Impact of Predation by the Invasive Crab Hemigrapsus
sanguineus on Survival of Juvenile Blue Mussels in Western
Long Island Sound
Diane J. Brousseau, Ronald Goldberg, and Corey Garza
Northeastern Naturalist, Volume 21, Issue 1 (2014): 119–133
Full-text pdf (Accessible only to subscribers. To subscribe click here.)
Access Journal Content
Open access browsing of table of contents and abstract pages. Full text pdfs available for download for subscribers.
Current Issue: Vol. 30 (3)
Check out NENA's latest Monograph:
Monograph 22
Northeastern Naturalist Vol. 21, No. 1
D.J. Brousseau, R. Goldberg, and C. Garza
2014
119
2014 NORTHEASTERN NATURALIST 21(1):119–133
Impact of Predation by the Invasive Crab Hemigrapsus
sanguineus on Survival of Juvenile Blue Mussels in Western
Long Island Sound
Diane J. Brousseau1, Ronald Goldberg2, and Corey Garza3
Abstract - Hemigrapsus sanguineus (Asian Shore Crab) has shown a remarkable ability
to colonize rocky intertidal communities along the east coast of the United States since its
introduction in the late 1980s and is an important predator of juvenile Mytilus edulis (Blue
Mussel) in invaded habitats. In this study, we used two field-caging experiments and the Kaplan-
Meier model to assess the impact of predation by Asian Shore Crab on the survival of
juvenile Blue Mussels in an intertidal habitat of western Long Island Sound along the Connecticut
coastline. Five treatment levels (high-density enclosure, low-density enclosure,
exclosure, partial cage, and open plot) were used in the 2007 experiment. The high-density
enclosure treatment was omitted in the 2010 experiment since there was no statistically
significant difference in the proportion of mussels surviving between low- and high-density
crab treatments in 2007. In 2007, we measured a statistically significant difference in mussel
mortality between exclosure and crab-enclosure cages, with crabs lowering the median
survival time for mussels from 15.4 to 7.6 days. In 2010, we ag ain measured a statistically
significant difference in mussel mortality between exclosure and crab-enclosure cages,
suggesting a crab effect on mussel survival. In the 2010 experiment, approximately 25%
of the mussel mortality was attributable to crab predation, which reduced median survival
time for mussels from 12.8 to 5.6 days. The median survival time for mussels exposed to
the full complement of factors affecting survival (open plots and partial cages) was only
2–3 days. Our study shows that predation by Asian crabs may account for up to 25% of the
Blue Mussel mortality in the intertidal zone at Black Rock Harbor. Further studies focusing
on the importance of other biotic and abiotic factors are needed to understand the apparent
declines in Blue Mussel populations and the interannual variability in recruitment success
in this area.
Introduction
Invasions of marine habitats by non-indigenous species can have significant
ecological and evolutionary consequences for native populations (Ruiz et al. 1997).
Invasive species have the potential to impact marine communities either by direct
predation or by competition with native species for critical resources (Cohen and
Carlton 1998), resulting in altered or impaired ecosystem function. The popular
argument that invasive species also pose a major threat to marine biodiversity
(Molnar et al. 2008) has only recently been challenged by Briggs (2007). He argues
1Biology Department, Fairfield University, Fairfield, CT 06824. 2National Oceanic and
Atmospheric Administration, Northeast Fisheries Science Center,Milford Laboratory,
212 Rogers Avenue, Milford, CT 06460. 3Division of Science and Environmental Policy,
California State University, Monterey Bay, 100 Campus Center, Seaside, CA 93955.*Corresponding
author - brousseau@fairfield.edu.
Manuscript Editor: Melisa Wong
Northeastern Naturalist
120
D.J. Brousseau, R. Goldberg, and C. Garza
2014 Vol. 21, No. 1
that major contemporary marine invasions have occurred via the opening of the
Suez Canal, in the Wadden Sea, along the European coast, and into the tropical eastern
Atlantic from the Indian Ocean, but there has been little evidence of impaired
biodiversity or ecosystem function as a result of these invasions (Briggs 2010).
Nonetheless, there are many examples in the literature which show that primary interactions
between native and invader species most often result in alterations in species
abundance or habitat shifts (Galil 2007, Reise et al. 2006, Thieltges 2005). The
effect of an invader on a native species, however, may not be the same throughout
the entire range of the invasion. Confounding factors such as local anthropogenic
stressors (Galil 2007) or improved prey defenses (Freeman and Byers 2006) may
alter the impact of a non-indigenous species on the native biota. More extensive
experimental field studies which document species impacts in different geographic
locations and under a range of environmental conditions are needed to better evaluate
the extent of the threat of invasive species to ecosystem function and worldwide
marine biodiversity.
Hemigrapsus sanguineus (De Haan) (Asian Shore Crab), indigenous to the
western Pacific, has been a particularly successful marine invader in the western
Atlantic. It was first observed in New Jersey in the late 1980s (Williams and Mc-
Dermott 1990) and since then has shown a remarkable ability to colonize rocky
intertidal habitats along the east coast of North America (McDermott 1998). It now
ranges from Maine to North Carolina and has become the most abundant species of
intertidal crab in southern New England and Long Island Sound, reaching densities
≥150 crabs m-2 in some locations (Ahl and Moss 1999, Gerard et al. 1999, Lohrer
and Whitlatch 2002).
Mytilid bivalves are prominent in the natural diet of the Asian Shore Crab in its
native environment (Lohrer et al. 2000), and several studies have identified this
crab species as an important predator of juvenile Mytilus edulis L. (Blue Mussel)
in invaded environments (Bourdeau and O’Connor 2003; Brousseau et al. 2000;
Gerard et al. 1999; Lohrer and Whitlatch 1997; McDermott 1991, 1999; Tyrell
and Harris 2000; Tyrell et al. 2006). Laboratory experiments have shown that
Asian Shore Crabs can consume large numbers of mussels daily (Brousseau et al.
2001), and that despite the species’ omnivorous diet, it exhibits a strong preference
for Blue Mussels over macroalgae (Brousseau and Baglivo 2005). Short-term
microcosm experiments run under both laboratory and natural conditions also
support the argument that predation by the Asian Shore Crab can cause significant
declines in juvenile mussels (Tyrell et al. 2006). In a study assessing the relative
impacts of crab predation, Lohrer and Whitlatch (2002) concluded that the predation
pressure exerted by Asian Shore Crabs was a significantly greater threat to
native mussel populations than that of the co-occuring exotic Carcinus maenas
(L.) (European Green Crab).
The Blue Mussel is an important prey item in northeast rocky intertidal communities,
utilized by a variety of native fauna, including birds, fish, and invertebrates
such as crabs and seastars (Lubchenco and Menge 1978). It is also a commercially
valuable species, harvested and farmed in coastal New England. The extremely high
Northeastern Naturalist Vol. 21, No. 1
D.J. Brousseau, R. Goldberg, and C. Garza
2014
121
densities of Asian Shore Crabs present in these habitats has prompted considerable
speculation about the role of this invader in restructuring prey populations and
decreasing the refuge value of intertidal areas for recruit and juvenile life-stages of
this mussel. Several published studies imply that the Asian Shore Crab may have
broad impacts on the native community (Bourdeau and O’Connor 2003, Ledesma
and O’Connor 2001, Tyrell and Harris 1999) as well as large species-specific effects
on bivalve prey (Lohrer and Whitlatch 2002). Reduction of mussel beds in
intertidal areas decreases the amount of complex habitat available for other faunal
assemblages, leading to a decrease in diversity of associated invertebrate communities
(Koivisto and Westerbom 2010, Seed and Suchanek 1992). Consequently, the
addition of another mussel predator, especially one that is so abundant, could potentially
have a severe impact on prey population stability and overall community
diversity.
As an ecosystem engineer species, Blue Mussels are important filter feeders
with the ability to process large volumes of water and remove particulate organic
matter such as bacteria, phytoplankton, microzooplankton, and detritus from the
water column (Commito and Boncavage 1989, Norling and Kautsky 2008). Oystergardening
efforts such as those in Chesapeake Bay, use bivalve suspension feeders
to reduce the nitrogen load and improve water quality. The decline or loss of intertidal
mussel populations in a eutrophic estuary like Long Island Sound could
remove an important shoreline “filter” of organic carbon, resulting in the loss of a
critical particle-clearance mechanism for the entire ecosystem.
In this study, we analyzed data from field-caging experiments with a Kaplan-
Meier survivorship model to measure the impact of predation by Asian Shore Crabs
on the survival of juvenile Blue Mussels in rock-strewn intertidal mudflats of the
type commonly found in western Long Island Sound. Our experiments were designed
to determine the contribution of Asian Shore Crab predation to the overall
predation pressure exerted on Blue Mussel populations and to assess its role in the
limited mussel recruitment observed in this area.
Materials and Methods
Caging experiments
To determine the effects of the invasive Asian Shore Crab on survival of juvenile
native Blue Mussels. we conducted two field-caging experiments in the
mid-intertidal zone in Black Rock Harbor, Bridgeport, CT (41°08.8'N, 73°13.5'W;
Fig. 1).This area is characterized by a gently sloping tidal flat densely covered with
rocks of various sizes. At both caging sites, seawalls form the shoreward boundary
of the study area. Environmental conditions and tidal immersion times at both sites
are similar (approximate tidal range: 2.1 m). We determined natural crab densities
in this area (10 ± 1.3 crabs per 0.125 m2) along 2 across-shore transects within the
intertidal zone by counting all Asian Shore Crabs present within a quadrat (0.25 m2)
placed on the substrate at each haphazardly determined sampling point (n = 15). An
ongoing multi-year study of stomach contents in free-ranging Asian Shore Crabs
from Black Rock Harbor shows crabs feed on macroalgae, barnacles, cyprid larvae,
Northeastern Naturalist
122
D.J. Brousseau, R. Goldberg, and C. Garza
2014 Vol. 21, No. 1
polychaetes, Blue Mussels, amphipods, salt marsh grass, and detritus at this site
(D.J. Brousseau, Unpubl. data).
Figure 1. Chart of a portion of the northern shore of Long Island Sound indicating the locations
of the 2007 and 2010 study sites in Black Rock Harbor , Bridgeport, CT.
Northeastern Naturalist Vol. 21, No. 1
D.J. Brousseau, R. Goldberg, and C. Garza
2014
123
We conducted the first experiment in May–June 2007 along a mudflat located
near the mouth of the harbor. To determine if the results of the first experiment were
repeatable across sites and years, we carried out a second experiment in May 2010
at a location approximately 1.5 km northeast of the first study location. We chose
the May–June experimental period because it coincides with the major spawning/
settlement season of Blue Mussels in Long Island Sound (Brousseau 1983, Newell et
al. 1982). This choice ensured that our estimates of crab predation were made under
environmental conditions (e.g., temperature and length of tidal immersion) similar to
those present when crabs are foraging naturally on mussel recruits in the field.
In the first caging experiment, we used five different treatments to test the null
hypothesis that Asian Shore Crab predation has no effect on juvenile Blue Mussel
survival. Enclosure cages with a low and a high crab density (8 and 23 per cage,
respectively) measured Asian Shore Crab predation on mussels. Exclosure cages
measured background mortality in the absence of Asian Shore Crab predators too
large to enter the cages (>3 mm CW). Exclosures also excluded other predators
such as fish, birds, and other crabs such as Panopeus herbstii (L.) (Mud Crab) and
European Green Crabs. We used open plots (no cages) to measure natural mortality,
and partial cages (two opposing sides of cage removed) to test for possible
cage artifacts. In the second experiment, we used only a low-density of crabs (9
per cage) since the first experiment showed no statistically significant difference
in Blue Mussel survival between low- and high-density crab treatments.
We used four replicates of each treatment in the experiment. The cages were
constructed of 10-mm vinyl-coated wire mesh with open bottoms and a single,
hinged access door on the top. Three-millimeter mesh plastic netting completely
lined the cages to prevent washout or emigration of mussels >3 mm SL. We partially
buried the cages in the sediment to an approximate depth of 10 cm, resulting
in an enclosed area of 0.3 m x 0.4 m x 0.2 m high. Rocks were present in the cages;
no additional rocks were added.
In 2007, we collected small Blue Mussel recruits from intertidal and shallow
subtidal rocks at Fort Weatherill, Jamestown, RI, using SCUBA, and held them in
flow-through seawater raceways at the Milford Laboratory (NMFS). In 2010, we
collected mussels by hand from the surface of the dam sluiceway at the southern
end of Holly Pond at Cove Island Park, Stamford, CT. Before the start of each experiment,
we placed 100 randomly selected Blue Mussels of 5–20 mm shell length
(SL) on a “conditioned” 3-M® Scotch Brite scrub pad (14 cm x 12 cm in size). Mussels
produce byssal threads quickly (in less than 24 hr) when held in the laboratory
(Young 1985). In our experiment, we held 100 mussels on each pad for two days
in a seawater table to allow for attachment. We considered mussels “attached” if
they remained fixed to the pad when it was turned over. At the beginning of each
experiment, we anchored pads with their attached mussels to the substrate in the
center of each cage and open plot.
Experimental crabs were collected at random by hand from the field sites and
were representative of the size distribution of the resident population. Median
carapace width of all crabs used in enclosures was 20.83 mm. There was no statistiNortheastern
Naturalist
124
D.J. Brousseau, R. Goldberg, and C. Garza
2014 Vol. 21, No. 1
cally significant difference in crab size between high- and low-density treatments in
2007 (Mann–Whitney U = 1452.5, n(low) = 32, n(high) = 92, P = 0.914) or across years
(Mann-Whitney U = 1873.5, n(2007) = 124, n(2010) = 36, P = 0.143). We brought crabs
to the Milford Laboratory for tagging and marked each crab by gluing a small color/
shape-coded plastic tag to the carapace with cyanoacrylate. We used both male and
female crabs whose chelae and other appendages were intact. The sex ratio in enclosure
cages was 1:1.
We held crabs overnight in running seawater and placed them in cages the following
day. Prior to release, we cleared caged plots of all visible Asian Shore Crabs.
We then added tagged crabs to the enclosure cages. At the end of the experiment,
average recovery rate of tagged crabs in low-density enclosures was 70% in 2007
and 63% in 2010. A 58% mean recovery rate was present in the high-density cages.
The presence of untagged crabs and carapace fragments in cage enclosures indicated
that missing crabs resulted from tag loss due to molting and/or cannibalism.
Griffen and Byers (2009) have shown that cannibalism occurs among Asian Shore
Crabs when densities are high.
To estimate survival, we censused the number of mussels surviving in all caged
and open plots eight times in the 2007 experiment and six times during the 2010
experiment. The 2007 experiment ran for 13 days. We terminated the 2010 experiment
on day 9 when a storm dislodged three of the experimental cages and the pads
with mussels attached were lost. At the conclusion of the experiment, we removed,
counted, and measured the remaining uneaten mussels in the enclosure cages. We
also counted and measured tagged and untagged Asian Shore Crabs remaining in
the cages. We analyzed for content the stomachs of a subsample of the crabs retrieved
from enclosure cages (2007: n = 30, 2010: n = 15). On collection day, we
removed the stomachs from live crabs, flushed their contents with seawater into a
Petri dish, and examined them under a dissecting microscope to determine food
type. We noted the presence of crushed mussels (shells).
Statistical analysis of survival data
In both experiments, we analyzed average survivorship across treatments using a
one-way ANOVA. In our model, treatments served as fixed, independent variables.
The proportion of mussels surviving (number surviving/original number present)
in each treatment served as the dependent variable. We further analyzed significant
treatment effects using Tukey tests (α = 0.05).
In order to assess the impact of the treatments on mussel survival time, we
used a Kaplan-Meier survival model (Lee 1992) to assess the difference in median
mussel survival time across each treatment. A Kaplan-Meier survival model is a
non-parametric method that can be used to calculate median survival time for one
or more groups. The survival model can be described as:
S(t) = S(t - 1)pt ,
where, the survivorship estimate, S(t), is calculated as the number of individuals
surviving divided by the total number of individuals at risk at time t. The
probability of surviving to a point in time pt is estimated from the cumulative
Northeastern Naturalist Vol. 21, No. 1
D.J. Brousseau, R. Goldberg, and C. Garza
2014
125
probability of surviving each of the preceding time intervals S(t - 1). The survival
estimate S(t) may therefore be thought of as the product of S(t - 1) and pt,
with a standard range of survivorship values of 0 (no survivorship) to 1 (total
survivorship). A Weibull, as opposed to normal, distribution is commonly used to
describe the distributional shape of data in a Kaplan-Meier model since mortality
in ecological systems does not follow a normal distribution across time (Garza
2005, Kalbfleisch and Prentice 1980). Standard analyses of predator impacts on
survivorship over time typically involve the use of repeated measures ANOVA.
However, one main assumption of repeated measures ANOVA is that over time,
data are normally distributed; often survivorship data are not and can exhibit
skewed or binomial type distributions (Fox 1993, Garza 2005, Lee 1992, Petraitis
1999). Survival models are robust enough to analyze nonparametric data (Lee
1992). We then used a chi-square analysis to assess differences in the median survival
time of mussels across our experimental treatments.
Results
A majority of the recovered Asian Shore Crabs examined (77% in 2007, 60% in
2010) had consumed food before capture; the rest had empty stomachs when dissected.
Food items included green algae, detritus, polychaete worms, and crushed
mussels (shells). Mussel shell fragments were found in approximately one-third of
the crab stomachs that contained food. Mean size of mussels not eaten by crabs in
enclosure cages was 14.5 ± 2.6 mm SL (mean ± SE, n = 205). No crabs less than 9 mm SL
were recovered in enclosure cages.
The results of both experiments show a decline in the proportion of mussels surviving
over the course of the experimental period (Fig. 2). The 2007 results reveal
significant differences among the five treatments (Table 1). A Tukey HSD post-hoc
analysis across the five treatments indicates that the exclosure treatment had the
highest average survivorship, which was significantly different from survivorship
in the low- and high-density enclosure treatments (Q = 3.0892, P < 0.05). The lowest
survival occurred in the partial cage and open plots (Fig. 3). The 2010 results
also reveal significant differences among treatments (Table 2). Mussel survivorship
in the exclosure treatement was again the highest and significantly different from
survivorship in the crab enclosure plots (Q = 2.9688, P < 0.05). The lowest survival
occurred in the partial cage and open plots, and mortality in these treatments differed
significantly from the crab-enclosure and crab-exclosure treatments (Fig. 3).
In both years of the study, mussels in the exclosure treatments experienced an aver-
Table 1. Result of one-way ANOVA of final mean number of mussels surviving (n = 4) across the five
experimental treatments in 2007, comparing exclosures, two crab densities, a partial-cage control,
and an open plot.
Source of variation df MS F P
Treatment 4 1733.88 7.514 0.0016*
Error 15 230.77
Total 19
Northeastern Naturalist
126
D.J. Brousseau, R. Goldberg, and C. Garza
2014 Vol. 21, No. 1
Figure 2. The plotted curves indicate the mean proportion of mussels surviving (n = 4, ± SE)
across treatments over time during the course of experiments in 2007 and 2010. All curves
are plotted assuming a Weibull distribution in the data.
Northeastern Naturalist Vol. 21, No. 1
D.J. Brousseau, R. Goldberg, and C. Garza
2014
127
Figure 3. Final average number of mussels surviving (n = 4, ± SE) among the five treatments
in 2007 and four treatments in 2010. Groups with a different letter are significantly different
according to Tukey’s HSD.
Northeastern Naturalist
128
D.J. Brousseau, R. Goldberg, and C. Garza
2014 Vol. 21, No. 1
age mortality of approximately 46%,
Analysis of median survival time across the five treatments in the 2007 experiment
revealed a significant difference among the five treatments (χ2 = 94.429, df =1,
P < 0.001). The shortest median survival time for mussels was observed within the
open and partial-cage control treatments (Table 3). The second longest median survival
times were observed in the high- and low-density crab treatments (Table 3). The
longest median survival time for mussels was observed in the absence of Asian Shore
Crab predators (Table 3). In the 2010 experiment, median survival time was again
longest in the exclosure and shortest in the open plot (χ2 = 498.987, df = 3, P < 0.001).
Survival times in the crab enclosure and partial-cage control were equal, but significantly
shorter than in the exclosure cage and longer than the open plot (Table 3).
Discussion
The higher survival of Blue Mussels protected from Asian Shore Crab predators
in our cage experiment supports the conclusion that some mussel losses were,
in fact, due to Asian Shore Crab predation. Statistical comparisons of mortality in
exclosure and enclosure treatments showed that Asian Shore Crab predation measured
in enclosure cages accounted for about 25% of the total mortality measured
in the 2010 experiment. In the 2007 experiment, a statistically significant difference
was also observed that suggested crab predation in the crab-enclosure treatments
accounted for 20% of the observed mussel mortality. Although these results do not
support the view that Asian Shore Crab predation is the major cause of juvenile
Blue Mussel mortality at our study site, they do support the conclusion of a minor
but measurable role for this predator.
Unlike other similar mussel caging studies in which the reported background
Table 3. Median survival time (n = 4, ± SE) in days of mussels across experimental treatments in
2007 and 2010.
Median survival (days)
Treatment 2007 2010
Exclosures 13.0 ± 1.20 12.8 ± 0.09
High crab density 7.0 ± 0.29 No treatment
Low crab density 7.0 ± .033 5.6 ± 0.10
Open control 2.0 ± 0.10 2.7 ± 0.07
Partial-cage control 2.0 ± 0.11 4.5 ± 0.10
Table 2. Result of one-way ANOVA of final mean number of mussels survivng (n = 4) across the four
experimental treatments in 2010, comparing exclosures, one crab density, a partial-cage control and
an open plot.
Source of variation df MS F P
Treatment 3 2153.06 7.953 0.0035
Error 12 270.73
Total 15
Northeastern Naturalist Vol. 21, No. 1
D.J. Brousseau, R. Goldberg, and C. Garza
2014
129
mortality rates were less than 10% (Carroll and Highsmith 1996, Lohrer and Whitlatch
2002), mortality in our predator exclosure cages was high. It is not likely that
mussel emigration or washout by waves was a confounding problem since even
the smallest mussels could not pass through the cage mesh. The high mortality
probably resulted largely from non-predatory sources such as dessication and high
temperature. Habitat characteristics of intertidal areas vary from west to east in the
Sound. Rocky intertidal flats in the western end are mainly sedimentary, with small
rocks and cobbles in some areas. There is little algal cover; most rocks are covered
by dense barnacle sets. East of New Haven, large rocks and boulders are more common,
and rocky intertidal areas have abundant algal cover keeping them moister
and cooler. These site differences in environmental conditions likely affect the relative
importance of various biotic and abiotic factors in causing mussel mortality. It
may be the reason for the different background mussel mortality rates reported in
other caging experiments. More importantly, it emphasizes the need to assess the
impact of invaders within different habitat types and geographic regions to fully
understand native-nonnative species interactions.
Since the aim of our study was to measure the effect of Asian Shore Crab predation
on mussel survival, we did not attempt to quantify other potential sources of
mortality. As discussed above, abiotic factors such as dessication and elevated temperatures
likely play a significant role in areas similar to our study site where habitat
complexity is low. Additionally, a number of predator groups including birds, fish
(Tautoga onitis (L.) [Tautog], Fundulus heteroclitus (L.) [Mummichog]), native
crab species (European Green Crab, Mud Crab) and polychaete worms can be found
foraging during both high and low tide. Together, these factors were likely the most
important causes of overall mortality, resulting in the nearly 100% mussel loss from
open and partial-cage treatments by the end of the experiment in both years.
Initially, we had hypothesized a predator-density effect, predicting lower mussel
mortality in the low-density crab treatment than in the high-density crab treatment.
There is a trend, but no statistically significant difference in final average mussel
survivorship between those treatments. This result may be due to caging artifacts
influencing crab behavior. Increased crab density can lead to increased agonistic
interactions among crabs resulting in less time spent foraging and lowered
consumption rates, or to eating less-preferred prey to minimize competition for
limited food resources (Clark et al. 1999, 2000). Studies have shown that increasing
conspecific densities in the laboratory leads to increased diet breadth in Asian
Shore Crabs (Brousseau and Baglivo 2005), suggesting foraging behavior may be
influenced by crab density in the cages.
Feeding patterns of Asian Shore Crabs on mytilids under field conditions differ
from those observed in the laboratory. High consumption rates of 10–18 mussels
day -1 are typical under laboratory conditions where crabs are allowed to feed continuously
(Boudreau and O’Connor, 2003, Brousseau et al. 2001, DeGraaf and
Tyrrell 2004), whereas crabs ate fewer than one mussel day -1 over the course of this
field study. Moreover, in a study of the diet of Asian Shore Crabs from Odiorne Point,
NH, Griffen et al. (2012) found that during April–October, mussels were present in a
Northeastern Naturalist
130
D.J. Brousseau, R. Goldberg, and C. Garza
2014 Vol. 21, No. 1
minority of the crabs guts sampled (25% in June, 11% in August), supporting the conclusion
that this food item is not the major component of its diet. These differences
between laboratory and field results may be due to increased food choice in the field,
limited foraging opportunities because of a semidiurnal tidal cycle (crabs forage primarily
during high tide at night) and/or the presence of occasional high wave action
hampering the ability of these small crabs to handle and open mussel prey. Other factors
such as water temperature and prey densities may also play a role.
Although Asian Shore Crabs prefer mussels ≤10 mm SL, they will feed on mussels
up to 20 mm SL in the lab (Brousseau et al. 2001, Gerard et al. 1999). Our data
indicate that smaller mussels (less than 9.0 mm) may have been preyed upon preferentially
by Asian Shore Crabs, suggesting that as mussels grow larger, they will experience a
size refuge from predation. This conclusion is supported by the argument that in nature
rapidly growing bivalves such as Blue Mussels can quickly move out of the size
range most vulnerable to predation from many predator groups including the Asian
Shore Crab (Suchanek 1978). Moreover, the recent work by Freeman and Byers
(2006) shows that mussels from locations in southern New England (including Long
Island Sound) have evolved an inducible shell-thickening response to waterborne
cues from Asian Shore Crabs, and that this presumed anti-predator response has
evolved rapidly, within approximately 20 years of its introduction. This work suggests
that there is considerable potential for interactions between native and invasive
species to vary temporally and geographically due to local selection pressures.
Although there are no historical records documenting mussel abundance and
distribution for this harbor, there have been many anecdotal reports over the past
few decades of mussel declines in this part of Long Island Sound. Many factors
may be responsible, and more research is needed to fully understand the role of
local physical and biological factors—such as wave action, temperature, recruitment
success, and the impact of all predator groups—in regulating abundance and
stability of intertidal mussel populations in this area. However, our study clearly
demonstrates that predation by Asian Shore Crabs plays a minor but measurable
role in Blue Mussel mortality in the intertidal zone at Black Rock Harbor. This finding
emphasizes the need to assess the impact of invaders within different habitat
types and geographic regions to fully understand the ways native-nonnative species
interactions can vary over the entire range of selection pressures and ecological
conditions in which they occur.
Acknowledgments
The authors would like to acknowledge the late Mr. A. Glowka, whose frequently asked
question, “Where have all the Blue Mussels gone?” served as an impetus for conducting this
study. We thank J. Prezioso, M. Dixon, and B. Smith for help collecting mussels for this study,
and the anonymous reviewers for helpful comments on the manuscript.
Literature Cited
Ahl, R.S., and S.P. Moss. 1999. Status of the nonindigenous crab, Hemigrapsus sanguineus,
at Greenwich Point, Connecticut. Northeastern Naturalist 6:221 –224.
Northeastern Naturalist Vol. 21, No. 1
D.J. Brousseau, R. Goldberg, and C. Garza
2014
131
Bourdeau, P.E., and N.J. O’Connor. 2003. Predation by the nonindigenous Asian Shore
Crab, Hemigrapsus sanguineus, on macroalgae and molluscs. Northeasteatern Naturalist
10:319–334.
Briggs, J.C. 2007. Marine biogeography and ecology: Invasions and introductions. Journal
of Biogeography 34:193–198.
Briggs, J.C. 2010. Marine biology: The role of accommodation in shaping marine biodiversity.
Marine Biology 157:2117–2126.
Brousseau, D.J. 1983. Aspects of the reproductive cycle of the Blue Mussel, Mytilus edulis
(Pelecypoda:Mytilidae), in Long Island Sound. Fisheries Bulleti n 81(4):733–739.
Brousseau, D.J., and J.A. Baglivo. 2005. Laboratory investigations of food selection by the
Asian Shore Crab, Hemigrapsus sanguineus: Algal versus animal preference. Journal of
Crustacean Biology 25(1):130–134.
Brousseau, D.J., and R. Goldberg. 2007. Effect of predation by the invasive crab Hemigrapsus
sanguineus on recruiting barnacles Semibalanus balanoides in western Long Island
Sound, USA. Marine Ecology Progress Series 339:221–228.
Brousseau, D.J., P.G. Korchari, and C. Pflug. 2000. Food preference studies of the Japanese
Shore Crab (Hemigrapsus sanguineus) from western Long Island Sound. Pp. 200–207,
In J. Pederson (Ed.). Marine Bioinvasions. Proceedings of the First National Conference,
Jan. 24–27, 1999. MIT SeaGrant College Program, Cambridge, MA.
Brousseau, D.J., A. Filipowicz, and J.A. Baglivo. 2001. Laboratory investigations of the
effects of predator sex and size on prey selection by the Asian crab Hemigrapsus sanguineus.
Jounal of Experimental Marine Biology and Ecology 262:199–210 .
Carroll, M.L., and R.C. Highsmith. 1996. Role of catastrophic disturbance in mediating
Nucella-Mytilus interactions in the Alaskan rocky intertidal. Marine Ecology Progress
Series 138:125–133.
Clark, M.E, T.G. Wolcott and D.L. Wolcott, and A.H. Hines. 1999. Intraspecific interference
among foraging Blue Crabs, Callinectes sapidus: Interactive effects of predator
density and prey-patch distribution. Marine Ecology Progress Se ries 178:69–78.
Clark, M.E, T.G. Wolcott , D.L. Wolcott, and A.H. Hines. 2000. Foraging behavior of
an estuarine predator, Callinectes sapidus, in a patchy environment. Ecogeography
23(1):21–31.
Cohen, A.N., and J.T. Carlton. 1998. Accelerating invasion rate in a highly invaded estuary.
Science 279:555–558.
Commito, J.A., and E.M. Boncavage. 1989. Suspension feeders and coexisting fauna: An
enhancement counter-example. Journal of Experimental Marine Biology and Ecology
125:33–42.
DeGraaf, J.D., and M.C. Tyrrell. 2004. Comparison of the feeding rates of two introduced
crabs species, Carcinus maenas and Hemigrapsus sanguineus, on the Blue Mussel,
Mytilus edulis. Northeastern Naturalist 11(2):163–167.
Fox, G.A. 1993. Failure-time analysis: Emergence, flowering, survivorship, and other waiting
times. Pp. 253–289, In S.M. Scheiner and J. Gurevitch (Eds.). Design and Analysis
of Ecological Experiments. Chapman and Hall, New York, NY.
Freeman, A.S., and J.E. Byers. 2006. Divergent induced responses to an invasive predator
in marine mussel populations. Science 313:831–833.
Galil, B.S. 2007. Loss or gain? Invasive aliens and biodiversity in the Mediterranean Sea.
Marine Pollution Bulletin 55:314–322.
Garza, C. 2005. Prey productivity effects on the impact of predators of the mussel, Mytilus
californianus (Conrad). Journal of Experimental Marine Biology Ecology 324:7 6–88.
Northeastern Naturalist
132
D.J. Brousseau, R. Goldberg, and C. Garza
2014 Vol. 21, No. 1
Gerard, V.A., R.M. Cerrato, and R.M. Larson. 1999. Potential impacts of a western Pacific
grapsid crab on intertidal communities of the northwestern Atlantic Ocean. Biological
Invasions 1:353–361.
Griffen, B.D., and J.E. Byers. 2009. Community impacts of two imvasive crabs: The interactive
roles of density, prey recruitment, and indirect effects. Biological Invasions
11:927–940.
Griffen, B.D., I. Altman, B.M. Bess, J. Hurley, and A. Penfield. 2012. The role of foraging
in the success of invasive Asian shore crabs in New England. Biological Invasions
14:2545–2558.
Kalbfleisch, J.D., and R.L. Prentice. 1980. The Statistical Analysis of Failure Time Data.
Wiley, New York, NY.
Koivisto, M.E., and M. Westerbom. 2010. Habitat structure and complexity as determinants
of biodiversity in Blue Mussel beds on sublittoral rocky shores. Marine Biological
157:1463–1474.
Ledesma, M.E. and N.J. O’Connor. 2001. Habitat and diet of the non-native crab Hemigrapsus
sanguineus in southeastern New England. Northeastern Naturalist 8:63–78.
Lee, E.T. 1992. Statistical Methods for Survival Data Analysis, 2nd Edition. Wiley, New
York, NY.
Lohrer, A.M., and R.B. Whitlatch. 1997. Ecological studies on the recently introduced Japanese
Shore Crab (Hemigrapsus sanguineus) in eastern Long Island Sound. Pp. 49–60,
In N.C. Balcom (Ed.). Proceedings of the Second Northeast Conference on Nonindigenous
Aquatic Nuisance Species. Connecticut SeaGrant College Program, Groton, CT.
Lohrer, A.M., and R.B. Whitlatch. 2002. Relative impacts of two exotic brachyuran species
on Blue Mussel populations in Long Island Sound. Marine Ecology Progress Series
227:135–144.
Lohrer, A.M., R.B. Whitlatch, K. Wada, and Y. Fukui. 2000. Using niche theory to understand
invasion success: A case study of the Asian Shore Crab, Hemigrapsus sanguineus.
Pp. 57–60, In J. Pederson (Ed.). Marine Bioinvasions. Proceedings of the First National
Conference, 24–27 January 1999. MIT SeaGrant College Program, Cambridge, MA.
Lubchenco, J., and B.A. Menge. 1978. Community development and persistence in a low
rocky intertidal zone. Ecological Monographs 48:67–94.
McDermott, J.J. 1991. A breeding population of the western Pacific crab Hemigrapsus
sanguineus (Crustacea: Decapoda: Grapsidae) established on the Atlantic coast of North
America. Biological Bulletin 181:195–198.
McDermott, J.J. 1998. The western Pacific brachyuran (Hemigrapsus sanguineus: Grapsidae),
in its new habitat along the Atlantic coast of the United States: Geographic distribution
and ecology. Journal of Marine Science 55:289–298.
McDermott, J.J. 1999. The western Pacific brachyuran (Hemigrapsus sanguineus Grapsidae)
in its new habitat along the Atlantic coast of the United States: Feeding, cheliped
morphology, and growth. Pp. 425–444, In F.R. Schram and J.C. von Vaupel Klein (Eds.).
Crustaceans and the Biodiversity Crisis. Leiden, The Netherlands.
Molnar, J.L., R.L. Gamboa, C. Revenga, and M.D. Spalding. 2008. Assessing the global
threat of invasive species to marine biodiversity. Frontiers in Ecology and Environment
6:485–492.
Newell, R.I.E., T.J. Hilbish, R.K. Koehn, and C.J. Newell. 1982. Temporal variation in the
reproductive cycle of Mytilus edulis L. (Bivalvia, Mytilidae) from localities on the east
coast of the United States. Biological Bulletin 162:299–310.
Norling, P., and N. Kautsky. 2008. Patches of the mussel Mytilus sp. are islands of high
biodiversity in subtidal sediment habitats in the Baltic Sea. Aquatic Biology 4:75–87.
Northeastern Naturalist Vol. 21, No. 1
D.J. Brousseau, R. Goldberg, and C. Garza
2014
133
Petraitis, P.S. 1999. Timing of mussel mortality and predator activity in sheltered bays of the
Gulf of Maine, USA. Journal of Experimental Marine Biology and Ecology 231:47–62.
Riese, K, S. Olenin, and D.W. Thieltges. 2006. Are aliens threatening European aquatic
coastal ecosystems? Helgoland Marine Research 60:77–83.
Ruiz, G.M., J.T. Carlton, E.D. Grosholz, and A.H. Hines. 1997. Global invasions of marine
and estuarine habitats by non-indigenous species: Mechanisms, extent, and consequences.
American Zoology 37:621–632.
Seed, R., and T.H. Suchanek. 1992. Population and community ecology of Mytilus. Pp.
87–157, In E. Gosling (Ed.). The Mussel Mytilus: Ecology, Physiology, Genetics, and
Culture. Elsevier, Amsterdam.
Suchanek, T.H. 1978. The ecology of Mytilus edulis L. in exposed rocky intertidal communities.
Journal of Experimental Marine Biology and Ecology 31:1 05–120.
Thieltges, D.W. 2005. Impact of an invader: Epizootic American Slipper Limpet, Crepidula
fornicata, reduces survival and growth in European mussels. Marine Ecology Progress
Series 2 86:13–19.
Tyrell, M., and L.G. Harris. 2000. Potential impact of the introduced Asian Shore Crab,
Hemigrapsus sanguineus, in northern New England: Diet, feeding preferences, and
overlap with the Green Crab, Carcinus maenas. Pp. 208–220, In J. Pederson (Ed.). Marine
Bioinvasions, Proceedings of the First National Conference, 24–27 January 1999.
MIT SeaGrant College Program, Cambridge, MA.
Tyrell, M.C., P.A. Guarino, and L.G. Harris. 2006. Predatory impacts of two introduced
crab species: Inferences from microcosms. Northeastern Naturali st 13(3):375–390.
Williams, A.B., and J.J. McDermott. 1990. An eastern United States record for the Western
Indo-Pacific Crab, Hemigrapsus sanguineus (Crustacea: Decapoda: Grapsidae). Proceedings
of the Biological Society of Washington 103:108–109.
Young, G.A. 1985. Byssus-thread formation by the mussel Mytilus edulis; Effects of environmental
factors. Marine Ecology Progress Series 24:261–271.