Download Herbivory in Crabs: Adaptations and Ecological

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). His ing manuscript preparation. Thanks to L.
HERBIVORY IN CRABS
Coen, M. Hay, A. Hines, J. McClintock, and
M. Wicksten for providing references and
manuscripts in press. Supported by a grant
from the National Science Foundation.
379
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DePatra, K. D. and L. A. Levin. 1989. Evidence of
the passive deposition of meiofauna into fiddler
crab burrows. J. Exp. Mar. Biol. Ecol. 125:173192.
Depledge, M. H. 1989. Observations on the feeding
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