarmatium smithi HERBIVORY IN CRABS (Giddins et al, 1986). Coen (1987) found that more elaborate teeth on gastric mills are characteristic of herbivorous species. Since crabs cannot synthesize all the enzymes necessary to digest plant cell walls, fine grinding breaks open cells and releases cell contents. Foregut volume. —According to optimal digestion theory, species that eat plants should have large guts to compensate for low assimilation rates (Sibly, 1981). Larger gut volume allows ingestion of more food during each foraging period, the duration of which often is limited in crabs by nocturnal, crepuscular or tidal activity patterns. As these considerations would predict, the largely carnivorous portunids, Scylla serrata (Hill, 1976), Liocarcinus puber, L. holsatus (Choy, 1986), and Portunus pelagicus (Wassenberg and Hill, 1987) have foreguts with only one-third or less the volume of those in the terrestrial herbivore, Gecarcinus lateralis, of comparable size (Wolcott and Wolcott, 1984). For deposit-feeding crabs, digestive theory predicts that guts should be structured to process large amounts of sediments quickly, and to shunt only the organically enriched fractions aside for complete digestion (review, Lopez and Levinton, 1987). Comparative studies linking diet and gut morphology in deposit feeders, carnivores and herbivores is an area for future research. Body size.—Many terrestrial vertebrate herbivores have evolved large body sizes, apparently in response to selection pressure for increased gut size (McNeill and Southwood, 1978; Sibly, 1981). This pattern is not seen in aquatic herbivorous crabs; however, terrestrial herbivorous crabs may grow to large size, e.g., the 3 kg anomuran Birgus latro. The morphology of the crustacean midgut gland may limit the benefits to be gained by increases in size. Both enzyme secretion and nutrient absorption occur in the blind-ended ducts of the gland (review, Gibson and Barker, 1979). Enzymes travel down the ducts to the mid- and foregut to mix with the food. Periodically, the direction of flow is reversed, and a slurry of partially digested food returns through the same ducts in the midgut gland. The essentially tidal function 373 of the organ may lower its efficiency at greater sizes, compared to the linear throughput system of intestinal absorption in vertebrates. Comparative studies could address these issues. Physiological adaptations to herbivory To date, the physiological adaptations of crabs to herbivory are largely unstudied. Some information is available on digestive enzymes, and on chemosensory abilities. Digestion.—Enzymes that can digest some of the material in the cell walls of vascular plants have been identified in the guts of a variety of crabs, both carnivorous and herbivorous (review, Gibson and Barker, 1979; Yokoe and Yasumasu, 1964; McClintock et al, 1991). Three classes of cellulases are required to completely digest cellulose, and additional enzymes are needed to attack the pectic polysaccharides and hemicelluloses in which the cellulose fibers are embedded (see Chamier and Willoughby, 1986). There are no reports of pectolytic enzymes in crustaceans, so like other detritivores, crabs may rely heavily on pre-degradation of the pectic and hemicellulitic matrices by fungal enzymes (Chamier and Willoughby, 1986; Barlocher, 1982). This would expose the cellulose fibers to the cellulases that have been identified in many species of crab (review, Gibson and Barker, 1979). Furthermore, microorganisms themselves contribute to the food value of detritus. Although the absolute biomass of microorganisms contributes only a small proportion of the total carbon and nitrogen consumed, it is of high quality and readily assimilated (reviews, Lopez and Levinton, 1987; Bowen, 1987). Enzymes capable of digesting the cell walls of the fungi that are ingested with vascular plant detritus, such as laminarinase and chitinase, occur in crabs from a variety of habitats (review, Gibson and Barker, 1979; Chamier and Willoughby, 1986). To determine if the type or activity of enzymes required for plant degradation have undergone adaptive evolution in herbivorous crabs, comparisons could be made between species that feed on fresh vs. detrital vascular plant material, or vascular plant vs. algal material, or between 374 D. L. WOLCOTT AND N. J. O'CONNOR omnivorous crabs and more specialized herbivores when both are fed plants. The hypothetical ability of crabs to digest plant material, deduced from the complement of enzymes identified in the gastric juice, needs to be substantiated by analysis of the amount of degradation of various compounds during passage through the gut. To this end, Neilson and Richards (1989) analyzed the mangrove leaf litter that constitutes the normal diet, and the fecal pellets subsequently produced, by the sesarmid, Neosarmatium smithi. As predicted from knowledge of their digestive enzymes, these crabs removed significant quantities of the neutral sugars, but uronic acid (a pectic compound) and lignin were undigested, and concentrated in the feces. In terrestrial ruminants and termites, symbiotic microorganisms (especially methanogens) are essential in extracting the nutrients from plant material and making them available to the host. Other microorganisms may also aid in digestion. As stated above, fungi have enzymes that crabs lack to degrade noncellulose polysaccharides in plant cell walls. Interestingly, the amount of eccrinid fungi (obligate gut associates) in the hindgut of estuarine species of crabs is positively correlated with herbivory (Mattson, 1988). Additional physiological adaptations of crabs to herbivory remain to be explored: gut cycling times (which should be shorter in herbivores eating poor quality food), variation in gut pH (which affects digestibility of plant material), and slow growth. Chemosensory adaptations and associated behaviors Physiological and behavioral adaptations to herbivory are inextricably linked, as illustrated by sensitivity of chemoreceptors and the behaviors that their stimulation elicits. As for all other crabs, chemoreception can be important in locating food and is critical for the stimulation of feeding (Fuzessery and Childress, 1975; Trott and Robertson, 1984; Zimmer-Faust, 1987a; Wellins <tf a/., 1989). Crabs that consume plants have integrated chemoreceptive and behavioral adaptations that subvert the defenses evolved against herbivores. These adaptations aid consumers in locating the most nutritious, readily harvested and digested plant material (Robertson et al, 1980, 1981; Zimmer-Faust, 1987a), and in avoiding chemical defenses (Coen, 19886; Coen and Tanner, 1989; Neilson et al, 1986; Camilleri, 1989). Chemical sampling of the environment, with consequent behavioral responses, is evident in both terrestrial and aquatic species that consume plants. Compared to more carnivorous crustaceans, species that utilize plant material employ a different suite of chemicals as foraging and feeding stimuli. In the largely carnivorous lobster, Homarus americanus, sugars elicit only a mild response from chemoreceptors (Derby and Atema, 1982), but carbohydrates stimulate feeding behavior in Petrolisthes cinctipes, a filter feeder (Hartman and Hartman, 1977), and Pugettia producta, which feeds on kelp (Zimmer et al., 1979). In terrestrial habitats, foraging can be initiated through olfaction of volatile cues from plant material (Rittschof and Sutherland, 1986; Wellins et al., 1989). Feeding behavior of terrestrial herbivorous crabs is elicited, as in aquatic crabs, by stimulation of contact chemoreceptors on the chelipeds and pereiopods. Sensitivity of terrestrial herbivorous crabs to amino acids is lower than in carnivorous crabs, and feeding is more readily elicited by compounds found in typical terrestrial foods. Depending on the spectrum of the diet, disaccharides (found in storage products of algae and in the sheaths of diatoms), monosaccharides (characteristic of fresh and rotting fruit), and compounds produced during putrefaction of animal tissue may be effective (Robertson et al., 1981; Rittschof and Sutherland, 1986; Trott and Robertson, 1984; Trott, 1987; Wellins et al, 1989). In crab species that consume living plants, a preference for certain species of plant or parts of plants is common. Most frequently, preferences seem to reduce the consumption of toxic or unpalatable secondary compounds (Coen, 19886; Smith, 1987). Coating palatable algae with extracts from chemically defended species results in reduced consumption by generalist herbivores such as fish and sea urchins (Hay and HERBIVORY IN CRABS Fenical, 1988). However, the same chemical that deters feeding in generalist herbivores may serve as a feeding stimulus to species that utilize the distasteful plant for food and shelter (Hay et ai, 1988, 1989, 1990). Association with a single plant type is very uncommon in the aquatic environment, compared to terrestrial systems, where many insects have monospecific diets (Hay et ai, 1990). In insects, adults are the dispersing stage and are responsible for locating the host plant that is used by the developing larvae. Most aquatic organisms disperse as juveniles, which have limited capacities to choose particular host plants. Specialization on a single plant type is rare in crabs. The two species identified so far in coral reef systems are small, highly cryptic, and are associated with a plant species with chemical defenses that deter feeding by fish (Hay etai, 1989,1991). Although neither sequesters toxins from its host plants, or is toxic itself, they both realize a reduced risk of predation by remaining associated with a plant shunned by predators. To date, plant consumption has not been linked to chronic toxicity in crabs. Chemically-mediated food preference in detritivores. — Selective foraging based at least in part on chemoreception contributes significantly to the nutrition of crabs that subsist on plant detritus. Several species of crabs that feed on leaf litter consistently prefer litter that has aged in situ for three to six weeks (van der Valk and Attiwill, 1984; Giddins et al., 1986; Camilleri, 1989; Lee, 1989). Aged litter has a more favorable carbon : nitrogen ratio (e.g., 100:1 vs. 183:1, Giddins et al., 1986), and lower concentrations of secondary compounds than fresh litter. Leaching by water during tidal immersion or rainfall removes much of the defensive compounds. Leaves that have become palatable by immersion in sea water become unpalatable again when the concentration of tannins is restored to preleached levels (Neilson et ai, 1986). Aging also reduces leaf toughness and exposes the more digestible cellulose fibers, as enzymes from microbes that colonize the surface of the leaves begin the process of breaking 375 down the sugar polymers. Aged litter considerably enhances the efficiency with which Neosarmatium smithi assimilates carbon, nitrogen and energy (Giddins et ai, 1986). Essentially no nutrients are available from litter aged two weeks, but after 8 weeks of aging, assimilation efficiencies rise to 50%56%, resulting in the enhanced fitness of crabs that select aged litter which is more digestible and nutritious, and contains a minimum of secondary chemicals. Caching behavior. —Caching (taking food into burrows), is common in many terrestrial and semiterrestrial species that consume leaf litter, and has several potential benefits. First, crabs that cache can sequester food resources when competition for food is intense. It is common in habitats with high crab densities, in which essentially all the litter that falls during the crabs' active season is removed immediately from the ground (Herreid, 1963; Fimpel, 1975; Wolcott and Wolcott, 1987; O'Dowd and Lake, 1989; Lee, 1989). Second, since cached leaves may remain in the burrow for some time, leaching and microbial colonization of litter in the burrow may enhance the nutritional quality for future consumption (Robertson and Daniel, 1989; O'Dowd and Lake, 1989; Garcia and Bonnelly de Calventi, 1983). Third, in intertidal areas, caching retains litter in the crabs' habitat, preventing leaves from being carried out by the tide (Robertson, 1986; Lee, 1989). Lastly, cached litter may allow crabs to forage underground when above-ground activity is reduced by periods of low humidity or high temperature. Understanding the role of caching is essential for calculating the nutritional input to crabs and their impact on nutrient cycling in the community. Plasticity of food preference. —Modifying feeding behavior in response to chemical or other cues may coordinate changes in digestive and nutritive requirements with changes in food availability. Food preference within a species of herbivore is not necessarily fixed. Frequently, conspecifics in different habitats have different preferences. For instance, the tree crab, Aratus pisonii, which feeds predominately on fresh mangrove leaves, ignores dead fish in estuarine habitats, but 376 D. L. WOLCOTT AND N. J. O'CONNOR members of the coastal population are attracted to it (Beever et al., 1979). Acutely switching the diet ofA pisonii from one type of mangrove leaf to another, or from scrapings off pilings to mangrove leaves, can be lethal, even though all these food sources support populations in the field (Beever et al., 1979). In another example of plasticity in food preference, propagules of the mangrove Ceriops tagal are consumed by sesarmid crabs in stands where it is the dominant species, but are avoided where it is rare. Conversely, four other mangrove species experience heaviest predation where they are rare and least where their conspecifics are dominant (Smith, 1987). The biochemical basis for changes in food preference in crabs is unknown, but the time required for enzyme induction may explain the toxicity of acute shifts in diet. Some dietary components may induce production of requisite digestive enzymes (Wainwright and Mann, 1982; Chamier and Willoughby, 1986), and it is possible that metabolic mechanisms that are responsible for detoxifying particular secondary compounds also are inducible. Omnivory. — Two aspects of crab behavior contribute to the flexibility seen in their diet. As a group, crabs are omnivorous, and tend to consume palatable food in proportion to its abundance in the microenvironment (Warner, 1977; Laughlin, 1982; Hines, unpublished data, but see Hines, 1982). They also are mobile, and may sample a variety of habitats during an activity period. Consuming a variety of food items may minimize the negative effects of secondary compounds (Kitting, 1980), for although toxins may be present in all the foods consumed, the level of any one toxin remains low. A varied diet also insures that herbivores acquire enough of those nutrients which are scarce in plant material. Animal tissue is commonly found in the guts of crabs feeding on plants (Beever et al., 1979; Choy, 1986; Malley, 1978; Giddins et al., 1986; Hines, 1982; Klumpp and Nichols, 1983); predation and cannibalism are common in herbivorous crabs (Warner, 1977). For both C. guanhumi and G. lateralis, the level of predation and cannibalism is higher in crabs that are maintained on a natural plant diet than in those offered a higher quality diet (Wolcott and Wolcott, 1984, 1987). In the habitat of terrestrial crabs, carrion or other high-protein food sources are surrounded by aggregates of crabs, the bulk of whose diet is leaf litter (Grubb, 1971; Wolcott and Wolcott, 1984). The land hermit crab Coenobita compressus is attracted to aggregates of conspecifics, thus enhancing the likelihood of consuming the occasional high-quality food item (Kurta, 1982). For aquatic herbivores, the epibiota (microalgae, microbes, and sessile and cryptic animals) present on macrophytes may play a similar role in supplying critical nutrients. Liocarcinus puber, a portunid whose main diet item in the summer in a temperate population is brown algae, scrapes off and consumes the epiphytic growth before consuming the thallus itself (Choy, 1986). The majid Microphrys bicornutus cannot survive when the epibiota are removed from its principal algal resource (Kilar and Lou, 1986). ECOLOGICAL IMPACT OF CRABS ON PLANT COMMUNITIES The impact on plants of herbivory by crabs varies between habitats, and includes both direct effects, such as seed predation, and indirect effects, such as enhanced nutrient cycling and altered rates of succession. Mangroves and terrestrial systems. — Herbivory by crabs perhaps has the greatest influence in mangrove systems. Where investigated, impact to primary leaf production is negligible, as Aratus pisonii damages less than 10% of total leaf area (Beever et al., 1979). Crabs do not eat living leaves in the Indo-Pacific region (Hartnoll, 1988), but may consume up to 79% of the total litter produced (van der Valk and Attiwill, 1984; Lee, 1989; Robertson, 1986; Robertson and Daniel, 1989). Of this, the majority is returned to the environment as finely shredded, partially digested fecal material (Camilleri, 1989; Robertson and Daniel, 1989). This rapid comminution of leaf litter into finer detritus greatly speeds the cycling of nutrients within the mangrove system, because shredding creates more surface area HERBIVORY IN CRABS for colonization by microorganisms that possess the necessary enzymes for degradation of polymeric carbohydrates. The shredding activity of crabs stimulates the microbial turnover of litter by over 99% (Robertson and Daniel, 1989), thus speeding the remineralization of nutrients required for tree growth. Crabs increase the amount, as well as the rate, of remineralization by caching leaves in their burrows, thus retaining nutrients in the mangrove habitat that otherwise would be transported away by the tide (Giddins et ai, 1986; Robertson, 1986; Lee, 1989). Crabs can affect the composition of mangrove forests directly by their predation on mangrove propagules (Smith, 1987; Smith et ai, 1989). Grapsid crabs consume 75% of the propagules in study plots in mangrove forests in Australia. By selectively consuming propagules, crabs may either encourage or discourage recruitment of particular species in certain habitats, and play a significant role in structuring mangrove communities (Smith, 1987; Smith et ai, 1989). In other habitats, such as island rainforests, crabs also play a role in structuring tropical terrestrial plant communities through litter consumption, seed predation and dispersal (Alexander, 1979; Lee, 1985, 1988;O'Dowd and Lake, 1989). 377 rax sculptus removes epiphytic algae from the coral Porites porites, preventing algal overgrowth and subsequent shading and death of the coral (Coen, 1988a). Crabs help to create and maintain patchiness in the distribution of species, and affect species' persistence. In holes and crevices, both crabs and palatable algae escape predation by fish. When crabs are excluded from holes in the Bay of Panama, the holes are colonized more rapidly by algae, and the early colonists, which are ordinarily rapidly replaced by less palatable species, persist longer (Menge et ai, 1983). Because crabs opportunistically consume animals while foraging on plants, they affect the distribution of solitary and colonial sessile organisms as well (Menge et ai, 1983, 1986). Temperate rocky shores.— Herbivorous crabs feed on macroalgae growing on rocky shores in temperate zones (Sousa, 1979; Hines, 1982; Menge and Lubchenco, 1981). The role of crabs appears to be similar to that in tropical systems. Only a small fraction of primary production is consumed by crabs, but indirect effects of their foraging help to structure the system. Selective pressures for herbivory. —Considering the difficulties faced by crabs in extracting sufficient nutrients from a plant diet, and their ability to take live prey, how Estuarine communities. —In estuarine have some crabs become predominantly systems, burrowing and foraging by Uca spp. herbivorous? Enhanced survival due to and sesarmids significantly enhances the reduced predation in vegetated areas and in productivity of the marshgrass, Spartina the intertidal, coupled with restricted availalterniflora (Bertness, 1985; Montague, ability of animal prey on a temporal and 1980, 1982), and influences the structure of spatial scale, may have fueled the evolution the benthic infaunal community (Bell et ai, of an increased reliance on plant material 1978; Hoffman et ai, 1984; DePatra and as a food source. Levin, 1989). Risk of predation may be the selection Coral reef communities. — In coral reef pressure that fuels the evolution of special systems, several species of crabs consume adaptations for feeding on some plants. Hay plants, but the impact on the community and coauthors stress predation as the factor itself is indirect. Compared to fish and sea which leads some small marine herbivores urchins, crabs consume little of the benthic to specialize on a particular plant species primary production (Menge et ai, 1983). (1989, 1991). Although they are readily On reef flats of the central Great Barrier consumed when exposed or when associReef, pagurids consume only about 2% of ated with palatable algae, the specialist crabs the benthic algal production (Klumpp and Caphyra rotundifrons and Thersandrus Pulfrich, 1989). Nevertheless, the reef com- compressus experience reduced predation munity would be altered without the activ- by associating with their highly unpalatable ity of herbivorous crabs. Foraging by Mith- and toxic algae which are shunned by both 378 D. L. WOLCOTT AND N. J. O'CONNOR herbivorous and carnivorous fish (Hay et al., 1989, 1991). Predator avoidance may select for herbivory indirectly by limiting the amount of time that is available for foraging. Predator avoidance is cited as the impetus for crabs to risk exposure to conditions high in the intertidal, or even above it, in a mangrove system (Wilson, 1989). The intertidal is a physically stressful environment, with extreme fluctuations in temperature, oxygenation, salinity, and exposure to air. Behavioral adaptations that enhance survival in a physically stressful environment include burrowing and rhythmic patterns of activity. These behaviors reduce the impact of adverse physical factors on the organisms, but also limit the amount of time available for foraging (Seiple, 1981; Wolcott and Wolcott, 1984, 1987). Under these circumstances, the ability to acquire substantial nourishment from plants would be adaptive. Plants, which are ubiquitous although variable in quantity and quality, could provide calories, while opportunistic consumption of higher quality food, through predation or scavenging, provides necessary supplementation of nitrogen and trace nutrients. response "When it is very young" holds true for many terrestrial herbivores, in which the young feed on high-protein food (e.g., milk in mammals, insects in birds) during their period of maximum growth. For herbivorous crabs, the degree of consumption of plant material by juveniles appears to be driven by the incidence of use of plant-dominated microhabitats, probably in response to predator avoidance. Thus, juveniles of the estuarine portunid, Callinectes sapidus, which occupy shallow, vegetated areas as refuges from voracious adult conspecifics and other predators (Orth and van Montfrans, 1987; Williams et al, 1990), consume more plant material as juveniles than as adults (Laughlin, 1982; Alexander, 1986), whereas L. puber juveniles utilize the spatial refuges of the rocky intertidal to reduce their dependence on plant material compared to adults (Choy, 1986). A combination of heavy predation pressure confining crabs to habitats with fewer animal prey and/or harsher physical conditions, and the concomitant evolution of behaviors that limit the impact of physical factors or predators, but also constrain the time available for foraging, are possible determinants of the degree of utilization of plants in the diet of crabs. In summary, crabs are a particularly useful group in which to test predictions about morphological and physiological adaptations to a herbivorous diet based on theory derived from studies in terrestrial systems. Crabs eat a variety of plant material in a wide range of habitats. They possess unique morphological and physiological characteristics that may shape their options for adaptation to a plant diet, such as a hard exoskeleton, cyclical molting, a digestive system that operates tidally, and unique chemoreceptive and enzymatic capabilities. Further laboratory and field studies of herbivory in these animals may modify our understanding of foraging and digestion for herbivores in general. Limited time available for foraging is cited as a likely reason for substantial consumption of brown algae by a nocturnally active portunid, Liocarcinus puber (Choy, 1986). Juveniles of this species, which can continue to forage in crevices, do not consume significant amounts of algae, nor does the closely related L. holsatus, which occurs subtidally. Limited time for food acquisition in the intertidal grapsid, Gaetice depressus, is postulated to have been the selection pressure which added deposit feeding and suspension feeding to the crabs' repertory of feeding behaviors (Depledge, 1989). Limitation of time for foraging also occurs in subtidal crabs, especially in the tropics, where nocturnal feeding by crabs is associated with high densities of diurnally active fish (Hay et al., 1983). On a rocky shore in Panama, herbivorous crabs occur ACKNOWLEDGMENTS in habitats least likely to be occupied by fish Thanks are due to Thomas Wolcott for (Lubchenco and Gaines, 1981). helpful discussion and criticism, and to him T. C. R. White asked the question "When and Scott Dobihal for spousal support duris a herbivore not a herbivore?" (1985). 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