JOURNAL OF CRUSTACEAN BIOLOGY, 24(4): 652–665, 2004
FACTORS INFLUENCING REFUGE OCCUPATION BY STONE
CRAB MENIPPE ADINA JUVENILES IN MISSISSIPPI SOUND
Virginia R. Shervette, Harriet M. Perry, Chet F. Rakocinski, and Patricia M. Biesiot
(VRS, PMB) University of Southern Mississippi, Department of Biological Sciences,
118 College Drive #5018, Hattiesburg, Mississippi 39406-0001 U.S.A.;
(VRS current address, correspondence) Texas A&M University, Department of Wildlife and
Fisheries Sciences, College Station, Texas 77843-2258, U.S.A. ([email protected]);
(HMP, CFR) Department of Coastal Sciences, University of Southern Mississippi, Gulf Coast
Research Laboratory, 703 East Beach Drive, Ocean Springs, Mississippi 39564, U.S.A.
ABSTRACT
A greater understanding of population dynamics is essential in the management of any species. The
Western Gulf stone crab, Menippe adina, is taken as incidental by-catch in the blue crab, Callinectes
sapidus, fishery in Mississippi. However, there is a lack of information on the ecology of M. adina in
estuaries of the northern Gulf of Mexico. We know that M. adina is associated with hard-bottom habitats
such as rock-rubble jetties and oyster reefs and that this habitat is sparse in Mississippi Sound, which
mainly consists of soft-bottom habitat. Many studies have demonstrated that habitat complexity is
important to several benthic crustaceans because it provides a matrix of different sized refuges that
organisms can use to escape from predation. The importance and availability of refugia varies throughout
the life history of organisms because of the increase in size of an organism as it grows. Refuge limitation
acting on a specific size class may create a demographic bottleneck thereby limiting the production of
a population through mortality, migration, or stunting of the affected size class. We tested this refuge
limitation bottleneck hypothesis in juvenile stone crabs by supplementing an existing oyster reef with four
different sizes of polyvinyl chloride (PVC) pipe. We found that lack of refuge affected both population
size structure and density of large juvenile stone crabs on the reef. We also found that competition for
available refuges may occur among M. adina and two other xanthid crab species, Eurypanopeus depressus
and Panopeus simpsoni. We examined the diet of oyster toadfish, Opsanus beta, in Mississippi Sound and
found that the three xanthid crabs comprised a significantly large portion of oyster toadfish diet. Predation
by O. beta emphasized the importance of the availability of suitable refugia for the xanthids.
The availability of suitable refuge may influence
the density and size structure of populations
(Holroyd, 1975; Hooper and Lennartz, 1983;
Jeffries and Lawton, 1984; Caddy, 1986; Caddy
and Stamatopoulas, 1990; Eggleston et al.,
1990; Wahle and Steneck, 1991; Eggleston
and Lipcius, 1992; Hixon and Beets, 1993;
Beck, 1995, 1997). The structural complexity of
a habitat can facilitate persistence of populations
by providing refuge from predation (Stein and
Magnuson, 1976; Holt, 1984, 1987), by reducing the impacts of physical disturbances
(Howard and Nunny, 1983), and by reducing
physiological stresses (Bertness, 1981). Studies
with shelter-dependent benthic crustaceans such
as hermit crabs (Clibanarius albidigitus Nobili,
1901, Calcinus obscurus Stimpson, 1859,
Pagurus sp. undescribed; Bertness, 1981);
American lobster (Homarus americanus H.
Milne Edwards, 1837; Wahle and Steneck,
1991); spiny lobster (Panulirus argus Latreille,
1804; Eggleston et al., 1990; Eggleston and
Lipcius, 1992); and an amphipod (Gammarellus
angulosus Rathke, 1843; Hacker and Steneck,
1990) have documented the importance of
shelter in the regulation of abundance, density,
and size structure of local populations.
The quality and quantity of refugia are
important factors regulating populations and
may restrict the abundance of a specific size
class or ontogenetic stage, thus creating a shelter
limitation bottleneck (Caddy, 1986; Caddy and
Stamatopoulos, 1990; Beck, 1995). Caddy
(1986) suggests that the importance and availability of refuge may vary throughout the life
history of growing organisms. Refuge limitation
acting on a specific size class may create
a population bottleneck that limits the overall
production of a population through mortality,
migration, or stunting of the size class affected
(Caddy and Stamatopoulos, 1990; Beck, 1995).
Previous studies of benthic decapods have
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SHERVETTE ET AL.: REFUGE UTILIZATION BY MENIPPE ADINA JUVENILES
illustrated that survival of individuals within
specific size classes is positively correlated with
the availability of refuge. Eggleston et al.
(1990) found that small- and medium-sized
juvenile spiny lobsters, P. argus, have lower
mortality rates in small- and medium-sized
refuges than in large refuges. In the American
lobster, H. americanus, the abundance of early
benthic stages depends on the percentage of
ocean bottom covered by cobble (Wahle and
Steneck, 1991). Also, Heck and Coen (1995)
have linked regional availability and suitability
of refuge to juvenile blue crab, Callinectes
sapidus Rathbun, 1896, abundance in the Gulf
of Mexico (GOM).
The Western Gulf stone crab, Menippe adina
Williams and Felder, 1986, is associated with
rock-rubble jetties and oyster reefs in northern
GOM estuaries (Stuck and Perry, 1992). Currently, the species supports small, developing
fisheries in Texas and Louisiana and occurs as an
incidental by-catch in the blue crab fishery in
Mississippi and Alabama (Guillory et al., 1995).
Stuck and Perry (1992) found that M. adina
completes its life cycle within Mississippi
waters; larvae are not exported offshore but
remain in the estuary. The species did not appear
to be recruitment limited (K. Stuck, personal
communication) because small juveniles (10–24
mm carapace width) were relatively abundant
(26 juveniles/0.1 m3 of oyster shell) in Mississippi Sound. Larger juveniles, however, were
not abundant (Stuck and Perry, 1992), and their
numbers may be related to quality and quantity
of suitable habitat. Other studies also suggest
that post- settlement habitat may regulate
population abundance in species of Menippe.
Gibbs (1994) found that shelter size and
abundance were limiting factors for juvenile M.
adina populations in Alabama. Beck (1995,
1997) reported that shelter limitation exerted
control on both size structure and density in
populations of hybrid stone crabs (M. adina/M.
mercenaria) in Florida waters.
Predation, lack of extensive hard-bottom
habitat, and competition for limited space may
interact to influence population levels of stone
crabs in Mississippi coastal waters. The objective of the present study was to examine factors
affecting seasonal and ontogenetic refuge utilization by juvenile M. adina in Mississippi
Sound. Specifically, we hypothesized that lack
of refuge controls the abundance of a specific
size class of juvenile M. adina. The establishment of low profile artificial reefs in Mississippi
653
Sound provided an opportunity to investigate
refuge limitation in stone crabs.
MATERIALS AND METHODS
Study Site
The study site is characterized by small subtidal patch oyster
reefs and located at 308209300N, 888469300W. Surrounding
sediments are primarily silty muds, which are responsible for
high turbidity in the nearshore waters. There is low tidal
amplitude, and water depth over the reefs ranges from 1.5 m
to 2 m. The natural habitat was enhanced in 1994 by addition
of a low profile artificial reef comprised of oyster shell. The
reefs provide habitat for an array of potentially interacting
benthic marine organisms, including the xanthid crabs M.
adina, Panopeus simpsoni Rathbun, 1930, and Eurypanopeus depressus Smith, 1869, and the oyster toadfish Opsanus
beta Goode and Bean, 1879, a known predator of xanthid
crabs (Gosline, 1996; VRS, personal observation).
Overview and Experimental Design
To determine whether the availability of refuges affected
certain size classes of juvenile stone crabs disproportionately,
we supplemented the reef with four different sizes of PVC
pipe embedded in concrete. We refer to these as our shelter
samplers. In addition, we examined ambient densities and
distributions of size class of juvenile stone crabs on the study
reefs to determine whether additions of refuge attracted
specific size classes of stone crabs. We refer to these as our
reef samplers. The refuge limitation bottleneck hypothesis
predicts that the class most likely to be shelter-limited is the
size class of crabs attracted to artificial refuges in the greatest
densities.
We deployed shelter samplers on a portion of the artificial
reef site at a distance of ;200 m from shore. The physical
conditions of the study site predicated sampler design. High
turbidity precluded in situ visual observation. Accordingly,
we designed samplers that could be removed from the water
for inspection. We constructed samplers out of sections of
PVC pipe embedded in cement (Fig. 1). We used four sizes of
pipe (13 mm, 26 mm, 39 mm, and 52 mm diameter) to sample
the size range of stone crab juveniles (, 60 mm carapace
width) occurring in the Mississippi Sound (Stuck and Perry,
1992). Shelter diameters were not mixed within a sampler in
order to minimize the influence of potential interactions
between large and small stone crabs. We embedded sections
of pipe at a 458 angle in a 0.5 m2 cement block so that the lip
of the pipe was flush with the cement. Pipe length was scaled
in proportion to pipe diameter to accommodate stone crab
morphometry; the two smaller diameters were scaled with
a diameter : length ratio of 1:2, whereas the two larger
diameters had a 1:3 ratio. Each sampler contained ten lettered
pipes of a single diameter (one treatment).
We randomly deployed twelve samplers, representing the
four size treatments with three replicates each. All samplers
were separated by at least 5 m over the artificial reef. Divers
deployed and retrieved the shelter samplers. We retrieved
samplers as close to midday as possible because stone crabs
are nocturnal and are found in shelter during the daytime
(Beck, 1995, HMP, personal observation). Prior to retrieval,
we covered samplers with foam-backed tops to prevent
escapement of animals. Upon retrieval of the shelter
samplers, we removed all organisms and placed them in
labeled containers corresponding to the shelter diameter and
tube position on the cement sampler and cleared away
biofouling organisms such as barnacles and oyster spat.
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 24, NO. 4, 2004
Immediately after removal of organisms, we returned
samplers to the water. We conducted the sampling routinely
twice each month from April 1999 to June 2000; in April
1999, June 1999, and April 2000 we retrieved shelter
samplers only once. On the three occasions when we lost
some of the shelter samplers, we replaced the missing
samplers before the next sampling period. We retrieved
a total of 291 shelter samplers during the study.
The animals were transported to the University of
Southern Mississippi, Gulf Coast Research Laboratory
(GCRL), Ocean Springs, Mississippi, for analysis. We measured crabs’ carapace width (CW) and carapace length (CL)
to the nearest mm and weighed them to the nearest 0.1 g.
We measured fish total length (TL) and standard length
(SL) to the nearest mm and weighed them to the nearest 0.1 g.
Background Population of the Stone
Crab Menippe adina
We estimated the ambient population abundance of M. adina
on the artificial reef quarterly. We deployed three crates,
each filled with 0.025 m3 of oyster shell, placed ;3 m apart
on the reef. We removed the three crates (reef samplers) after
a soak time of three months (one quarter) and replaced them
with fresh crates of oyster shell. During the first quarter, we
were able to retrieve only two crates. No reef sampler data
were available for the fourth quarter (January–March 2000).
After we removed the reef samplers from the water, we
immediately placed them in seawater-soaked oyster sacks
and returned to GCRL for processing. We washed the
contents of each reef sampler over 1-mm mesh screening
and collected all organisms. We froze samples at 208C until
analysis. After thawing, we sorted each sample and recorded
the total number of each species. We measured crab
specimens to the nearest 0.1 mm CW.
Diet Characterization of the Oyster
Toadfish Opsanus beta
To quantify predation on xanthid crabs by O. beta, we
analyzed gut contents. After collecting toadfish from the
shelter samplers during April–September 1999, we placed
them on ice and transported them to GCRL. We removed and
opened digestive tracts, including the esophagus, stomach,
and intestine, and designated them as either empty or
containing food. We used 10% buffered Formalin to fix the
contents of each digestive tract for 48 h and then transferred
contents to 90% ethanol. We placed digestive tract contents
onto a 0.42-mm mesh sieve and gently rinsed them with fresh
water. We identified prey items to the lowest taxon possible,
then counted, and weighed (blotted wet weight) them to the
nearest 0.01 g. We measured any crab parts found in O. beta
digestive tracts to the nearest 0.1 mm.
Gut content analysis followed standard techniques
described in Hyslop (1980). We pooled dietary data from
all digestive tracts. We calculated percent numeric abundance (% N), percent total weight (% W), and percent
frequency of occurrence (% F) of prey items as: % N ¼
(number of individuals of prey taxon / total number of all
prey) 3 100; % W ¼ (weight of one prey taxon / total weight
of all prey) 3 100; and % F ¼ (number of stomachs
containing prey of one taxon / total number of stomachs that
contained any prey item) 3 100. We calculated the index of
relative importance (IRI), where the importance of an item
is directly related to the magnitude of the value, as: IRI ¼
(% N þ % W) 3 % F.
We calculated percent IRI (% IRI) as the IRI value of
each prey taxon divided by the sum of the IRI values
Fig. 1. Diagram of 0.5 m2 shelter samplers used in this
study. Top view of sampler showing the relative placement
and identification of the ten shelters within each sampler.
Side view of sampler showing 458 angles of shelters within
each sampler.
multiplied by 100 (Pinkas et al., 1971; Eggleston and
Bochenek, 1990; Cortés, 1997, 1998). Although recent
authors (MacDonald and Green, 1983; Hansson, 1998) have
criticized IRI and % IRI, this index is widely used and
accepted (Liao et al., 2001; Hahn and Delariva, 2003). It
enables comparisons with other studies and provides a single
measure of diet that is less biased than % N, % W, and % O
(Cortés, 1997, 1998; Liao et al., 2001; Bush, 2003).
We found O. beta in the shelter samplers only during
their reproductive period. After examination of their guts,
we realized that toadfish were consuming toadfish eggs and
newly hatched juveniles. We collected a set of O. beta from
Mississippi Sound in October 1999 for comparison of O.
beta diet outside of their reproductive period, when toadfish
eggs and juveniles were not available for consumption. Once
caught, O. beta were placed on ice and transported to
GCRL. Examination and analysis of gut contents were
performed in the same manner as fish collected from shelter
samplers. We excluded empty digestive tracts from the
computations.
Statistical Analyses
Occupation rates for each of the four shelter sizes were
calculated on a quarterly basis for M. adina. Low occupation
rates and non-normal distribution of data precluded the use
of parametric tests. We constructed three-dimensional
contingency tables (Zar, 1984) for the first four quarters in
order to test the null hypothesis that shelter size, quarter, and
occupation were mutually independent of each other. We
conducted tests of partial independence to test whether each
variable was independent of the other two. Chi-square tests
were performed using a rejection level of P , 0.05, and all
assumptions for this analysis were met.
In order to determine whether similar-sized crabs of
different species inhabited the same sizes of shelter, we
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SHERVETTE ET AL.: REFUGE UTILIZATION BY MENIPPE ADINA JUVENILES
Table 1. Species associated with the shelter samplers. Total number of individuals found are given; the percentages of total
shelters occupied are in parentheses. A total of 291 shelter samplers were analyzed during the study.
Shelter diameters
Species
Common name
13 mm
26 mm
39 mm
52 mm
Menippe adina
Eurypanopeus depressus
Panopeus simpsoni
Callinectes sapidus
Clibanarius vittatus
Palaemonetes vulgaris
Alpheus angulatus
Stramonita haemastoma
Opsanus beta
Hypsoblennius ionthas
Hypsoblennius hentzi
Gobiesoma robustum
Gobiesox stromosus
Myrophis punctatus
Lutjanus griseus
Unoccupied
Stone crab
Flat mud crab
Mud crab
Blue crab
Striped hermit crab
Grass shrimp
Snapping shrimp
Oyster drill
Oyster toadfish
Freckled blenny
Feather blenny
Code goby
Skilletfish
Speckled worm eel
Gray snapper
47 (6.4%)
39 (5.3%)
31 (4.2%)
5 (0.7%)
5 (0.7%)
1 (0.1%)
0 (0.0%)
0 (0.0%)
1 (0.1%)
7 (1.0%)
1 (0.1%)
17 (2.3%)
3 (0.4%)
0 (0.0%)
0 (0.0%)
573 (78.5%)
60 (8.1%)
17 (2.3%)
45 (6.1%)
4 (0.5%)
3 (0.4%)
0 (0.0%)
2 (0.3%)
0 (0.0%)
1 (0.1%)
11 (1.5%)
3 (4.1%)
16 (2.2%)
6 (0.8%)
0 (0.0%)
0 (0.0%)
578 (77.3%)
44 (6.1%)
10 (1.4%)
17 (2.4%)
7 (1.0%)
6 (0.8%)
6 (0.8%)
0 (0.0%)
1 (0.1%)
15 (2.1%)
3 (0.4%)
0 (0.0%)
15 (2.1%)
15 (2.1%)
2 (0.3%)
2 (0.3%)
577 (80.1%)
40 (5.5%)
4 (0.5%)
1 (0.1%)
5 (0.7%)
3 (0.2%)
10 (1.4%)
2 (0.3%)
0 (0.0%)
128 (17.5%)
4 (0.5%)
0 (0.0%)
12 (1.6%)
12 (1.6%)
15 (2.1%)
1 (0.1%)
493 (67.5%)
compared carapace widths of the three xanthid crab species
occupying all but the largest diameter shelter using one-way
ANOVA (Zar, 1984). Small sample sizes precluded testing
the 52-mm diameter shelters. Because variances were
heterogeneous and transformation of data did not correct
this, post hoc comparisons among pairs of means followed
the Games-Howell method (Sokal and Rohlf, 1981). Due to
the repetitive calculations of the hypothesis, the P was
adjusted using the Dunn Sidak procedure (Sokal and Rohlf,
1981), which produced a P value of 0.013 rather than 0.05
for these comparisons. We compared the size distributions
of xanthid crabs in the shelter samplers to the size distributions of crabs found in the artificial reef samplers by
using Smirnov-Kolmogorov two-sample tests (Sokal and
Rohlf, 1981). We used v2 tests with Yates correction for
continuity (Zar, 1984) to compare frequencies of large
(CW . 36 mm) and small (CW 36 mm CW) M. adina
occurring in shelter samplers and reef samplers. This size
breakpoint was chosen because it was the upper limit of
carapace width for the other xanthid species.
We compared co-occurrence of the three xanthid species
among seasons and by sampler type using three-dimensional
contingency tables. Because sampling effort was unequal,
the frequencies of crabs within the shelter samplers were
scaled accordingly (i.e., without changing the total frequency). We conducted tests of partial independence to determine whether each variable was independent of the other
two. Finally, we used Spearman rank-order correlation
analysis (Dytham, 2003) on the percent occupation of M.
adina and O. beta in the 52-mm diameter shelters in order to
test the null hypothesis that no correlation existed between
M. adina and O. beta occupation of 52-mm shelters over
time. In this case, we determined percent occupation by
dividing the number of shelters M. adina and O. beta
occupied individually by the total number of occupied
shelters for a particular month.
The diet of O. beta during the reproductive period was
compared statistically with their diet outside of the reproductive period by using a 2-way contingency table. Chisquare tests were performed with the frequency of
occurrence data using a rejection level of P , 0.05 in order
Total
191
70
94
21
17
17
4
1
145
24
4
85
36
17
3
2215
(6.5%)
(2.4%)
(3.2%)
(0.7%)
(0.6%)
(0.6%)
(0.2%)
(0.02%)
(5.0%)
(1.1%)
(0.1%)
(2.9%)
(1.3%)
(0.6%)
(0.1%)
(75.9%)
to test the null hypothesis that diet composition of O. beta is
independent of their reproductive period.
RESULTS
Organisms Found in Association with
Shelter Samplers
The stone crab M. adina was the most abundant
species occupying shelter samplers, followed by
the xanthid crabs P. simpsoni and E. depressus
(6.5%, 3.2%, and 2.4% total occupancy, respectively) (Table 1). The blue crab, C. sapidus,
occurred occasionally (0.7%). The striped hermit
crab, Clibanarius vittatus, (Bosc, 1802), was the
only anomuran crab collected on the samplers
(0.6 %). Several other invertebrates inhabited the
shelter samplers infrequently. Grass shrimp
Palaemonetes vulgaris (Say, 1818); snapping
shrimp Alpheus angulatus McClure, 1995; and
the oyster drill Stramonita haemastoma (Linnaeus, 1758) occurred in 0.6%, 0.1%, 0.02% of
the shelters, respectively. Seven species of fish
were found in the shelter samplers. The oyster
toadfish, O. beta, occurred most often and
occupied 5.0% of the shelters, followed by the
code goby, Gobiosoma robustum Ginsburg,
1933 (2.9%). Skillet fish, Gobiesox strumosus
Cope, 1870; speckled worm eel, Myrophis
punctatus Luetken, 1852; freckled blenny,
Hypsoblennius ionthas (Jordan and Gilbert,
1882); feather blenny, Hypsoblennius hentzi
(Lesueur, 1825); and juvenile gray snapper,
Lutjanus griseus (Linnaeus, 1758) were also
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 24, NO. 4, 2004
Fig. 2. Quarterly occupation by Menippe adina for each shelter diameter. Number before each slash represents the number
of shelters occupied during that quarter. Number after each slash represents total number of shelters available for that size
class during that quarter.
found occasionally in the shelters. A large
percentage of shelters were empty (75.9%).
Occupation of Shelter Samplers and Reef
Samplers by Xanthid Crabs
Menippe adina first appeared in shelter samplers
in June of the first quarter, with percent
occupation ranging from 1% to 2% in the four
different sizes of shelter. Occupation rates were
highest in the second quarter for the two
smallest diameter shelters and were highest in
the third through fifth quarters for the 26-mm
and 39-mm diameter shelters, reflecting temporal shifts in crab size distributions (Fig. 2).
Occupation rate, shelter diameter, and quarter
were not mutually independent (v2 ¼ 80.79,
d.f. ¼ 24; P , 0.001). Subsequent v2 tests for
partial independence demonstrated that none of
the three factors could be eliminated from consideration (v2 . 44, d.f. ¼ 15–21; P , 0.005).
Together this means that occupation of shelter
samplers by M. adina was correlated with
quarter and shelter size.
Menippe adina in the shelter samplers were
significantly larger than those in the reef
samplers (Fig. 3) (Smirnov Z ¼ 2.598; P ,
0.001). Seventeen percent of crabs in the shelter
samplers were greater than 36 mm CW, whereas
4% of crabs in reef samplers were greater than
36 mm CW (v2c ¼ 7.4; P , 0.01). When the
three smallest size classes were excluded from
consideration, 23% of crabs in the shelter
samplers were greater than 36 mm CW and
7% of crabs in reef samplers were greater than
36 mm CW (v2c ¼ 4.4; P , 0.05).
Eurypanopeus depressus in the shelter samplers were significantly larger than those found
in the reef samplers (Fig. 4) (Smirnov Z ¼
2.940; P , 0.001). Crabs in the reef samplers
were smaller, with the mode at 4–6 mm CW,
whereas the mode was 10–12 mm CW in the
shelter samplers. In contrast, the size distributions of P. simpsoni were not significantly
different between the two sampler types (Fig. 5)
(Smirnov Z ¼ 1.021; P ¼ 0.253).
Co-occurrence of Menippe adina
and Other Species
For all xanthid crabs, the range of carapace
widths increased with increasing shelter diameter for the first three sizes (Fig. 6). Small
xanthid crabs (CW , 10 mm) occurred in all
SHERVETTE ET AL.: REFUGE UTILIZATION BY MENIPPE ADINA JUVENILES
Fig. 3. Size distribution of the stone crab Menippe adina in
(A) shelter samplers (n ¼ 134) and (B) reef samplers (n ¼
85). Data are for the April–June 1999, July–September
1999, and October–December 1999 quarters. Abscissa
values are the upper bound of each carapace width category.
four sizes of shelter, but presence in the largersized shelters appeared to be associated with
biofouling. In the 13-mm diameter shelters,
mean carapace widths were 11.3, 11.6, and
9.8 mm for M. adina, P. simpsoni, and E.
depressus, respectively. Although the degree of
difference among the mean carapace widths was
slight, P. simpsoni were significantly larger than
E. depressus (one-way ANOVA: Sidak’s correction for P ¼ 0.013; Games-Howell post hoc, P
¼ 0.005). In the 26-mm diameter shelters, the
mean carapace width of E. depressus was
significantly smaller (10.7 mm; P , 0.001) than
both of the other crabs (M. adina, 19.5 mm; P.
simpsoni, 20.0 mm). In the 39-mm diameter
shelters, M. adina (30.0 mm CW) was significantly larger (P , 0.005) than P. simpsoni (CW
20.3 mm) and both were significantly larger
(P , 0.005) than E. depressus (CW 10.6 mm).
The relative abundance of small xanthid
crabs (CW , 36 mm) varied monthly, but the
657
Fig. 4. Size distribution of Eurypanopeus depressus in (A)
shelter samplers (n ¼ 51) and (B) reef samplers (n ¼ 758).
Data are for the April–June 1999, July–September 1999, and
October–December 1999 quarters. Abscissa values are the
upper bound of each carapace width category.
species still co-occurred seasonally in the
shelter samplers (Fig. 7). During the first two
months of the study, we collected only P.
simpsoni and E. depressus. However, during
June 1999–March 2000, M. adina occurred in
greater numbers than either of the other two
xanthids. During April–June 2000, P. simpsoni
occurred in greater numbers than M. adina and
E. depressus.
Overall, M. adina was predominant in the
shelter samplers, comprising 59.3% of xanthid
crabs collected, whereas E. depressus and P.
simpsoni comprised 20.5% and 20.2%, respectively (Table 2). In the artificial reef samplers,
E. depressus was the dominant species, comprising 86.5%, followed by M. adina with 9.7%
and P. simpsoni at 3.8%. Occurrence of the
three xanthid species was not independent of
sampler type or quarter (v2 ¼ 690, d.f. ¼ 12; P ,
0.001). Subsequent v2 tests for partial independence demonstrated that none of the three
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 24, NO. 4, 2004
factors could be eliminated from consideration
(v2 . 173, d.f. ¼ 8–10; P , 0.001). These
results indicate that occurrence of the three
xanthid species was significantly correlated with
sampler type and quarter.
An inverse relationship existed in the temporal distribution of M. adina and the oyster
toadfish O. beta in the 52-mm diameter shelters
(Fig. 8). Occupation of each species was
significantly correlated (Spearman rank-order
correlation: rs ¼ 0.805, P , 0.001, n ¼ 15).
Opsanus beta showed a peak occupation of
100% in April and May 1999 with a decline to
22% by September. No O. beta occurred in the
shelters from October 1999 through February
2000, but it recurred in March 2000. Menippe
adina began occupation of the 52-mm shelters
in June 1999 and continued to occupy these
shelters through May 2000, peeking in October
1999, utilizing 80% of occupied shelters.
Diet Characterization of the Oyster
Toadfish, Opsanus beta
We examined the gut contents from 27 toadfish
collected in shelter samplers during April–
September 1999. These fish ranged in size from
97 mm to 198 mm TL (24–128 g total weight).
The diet comprised six main prey types: M.
adina, E. depressus, P. simpsoni, miscellaneous
crustaceans (which included Callinectes spp.
and Palaemonetes spp.), molluscs (which included unidentified gastropods and hooked
mussel Ischadium recurvum (Rafinesque,
1820)), and the eggs and juveniles of O. beta
(Fig. 9). Xanthid crabs were an important
component of the diet. They occurred in 63.1%
of the digestive tracts containing food, represented 17.8% of the total number of prey, and
made up 58.0% of the total weight of prey. The
xanthid crabs had a total %IRI of 34.4, second
only to that of toadfish eggs (%IRI ¼ 58.0). The
stone crab M. adina accounted for 7.5% of the
total number, 26.0% of the total weight, and
26.0% of the occurrence in the diet. Eurypanopeus depressus was equally important, comprising 7.5% of the total number, 21.1% of the total
weight, and 26.0% of the occurrence. In
contrast, P. simpsoni comprised 2.8% of the
total number, 10.9% of the total weight, and
11.1% of the total occurrence.
We examine the gut contents of 51 toadfish
caught in Mississippi Sound outside of the
reproductive period (October 1999). These fish
ranged in size from 90 mm to 230 mm TL. The
diet comprised five main prey types: Menippe
Fig. 5. Size distribution of Panopeus simpsoni in (A)
shelter samplers (n ¼ 57) and (B) reef samplers (n ¼ 33).
Data are for the April–June 1999, July–September 1999, and
October–December 1999 quarters. Abscissa values are the
upper bound of each carapace width category.
adina, Eurypanopeus depressus, Panopeus
simpsoni, miscellaneous crustaceans (which included Callinectes spp. and Palaemonetes spp.),
and molluscs (which included unidentified
gastropods and hooked mussel Ischadium recurvum) (Fig. 10). Xanthid crabs were a significantly more important component of toadfish
diet outside of the reproductive period (v2 ¼ 126,
d.f. ¼ 5; P , 0.0001). They occurred in 84.3% of
the digestive tracts containing food, represented
69.2% of the total number of prey, and made up
90.4% of the total weight of prey. The xanthid
crabs had a total %IRI of 83.7. The stone crab M.
adina accounted for 36.2% of the total number,
73.4% of the total weight, 51.0% of the
occurrence in the diet, and had a %IRI of
61.0%. Eurypanopeus depressus comprised
27.7% of the total number, 7.6% of the total
weight, and 47.1% of the occurrence. In contrast,
P. simpsoni comprised 5.4% of the total number,
SHERVETTE ET AL.: REFUGE UTILIZATION BY MENIPPE ADINA JUVENILES
659
Fig. 6. Size frequency distribution of xanthids Menippe adina, Panopeus simpsoni, and Eurypanopeus depressus by shelter
diameter. Rectangles represent the middle half of the sample with an end at each quartile. The horizontal line inside the box
represents the median. Vertical lines with horizontal line attached at extremes represent the range of data excluding outliers.
Circles represent outliers.
2.0% of the total weight, and 7.8% of the total
occurrence.
DISCUSSION
Refuge Limitation
Mollusc shells, seagrass meadows, and other
substrates provide refuge for various marine
organisms, thereby reducing predation and
enhancing survival of resident species including
shrimp (Everett and Ruiz, 1993), spiny lobster
(Herrnkind and Butler, 1986; Lozano-Alvarez
et al., 1994), European lobster (Howard, 1980),
crabs (Heck and Thoman, 1981; Heck and
Wilson, 1987; Orth and van Montfrans, 1990;
Williams et al., 1990; Wilson et al., 1990; Beck,
1995, 1997), and fishes (Jara and Cespedes,
1994; Potts and Hulbert, 1994). Refuge requirements change throughout ontogeny, and the
availability of suitable shelter may decline as
organisms increase in size (Caddy, 1986). A
demographic bottleneck occurs when the rate of
decline in the availability of refugia falls below
the rate of decline in the number of older and
larger individuals in the population. Past research demonstrated that size-specific refuge
bottlenecks influence population abundance of
M. adina juveniles in Alabama (Gibbs, 1994)
and juveniles and adults of Menippe hybrids in
Florida (Beck, 1995, 1997). Our study demonstrated ontogenetic and seasonal changes in
utilization of shelter in populations of M. adina
in Mississippi Sound. Although, the overall
occupation rate of shelter samplers by M. adina
was low. Large M. adina (CW . 36 mm) were
more common in shelter samplers than in reef
samplers, whereas small crabs (CW , 36 mm)
were more abundant in the reef samplers. This
suggests that refuge limitation is occurring,
assuming that the size distribution of refugia
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 24, NO. 4, 2004
Fig. 7. Monthly occupation of all shelters combined by Menippe adina, Panopeus simpsoni, and Eurypanopeus depressus
with CW , 36 mm. Data are reported as total number of crabs caught per sampling month. Numbers at each point represent
actual number of crabs collected from shelters for specified month.
within the reef samplers reflects that of the
natural environment. Even when small size
classes were excluded from the analysis to
eliminate possible size biases between collector
types, large crabs were still significantly more
common in shelter samplers. Stuck and Perry
(1992) reported size class distributions of M.
adina juveniles collected from all over Mississippi Sound that were similar to what we
found in reef samplers, although a direct comparison is difficult because they utilized different
sampling methods. Gibbs (1994) also found that
larger refuges may be limiting for juvenile M.
adina in Alabama waters.
Quarterly occupation rates by M. adina in the
shelter samplers never exceeded 20%. Overall
occupation rate of shelter samplers may reflect
low ambient population densities at the study site
or may be a function of the sampling design and
methodology. Lindberg et al. (1990) and Frazer
and Lindberg (1994) found that the spacing of
shelter samplers (‘‘artificial reef modules’’) was
directly related to the number of adult Menippe
(predominantly M. mercenaria-like hybrids) in
Table 2. Total numbers of xanthid crabs Menippe adina, Eurypanopeus depressus, and Panopeus simpsoni occurring in
shelter samplers and reef samplers. Shelter samplers were collected every two weeks; the numbers represent the cumulative
number of crabs for each quarter. Reef samplers were collected every three months. Percentage of total crabs is given in
parentheses. ND, no data collected.
Shelter samplers
Date
April–June 1999
July–September 1999
October–December 1999
January–March 2000
Total
M. adina
7
74
53
42
176
(14.6%)
(67.9%)
(62.4%)
(76.3 %)
(59.3%)
E. depressus
12
16
23
10
61
(25.0%)
(14.7%)
(27.1%)
(18.2%)
(20.5%)
Reef samplers
P. simpsoni
29
19
9
3
60
(60.4%)
(17.4%)
(10.6%)
(5.5%)
(20.2%)
M. adina
E. depressus
P. simpsoni
12 (2.8%)
24 (9.8%)
49 (23.6%)
ND
85 (9.7%)
389 (91.7%)
210 (86.1%)
159 (76.4%)
ND
758 (86.5%)
23 (5.4%)
10 (4.1%)
0 (0.0%)
ND
33 (3.8%)
SHERVETTE ET AL.: REFUGE UTILIZATION BY MENIPPE ADINA JUVENILES
661
Fig. 8. Monthly changes in total percent occupation of 52-mm shelters by Menippe adina and Opsanus beta. Number
before each slash represents the number of shelters occupied by specified species. Number after each slash represents total
number of shelters occupied that month by all species combined.
their samplers. Widely spaced refuges (;60 m
apart) attracted significantly more crabs than
closely spaced shelters (;2 m apart). The
authors suggested that density-dependent prey
depletion was a function of refuge dispersion.
More widely spaced shelters within a sampler (in
general and/or in concert with increasing shelter
diameter) or more widely spaced shelter samplers across the reef may have increased
occupation rates in the present study; however,
differences in ecology of the two taxa complicate
direct comparisons. Juvenile M. adina are
usually associated with oyster reefs (Stuck and
Perry, 1992) where prey densities are high (Perry
et al., 2001).
Sinclair (1977) emphasized the highly agonistic (attack-escape) behavior of M. mercenaria in Florida in which dominance was
correlated with larger size, the male sex, and
prior possession of a shelter. Although M. adina
exhibit less aggressive behavior (HMP, personal
observation) than M. mercenaria, intraspecific
competition among the larger juveniles manifested through agonistic behavior could have
affected the occupation rate of shelter samplers
because actual shelters within each sampler
were closely spaced. Large juveniles may have
prohibited other juveniles of similar size access
to shelters within the same shelter sampler
through aggressive encounters.
The level of structural complexity of the
natural reef at the study site may have been an
important factor in limiting stone crab population abundance. The distribution and abundance
of large juvenile M. adina could, in part, be
dependent on the age and extent of oyster reef
habitats. The current study was conducted in an
area of small, low relief, patch oyster reefs. An
older, more extensive oyster reef with greater
complexity of shelter sizes may have supported
more and larger stone crabs.
Potential Interactions Among Xanthid Crabs
Menippe adina, E. depressus, and P. simpsoni
are common on local oyster reefs in Mississippi
Sound (Perry et al., 2001) and may compete for
food and space.
Indeed, size ranges of small crabs and
seasonal occurrences of the three species overlapped considerably. Panopeus simpsoni
662
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 24, NO. 4, 2004
Fig. 9. Percent numerical abundance (% Number), percent total weight (% Weight), percent frequency of occurrence
(% Frequency), and percent index of relative importance (% IRI) for prey items in the diet of Opsanus beta found in the
shelter samplers during reproductive period.
dominated the shelter samplers during the first
quarter of sampling when few M. adina were
present. In the remaining three quarters of
sampling, M. adina occurred in greater numbers
in all shelter sizes than did the other two
xanthids. There was little difference in the
proportion of E. depressus and P. simpsoni
during this time period. In contrast, the reef
samplers were dominated by E. depressus
(; 87% of the crabs), a smaller, less aggressive
species. Elevated numbers of E. depressus in
reef samplers may also reflect the relatively high
availability of small refugia in this sampler type.
Competition appears to influence the pattern of
shelter occupation by xanthid crabs. Juvenile M.
adina exhibited intraspecific competition as well
as interspecific competition with E. depressus for
shelter in coastal Alabama waters (Gibbs, 1994).
In that study, only one M. adina was found per
clump of oyster shells in the field, whereas
sometimes several E. depressus occurred in
a clump of shells that also contained M. adina
in one of the shells. In the laboratory portion of
that study, M. adina outcompeted similar-sized
E. depressus for shelter. These observations may
help to explain the differences in distribution
pattern of the xanthid species between the two
sampler types in the present study.
Interactions Between Opsanus beta
and Xanthid Crabs
The inverse temporal relationship between the
occurrence of M. adina and O. beta in the 52-mm
diameter shelters suggests a potential interaction,
either competition or predation. Alternatively,
this relationship may be a function of their offset
seasonal life-history patterns. Beck (1995) demonstrated that Menippe hybrids outcompeted O.
beta in his 50-mm diameter shelters; however,
his experiments were conducted outside of the
toadfish reproductive season when it would not
normally occupy shelters. In the present study,
O. beta occurred in the 52-mm diameter shelters
from March through September. Lack of year
class one (1þ) M. adina in the large sized shelters
during the reproductive period of O. beta may
simply reflect emigration of larger stone crab
juveniles to more suitable habitats rather than
competition or predation.
Predation by O. beta may affect the distribution and abundance of xanthid crabs. Larsen et
al. (2001) documented the occurrence of O. beta
in our study area during June–August 1998 and
December–March 1998/99. We collected O.
beta in the 39- and 52-mm shelter samplers
during April–June 1999 and July–September
SHERVETTE ET AL.: REFUGE UTILIZATION BY MENIPPE ADINA JUVENILES
663
Fig. 10. Percent numerical abundance (% Number), percent total weight (% Weight), percent frequency of occurrence
(% Frequency), and percent index of relative importance (% IRI) for prey items in the diet of Opsanus beta found in
Mississippi Sound outside of reproductive period.
1999 and in the 13- and 26-mm shelter samplers
during October–December 1999. Our diet study
suggested that the toadfish analyzed fed mainly
on xanthid crabs and toadfish eggs. Gut content
analysis of toadfish collected from other areas of
the Mississippi Sound in October 1999 also
revealed a high frequency of occurrence for
xanthid crabs when toadfish eggs and juveniles
were no longer available. Schwartz and Dutcher
(1963) found similar results for Opsanus tau
Linnaeus, 1766; toadfish eggs were eaten
readily during the spawning season but xanthid
crabs dominated the diet at other times.
Opsanus tau feeds on mud crabs Panopeus
herbstii (H. Milne Edwards, 1834), E. depressus, and Neopanope sayi; blue crab, C. sapidus;
grass shrimp Palaemonetes spp.; squid Loligo
spp.; and fishes G. bosc, G. strumosus, and
Menidia spp. (Schwartz and Dutcher, 1963;
Wilson et al., 1982; Bisker et al., 1989). The
fact that O. beta appear to feed primarily on
xanthid crabs and that they were collected from
our study area year-round may indicate that O.
beta is a dominant predator of xanthids. This
kind of predation pressure on the xanthid crabs
indicates a need for refuge.
Competition for shelter and food may be
stronger among the three xanthid species in the
presence of toadfish and/or other predatory fish.
Local fishers from Mississippi Sound catch
Sciaenops ocellatus (Linnaeus, 1766) and Pogonias cromis (Linnaeus, 1766), both of which
are documented xanthid predators (Scharf and
Schlicht, 2000; VRS, personal observation).
Predators shape the patterns of habitat use and
species interactions by more than just removal of
individuals. In the course of foraging for food,
many mobile benthic animals routinely choose
among habitats and feeding sites that differ in
the net energetic return and the risk of death
(Holt, 1984; Gilliam and Fraser, 1987; Hixon
and Menge, 1991). Foragers may shift habitats
or demonstrate other behavioral changes when
predators are present (Schmitt, 1985, 1987;
Gilliam and Frazer, 1987). Obviously predation
is an important factor in the lives of xanthid
crabs. In the case of this study, M. adina may be
limited by shelter availability because of its
vulnerability to predation.
Summary
Evidence presented in this study emphasizes the
importance of comparing responses to refuge
throughout juvenile ontogeny for M. adina in
order to evaluate the critical features of the
habitat affecting Mississippi Sound populations.
664
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 24, NO. 4, 2004
Our experiment points to the class most likely to
be shelter limited and suggests that shelter
availability may have strong effects on demographic parameters. The oyster reef appears
to provide ample refuge for smaller juveniles,
but large juveniles find few areas with appropriate structural relief in which to shelter.
Currently, the theoretical and empirical frameworks suggest that the strongest associations
with refuge are related to predation (Holt 1987;
Hixon and Menge, 1991), which our study
supports in the case of M. adina juveniles. As
illustrated from the diet analyses, toadfish predominately consumed M. adina and two other
xanthid species, providing evidence of the
importance of refuge availability from predation
for juvenile M. adina and other xanthids. We
also found that competition for available habitat
may occur among M. adina, E. depressus, and P.
simpsoni, but its effect on the population
dynamics of these species is not clear.
ACKNOWLEDGEMENTS
Thanks go to James Warren and the Fisheries Assessment
and Monitoring Group (L. Engel, R. McCall, W. Devers, J.
Anderson, B. Randall, J. LeDoux), W. Aguirre, D. Chiluiza,
L. Salazar, A. Soto, J. Lemus, R. Bond, E. Pederson, G.
Hendrix, T. Randall, L. Kelley, P. Schofield, G. Zapfe, C.
Flowers, B. Blackburn, A. Bullard, G. Sanchez, G. Fulling,
and L. Shervette for their essential help in the field and for
other support.
This study was part of a Master’s thesis submitted by
VRS to the Department of Biological Sciences, University
of Southern Mississippi. The work was sponsored in part by
the National Oceanic and Atmospheric Administration
(NOAA), U.S. Department of Commerce, the MississippiAlabama Sea Grant Consortium (MASGC) Marine Science
Scholar’s Award E/O-16, and the University of Southern
Mississippi, Gulf Coast Research Laboratory. The U.S.
Government and the MASGC are authorized to produce and
distribute reprints notwithstanding any copyright notation
that may appear hereon. The views expressed herein are
those of the authors and do not necessarily reflect views of
NOAA or any of its subagencies and MASGC.
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RECEIVED: 13 August 2003.
ACCEPTED: 11 May 2004.