Download Facultative mutualism between an herbivorous crab and a coralline

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