Freshwater Biology (2005) 50, 1323–1336
doi:10.1111/j.1365-2427.2005.01398.x
Stable isotopes, mesocosms and gut content analysis
demonstrate trophic differences in two invasive decapod
crustacea
DEBORAH RUDNICK AND VINCENT RESH
Department of Environmental Science, Policy and Management, University of California, Berkeley, CA, U.S.A.
SUMMARY
1. Improving our understanding of dietary differences among omnivorous, benthic
crustacea can help to define the scope of their trophic influence in benthic food webs. In
this study, we examined the trophic ecology of two non-native decapod crustaceans, the
Chinese mitten crab (Eriocheir sinensis) (CMC) and the red swamp crayfish (Procambarus
clarkii) (RSC), in the San Francisco Bay ecosystem to describe their food web impacts and
explore whether these species are functionally equivalent in their impacts on aquatic
benthic communities.
2. We used multiple methods to maximise resolution of the diet of these species, including
N and C stable isotope analysis of field data, controlled feeding experiments to estimate
isotopic fractionation, mesocosm experiments, and gut content analysis (GCA).
3. In experimental enclosures, both CMC and RSC caused significant declines in
terrestrially derived plant detritus (P < 0.01) and algae (P < 0.02) relative to controls, and
declines in densities of the caddisfly Gumaga nigricula by >50% relative to controls.
4. Plant material dominated gut contents of both species, but several sediment-dwelling
invertebrate taxa were also found. GCA and mesocosm results indicate that CMC feed
predominantly on surface-dwelling invertebrates, suggesting that trophic impacts of this
species could include a shift in invertebrate community composition towards sedimentdwelling taxa.
5. Stable isotope analysis supported a stronger relationship between CMC and both algae
and algal-associated invertebrates than with allochthonous plant materials, while RSC was
more closely aligned with terrestrially derived detritus.
6. The trophic ecology and life histories of these two invasive species translate into
important differences in potential impacts on aquatic food webs. Our results suggest that
the CMC differs from the RSC in exerting new pressures on autochthonous food sources
and shallow-dwelling invertebrates. The crab’s wide-ranging foraging techniques, use of
intertidal habitat, and migration out of freshwater at sexual maturity increases the
distribution of the impacts of this important invasive species.
Keywords: Chinese mitten crab, crayfish, estuary, food web, stream
Introduction
Correspondence: Deborah Rudnick, Integral Consulting,
Inc. 7900 SE 28th Street, Ste 300. Mercer Island,
WA 98040, U.S.A.
E-mail: [email protected]
2005 Blackwell Publishing Ltd
Omnivory is widely recognised as a key component of
how benthic decapod crustaceans regulate energy and
nutrients in aquatic ecosystems (Lodge et al., 1994;
Evans-White et al., 2001; Buck et al., 2003). A general
1323
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D. Rudnick and V. Resh
classification of benthic crustaceans as omnivores,
however, overlooks the details of their dietary preferences and feeding habits that define the scope of
their trophic influence on other organisms. For example, introduced freshwater crayfish can have substantially different trophic impacts than their native
counterparts (Nyström, Bronmark & Granéli, 1999;
Renai & Gherardi, 2004), even for congeneric species
(Lodge et al., 2000).
Two large, benthic, non-native decapods, both of
which have world-wide introduced distributions, are
well established in the freshwater tributaries to San
Francisco Bay, California, U.S.A. The Chinese mitten
crab (CMC), Eriocheir sinensis H. Milne Edwards, was
discovered in 1992 in San Francisco Bay (Cohen &
Carlton, 1997), and has generated widespread concern
about potential impacts on aquatic ecosystems. Prior
to the arrival of CMC, the red swamp crayfish (RSC),
Procambarus clarkii Girard, native to the south-central
U.S.A., was introduced to San Francisco Bay tributaries within the past century (Riegel, 1959).
The introduction of these two invasive species may
impact benthic communities of San Francisco Bay
watersheds. However, no information has been available regarding the trophic ecology of either species in
this ecosystem that would enable scientists or managers to assess the effects on the food web of either
invader. It is also unclear whether these two species
differ in dietary preferences, and therefore to what
extent mitten crabs are adding to, or differing from,
trophic impacts of crayfish already present in these
streams.
The diet of both CMC and RSC in other ecosystems
has been described as opportunistic and omnivorous
(Panning, 1939; Huner & Barr, 1981; Correia, 2003).
The breadth of these species’ diets suggests that
multiple methods may be needed to accurately delineate their trophic ecology. Naturally occurring stable
isotopes can provide an important tool in food-web
research (Peterson & Fry, 1987). Because stable
isotopes are assimilated continuously as the organism
feeds and grows, they can provide a picture of the
long-term dietary intake of the organism being
analysed.
The use of additional methods, such as gut
content analysis (GCA) and experimental enclosures,
can aid in interpretation of isotope studies. Experimental enclosures are often used as a successful
approach to examining diet, because they simplify
the food web structure so that changes in this
structure can be more easily assessed. However, this
method has several limitations, including a limited
time scale for observing effects and the constraints
they impose on the natural diet of the organism of
interest (Schindler, 1998). GCA tends to be biased
towards foods that are harder to digest (Sarda &
Valladares, 1990), is difficult for animals such as
crustaceans that have gastric mills that finely grind
their food, and provides only a snapshot of the diet
at the moment of collection. The use of multiple
methods can complement some weaknesses of each
individual method, providing a weight-of-evidence
approach that can strengthen the interpretation of
results.
This study used experimental mesocosms, stable
isotope analysis, and GCA to examine: (i) whether
CMC and RSC have detectable effects on the aquatic
communities they invaded; (ii) how spatial and
temporal gradients affect these impacts; and (iii)
whether the diets of CMC and RSC differ, which
would suggest different trophic roles for these
species.
Methods
Study organisms
Both CMC and RSC are abundant in the lower
portions (up to approximately 20 km upstream) of
freshwater tributaries to South San Francisco Bay
(Rudnick et al., 2003). CMC were first collected in San
Francisco Bay in 1992 and quickly became abundant
in the Bay and its tributaries (Rudnick et al., 2003).
This species is catadromous, beginning life in winter
or spring in the brackish waters of the Bay and
migrating into freshwater streams in spring and
summer as juveniles. After CMC have reached sexual
maturity, estimated at 2–5 years of age (Rudnick et al.,
2005), they congregate in the lower portions of these
tributaries and migrate rapidly to the open waters of
the Bay in fall to reproduce.
The RSC has been introduced nearly worldwide,
primarily for aquaculture purposes. These crayfish
develop quickly and can achieve sexual maturity
within their first year of life (Huner & Barr, 1981).
Their habitat includes a wide variety of slow-moving
freshwater habitat, including stream margins,
backwater channels, and shallow pools, usually in
2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 1323–1336
Trophic differences in invasive decapods
association with cover such as rocks or dense
vegetation.
Mesocosm experiment
We constructed 24 pools to examine effects of CMC
and RSC on a benthic community. Pools, 1.0 m in
diameter (0.78 m2) and 0.25 m depth, were placed
outdoors in a screened room and randomly assigned
one of four treatments (CMC, RSC, both, or none);
each treatment was replicated six times. The experiment took place between 8 July and 20 September
2001; each pool experiment lasted 60 days. Each pool
was filled to a depth of 10 cm with sterilised sand and
sun-dried cobble to provide a substrate for experimental animals and plants that approximated their
natural environment. Dechlorinated water was maintained to a depth of 20 cm, and pools were aerated.
We inoculated pools with particulate organic matter
(POM) collected with plankton net (mesh size ¼
153 lm). Water quality tests included: dissolved
oxygen, pH, conductivity, and temperature tested
weekly; ammonia and nitrate tested twice during the
experiment; and nitrate, nitrite, and soluble phosphorus tested at the end of the experiment.
We used treatment densities of crustaceans comparable with field densities based on trapping and
visual observations (Rudnick, 2003). Four individuals
per pool (5 m)2) were chosen as representative of
moderately high field densities. Pools were randomly
assigned a treatment: four CMC, four RSC, two CMC
and two RSC, or neither (control). CMC and RSC were
collected from Coyote and Calabazas Creeks in Santa
Clara County, California. CMC used in this experiment ranged between 30 and 50 mm in carapace
width (CW; 41.2 ± 5.8 mm, mean ± SD), and RSC
between 30 and 45 mm carapace length (CL;
42.0 ± 4.3); these sizes correspond to 1–2 year olds of
both species (Huner & Barr, 1981; Rudnick et al.,
2005). In one CMC pool, two individuals escaped
through a hole in the caging within 2 weeks of the
experiments’ end; in an RSC pool, one individual
escaped and one died; both pools were removed from
analysis.
Macroinvertebrates corresponding to four of the
most abundant taxa found in South San Francisco Bay
tributaries (Carter & Fend, 2000), and representing a
range of functional feeding groups, were chosen as
potential prey. Each pool received densities similar to
2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 1323–1336
1325
those found in the lower reaches of tributaries to
South San Francisco Bay (Carter & Fend, 2000): 4 g
(approximately 400 individuals) of Oligochaetes
(Tubificidae), with guts cleared for 48 h prior to
placement in pools; 200 Trichoptera (Gumaga nigricula);
350 Ephemeroptera (Trichorythidae and Leptophlebiidae); and 15 large (>20 mm shell width) and 15
small (<15 mm shell width) Corbicula fluminea (an
abundant introduced bivalve). At the end of the
experiment, invertebrates were separated from the
sediment by elutriation; recovery rates were ‡95% for
three trials of this method. Elutriated material was
preserved, sorted, and invertebrates (except oligochaetes, which fragment too easily to hand-count) were
counted under a dissecting microscope. Oligochaetes
were dried at 60 C for 48 h then burned in a muffle
furnace at 550 C for 1 h to obtain ash-free dry mass.
Ludwigia sp., an abundant aquatic macrophyte in
South San Francisco Bay tributaries, was collected
live, rinsed, and planted in each pool (203 ± 4.2 g per
pool, mean ± SD). At the end of the experiment,
plants were harvested from the pools and attached,
uneaten leaves were collected. Detritus of common
terrestrial plants were added to each pool: 30 g of
Platanus racemosa; 25 g of Salix laevigata; and 15 g of
Salix hindsiana. Salix species were combined in analysis because decomposed fragments could not be
differentiated by species.
Algae (Cladophora sp.) colonised for 4–6 weeks on
concrete bricks (8.2 cm2 surface area) in Coyote Creek
were hand-cleaned of invertebrates and added to
pools. Because the closed system of the pools did not
provide for new algal sources, we added a second
brick of algae to each pool between 30 and 35 days
from the start of the experiment.
At the end of the experiment, macrophytes, plants,
and algae were hand-cleaned of invertebrates, rinsed
with DH2O, and dried at 60 C for 24 h to obtain dry
weight. Algae were combusted to obtain AFDM using
the same protocol as for oligochaetes (see above).
We log-transformed data, including AFDM of leaf
detritus, macrophytes, algae, and counts of invertebrates to meet assumptions of normality and homogeneity of variance (JMP 4.0). Heterogeneity of
variance was ameliorated, but not resolved for algal
data; transformation was deemed sufficient because
A N O V A tends to be robust to heterogeneity for
designs with n > 5 (Underwood, 1997). We used
M A N O V A (Pillai’s Trace test statistic) to compare
1326
D. Rudnick and V. Resh
dependent variables among treatments (Systat 8.0).
Each significant response variable was analysed by a
protected A N O V A , followed by post hoc Tukey tests.
We applied a sequential correction of P-values to
reduce the risk of type I error associated with multiple
comparisons (Rice, 1990). We conducted power
analyses (JMP 4.0) for analyses in which no statistical
significance was found. Regression of treatment
weights of CMC and RSC against dependent variables
provided little explanatory power, except for the
relationship between treatment weights and remaining oligochaete biomass; therefore, we included
weight as a covariate in univariate analysis.
Stable isotope analysis field study
We collected samples of CMC, RSC, and potential
prey items from three sites on Coyote Creek (3720¢N,
12147¢W), a tributary feeding the south end of San
Francisco Bay. Samples were collected within a 50 m
reach at each site during three periods in July to
August 2001, October to November 2001, and April to
May 2002. The furthest downstream site (site 1)
received tidal inflow over approximately one-half
the tidal cycle and had salinities ranging from 1 to
10 ppt over the tidal cycle; the middle site (site 2) was
located just above the zone of tidal influence; and site
3 was located in fresh water approximately 3 km
upstream of the middle site. In summer and autumn
2001, one or two composite samples of each potential
prey item were collected at each site and analysed for
carbon and nitrogen isotope signatures. In spring
2002, we collected multiple composite samples from
each site (Table 1).
Chinese mitten crab were collected during all three
sampling seasons at site 1; from site 2 in spring and
autumn but were not found at this site in summer; in
summer and autumn at site 3 but were not found at
this site in spring (Table 1). RSC were collected from
sites 2 and 3 during spring and summer (Table 1).
Few RSC were found in, and therefore were not
collected from, the tidally influenced portion of the
stream (site 1). RSC were seldom found in autumn,
probably because they were dormant (Gherardi,
2002). CMC and RSC were collected by hand and
passive traps and frozen in the field. Individuals were
weighed, sexed, and measured (CL for RSC; CW for
CMC). Muscle tissue was dissected under a microscope.
Invertebrate taxa were chosen for sampling based
on the results of a CMC gut contents pilot study
(L. Rogers, University of California at Berkeley, pers.
comm.) and from taxa known to be abundant at these
sites (Carter & Fend, 2000). Oligochaetes, chironomids, C. fluminea, and Nereis sp. (polychaetes) were
collected from all three sites (Table 1) using a kick-net
Table 1 Sample sizes of isotope field collections, Summer 2001 to Spring 2002
CMC RSC
(1)*
(1)
Site 1
Summer
Fall
Spring
Site 2
Summer
Fall
Spring
Site 3
Summer
Fall
Spring
14
18
43
n.a.
n.a.
n.a.
Oligochaetes Chironomids Polychaetes Corbicula Ludwigia Typha Scirpus Populus Salix Algae
(10–15)
(30–50)
(5–10)
(3–6)
(3–5)
(3–5) (3–5)
(3–5)
(3–5) (3–4)
1
2
5
0
1
3
0
1
0
1
1
3
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
1
0
0
0
1
2
1
1
3
2
0
4
n.a.
5
13
13
0†
n.a. 0
15
3
1
1
4
1
2
5
1
1
3
0
0
3
1
0
0
1
0
0
1
0
3
1
1
3
1
0
5
13
14
n.a.
10
n.a.
13
1
1
2
0
1
4
1
2
3
0
0
3
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
1
1
2
1
2
3
1
0
5
1
2
4
*Numbers outside of parentheses are numbers of composite samples analysed; numbers in parentheses in the header column are
approximate numbers of individual samples comprising each composite. For plants (Ludwigia, Typha, Scirpus, Populus, Salix), individual samples comprising the composite are individual leaves; for algae, individual samples comprising the composite are samples
scrubbed from an individual rock or tile.
†
With respect to 0s: in the case of macrophytes (Ludwigia, Scirpus, Typha), collections were restricted to one season; other 0s occur
because insufficient sample was collected for analysis or lost during preparation.
n.a., not applicable, because this item was not present at the site in the given season.
2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 1323–1336
Trophic differences in invasive decapods
and kept in distilled water for 3 days to clear gut
contents.
Leaves from terrestrial riparian plant species
S. laevigata and Populus trichocarpa were collected
from the stream. Cladophora algae was collected from
rocks and artificial substrates from riffles and shallow
pools in summer and spring (Table 1). The macrophytes Ludwigia, Scirpus, and Typha latifolia, common
in Coyote Creek, were found not to be eaten by either
CMC or RSC (see mesocosm study above; Rudnick,
2003; L. Rogers, pers. comm.), and were confined to a
few samples collected in one season (Table 1).
Invertebrate and crustacean samples were freezedried for 24 h and all plant and algal samples were
oven dried at 60 C for 48 h. All samples were
homogenised using a freezer mill or Wig-L-Bug.
Samples were analysed at the UC Berkeley Center
for Stable Isotope Biogeochemistry on a PDZ Europa
Scientific 20/20 CF-IRMS (precision ±0.1&) to obtain
values for carbon (C) and nitrogen (N) concentrations,
13
C/12C relative to the Vienna-PDB standard, and
15
N/14N relative to atmospheric N2. This process
generated d values for each sample, where d ¼
[(R sample / R standard) ) 1] · 1000 where R is the
ratio of heavy to light isotopes (e.g. 13C/12C).
We created dual-isotope plots of carbon and nitrogen d values of CMC, RSC, and potential food sources
at each site, which were corrected for fractionation
values estimated from the controlled feeding study
(see below). Likelihood of contribution to the diet is a
function of the graphic proximity of a resource’s
signature to that of the consumer. Seasonal changes in
isotopic signatures of consumers were tested using
A N O V A , followed by Tukey tests for significance
among pairs.
We used a linear mixing model for site 1, where
potential food sources could be categorised into three
distinct groups (algae, invertebrates, and plant detritus) to estimate contributions of each food type
(IsoError: Phillips & Gregg, 2001, available at
http://www.epa.gov/wed/pages/models.htm).
Stable isotope analysis controlled feeding study
We conducted a controlled feeding study with CMC
and RSC to account for fractionation processes in our
field isotope study, because estimates for field studies
are strengthened by understanding how physiological
processes in the consumers of interest change, or
2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 1323–1336
1327
fractionate, the isotopic signatures of their prey. Lack
of knowledge about these rates when collecting data
on trophic relationships in the field can lead to
mistakes about the true relationships between isotope
data of consumers and their prey (France, 1996; Post,
2002; McCutchan et al., 2003).
Chinese mitten crab used were raised from eggs in
the laboratory; larval crabs hatched from the same
cohort (i.e. hatched on or near the same date) were
kept colonially in aerated containers and fed brine
shrimp. After metamorphosis, juvenile CMC were
kept individually in small containers. Because nitrogen concentration has been shown to effect fractionation rates (Adams & Sterner, 2000; Vanderklift &
Ponsard, 2003), two food items, one with high and the
other with low percentage carbon : percentage nitrogen (C : N) ratios, were offered to both CMC and RSC.
Juvenile CMC were provided with salmon food
pellets (Nelson’s Silver Cup Fish Feed Co, Murray,
UT, U.S.A.: a mixture of soy and animal proteins; low
C : N ratio food) and the aquatic macrophyte Egeria
densa (high C : N ratio food). Juvenile CMC were fed
on this diet for 6 months prior to carbon and nitrogen
isotope analysis.
Red swamp crayfish also were raised from eggs in
the laboratory. Upon hatching, RSC were separated
into groups of five fed either a diet consisting of
ground carrots or (in a separate aquarium) a diet
consisting of a mixture of carrots and oligochaetes.
Two RSC on the mixed diet died during the experiment and were removed. RSC were fed on these diets
for a period of 3 months before harvesting.
Muscle tissue of 10 juvenile CMC, three samples of
E. densa, and four samples of pellet food were
analysed. Muscle tissue of three RSC on the mixed
diet, five RSC on the carrots-only diet, and three
composite samples each of carrots and oligochaetes
were analysed. All samples were prepared and
analysed for C and N analysis as described above
for the field study samples.
Isotopic signatures of the food of consumers fed on
a single-item diet were subtracted directly from those
of the consumer to obtain C and N fractionation
values. For mixed diets, where nitrogen concentrations differed among food sources, nitrogen fractionation was estimated using a concentration-dependent
mixing model that uses information about the isotopic
signature of the consumer and of a known food item
to back-calculate the fractionation rate of nitrogen
1328
D. Rudnick and V. Resh
obtained from the other food item (Phillips & Gregg,
2001; Phillips & Koch, 2002). The model does not
require information about the quantity of food
ingested. The model describes the mathematical
relationship between the signature of the consumer
and its foods. A spreadsheet for calculations with this
linear mixing model is available at http://www.epa.
gov/wed/pages/models.htm.
Gut content analysis
To provide additional information about diet, we
analysed gut contents of CMC and RSC collected
during the spring sampling period of the isotope
study. Sample selection was based on seasonal
availability of both species and so that comparisons
could be conducted within and between species (site
1 ¼ 20 CMC analysed; site 2 ¼ 13 CMC and 15 RSC;
site 3 ¼ 10 RSC).
Foregut contents of an individual were distributed
across a gridded (24 squares, approximately 1 cm2
each) Petri dish and identified, under a microscope,
within each square to one of five major categories of
food types: terrestrial leaf matter; aquatic macrophytes; inorganic material; algae; and invertebrates
identified to order. Categories were assigned an
abundance ranking between 1 and 10, and then
averaged across all squares to obtain relative abundance of each food type for an individual (sensu
Amundsen, Gabler & Staldvik, 1996). Percentage
abundance and occurrence were calculated for each
food category and tested for differences within species
among sites and between species within sites. Because
data did not fit assumptions of homogeneity of
variances, a nonparametric Kruskal–Wallis test was
used for comparisons (Systat 8.0), with a correction
(Rice, 1990) to account for multiple comparisons.
Results
Mesocosms
No significant differences were found (A N O V A , 3 d.f.)
among treatments for temperature (P > F ¼ 0.77),
dissolved oxygen (P > F ¼ 0.40), pH (P > F ¼ 0.70),
or conductivity (P > F ¼ 0.55). Temperature (17.7 ±
0.6 C, mean ± SD) was similar to summer temperatures of South Bay tributaries (Rudnick, 2003). Most
ammonia, nitrate, and phosphate levels remained
below detectable limits throughout the experiment
and were not significantly different among treatment
types.
Neither CMC nor RSC showed significant changes
in weight during the experiment (CMC P ¼ 0.84, RSC
P ¼ 0.10, two-tailed paired t-test) or within treatments. Few individuals were observed to moult
during the experiment; moults were removed from
the pools immediately upon detection.
In all treatments, the biomass of algae (M A N O V A :
F ¼ 19.7, P < 0.001, 3 d.f.) and detritus (F ¼ 40.1 for
Salix, 33.8 for Platanus; P < 0.001, 3 d.f. for both)
declined by more than 50% relative to the control
(Fig. 1). Macrophytes did not significantly decline in
any of the treatments (P ¼ 0.06). High variability in
remaining plant and algal biomass precluded our
ability to detect differences in biomass among noncontrol treatments.
Both CMC and RSC reduced the abundance of the
caddisfly Gumaga, on average 90%, for all treatments
relative to control (Fig. 1). Clam abundance declined
significantly in the CMC treatments relative to the
control (P ¼ 0.025), while abundance in the RSC
treatment remained similar to the control (Fig. 1).
Power was low (<50%) for comparisons of invertebrate abundance among treatments. All pools had
extremely low numbers of Ephemeroptera at the end
of the experiment, including the controls. Large
numbers of exuviae observed on surfaces of the pools
suggested that most Ephemeroptera had emerged
over the course of the experiment.
Average oligochaete biomass increased in the CMC
treatment >150% relative to the control, while RSC
and combination treatments were similar to control
(Fig. 1). A significant positive correlation (r2 ¼ 0.57,
P < 0.007) was evident between oligochaete abundance and CMC weights.
Other invertebrate taxa accidentally entered the
pools, including corixids, chironomid larvae, and
isopods (<10 per pool), probably with transplanted
macrophytes or by aerial entry after pools were
constructed. A few pools had high numbers (>100)
of freshwater leeches and two pools had high
numbers of dragonfly larvae (>30). No significant
relationship was found between these high numbers
and changes in the four invertebrate taxa purposefully
added to pools. We found a large number of freshwater snails (Physidae and Planorbidae) in control
pools (450 ± 167, mean ± SD) relative to the three
2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 1323–1336
Trophic differences in invasive decapods
1329
300
Both
CMC
RSC
250
% Difference from control
200
150
100
50
0
–50
–100
* * *
* * *
* * *
* * *
*
*
Clams
(corbicula)
(P = 0.025)
Oligochaetes
(P = 0.001)
–150
–200
Detritus
(platanus)
(P = 0.007)
Detritus
(salix)
(P = 0.009)
Algae
Macrophytes
(cladophora) (ludwigia)
(P = 0.013)
Caddisflies
(gumaga)
(P = 0.01)
Fig. 1 Changes in prey items in experimental mesocosms for each treatment: Chinese mitten crabs (CMC), red swamp crayfish (RSC),
or both, relative to control. Changes are measured in: abundance for clams and caddisflies; dry weight for macrophytes and detritus;
ash-free dry mass for oligochaetes and algae. Error bars are ±1 SD. Significant differences among treatments relative to the control
(indicated with asterisks) are determined by post hoc Tukey test; P-values (sequential test corrected) associated with each significant
test are shown below each category. Power analysis showed a low power to detect differences among CMC, RSC, and combination
treatments for detritus, algae, or caddisflies (1 ) b < 50%).
treatment pools (CMC ¼ 31 ± 18, RSC ¼ 16 ± 7,
combined ¼ 16 ± 7). Although it cannot be established whether these differences were from feeding by
CMC and RSC, snails were likely consumed by these
non-native decapods.
pellet food in the controlled feeding study. These
values were applied as corrections to foods with low
C : N ratios in the field study (Table 2). We assumed
CMC fed nearly exclusively on salmon pellets, based
on two lines of evidence. First, the average nitrogen
isotopic ratio of CMC (d15N ¼ 11.7 ± 0.4, mean ± SD)
was very different from that of E. densa (d15N ¼
2.1 ± 0.02; Table 2). Although the CMC’s isotope
value could be expected to be depressed by the values
of E. densa if it was eating the plant, CMC signatures
Stable isotope analysis: controlled feeding studies
Chinese mitten crabs were enriched in nitrogen
(2.9 ppt) and carbon (1.9 ppt) relative to the salmon
Table 2 Mean isotope ratio and carbon and nitrogen constitution of Chinese mitten crabs (CMC), red swamp crayfish (RSC), their
diets, and derived fractionation values in the controlled feeding experiment. As CMC consumed little Egeria densa during the
experiment, C fractionation values for pellets, and N-fractionation values for high C : N ratio food from RSC, were used as estimates.
Oligochaete samples are each a composite of 10–20 individuals.
Source
Number of
samples
d13C (SD)
d15N (SD)
%C
%N
CMC: salmon pellet diet
CMC food: Salmon pellets (low C : N ratio)
CMC food: E. densa (high C : N ratio)
RSC: carrots only diet
RSC: mixed diet
RSC food: oligochaetes (low C : N ratio)
RSC food: carrots (high C : N ratio)
10
4
3
5
3
3
3
)19.4
)21.3
)22.2
)23.8
)18.3
)14.9
)25.7
11.7
8.8
2.1
7.9
10.0
9.8
1.9
44.3
46.9
38.1
45.9
45.9
43.5
39.6
11.8
7.7
1.5
13.7
14.3
9.9
1.4
(0.5)
(0.07)
(0.02)
(0.4)
(0.7)
(0.03)
(0.07)
2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 1323–1336
(0.4)
(0.2)
(0.08)
(0.6)
(0.4)
(0.1)
(0.1)
C fractionation
values
N fractionation
values
1.9
1.9
2.9
6.0
2.0
1.9
1.0
6.0
1330
D. Rudnick and V. Resh
for carbon and nitrogen actually were enriched in the
heavy isotope of nitrogen relative to just the salmon
pellets. Second, laboratory observations supported
that pellets were preferred by the crabs over E. densa
(D. Tullis, Department of Biology, California State
University, pers. comm.). As carbon fractionation
rates tend to be less variable than nitrogen across
food types (Michener & Schell, 1994), the estimated
carbon fractionation ratio for low C : N ratio diet (1.9)
was also used as the fractionation rate for high C : N
ratio foods, and the nitrogen fractionation value for a
high C : N ratio diet generated from the RSC study
(see below) was applied to CMC fractionation corrections.
Red swamp crayfish fed only on carrots were
enriched in heavy isotopes of both carbon (2.0 ppt)
and nitrogen (6.0 ppt) relative to their food source.
These values were applied as corrections to foods
with high C : N ratios in the field study (Table 2). RSC
fed on a mixture of carrots and oligochaetes displayed
intermediate signatures relative to the two food
sources. RSC fed carrots were used to generate the
carbon and nitrogen fractionation estimates for high
C : N ratio foods. As with the mitten crab study, the
estimated carbon fractionation ratio of 2.0 for the high
C : N ratio diet was used to provide a fractionation
correction for the carbon signature of the low C : N
ratio food (oligochaetes d13C ¼ )14.9, )12.9 after
correction). The concentration-dependent mixing
model was used to resolve fractionation values for
low C : N ratio food sources and to generate the RSC
nitrogen fractionation rate for the low C : N ratio food
(oligochaetes; Table 2).
Stable isotope analysis: field study
Site 1 stable isotope values of CMC [CMC d13C ¼
)27.2 ± 3.7 (mean ± SD); d15N ¼ 15.5 ± 0.8] were
more closely aligned with algal and invertebrate food
sources than with terrestrially derived detritus
(Fig. 2). d15N values of terrestrially derived leaf
materials were low relative to those of CMC, ranging
between 0 and 7 ppt (Fig. 2). CMC d13C values varied
seasonally: d13C was significantly lower in spring
relative to summer and autumn signatures (A N O V A ,
P < 0.001, Tukey test). A similar pattern was reflected
in some of the potential foods: algal carbon isotope
values were lower in spring (d13C ¼ )38.5 ± 1.6;
d15N ¼ 10.9 ± 0.4) than in summer (d13C ¼ )34.0 ±
1.8; d15N ¼ 13.1 ± 0.9). Chironomids, often collected
in association with algae, had lower d13C values
in spring relative to summer and autumn. In contrast, non-algal affiliated invertebrates and terrestrial
detritus did not show distinct seasonal isotope
patterns.
Chinese mitten crab size had a positive relationship
with d15N values over all seasons of sampling at site 1,
although a low percentage of the variance was
ascribable to size (r2 ¼ 0.23, P < 0.001). Variation in
d13C values did not correlate with size of the crab.
Mixing models used to estimate the relative contribution of three major categories of food resources to
CMC diet at site 1 suggested a strong reliance on
invertebrates and a smaller contribution of plant and
algal materials (Table 3). The concentration-dependent model gave greater importance (27% of diet) to
terrestrial detritus relative to the concentration independent model (95% confidence interval ¼ 5–16% of
diet) because the former model compensates for the
lower nitrogen concentration of this material.
Chinese mitten crab isotope values from site 2
were intermediate to many of the potential food
sources (Fig. 2). Depletion of 15N in plant detritus
was not as great as at site 1, and could not be
excluded as a potential food for CMC at this site.
Seasonal shifts in several potential foods were
detected: chironomids, polychaetes, and Corbicula
had higher values of d13C and lower d15N in spring
relative to autumn, with the same trend for algae
between summer and the following spring. Although
there is substantial overlap in CMC isotope values,
CMC d13C and d15N also reflect this same pattern
between autumn and spring.
Chinese mitten crab had an intermediate relationship to potential foods at site 3 (Fig. 2). Carbon and
nitrogen values for CMC sampled in summer (d13C ¼
)30.5 ± 0.9; d15N ¼ 15.1 ± 1.2) were nearly identical
to those for autumn (d13C ¼ )30.1 ± 1.7; d15N ¼
15.0 ± 1.0). No consistent seasonal pattern in food
resources was seen at this site.
The average isotopic signature of RSC at site 2 was
intermediate to several potential foods but was more
closely aligned with terrestrial plant material and
some invertebrates, including oligochaetes, than it
was with algae and chironomids (Fig. 2). Chironomids had lower d13C and lower d15N values relative to
RSC, and algae had substantially lower d13C values
than RSC. Site 2 RSC were similar in isotope values
2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 1323–1336
Trophic differences in invasive decapods
CMC
24
22
20
18
16
14
12
10
8
6
4
2
0
24
22
20
18
16
14
12
10
8
6
4
2
0
24
22
20
18
16
14
12
10
8
6
4
2
0
–40
1331
RSC
Site 1
24
22
20
18
16
14
12
10
8
6
4
2
0
Site 2
24
22
20
18
16
14
12
10
8
6
4
2
0
–40
Site 3
–35
–30
–25
–20
Site 2
Site 3
–35
–30
–25
–20
δ13C
Cladophora
Polychaetes
Typha sp.
Chironomids
Scirpus sp.
Populus trichocarpa
Corbicula fluminea
Ludwigia
CMC (E. sinensis)
Oligochaetes
Salix laevigata
RSC (P. clarkii)
Fig. 2 Dual isotope plot for Chinese mitten crabs (CMC), red swamp crayfish (RSC), and potential food sources. Values are corrected
for fractionation. Error bars are ±1 SD. Invertebrates are shown in four-sided symbols; terrestrial and aquatic plants as three-sided
symbols; algae as circles; CMC and RSC as stars. Colour of symbol denotes season: grey are summer samples; black are autumn
samples; white are spring samples.
2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 1323–1336
1332
D. Rudnick and V. Resh
Table 3 Estimated contributions of major categories of food
sources to the diet of Chinese mitten crabs at site 1, using
dual-isotope mixing models (A spreadsheet for mixing model
calculations is available at http://www.epa.gov/wed/pages/
models.htm). The macrophyte Scirpus was analysed at this site
and found to be indistinguishable from invertebrate isotope
signatures, but was not included in this model as this plant was
not found to be consumed by the crab.
Mean fraction of
95% CI for
diet variance
method*
variance
method
(mean ± SD)
Invertebrates
0.88 ± 0.13
Algae
0.0093 ± 0.13
Detritus
0.10 ± 0.026
0.62–1.00
0.00–0.27
0.047–0.16
Mean fraction of
diet concentrationdependent
method†
0.68
0.051
0.27
*The variance method incorporates the variance of the isotopic
signatures to derive confidence intervals of dietary contributors.
†
The concentration-dependent method uses information about
the diet’s C and N concentrations to generate estimated contributions.
between summer (d13C ¼ )29.0 ± 1.0; d15N ¼ 14.5 ±
2.6) and the following spring (d13C ¼ )29.5 ± 1.3;
d15N ¼ 14.2 ± 1.4; Fig. 2). These values did not appear
to change with seasonal shifts in potential food
sources.
Site 3 RSC isotope values were aligned with detrital
isotope values (Fig. 2). Spring d15N RSC values were
significantly lower than summer values (P < 0.001,
t-test). Similarly, Populus d15N values were lower in
spring than summer. In contrast, most invertebrates
and algae showed little change or slight enrichment in
15
N in spring relative to summer values. Algal (spring
d13C ¼ )36.2 ± 0.7) and chironomid (spring dC ¼
)32.1 ± 0.3) signatures at site 3 were depleted in
carbon relative to RSC.
Gut content analysis of CMC and RSC
Gut contents of site 1 CMC were dominated by algae
and terrestrial detritus (Table 4). Invertebrate abundance was low in CMC gut contents (<5%), with
gastropods being the most frequently occurring
invertebrate in gut contents, found in approximately
40% of crabs analysed (Fig. 3). CMC collected from
site 2 had gut contents similarly dominated by algae
and detritus. Algae were lower in abundance in gut
contents than at site 1 (P ¼ 0.016), and both invertebrates and inorganic materials were significantly more
abundant than at site 1 (Table 4). Chironomids and
gastropods were the two most prevalent taxa found in
crabs at this site (Fig. 3).
Gut contents of RSC from sites 2 and 3 were
dominated by terrestrially derived detritus (Table 4).
Abundance of algae was lower (although non-significant after sequential test correction) at site 3 than at
site 2. A low abundance of invertebrates was found in
gut contents at both sites; occurrence rates of prey
differed between sites 2 and 3, particularly for
polychaetes (>70% of stomachs from site 2 vs. <10%
of stomachs from site 3), and chironomids (40% vs.
none; Fig. 3). No gastropods were found in the gut
contents of RSC at either site.
Gut content composition differed between CMC
and RSC from the same site (Table 4). Detritus was
significantly more abundant in RSC than in CMC
(P ¼ 0.005), while inorganic material was less abundant. Invertebrates were more abundant in CMC gut
contents than in RSC (P ¼ 0.005). While similar taxa
were eaten by both species, there were distinct
differences in their abundance: prevalent invertebrates in mitten crab guts included gastropods and
Table 4 Percentage abundance of food types from gut content analyses of Chinese mitten crab (CMC) and red swamp crayfish (RSC)
collected in spring 2002
CMC site 1
(n ¼ 15)
Detritus
Algae
Invertebrate
Inorganic
45.2
33.8
2.6
14.6
(3.7)†
(4.0)
(0.5)
(1.6)
P-values
CMC site 1
versus site 2*
CMC site 2
(n ¼ 13)
P-values
CMC versus
RSC site 2
RSC site 2
(n ¼ 15)
P-values
RSC site 2
versus site 3
RSC site 3
(n ¼ 9)
n.s.
0.006
0.012
0.018
53.7
18.1
5.6
22.3
0.005
n.s.
0.005
0.019
70.0
13.6
2.1
13.1
n.s.
n.s.
n.s.
n.s.
72.0
8.0
1.2
18.8
(4.5)
(2.3)
(1.1)
(2.0)
(2.5)
(3.9)
(0.5)
(2.0)
(1.5)
(0.5)
(0.2)
(1.2)
n ¼ number of guts analysed.
*P-values are from Kruskal–Wallis nonparametric tests of significance between groups. All P-values have been Rice-corrected for
multiple comparisons between groups.
†
Numbers in parentheses are standard deviation of the mean percentage abundance.
2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 1323–1336
Trophic differences in invasive decapods
1333
Percent occurrence of taxon in guts
100
80
CMC site 1
CMC site 2
RSC site 2
RSC site 3
60
40
20
0
Oligochaetes
Chironomids
Polychaetes
Clams
Fig. 3 Occurrence rates (proportion of total individuals sampled in which the item was found) of the four most common invertebrates
found in gut contents in Chinese mitten crabs (CMC) collected in spring 2002 at sites 1 and 2 and from red swamp crayfish (RSC)
collected in spring 2002 at sites 2 and 3.
chironomids, while RSC gut contents were dominated
by polychaetes at site 2, and held no gastropods at
either site.
Discussion
Food web impacts of the CMC compared with the RSC
Both CMC and RSC function as omnivores in these
stream habitats. However, the use of multiple approaches revealed differences in the two species’ diets that
have important implications for their trophic ecology
and impacts on the ecosystems they inhabit.
Results support distinctions in the pathways of
nutrients to these species, suggesting that RSC may
rely more heavily on allochthonous energy sources,
while CMC have a stronger link to in-stream food
resources. CMC isotope values were more centrally
positioned between algal and detrital signatures. The
correlation of CMC’s seasonal shift in d13C with that
of algae also suggests a close relationship, while RSC
values were aligned and varied seasonally with
detrital isotope values.
Our results indicate that CMC may forage even
more superficially than RSC, and suggest that CMC
2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 1323–1336
could influence shifts in community invertebrate
composition towards deeper sediment-dwelling species. For example, the diet of CMC is more closely
associated with algal-associated invertebrates (chironomids) and shallow-dwelling invertebrates (gastropods, notably Corbicula) than the diet of RSC, which
had a higher prevalence of sediment-dwelling oligochaetes and polychaetes in gut contents. The increased
oligochaete biomass in CMC mesocosm treatments
may have resulted from CMC’s tendency to forage
less intensively for sediment-dwelling species.
The trophic ecology of RSC appears to be more
variable and site-specific than that of CMC. RSC d 15N
values were lowest at the site furthest upstream,
where nearly all RSC were located in a backwater
channel, whereas CMC were captured throughout
riffles and glides at this site. At the downstream
freshwater site, RSC were collected in the same riffle
and glide areas as CMC, and the nitrogen values of
the two species were more similar to each other but
intermediate to several food sources tested. In contrast, the consistency of isotope values of CMC across
freshwater sites fits with field observations that CMC
forages widely and without regard to stream microhabitat (D. Rudnick, pers. obs.).
1334
D. Rudnick and V. Resh
The distinct life histories of these two species result
in remarkably different impacts in terms of nutrient
dynamics. Terrestrial predators remove crayfish from
streams, preventing the recycling of nutrients back
into the stream ecosystem. However, a large proportion of crayfish are recycled back into the stream as a
nutrient base, either through death or predation by
aquatic or semi-aquatic predators (Nyström, 2002). In
contrast, CMC that survive to adult age actively
migrate out of the stream system to reproduce and die
in San Francisco Bay. This process is a new, substantial vehicle for export of biomass out of freshwater
ecosystems to San Francisco Bay.
Food web impacts of CMC and RSC
Our research agrees with a large body of literature
that has shown that freshwater benthic decapods can
play important roles in structuring food webs, by
changing abundance and species composition of
periphyton, plants, and macroinvertebrate abundance
(e.g. Feminella & Resh, 1989; Lodge et al., 1994;
Whitledge & Rabeni, 1997). In our mesocosm experiments, both CMC and RSC had direct, negative
impacts on detritus, algae, and macroinvertebrates.
Substantial predation on shallow-dwelling invertebrates in mesocosms supported a larger role for
invertebrates in the diets of both CMC and RSC than
is suggested by GCA alone. Isotope data indicated
that the signatures of several plant and animal
resources bracket the signatures obtained for both
crustaceans. The large volume of plant and algal
detritus in gut contents of both species suggests that
both RSC and CMC may play an important role in
transforming organic detritus, which can both directly
and indirectly impact freshwater benthic food webs
by changing both the quantity and form of these
nutrients available to other aquatic biota (Momot,
1984; Nyström, 2002).
Results of the isotope study suggest a strong
reliance of CMC on invertebrates, and a smaller role
for terrestrially derived detritus and algae, in its
intertidal habitat. In fresh water, these relationships
are less clear because combinations of resources
bracket CMC isotope values. However, several lines
of evidence suggest that invertebrates remain important as a food source as CMC migrates into freshwater
habitats. Although prevalence of invertebrate taxa in
gut contents from both fresh and saline sites is low,
invertebrates are more abundant in the guts of CMC
collected from fresh water than from its intertidal
habitat. In addition, a positive correlation of 15N
values of crabs from intertidal habitat with their
weight suggests that, as crabs grow larger, they may
incorporate more high-nitrogen foods such as invertebrates into their diet. These findings are consistent
with the results of a study of CMC in its native habitat
that suggested the crabs increase consumption of
animal matter as they age (Dan et al., 1984).
It is difficult to know what the food web of South
Bay tributaries might have looked like prior to the
introduction of these two species. A native crayfish
species (Cambarus nigrescens) is likely to have lived in
this region, although little is known of its local ecology
and it is believed to have been extirpated from the
area by the turn of the century (Riegel, 1959).
Invertebrate food resources encountered by both these
invaders are likely drastically impoverished in diversity and abundance of invertebrates relative to the
past ecology of this area, particularly in the lower
reaches of these streams that have become heavily
urbanised and channelised over the last century
(Nichols et al., 1986).
Factors influencing the food web impacts of CMC
and RSC
Trophic impacts of these introduced crustaceans are
undoubtedly influenced by their abundances over
time and space. Studies in San Francisco Bay and
other regions have found dramatic fluctuations in
CMC distribution and abundance over time (Rudnick
et al., 2003). Densities of CMC found during the
period of this study were low relative to densities
recorded during previous years (Rudnick et al., 2003).
Although little is known about population dynamics
of RSC in these stream systems, broad fluctuations in
other crayfish species’ abundance over time have been
documented (Momot, 1984). Trophic impacts may
fluctuate dramatically depending on population densities and the extent of their distribution throughout
the watershed in a given year.
In summary, while CMC and RSC overlap in many
aspects of resource use, these two non-native crustaceans are not functionally equivalent in their trophic
impacts. The mitten crab is a consumer of autochthonous nutrient sources including benthic macroinvertebrates, and represents new predation pressure
2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 1323–1336
Trophic differences in invasive decapods
particularly in intertidal areas that previously had few
large benthic crustaceans. The crab also provides a
major new route of nutrient export out of freshwater
ecosystems. Given the periodic abundance and widespread distribution of both species throughout this
ecosystem, the scale and magnitude of their trophic
impacts are likely to be substantial.
Acknowledgments
Thanks to L. Aguas, L. Cao, V. Chan, and M. Konar
for research assistance; R. del Rosario, F. Kearns, M.
Meyers and L. Bêche for study design, review, and
field assistance; the Santa Clara Valley Water District
for field site access; the UC Berkeley Gill Tract
Research Station for space and equipment; R. Tullis,
California State University, Hayward, for mitten crabs
for the controlled feeding study; T. Dawson, S.
Mambelli, and P. Brooks, UC Berkeley Center for
Stable Isotope Biogeochemistry, for help with sample
preparation, analysis, and data review and discussion;
J.L. Grenier for research consultation; and D. Phillips,
US EPA, for assistance with isotope mixing models.
The CALFED Bay-Delta Program (Project No. 99N10), Sigma Xi National Scientific Honors Society,
and National Sea Grant provided funding for this
research.
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