J OURNAL OF C RUSTACEAN B IOLOGY, 34(6), 731-738, 2014
LONG-TERM CHANGES IN AN ESTUARINE MUD CRAB COMMUNITY:
EVALUATING THE IMPACT OF NON-NATIVE SPECIES
Wendy E. Eash-Loucks 1,2,∗ , Matthew E. Kimball 1,3 , and Kathryn M. Petrinec 1
1 Guana
Tolomato Matanzas National Estuarine Research Reserve,
505 Guana River Road, Ponte Vedra Beach, FL 32082, USA
2 Department of Natural Resources and Parks, King County, 201 South Jackson Street, Seattle, WA 98104, USA
3 Baruch Marine Field Laboratory, University of South Carolina, P.O. Box 1630, Georgetown, SC 29442, USA
ABSTRACT
Along the US Atlantic coast, oyster reefs support a large number of estuarine species including ecologically important and abundant mud
crabs. Multiple factors including environmental conditions, the introduction of non-native species, parasites, and interspecific competition
can change the structure of these communities over time. To examine long-term changes in mud crab communities, crabs were sampled
quarterly for ten years in a mixed oyster/mud habitat in a northeast Florida estuary. A total of 6935 individuals comprised of 10 species
were collected, including two non-native crab species: Petrolisthes armatus (Gibbes, 1850) and Charybdis hellerii (Milne-Edwards, 1867).
Three species (Panopeus herbstii Milne Edwards, 1834, P. armatus, and Eurypanopeus depressus (Smith, 1869)) made up 97.3% of adult
specimens collected, and were observed throughout the study period in varying abundances. Non-metric multi-dimensional scaling (MDS)
conducted on species abundances revealed that the community underwent significant long-term, rather than cyclical seasonal, changes.
Most noteworthy were the similarities in community assemblages observed in the years prior to, and soon after, the introduction of a nonnative parasite, Loxothylacus panopaei (Gissler, 1884), which preferentially infects E. depressus. The significance of the presence/absence
of the parasite on the community structure was confirmed through an analysis of similarities test (ANOSIM). While E. depressus abundance
declined in the early years of the study after the introduction of L. panopaei, and never recovered, abundance of P. herbstii did not
significantly change. Temperature and salinity likely only briefly impacted individual species on a seasonal or yearly basis including P.
armatus, whose abundance reached an all-time low in the winter of 2010-2011 along with extreme winter temperatures.
K EY W ORDS: invasive species, Loxothylacus panopaei, mud crab, parasitic castrator, rhizocephalan
barnacle
DOI: 10.1163/1937240X-00002287
I NTRODUCTION
Along the Atlantic coast of North America, reefs composed
of Crassostrea virginica (Gmelin, 1791) (the eastern oyster) support a high diversity of algae, invertebrates, and
vertebrates (Kennedy et al., 1996; Lenihan and Peterson,
1998). One of the most conspicuous and abundant taxonomic groups inhabiting these estuarine habitats are mud
crabs, which are important in maintaining community structure as they feed on, and therefore control numbers of, molluscs and other crustaceans on reefs (Ryan, 1956; McDermott, 1960; McDonald, 1982; Lee and Kneib, 1994; Meyer,
1994). Two common co-occurring species of native mud
crabs, Panopeus herbstii Milne Edwards, 1834 and Eurypanopeus depressus (Smith, 1869), are both able to tolerate
a wide range of environmental conditions (Williams, 1965,
1984; McDonald, 1982), but environmental factors could affect other species and additional factors such as intraspecific
competition and the introduction of non-native species to
oyster reefs may alter community dynamics.
Non-native species are regularly introduced into marine
and estuarine systems (Ruiz and Carlton, 2003), where
their introduction often has significant negative impacts
∗ Corresponding
(Carlton and Geller, 1993; Ruiz et al., 1997). In particular,
non-native species can adversely affect oyster reefs and
the diversity they support by disrupting natural trophic
cascades (Kimbro et al., 2009). Often, the transportation
of oysters themselves introduces new fauna that may be
detrimental to a system (Andrews, 1980). In North America,
crustaceans are the most prevalent taxonomic group of nonnative marine and estuarine invaders (Ruiz et al., 2011), and
crabs, in particular, can have significant effects on native
communities in introduced habitats (Griffen and Byers,
2009; Ruiz et al., 2011).
Several crab species including Petrolisthes armatus
(Gibbes, 1850) and Charybdis hellerii (Milne-Edwards,
1867) have recently invaded estuarine waters along the
southeastern US Atlantic coast (Lemaitre, 1995; Knott et
al., 2000). Petrolisthes armatus was first reported north of
Cape Canaveral, FL in 1994 (Knott et al., 2000), while its
native range includes shallow habitats of more tropical and
sub-tropical latitudes, including coastal Brazil, the central
and northern Gulf of Mexico, the Caribbean islands, the
central eastern Pacific Ocean, and the west coast of Africa
(Oliveira and Masunari, 1995; Hollebone and Hay, 2007).
author; e-mail: [email protected]
© The Crustacean Society, 2014. Published by Brill NV, Leiden
DOI:10.1163/1937240X-00002287
732
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 6, 2014
Charybdis hellerii was introduced from the Indo-Pacific and
first recorded in the continental US in 1995 in the Indian
River Lagoon, FL (Lemaitre, 1995). Because of the relative
recentness of these introductions, little is known about the
long-term effects these crab species may have on native crab
populations (but see Dineen et al., 2001; Hollebone and Hay,
2007).
The introduction of non-native parasites may also impact native mud crab communities. Loxothylacus panopaei
(Gissler, 1884) is a widespread non-native parasite along the
Atlantic coast of North America that is known to infect several species of mud crab (Kruse et al., 2012). This species
castrates its host and feminizes males, which stops reproduction at the level of the individual and, if widespread,
can potentially affect the health of the host species population (Dillon and Zwerner, 1966; O’Brien and Van Wyk,
1985; Alverez et al., 1995; Høeg, 1995; Hines et al., 1997).
It was thought to be introduced to the US Atlantic coast from
the Gulf of Mexico, likely by crabs brought to Chesapeake
Bay in oysters used to replenish ailing stocks (Van Engel et
al., 1966; Kruse et al., 2012). Loxothylacus panopaei now
occurs from Long Island Sound to northeast Florida, and
infects nine species of mud crab, occurring at frequencies
ranging from sporadic to as high as 93% throughout its introduced range (Daugherty, 1969; Hines et al., 1997; Kruse
and Hare, 2007; Kruse et al., 2012; Freeman et al., 2013).
While studies have investigated the short-term (2 years)
impacts of non-native species on crab communities (Hollebone and Hay, 2007, 2008; Griffen and Byers, 2009), and
the effects of physical parameters on a single species (Stillman and Somero, 2000), potential long-term (decadal) impacts of multiple factors on communities have not been examined. Short-term studies are likely to only capture instantaneous effects of various physical or environmental factors, while long-term studies may elucidate chronic effects
on mud crab communities and demonstrate the resilience of
impacted species. To determine the long-term effects of nonnative species and parasites on estuarine mud crab communities, we examined changes in the diversity and abundance
of mud crabs over a 10-year period in a mixed oyster/mud
habitat in a northeast Florida estuary.
M ATERIALS AND M ETHODS
Crab Communities
Sampling occurred at a single mixed oyster/mud habitat site within the
Guana Tolomato Matanzas National Estuarine Research Reserve (GTM
NERR) located in northeast Florida (29.6708°N, 81.2159°W). The sample
site, which was undisturbed throughout the study period, was within a
mosaic of intertidal and subtidal flats and creeks adjacent to the main
channel of the Matanzas River (Fig. 1). The Matanzas River is one of
the main tributaries forming the Guana Tolomato Matanzas estuary, which
is a well-mixed, high salinity (polyhaline) lagoonal estuary consisting
of Spartina alterniflora-dominated marshes as well as mixed salt marshmangrove areas (Webb et al., 2007; Valle-Levinson et al., 2009; Williams
et al., 2014).
Mud crabs were sampled using seven replicate habitat trays deployed
1 m apart among naturally-occurring oysters along the low tide line (at
approximately the same depth), and were subtidal except during extreme
low tides. Total tray coverage was less than 1% of the available reef habitat.
Individual habitat trays consisted of ventilated plastic trays measuring
approximately 63 L × 52 W × 12 H cm, lined with 4 mm plastic vexar
screening and filled to the top of the tray with a loose mix of un-cleaned
living and dead C. virginica clusters collected from nearby reefs at the
Fig. 1. Sampling site of mixed oyster/mud habitat within the Guana Tolomato Matanzas National Estuarine Research Reserve (GTM NERR) located
in northeast Florida (29.6708°N, 81.2159°W). Box indicates approximate
location of sampling trays, submerged at a near low tide.
sampling site (Fig. 1). Approximately 30-50% of the C. virginica in the
trays throughout the study was living.
From fall 2002 through summer 2012, trays were sampled seasonally
(quarterly: fall, winter, spring, summer) at low tide. During each seasonal
sampling event, trays were quickly retrieved from approximately 0.5 m
of water, crabs were examined, and then all trays were redeployed the
same day. Trays were not cleaned after a sampling event and were allowed
to be fouled, mimicking the proximal oyster habitat. Due to unexpected
circumstances, some sampling events did not take place (fall and winter
2006; spring, fall, and winter 2007; fall 2008; spring 2009), so the actual
number of seasons sampled (n = 33) during the ten-year period is slightly
smaller than the balanced number (n = 40).
Trays were collected one-at-a-time and the contents of each tray were
emptied into a large wood-framed sieve (5 mm mesh), rinsed, and sorted.
Large crabs, including specimens of Menippe mercenaria (Say, 1818),
Callinectes sapidus Rathbun, 1896, and C. similis Williams, 1966 were
identified, measured (carapace width to the nearest 0.1 mm), sexed, assessed
for presence of eggs or parasites, and released away from the sampling
site. Specimens of the non-native species C. hellerii and all other crab
specimens were placed in containers labeled by tray number and either
frozen or preserved in 70% EtOH to be examined and sorted later following
the same protocol as that used for larger specimens in the field. Native
mud crabs including P. herbstii and E. depressus are not reproductive until
they reach approximately 6 mm or greater (Ryan, 1956; McDonald, 1982),
therefore all crabs with a carapace of <6 mm were considered recruits and
not identified to species in the early years of the study. Because not all crabs
were saved, later re-identification of smaller specimens was not possible.
For consistency, no crabs smaller than 6 mm were identified to species.
All specimens of E. depressus collected and preserved during the tenyear study were re-examined in 2012 after the presence of the parasitic
rhizocephalan barnacle, L. panopaei, which targets and infects E. depressus,
was detected. Because of the resemblance of L. panopaei to a gravid
female’s egg sac, it was suspected that at least some crab specimens that
had been recorded as gravid during the study were actually infected by the
parasite. Not all crab specimens from the study were available (samples
from winter 2002, summer 2004 and spring 2005 were not archived),
therefore, only a subset of all E. depressus specimens could be re-examined.
This subset was used for examining changes in the number of gravid and
infected specimens (as indicated by the presence of externae) over time.
Data Analysis
Seasonal abundance for all species collected (individually and combined)
was expressed as the mean number of crabs per tray (NPT) and its
standard deviation. Mud crab communities were compared by year and
season using non-metric multi-dimensional scaling (MDS). A Bray-Curtis
similarity matrix was constructed using the fourth root of mean NPT
(n = 7) of all species per sample date, and was used for MDS and
further analyses. The transformation reduced the weight of abundant
EASH-LOUCKS ET AL.: LONG-TERM CHANGES IN AN ESTUARINE MUD CRAB COMMUNITY
species, allowing less abundant species to contribute to the community
classification. The similarity matrix was used to conduct one-way analysis
of similarity (ANOSIM) on community separation based on season and
year. Further analyses were conducted on the community separation based
on the presence/absence of an introduced parasite. The importance of
individual species in the overall community structure was determined using
a BEST match permutation test on the transformed species abundance
matrix. Effects of environmental parameters (temperature and salinity) on
community composition were analyzed with BEST relating the species
abundance matrix to the Euclidean distance matrix of environmental
parameters (normalized 30-day pre-collection average). PRIMER 6.0 was
used for all multivariate analyses.
Long-term trends in species abundance were examined through a
seasonal Mann-Kendall’s test with a correction for covariance between
seasons (R statistical package) on the NPT by season for the three most
abundant species, E. depressus, P. herbstii, and P. armatus. Comparisons
between individual species abundances by season were made using oneway analysis of variance (ANOVA) tests (R statistical package).
Environmental Parameters
Temperature and salinity were measured using a YSI handheld meter during sampling events from 2011-2012. In addition to these discrete measurements, temperature and salinity were measured continuously throughout the
study period by a YSI datasonde deployed at a nearby GTM NERR SystemWide Monitoring Program station, Ft. Matanzas (29.7370°N, 81.2460°W)
(NERRS, 2013). Because the measurements were taken 7.9 km away from
the study site, a regression analysis was conducted to estimate conditions at
the study site using a subset of paired measurements from the Ft. Matanzas datasonde and study site (38 temperature and 39 salinity measurements). The resulting equations for estimating conditions at the study site
were: temperature = 0.9612x + 1.1725°C (R 2 = 0.9016) and salinity =
1.7926x − 31.6780 ppt (R 2 = 0.6061). Regression-estimated parameters
were used to examine extreme environmental conditions during the study,
and were used in multivariate analyses on community composition.
R ESULTS
Crab Diversity
A total of 6935 individuals of ten species of crab were collected over the course of the study including two species of
non-native crabs: P. armatus, which was abundant, and C.
hellerii, which was extremely rare (Table 1). Species collected included members of eight genera and five families:
Grapsidae (shore crabs), Menippidae (includes stone crabs),
Panopeidae (mud crabs), Porcellanidae (porcelain crabs) and
Portunidae (swimming crabs). Three species dominated the
catch (E. depressus, P. herbstii, and P. armatus), each accounting for at least 10.0% of the total number of crabs collected. The remaining catch was made up of seven species
(C. sapidus, C. similis, C. hellerii, Dyspanopeus sayi (Smith,
1869), M. mercenaria, Pachygrapsus gracilis (De Saussure, 1858) and Panopeus occidentalis (De Saussure, 1857)),
which together comprised 2.5% of the crabs collected, and
recruits (<6 mm carapace width), which comprised 9.9% of
the crabs collected.
Mud crab communities were most similar depending on
the phase (pre, early, and post) of the parasitic L. panopaei
invasion in 2004, with samples separating out by year,
regardless of season (Fig. 2). A one-way ANOSIM of the
Bray-Curtis resemblance matrix confirmed that year was
a significant factor (p < 0.01), while season was not
(p = 0.08). The species that best described the changes
in the overall community (correlation = 0.970) included
(in no particular order): C. sapidus, D. sayi, E. depressus,
M. mercenaria, P. armatus, P. herbstii, and P. occidentalis.
Callinectes similis, C. hellerii, and P. gracilis did not have
733
a significant effect on the overall community during the
study period. Sampling without replacement likely did not
influence study results, as no abnormal increases in species
abundances were observed after missed sampling events;
in fact abundances for some species (P. armatus) even
decreased in such instances (Fig. 3).
More detailed analyses focus on changes that occurred
in the three most common species that comprised 87.6% of
the total catch (97.3% of the adult crabs) collected during
the ten-year study period: P. herbstii, P. armatus, and E.
depressus.
Eurypanopeus depressus.—At the initiation of the study E.
depressus was the third most abundant species (maximum
density was 53.6 m−2 ), but its numbers declined during
the fall of 2004 and did not increase for the remainder
of the study period (Tau = −0.721, slope = −2.733
NPT/year, p < 0.01) (Fig. 3). Specimens of E. depressus
collected at the start of the study, during the winter of
2002 thru the winter 2003, did not contain the parasitic
rhizocephalan barnacle L. panopaei. The first collection of
a parasitized crab occurred during spring 2004 (one of 62
crabs was parasitized). Of the archived specimens we were
able to re-examine, only one female (from the summer of
2007) was found to be gravid (and unparasitized) after the
presence of L. panopaei was first recorded. That female
was within one standard deviation of all previously collected
ovigerous females. Regardless of season, after L. panopaei
was first detected; most specimens collected after spring
2004 were of similar size, but parasitized (Table 2). The
presence of the parasite had a significant effect on the overall
community structure. A one-way ANOSIM of the species
abundance resemblance matrix and the presence of the
parasite (pre/post introduction) demonstrated the significant
(p = 0.04) impact of the species’ presences on the crab
community.
Panopeus herbstii.—Abundances of P. herbstii at the study
site were more consistent than for other species throughout
the study, and the species was collected with a maximum
density of 58.9 m−2 . There was no significant change in
the number of P. herbstii collected per tray during the study
(Tau = 0.112, slope = 1.125 NPT/year, p = 0.48) (Fig. 3).
More crabs were collected during the fall (likely reflecting
summer recruitment); however, NPT by season was not
significantly different (p = 0.54).
Petrolisthes armatus.—The number of P. armatus per tray
was high during the first five years of the study (highest
density was 89.8 m−2 ), but decreased during early 2008
and remained low (lowest density was 3.1 m−2 ) until
2011, when the number collected began to increase again
(Fig. 3). Overall, there was no significant trend in P. armatus
abundances over the study period (Tau = −0.287, slope =
−6.575 NPT/year, p = 0.15). More crabs were collected
during the fall, but the NPT did not differ significantly
by season (p = 0.42). The smallest gravid specimen of
P. armatus collected was 4.8 mm. The bopyrid isopod
Aporobopyrus curtatus (Richardson, 1904) was detected in
specimens of P. armatus throughout the course of the study
(as noted by a bulge in the posterolateral carapace), with a
mean infection rate of P. armatus by A. curtatus of 1.8%.
734
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 6, 2014
Table 1. Mean number of crabs per tray (NPT) and standard deviation (in parentheses) by season for all species with more than 10 individuals total (n = 5)
and recruits. The remaining five less-abundant species (Callinectes sapidus, n = 7; C. similis, n = 2; Charybdis hellerii, n = 7; Pachygrapsus gracilis,
n = 1; Panopeus occidentalis, n = 3) were included in the total numbers for each season (n = 6935 total). F, fall; W, winter; Sp, spring; Su, summer.
Sampling event
F
W
Sp
Su
F
W
Sp
Su
F
W
Sp
Su
F
W
Sp
Su
F
W
Sp
Su
F
W
Sp
Su
F
W
Sp
Su
F
W
Sp
Su
F
W
Sp
Su
F
W
Sp
Su
Total
% Total
09/20/02
12/19/02
03/18/03
06/20/03
09/24/03
12/19/03
03/30/04
06/28/04
11/11/04
12/10/04
03/23/05
06/21/05
09/13/05
01/11/06
04/20/06
06/16/06
2006
2006
2007
06/01/07
2007
2007
03/22/08
07/01/08
2008
02/19/09
2009
06/29/09
09/24/09
01/21/09
05/06/10
08/30/10
11/17/10
01/24/11
04/11/11
07/22/11
10/08/11
02/04/12
05/11/12
07/25/12
Dyspanopeus
sayi
Eurypanopeus
depressus
Menippe
mercenaria
Panopeus
herbstii
Petrolisthes
armatus
Recruits
(<6 mm)
Season
total
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
0.1 (0.4)
0 (0)
0 (0)
–
–
–
0 (0)
–
–
8.3 (3.8)
0 (0)
–
1.6 (3.1)
–
0 (0)
0.1 (0.4)
0.4 (0.8)
0.7 (1.1)
0 (0)
0 (0)
0.3 (0.5)
1.6 (2.2)
0 (0)
0.9 (1.1)
1.1 (1.9)
0.6 (0.8)
0.9 (1.1)
116
1.7
6.6 (4.2)
11.9 (4.4)
17.6 (9.8)
16.3 (5.3)
14.7 (7.7)
14 (3.5)
8.9 (3.7)
8.9 (7.6)
2 (1.6)
1.1 (2.6)
2.7 (0.8)
1.6 (0.8)
2 (1.6)
0.6 (0.5)
0.3 (0.5)
0.4 (0.8)
–
–
–
0.1 (0.4)
–
–
0.1 (0.4)
0.4 (0.8)
–
0.6 (0.8)
–
1 (2.7)
1.3 (1.1)
0.4 (0.8)
0.3 (0.5)
0 (0)
0 (0)
0.1 (0.4)
0.4 (0.5)
0.3 (0.5)
0.9 (1.2)
0.3 (0.5)
0.1 (0.4)
0 (0)
813
11.7
0.1 (0.4)
0.1 (0.4)
0 (0)
0.1 (0.4)
0 (0)
0 (0)
0 (0)
0 (0)
0.1 (0.4)
0.1 (0.4)
0.1 (0.4)
0 (0)
0 (0)
0.1 (0.4)
0 (0)
0 (0)
–
–
–
0 (0)
–
–
0 (0)
0 (0)
–
0 (0)
–
0 (0)
0 (0)
0 (0)
0.1 (0.4)
0 (0)
0 (0)
0.1 (0.4)
0.3 (0.5)
0.6 (0.5)
2 (1.4)
0 (0)
0.3 (0.5)
0.6 (0.5)
35
0.5
3.9 (2)
4.9 (2.5)
6.4 (2.4)
11.9 (2.9)
11.9 (2.5)
12.1 (4.4)
12.7 (3.3)
17.3 (4.4)
8.7 (2.8)
13.7 (2.4)
10 (1.7)
16.9 (5.2)
3.9 (16.9)
5.1 (2.6)
12.1 (3.3)
14.1 (2.5)
–
–
–
13.9 (3.5)
–
–
6.4 (2.6)
12.4 (2.5)
–
19.3 (3.7)
–
13.1 (5.9)
13.3 (2.2)
10.7 (2.1)
13.6 (2.5)
6.4 (2.4)
9.4 (3.9)
4.7 (2.3)
16.7 (4.7)
13.4 (4.3)
16.4 (3.3)
12.9 (3.6)
14.1 (4.3)
13.7 (3.6)
2718
39.2
10.6 (7.5)
19.6 (11.9)
8.9 (2.9)
29.4 (8.3)
10.9 (3.1)
11.4 (4.6)
5.4 (2.3)
16.6 (4.7)
19.9 (7.8)
19.4 (10.7)
11.4 (3.2)
22.4 (5.6)
2.9 (22.4)
11.3 (5.6)
16 (5.6)
19.7 (4.3)
–
–
–
17.7 (11.7)
–
–
1.6 (2.4)
2.4 (1.7)
–
2.6 (2.2)
–
2 (1.6)
5.4 (5.4)
3.4 (1.9)
3 (2.6)
4.6 (1.9)
6.9 (4.9)
1 (0.8)
7.7 (5.7)
15.1 (7)
19.6 (7.1)
11.9 (6.1)
9.7 (3.6)
7.9 (2.7)
2548
36.7
2.7 (1.7)
19.6 (10.8)
6.3 (3.1)
0.3 (0.8)
2.1 (1.7)
16 (5.5)
3 (1.9)
0.6 (1.1)
1.6 (1.3)
2.7 (1.9)
1.1 (0.9)
1.4 (1.5)
0.4 (1.4)
9.9 (7.1)
2 (2.1)
0.3 (0.8)
–
–
–
0.3 (0.5)
–
–
0 (0)
0.4 (0.8)
–
0.1 (0.4)
–
0.9 (1.1)
1.7 (1.1)
0.9 (1.2)
0 (0)
0.4 (0.5)
2 (1.9)
0.4 (0.5)
0.9 (1.1)
1.1 (1.9)
7 (1.6)
6.3 (2.2)
1.6 (1.6)
4.1 (0.7)
685
9.9
168
392
274
406
277
375
210
303
226
261
182
191
296
190
213
242
–
–
–
224
–
–
115
110
–
169
–
119
153
111
124
80
128
47
194
214
327
230
191
193
Environmental Parameters
The BEST analysis demonstrated that temperature and salinity were not significant factors in determining the overall crab community structure (p = 0.32, correlation =
0.064). Nonetheless, several instances of extreme environmental conditions may have had brief impacts on individual
crab species during the study period. Extreme low temperatures occurred during the 2009-2010 and 2010-2011 winters
when water temperatures fell below 10°C in January of each
season (Fig. 4). During this period, a reduction in the number
of P. armatus species was observed (Table 1). Additionally,
animals were exposed to salinities of less than 5 ppt in September of 2004 during Hurricane Frances and May of 2009
due to heavy rainfall (Fig. 4). However, these brief periods
of reduced salinity did not appear to affect the number of the
three dominant species at the study site (Table 1).
D ISCUSSION
Mud crab species composition in the mixed oyster/mud
habitat investigated in this study was stable during the ten
year period examined, however, the abundance ratios for
some of the most frequently occurring species changed
over the course of the study. Of these frequently occurring
species, decreased abundance was observed for E. depressus, a slightly increased, although not significant, change in
abundance was observed for P. herbstii, and a decline and re-
EASH-LOUCKS ET AL.: LONG-TERM CHANGES IN AN ESTUARINE MUD CRAB COMMUNITY
735
Fig. 2. Spatial similarity of seasonal crab communities demonstrated with
non-metric multi-dimensional scaling over a ten year period (autumn 2002 –
summer 2012). Each point represents a crab community during one season.
Ovals indicate a similarity of 76% and classify seasonal assemblages into
groups based on the introduction of the parasite Loxothylacus panopaei.
Fourth root transformed data, similarity: 76, 2-D stress: 0.14.
covery in abundance was observed for P. armatus. Thus, not
surprisingly, these same three highly abundant and ubiquitous species (E. depressus, P. herbstii, and P. armatus) were
also included in the group that best characterized changes
in community structure over time. Less abundant and infrequently occurring species (7 of the 10 crab species) included
members of Portunidae and Menippidae, which were typically larger than other species observed and likely rarely collected because of: 1) size constraints which limit the number
of individuals occupying a tray, and 2) their ability to escape
from the tray (rapidly in the case of the portunids) during retrieval of trays from the water. Only one specimen of D. sayi
was collected during the first five years of the study, but sporadic collections occurred during the final years. Abiotic and
biotic factors, including the presence of parasites, appeared
to affect the overall crab community.
Parasites
Two species of introduced parasites, A. curtatus and L.
panopaei, both of which are parasitic castrators, were
found to infect P. armatus and E. depressus respectively.
No individuals of other crab species collected had visible
signs of parasitization. The bopyrid isopod A. curtatus cooccurs with its host in its native habitat (Oliveira and
Masunari, 1998). The infection rate of P. armatus by A.
curtatus was 1.8% during the ten-year study, which is lower
than rates observed (9.5 and 3.1%) in previous studies in
its native range of coastal Brazil (Oliveira and Masunari,
1998; Miranda and Mantelatto, 2010). One reason for the
low parasite densities may be that presence/absence was
determined visually (by existence of a carapace bulge)
rather than through dissections, thus potentially leading to
young parasites being overlooked. Despite varying levels of
infection, previous studies have indicated no negative effects
of this parasite for host crabs in their native range (Oliveira
and Masunari, 1998; Miranda and Mantelatto, 2010).
An abrupt decrease in the number of E. depressus occurred in fall 2004, after which the population continued to
Fig. 3. Mean number of crabs per tray (NPT, with standard error) for
Eurypanopeus depressus, Panopeus herbstii, and Petrolisthes armatus from
fall 2002 through summer 2012. An asterisk (∗ ) indicates a season that was
not sampled.
decline with low densities consistently observed during the
remaining eight years of the study. Specimens from the summer 2004 were not available for re-examination, however,
one crab (of 62 collected) was found to be parasitized by L.
panopaei in the spring 2004 collection. Concurrently, a July
2004 study reported an absence of parasites in E. depressus
in the same northeast Florida marsh and several sites south
to Cape Canaveral (Kruse and Hare, 2007), while infected E.
depressus specimens were found south of the sampling site
in another study in 2006 (Kruse et al., 2012). It appears that
L. panopaei was introduced to the study site near the spring
of 2004 and that the introduction resulted in a population decline months later due to the impeded reproductive capabilities of infected crabs. The decline of E. depressus mirrors
the collapses of local populations of mud shrimps Upogebia spp. along the US Pacific coast after the introduction of
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 6, 2014
Table 2. Specimens of Eurypanopeus depressus re-examined to determine
the percentage of gravid females and crabs parasitized by Loxothylacus
panopaei by year. The percent of gravid females was calculated from reexamined female crabs, and the percent crabs parasitized was calculated
from both male and female crabs that were re-examined. F, fall; Su, summer.
Year
Season
1
2
3
4
5
6
7
8
9
10
F02-Su03
F03-Su04
F04-Su05
F05-Su06
F06-Su07
F07-Su08
F08-Su09
F09-Su10
F10-Su11
F11-Su12
Examined/
Collected
% Females
gravid
% Crabs
parasitized
283/366
263/325
30/57
19/20
1/1
4/4
11/11
14/14
6/6
9/9
9.89
9.89
0.00
0.00
100.00
0.00
0.00
0.00
0.00
0.00
0.00
0.04
66.67
57.89
0.00
25.00
81.82
57.14
66.67
55.56
the non-native bopyrid isopod Orthione griffenis Markham,
2004 (Chapman et al., 2012).
Laboratory experiments on larval L. panopaei have shown
that the parasite is unable to successfully proliferate in
salinities below 10 ppt (Reisser and Forward, 1991; Walker
and Clare, 1994) and field experiments have shown that
infection rates in Panopeus obesus Smith, 1869 were lower
Fig. 4. Mean daily temperature and salinity at the study site during the
ten-year study period (fall 2002 through summer 2012).
when salinities were reduced (Tolley et al., 2006). Although
E. depressus can survive in salinities as low as 5 ppt (Gracés,
1987), salinities during the course of this study were rarely
below 10 ppt, offering little to no refuge for the crabs. The
decline in E. depressus may therefore be highly localized
with infection rate being dependent on salinity. Further
examination of crab densities and parasitization rates at sites
with greater freshwater influence is necessary.
A high parasite load can greatly reduce the number of
crabs and restructure the mud crab community as evidenced
by the structuring of the crab community around the occurrence of L. panopaei in the present study. Based on sample
separation using MDS, the early stage of L. panopaei introduction was determined to be from winter 2004 thru 2007,
after which the crab community changed and did not return
to its original composition. The most notable change in the
community was the decline in abundance of E. depressus,
which remained low through the completion of the study.
The decline of E. depresses at the study site mirrors
the decline of the species in Virginia where the dominant
species of mud crabs, E. depressus and R. harrisii (Gould,
1841), were replaced by D. sayi, a formerly rare species in
that region, after the introduction of L. panopaei (Andrews,
1980). Although infected specimens of D. sayi have been
reported (Hines et al., 1997), it appears to be less susceptible
to infection than E. depressus, and no infected individuals of
D. sayi were observed during our study.
Environmental Parameters
Although environmental parameters did not have a significant impact on the overall crab community composition, the
dominant mud crab species displayed different responses to
varying temperatures and salinities. Two species, P. herbstii
and E. depressus, did not appear to be impacted by temperature or salinity variability. These crabs are native to southeastern US estuaries, and are able to tolerate a wide range of
environmental conditions (Williams, 1965, 1984; McDonald, 1982). However, the brief fluxes in abundance observed
for the introduced species, P. armatus may have been a result
of extreme environmental variation.
Petrolisthes armatus can tolerate temperatures of up to
40.5°C (Stillman and Somero, 2000), which is above the
maximum temperature recorded at our study site. These
animals were observed in high densities north of our study
site in Georgia (Hollebone and Hay, 2007), where winter
temperatures are generally lower than those observed in
northeast Florida. However, only 39% of crabs survived
oscillating water temperatures of 5.3-14.4°C that mimicked
temperatures along the southern US coast in January 2010
(Canning-Clode et al., 2011). Consequently, the fewest crabs
were collected during the winters of 2009-2010 and 20102011 following the lowest recorded temperatures (<10°C) in
the study area. The population was able to recover somewhat
during the following year suggesting that their thermal
minimum may be near 10°C and that low temperature
tolerance currently limits their northern distribution. Despite
occasional near-lethal extreme winter water temperatures, it
appears that P. armatus can overwinter in introduced waters.
Unlike temperature, salinity did not appear to have an
effect on the seasonal density of P. armatus. This is contrary
to a study of crab densities in southwest Florida, which
EASH-LOUCKS ET AL.: LONG-TERM CHANGES IN AN ESTUARINE MUD CRAB COMMUNITY
suggested that P. armatus is a stenohaline species that
prefers high salinities (Shirley et al., 2004). Although higher
salinities may be more preferable (Shumway, 1983), P.
armatus occurs in high densities in its natural range at
salinities of 6.7 to 31.5 ppt (Oliveira and Masunari, 1995).
This suggests that P. armatus may be better classified as a
euryhaline species and that salinity is unlikely to have a large
effect on densities. To this end, in the present study there
were no effects on P. armatus densities observed following
periods of decreased salinity after storm events.
Non-Native Species
Over the long-term, the population of P. herbstii appears
to be stable and has neither significantly decreased or increased despite the presence of introduced crab species. Previous studies have observed no negative effect on mud crab
populations due to the presence of P. armatus (Hollebone
and Hay, 2007), likely due to differences in feeding strategy.
A slight, although statistically insignificant, increase in the
number of P. herbstii collected during the course of the study
(1.125 NPT/year) may be due to the large food source provided by the non-native P. armatus, which P. herbstii have
been observed to preferentially feed on (Hollebone, 2006;
Hollebone and Hay, 2008). Alternatively, the slight population increase observed for P. herbstii may be attributable to
the decrease in competition for food and habitat following
the decline of the smaller E. depressus. Although E. depressus is a smaller species and tends to be more omnivorous
than adults of P. herbstii, young P. herbstii have a diet and
habitat preference that is similar to adults of E. depressus
(McDonald, 1977, 1982).
Non-native species can threaten the natural balance of
native communities (Carlton and Geller, 1993), however, the
intensity of their impact often varies. We observed little to no
effect on native crab communities due to the presence of the
non-native crab species P. armatus over a ten-year period.
Although the density of P. armatus changed during the study,
the species has persisted and has not appeared to negatively
affect the native P. herbstii population, confirming earlier
conclusions made by Hollebone and Hay (2007). In contrast,
the non-native parasitic barnacle, L. panopaei, appears to
have had a dramatic effect on the density of E. depressus
and significantly influenced crab community structure over
the ten-year study period. Additional studies targeting oyster
reefs elsewhere in the region are necessary to determine
if these changes are localized or more widespread. The
impacts of the altered mud crab community on the oyster
reef habitat and greater biological community, if the effects
of the introduction are permanent, have yet to be determined.
ACKNOWLEDGEMENTS
We would like to thank GTM NERR researchers L. Herren and R. Gleeson
for initiating this study in 2002, as well as J. Brucker for overseeing
this work for several years thereafter. We are indebted to the numerous
GTM NERR volunteers and staff that assisted with crab collection and
identification throughout the ten year study period. We thank R. Gleeson, B.
Griffen and three anonymous reviewers for their insightful reviews of this
manuscript. The findings and conclusions presented in this paper are those
of the authors and do not necessarily represent the views of the NOAA
National Estuarine Research Reserve system. This research was conducted
pursuant to the Florida Fish and Wildlife Conservation Commission license
number SAL-11-1035B-SR.
737
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R ECEIVED: 4 March 2014.
ACCEPTED: 20 September 2014.