Download Effects of Food Type, Habitat, and Fish Predation on the Relative

J. Great Lakes Res. 30(1):100–113
Internat. Assoc. Great Lakes Res., 2004
Effects of Food Type, Habitat, and Fish Predation on the
Relative Abundance of Two Amphipod Species,
Gammarus fasciatus and Echinogammarus ischnus
María J. González* and Greta A. Burkart1
Department of Zoology
Miami University
Oxford, Ohio 45056-1400
ABSTRACT. We evaluated the abundance patterns of Gammarus fasciatus and Echinogammarus
ischnus in dreissenid and macrophyte areas in Hatchery Bay, Lake Erie before (1997) and after round
goby (2001, 2002) invaded the area. Total amphipod abundance was higher before round goby invasion in
both habitats. In mussel beds, E. ischnus abundance was similar or significantly higher than G. fasciatus.
In macrophytes, G. fasciatus was significantly more abundant than E. ischnus. In laboratory experiments,
we compared amphipod survivorship and growth when fed mussel feces and pseudofeces (F+P) or macrophytes with epiphytes (M+E). Gammarus fasciatus survivorship and growth were higher when fed F+P
than M+E. Echinogammarus ischnus showed similar survivorship under both diets, but significantly higher
growth when fed M+E than F+P. Therefore inter-habitat differences in food resources cannot explain the
abundance patterns observed in the lake. We also estimated the relative vulnerability of G. fasciatus and E.
ischnus to yellow perch (Perca flavescens) and round goby (Neogobius melanostomus) predation in laboratory feeding trials using mussel colonies or macrophyte beds as substrate. Both fish strongly preferred E.
ischnus in macrophytes, but consumed relatively more G. fasciatus than E. ischnus in dreissenid habitats.
Our results suggest that dreissenid establishment may have facilitated the invasion of E. ischnus. However,
habitat-specific differences in vulnerability to fish predation may mediate the coexistence of G. fasciatus
and E. ischnus by minimizing expansion of E. ischnus to macrophyte areas. Our results also suggest that
round goby invasion can alter amphipod abundance patterns in Lake Erie.
INDEX WORDS:
tence.
Amphipods, Dreissena spp., macrophytes, round goby, yellow perch, species coexis-
INTRODUCTION
The success of biological invasions depends upon
physical and biotic conditions in the target community (Elton 1958, Simberloff 1986). However, once
an exotic species is established, it can modify abiotic and biotic conditions and facilitate the colonization success of future invaders (Aplet 1990).
Introduced species can increase resource availability (Vitousek et al. 1987, Vitousek and Walker
1989), which can facilitate invasibility by other exotic species (Vitousek 1990, Aplet 1990). Furthermore, if invaders can increase resource
heterogeneity they may increase the number of
species that can coexist (MacArthur et al. 1972,
Huston 1994). The success of an invader, however,
may be constrained by predation risk (Robinson
and Wellborn 1988). Predators can often decrease
success of invaders by selectively consuming an exotic prey (Orians 1986). Conversely, predators can
also enhance invasibility by selectively consuming
a competitively superior native prey, therefore reducing interspecific competition and allowing coexistence of competitors (Lodge 1993).
Habitat heterogeneity can be an important factor
mediating predator-prey interactions among native
and exotic species (Crowder and Cooper 1982).
Differences in refuge availability among habitats
can mediate interspecific competition and lead to
differences in the distribution of potential competitor species (Sih 1987, Duffy and Hay 1991). Predator-prey interactions also are dependent on
differences in prey vulnerability to predation, which
*Corresponding
author. E-mail: [email protected]
address: Utah State University, Department of Fisheries and
Wildlife, Logan UT 84322.
1Current
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Amphipod Abundance Patterns in Macrophyte and Dreissenid Habitats
are determined by the size, coloration and behavior
of prey in relation to the habitat (see Heck and
Crowder 1991 for a review).
The Great Lakes have been drastically affected
by exotic species. The remarkable abundance of the
exotic zebra (Dreissena polymorpha) and quagga
(Dreissena bugensis) mussels have greatly modified
littoral habitats and energy flow in the Great Lakes.
Habitat complexity is greater in Dreissena clusters
compared to bare rocks (González and Downing
1999). Dreissenids filter seston from the water column and subsequently deposit feces and pseudofeces (seston that is filtered, coated with mucous,
then ejected without being ingested) at the lake bottom. Their high filtering capacity has led to increased water clarity (Leach 1992, Budd et al.
2001) and increased light penetration has led to an
increase in near-shore macrophytes abundance
(Stuckey and Moore 1995, Skubinna et al. 1995)
and periphyton (Lowe and Pillsbury 1995). Thus,
the dreissenid invasion has diversified littoral habitats due to increased habitat complexity in mussel
colonies and increased macrophytes abundance.
Mussel colonies and macrophytes may provide
macroinvertebrates with different food resources
and refuge from predation.
The effects of dreissenid invasion on macroinvertebrates on rocky substrates have been extensively
studied in the last decade, while the role of increased macrophytes resulting from the dreissenid
invasion is not well understood. Benthic invertebrate abundance on rocky substrates increased dramatically following the dreissenid invasion
(Dermott et al. 1992, Stewart and Haynes 1994). In
particular Gammarus fasciatus, a widely distributed
amphipod species in North America (Clemens
1950), became one of the most abundant macroinvertebrates associated with dreissenid colonies
(Dermott et al. 1992, Stewart and Haynes 1994,
Ricciardi et al. 1997). Higher amphipod abundance
on mussels is related to increased habitat complexity (Ricciardi et al. 1997, Stewart et al. 1998,
González and Downing 1999). Macrophytes also increased the littoral habitat complexity and are utilized by benthic invertebrates (Gilinsky 1984).
Information about amphipod populations in macrophytes in the Great Lakes is scarce, although amphipods can utilize such habitat (Clemens 1950,
Dermott et al. 1998, Kashian and Burton 2000).
Recently two species from the Ponto-Caspian region have invaded the Great Lakes: the amphipod,
Echinogammarus ischnus (Witt et al. 1997) and a
fish, the round goby, Neogobius melanostomus
101
(Jude et al. 1992). Echinogammarus ischnus, commonly associated with dreissenid colonies (Köhn
and Waterstraat 1990), invaded Lake Erie in 1994
(Witt et al. 1997). Dermott et al. (1998) documented a higher abundance of E. ischnus than G.
fasciatus on mussel colonies in several areas in the
Great Lakes and suggested that E. ischnus had displaced G. fasciatus from mussel colonies.
Echinogammarus ischnus, however, was scarce in
macrophyte beds in Lake St. Clair and Lake Ontario (Witt et al. 1997, Dermott et al. 1998). In Lake
Michigan, E. ischnus was abundant in sites with
dreissenid colonies but was not present in sites with
submerged vegetation (Nalepa et al. 2001). Round
goby, a benthivorous fish species associated with
riprap, vegetated areas and dreissenid colonies
(Jude and DeBoe 1996), invaded Lake Erie in 1996
(Charlebois et al. 1997). Round gobies can feed on
soft benthic invertebrates, including amphipods, but
also prey on dreissenids (Charlebois et al. 1997,
Ghedotti et al. 1995, Jude et al. 1995).
These two exotic species are likely to interact
with G. fasciatus and native fish species such as
yellow perch (Perca flavescens). Yellow perch is an
important component of the commercial and sport
fisheries in the Great Lakes, especially Lake Erie
and Lake Michigan (Francis et al. 1995). Perch undergo three ontogenetic niche shifts (Wu and Culver 1991). Larval perch are pelagic and feed
predominantly on zooplankton. Juveniles (30–200
mm) shift to become more littoral in their habitat
and feed mainly macroinvertebrates. Perch spend
several years at this feeding stage until they are
large enough to become piscivorous (Hayes and
Taylor 1990). In Lake Erie and Lake Michigan,
benthic invertebrates such as amphipods are a
major component of juvenile yellow perch diet, particularly after Dreissena spp. invasion (Robillard et
al. 1999, Tyson and Knight, 2001). Yellow perch
also consume Dreissena spp. (Morrison et al.
1997).
Food resources vary between mussel colonies
and macrophytes beds. Biodeposition of organic
matter, mainly in the form of feces and pseudofeces, is higher in the presence than in the absence of
mussels (Klerks et al. 1996, Stewart et al. 1998).
Feces and pseudofeces are consumed by amphipods
(Fisher et al. 1992), although the implications for
amphipod fitness are not well understood. Amphipods can also consume macrophytes and associated epiphytes (Clemens 1950, Newman 1991,
Delong et al. 1993). Therefore, dreissenid establishment may facilitate the invasion of E. ischnus by
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González and Burkart
providing increased food resources. In addition differences in food resources between dreissenid and
macrophyte dominated habitats may determine spatial distributions of E. ischnus and G. fasciatus.
Differences between the type of refuge from fish
predation provided by mussel and macrophytes may
also mediate the distribution of native and exotic
amphipods, although the value of the refuge provided by each habitat may depend on predator
species. Similar benthic invertebrate biomass was
observed in experimental ponds colonized by zebra
mussels, with and without yellow perch (Thayer et
al. 1997). Kuhns and Berg (1999) reported higher
total invertebrate densities in colonization cages
with zebra mussel colonies when round gobies were
excluded. Therefore, yellow perch and round goby
have the potential to affect amphipod abundance
patterns.
Here we document differences in the distribution
of G. fasciatus and E. ischnus in mussel colonies
and macrophytes before and after the invasion of
round goby. We also analyze how habitat differences in food resources (dreissenid egestion products vs. macrophytes and epiphytes) and predation
by native yellow perch and the exotic round goby
may influence abundance patterns of these amphipod species.
METHODS
Amphipod Abundance Patterns
We estimated the abundance of G. fasciatus and
E. ischnus in mussel colonies and macrophyte beds
during late summer in 1996, 2001, and 2002. In
1996, sample sites were chosen at random within
habitats dominated by dreissenids (100–80% dreissenid; 0 –20% macrophytes) or macrophytes
(100–80% macrophytes; 0–20% dreissenids) in
Hatchery Bay (Peach Point and Gibraltar Island).
We collected three samples from each habitat type
(Dreissena spp. and macrophytes). In each habitat,
a bucket (30-cm diameter) with a 90-µm sieve attached to the bottom was placed upside-down and
buried 2 cm into the substrate. A thin metal sheet,
attached to the bucket using bungee cords, was slid
between the bucket and the substrate, and the
bucket was carefully lifted from the sediment and
placed into a pillowcase. Pillowcases were transported to the laboratory inside coolers in less than 2
hours. Substrates were agitated in a bucket with
lake water for at least 25 min to remove amphipods.
Amphipods samples were preserved with a 10%
formalin solution and identified to species using a
dissecting microscope.
In 2001 and 2002 (after round goby establishment), amphipod densities were considerably lower
than in 1996 and we modified our sampling
methodology. A 1 m2 quadrat was randomly placed
on the substrate and four samples from each quadrat
were taken using the bucket sieve method described
above. Samples from each quadrat were pooled. In
2001, we only collected samples from six randomly
placed quadrats in areas dominated by dreissenids
(100% dreissenids). In 2002, we collected samples
from 14 quadrats chosen at random along two 50-m
transects (Peach Point and near Perry’s Monument,
seven quadrats in each transect). However one
quadrat sample from Perry’s Monument was not included in the analysis because no amphipods were
present in the sample. The habitat composition (%
dreissenids and % macrophytes) in the quadrats was
more variable in 2002, so samples were categorized
into three groups according to mussel cover
(100–70%, n = 3; <70–30%, n = 4; and < 30–0%,
n = 6). Macrophytes occupied substrate without
dreissenids, except in one quadrat, where the macrophyte cover was 30% and the remaining 70% was
bare rock. In both surveys, amphipods were removed from the substrate similarly to 1996, but amphipods were identified and counted immediately
without preservation.
The percentage of juvenile amphipods that could
not be identified was high only in 2001, so we did
not include these individuals in our statistical
analysis. In 1996 and 2002, we tested for differences in amphipod abundance among habitats using
fixed-effects multivariate analysis of variance
(MANOVA: treating the abundance of the two amphipod species as dependent variables, SAS Institute 1990). Since significant treatment effects were
detected in the MANOVA, we performed interhabitat comparisons (mussel vs. macrophytes) for
each species and inter-species comparisons (G. fasciatus vs. E. ischnus) within each habitat using ttests. In 2001, we performed inter-specific
comparisons in dreissenid dominated habitat using
a Hotelling t-test. All data were log-transformed to
meet assumptions of variance homogeneity (Sokal
and Rohlf 1988).
Effect of Diet on Amphipod
Survivorship and Growth
We determined the effect of diet on survivorship
and growth of G. fasciatus and E. ischnus by rear-
Amphipod Abundance Patterns in Macrophyte and Dreissenid Habitats
ing each species on two different foods for eight
weeks. Individuals of both amphipod species were
collected from both mussel colonies and macrophytes in Hatchery Bay during late June, 1997. Amphipods were transported to the laboratory,
identified as G. fasciatus or E. ischnus, and placed
into two separated aerated tanks containing both
mussel egestion products and macrophytes. Therefore we used amphipods from both habitats in the
experiment. After 24 hours, ovigerous females of
each species were placed in individual cups of lake
water. As the F 1 generation hatched, the mother
was removed and the new generation was acclimated and fed 5-cm-long macrophyte pieces (Vallisneria americana) for 5 days. We used
macrophytes instead of mussel egestion products as
a food source during acclimation because in preliminary experiments recently hatched amphipods incubated clung to macrophytes. This facilitated
finding and transferring amphipods with minimum
handling because there was no detritus accumulation in the bottom of the cups in comparison to cups
with egestion products.
After 5 days of acclimation amphipods were
raised on one of two diets: mussel feces and pseudofeces (F+P) or macrophytes (V. americana) with
epiphytes (M+E). Vallisneria americana was used
in the M+E treatment because it was the dominant
macrophyte in Hatchery Bay (Stuckey and Moore
1995). To ensure that no other food source was present, we filtered lake water used in the experiment
through a 1-µm glassfiber filter before adding it to
each cup. We also raised amphipods in filtered lake
water (no food treatment) to assess the effect of
food deprivation on amphipod survivorship and
growth.
In preliminary observations using several amphipods per cup dead organisms were consumed by
live amphipods within a few hours. Therefore we
used one amphipod per cup for our experiments.
Each amphipod was placed in a 300-mL plastic cup
containing 250 mL of filtered lake water and a
1 × 1-cm piece of plastic netting as a substrate.
Cups were randomly arranged in six rows, with 27
cups per row. We added 2 mL of a concentrated
mixture of feces and pseudofeces or a 15-mm
macrophyte segment to each replicate. Feces and
pseudofeces for the experiment were collected in a
funnel trap placed underneath suspended mussels in
a flow-through tank containing Lake Erie water.
Fresh macrophytes were collected from the Hatchery Bay on each feeding day. Macrophytes were
rinsed gently with filtered lake water to remove at-
103
tached macroinvertebrates without disturbing epiphytes. Food and water were changed weekly. Food
was always present in the cups, indicating that amphipods did not starve. Once a week, dissolved oxygen was measured in a randomly chosen sample of
each treatment. Dissolved oxygen never dropped
below 6.6 mg/L during the entire experiment. Temperature during the experiment was 22.5–23.5°C
Each treatment for G. fasciatus had 33 replicates.
Replicate numbers for E. ischnus treatments were
lower because we obtained fewer offspring from
ovigerous E. ischnus than from G. fasciatus. The
F+P, M+E and no food treatments for E. ischnus
had 24, 19, and 20 replicates respectively. Number
of amphipods in E. ischnus treatments was chosen
based on preliminary data that suggested amphipod
growth was more variable in F+P treatments than in
M+E and no food treatments.
Amphipod survivorship was measured weekly.
Following the recommendations of Pyke and
Thompson (1986), survivorship was analyzed using a
non-parametric test for estimating survival distributions when not all individuals under treatment conditions are followed until death (LIFETEST procedure,
SAS Institute 1990). We performed intraspecific
comparisons among food treatments (M+E vs. F+P)
and interspecific comparisons (G. fasciatus vs. E. ischnus) within each food treatment.
To quantify growth, we measured head length
weekly by gently pouring an individual onto a 100
µm sieve and measuring from the rostrum tip to the
posterior margin of the head using a microscope
with an ocular micrometer. Following measurement, the amphipod was placed in a clean cup containing filtered lake water and fresh food. The
measurement of head length instead of body length
minimized the time that amphipods were under the
microscope. Previous studies have shown a positive
correlation between amphipod head length and total
body length (Cooper 1965, Delong et al. 1993,
Morrison et al. 1997). To verify this relationship we
collected amphipods from Lake Erie and regressed
total body length (TL) against head length (HL) for
both amphipods. The results of the statistical analysis were similar using either head length or body
length estimates. Here we present the results from
the analysis using head length.
We calculated weekly growth (head length(week n)
– head length(week n–1)) for each treatment using amphipods that survived to the end of each week. We
tested for intraspecific differences in growth among
treatments using a repeated measures ANOVA
(SAS Institute 1990). We tested for differences only
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González and Burkart
between the F+P and M+E because after the first
week there were not enough survivors in the nofood treatment to satisfy ANOVA assumptions.
We evaluated interspecific differences in mean
growth using a two-way ANOVA to test for diet
(F+P vs. M+E) and species (G. fasciatus vs. E. ischnus) effects. Because we detected a strong
species*diet interaction (see results) we compared
treatment means using a Tukey-Kramer test (Sokal
and Rohlf 1988). All data were log-transformed to
meet assumptions of variance homogeneity (Sokal
and Rohlf 1988).
Fish Predation Experiments
We conducted laboratory experiments to estimate
the relative vulnerability of G. fasciatus and E. ischnus to predation by yellow perch and round goby
in two simulated habitats, mussel colonies and
macrophyte beds.
Experiments were conducted in 80-L aerated
aquaria containing either cobbles with dreissenid
colonies or macrophytes in a 0.0625 m 2 area.
Macrophyte habitats consisted of 17 shoots of V.
americana (shoot density, 272 shoots/m2) cut to the
height of the aquarium (30 cm) and weighted down
by metal nuts. Mussel habitats consisted of three
pieces of cobble (cobble density, 48/m2) colonized
by mussels (mean # mussels/m2 = 1,203 ± 44SD).
Mean # of mussels/tank was never significantly different among tanks (p > 0.9). Shoot and mussel
densities used in the trials were within the range observed in the lake during early August (215–312
shoots/m2, 906–2,172 mussels/m2). Aquarium walls
were covered with black plastic material to minimize disturbance of fish and to ensure that fish
were not influenced by activity in neighboring
tanks. Laboratory temperature during the fish experiments was 23–24°C .
Yellow perch and round goby were collected in
Hatchery Bay by seining or cast netting. Fish were
acclimated in the laboratory for two weeks during
which they were fed both amphipod species. Fish
were starved for 48 hours prior to an experiment. In
all experiments we removed the fish after 24 hours,
and the remaining amphipods were counted by
species. Fish were measured and weighed at the end
of each experiment.
Yellow Perch Experiments
We estimated yellow perch predation rates in August 1997 and June 2001. In both experiments we
added 100 G. fasciatus and 100 E. ischnus to each
aquarium and allowed them to acclimate for 12
hours. We then added three fish to each aquarium.
In 1997 there were three replicates per habitat,
while in 2001 there were four replicates per habitat.
A two-way ANOVA (date and habitat effects) indicated significant differences in total fish length and
biomass between dates. Because consumption rates
can depend on fish size (Kitchell et al. 1977), we
analyzed each experiment independently.
Round Goby Experiments
We estimated round goby predation rates in August 2000 and 2001. We had difficulty collecting E.
ischnus during summer 2000, therefore we only
added 65 G. fasciatus and 65 E. ischnus to each
aquarium. We added only two fish per tank due to
the lower amphipod number. Fish mortality in two
tanks (one dreissenid and one macrophyte habitat)
reduced the number of replicates in both treatments
to only two. In 2001 there were four replicates per
habitat. Similar to the yellow perch experiments,
we added 100 G. fasciatus and 100 E. ischnus and
three round gobies to each tank. A two-way
ANOVA detected significant differences in fish biomass/tank between dates. Due to the differences in
fish biomass and amphipod density we decided to
analyze each experiment independently.
In all experiments, fish consumption rates (total
number of amphipods consumed/g fish biomass/
day) and the ratio of the number of G. fasciatus and
E. ischnus consumed (G:E) were analyzed using ttests (SAS Institute 1990) to assess differences in
fish predation between mussel and macrophyte
habitats. Data were log-transformed to meet assumptions of variance homogeneity (Sokal and
Rohlf 1988). We also tested if the Gammarus:
Echinogammarus ratio consumed in each habitat
was different from one using a two-tailed t-test. Ratios > 1 indicated a higher vulnerability of G. fasciatus to fish predation, while ratios < 1 indicated a
higher vulnerability of E. ischnus to fish predation.
RESULTS
Amphipod Abundance Patterns
In 1996, we detected significant differences in
amphipod abundance patterns between habitats
(Wilk’s lambda value = 0.148, F 1,4 = 22.94, p =
0.009). Inter-habitat comparisons showed that G.
fasciatus abundance was significantly higher in
macrophytes than in dreissenid colonies (Fig. 1a,
Amphipod Abundance Patterns in Macrophyte and Dreissenid Habitats
105
abundance tended to be slightly higher than G. fasciatus, although this trend was not statistically significant (t0.05,4 = 1.73, p = 0.15).
In 2001 and 2002, total amphipod abundance was
ten-fold lower than in 1996. Echinogammarus ischnus abundance was significantly higher than G.
fasciatus abundance in dreissenid colonies in 2001
(Fig. 1b; Hotelling-Law value = 172.5, F2,3 = 258.8,
p = 0.0004).
In 2002, we also detected significant differences
in amphipod abundance patterns between habitats
(Wilk’s lambda value = 0.153, F 2,10 = 27.6, p <
0.001). Inter-habitat abundance patterns differed
from those found in 1996. Gammarus fasciatus
abundance was similar among habitats (F 2,10 =
4.74, p = 0.09), while E. ischnus abundance was
significantly higher in dreissenid dominated habitat
(100 –70%) than in habitats with < 70% dreissenid
cover (Fig. 1.c, F 2,10 = 77.75, p < 0.001). As in
1996, inter-species comparisons showed that G. fasciatus was significantly more abundant than E. ischnus in habitats with a < 70% dreissenid cover
(F1,6 = 8.36, p = 0.03 in < 70–30% and F1,10 = 230,
p < 0.0001 in 0 – < 30%). Echinogmmarus ischnus
abundance also tended to be higher in dreissenid
dominated habitat, but the trend was not statistically significant (F1,4 = 6.07, p = 0.06).
FIG. 1. Mean abundance (± 1 SE) of G. fasciatus and E. ischnus in dreissenid colonies and
macrophyte beds in (a) 1996, (b) 2001, and (c)
2002. In 2001 samples were only collected in
dreissenid colonies. Error bars that are not apparent are smaller than the symbols.
t0.05,4 = 4.92, p = 0.008), while E. ischnus abundance was similar in both habitats (Fig. 1a, t0.05,4 =
0.12, p = 0.70). Inter-species comparisons revealed
that G. fasciatus was nearly 2.5 times more abundant than E. ischnus (t 0.05,4 = 3.94, p = 0.02) in
macrophyte beds. In dreissenid colonies, E. ischnus
Effect of Diet on Amphipod
Survivorship and Growth
Survivorship of both amphipod species was significantly lower in the no food treatment than in the
food treatments (G. fasciatus: X2(1, 0.05) = 19.7 for
F+P and 34.2 for M+E; E. ischnus: X2(1,0.05) = 23.3
for F+P and 19.02 for M+E; p = 0.0001; Fig. 2).
Survivorship of G. fasciatus fed F+P was significantly higher than those fed M+E (X2(1, 0.05) = 5.5;
p = 0.02; Fig. 2a), but E. ischnus showed similar
survivorship when fed either F+P or M+E (X2(1,
0.05) = 0.18; p = 0.6; Fig. 2b)
Interspecific comparisons showed that E. ischnus
survivorship was significantly higher than G. fasciatus survivorship when fed M+E (X 2 (1, 0.05) =
5.80; p = 0.02; Fig. 2). However, there were no significant differences between the two species when
raised on F+P (X2 (1, 0.05) = 0.09; p = 0.8; Fig. 2).
We found a strong correlation between total body
length and head length for G. fasciatus (TL (mm) =
10.768 (HL) – 1.460; r2 = 0.91 n = 64) and E. ischnus (TL (mm) = 9.554 (HL) - 0.871; r2 = 0.86 n =
123). Both amphipod species showed an increase in
mean body length over the eight-week period (Fig.
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González and Burkart
FIG. 2. Weekly survivorship of (a) G. fasciatus
and (b) E. ischnus in the feces and pseudofeces
(F+P), macrophytes (M+E) and no food (NF)
treatments over an 8-week period.
3). Intraspecific comparisons detected significant
date effects for both species (F8,296 = 115.2 for G.
Gammarus and F8,296 = 58.56 for E. ischnus; p <
0.0001) and a significant diet effect only for G. fasciatus (F1,395 = 27.2, p < 0.001). However the date
*diet interactions were significant for both species
(F8,395 = 2.64, p < 0.02 for G. fasciatus and F8,296 =
5.46, p < 0.0001 for E. ischnus), mainly because
differences in growth between treatments varied
with time. In 5 out of 8 weeks, G. fasciatus grew
more when fed F+P than when fed M+E, while in
the other 3 weeks growth was similar on both diets
(Fig. 3a). Echinogammarus ischnus grew more
when fed M+E than when fed F+E only during the
last 2 weeks of the experiments (Fig. 3b).
Interspecific comparisons of mean growth at the
end of the experiment showed significant species
effects (F1,65 = 171.6, p < 0.0001), but a species*
diet interaction (F1,65 = 25.5, p < 0.0001). Gammarus fasciatus grew more when fed F+P than
when fed M+E, whereas E. ischnus showed the opposite pattern (Fig. 4).
FIG. 3. Weekly mean body length (± 1 SE) of (a)
G. fasciatus and (b) E. ischnus in the feces and
pseudofeces (F+P), macrophytes (M+E), and no
food (NF) treatments over an 8-week period. Error
bars that are not apparent are smaller than the
symbols.
FIG. 4. Mean growth (± 1 SE) of (a) G. fasciatus and (b) E. ischnus fed feces and pseudofeces
(F+P) or macrophytes (M+E). Letters indicate that
growth was different at a 0.05 significance level
(Tukey-Kramer).
Amphipod Abundance Patterns in Macrophyte and Dreissenid Habitats
Fish Predation Experiments
Yellow Perch Experiments
Yellow perch consumption rate was higher in the
1997 than in the 2001 experiments, probably because yellow perch individuals were smaller in
1997 than in 2001. We observed significant differences in total fish length (6.6 cm ± 0.1 TL in 1997
and 14.0 cm ± 0.2 in 2001; F 1,10 = 329.7, p <
0.0001) and biomass (14 g ± 0.4 in 1997 and 87g ±
4.2 in 2001; F 1,10 = 856.7, p < 0.0001) between
dates. However no significant habitat effects or
date*habitat interactions were observed in total fish
length and fish biomass/tank.
In both experiments, yellow perch consumption
rates were similar between habitat treatments (Fig.
5a and b). However, G:E ratios were significantly
lower in the macrophyte than in the mussel treatments (t0.05,4 = 8.63, p = 0.04 in 1997; t0.05,6 = 2.94,
p = 0.03 in 2001; Fig. 5c and d). G:E ratios were
107
significantly less than 1 in macrophyte treatments
indicating a higher vulnerability of E. ischnus to
yellow perch predation in this habitat (t 0.05,2 =
18.58, p = 0.001 in 1997; t0.05,3 = 4.57, p = 0.01 in
2001). In mussel treatments the G:E ratios were not
significantly different than 1, indicating similar vulnerability of G. fasciatus and E. ischnus to yellow
perch predation.
Round Goby Experiments
No significant differences in size (9.7 cm ± 0.2
TL in 2000 and 9.8 cm ± 0.2 in 2001) were detected
between dates. However, the fish biomass/tank was
significantly lower in 2000 that in 2001 (27.1 g ±
0.2 in 2000 and 38.6 g ± 0.5 in 2001, F1,8 = 58.1, p
< 0.001). No significant habitat effects or
date*habitat interactions were observed in total fish
length and fish biomass/tank.
Round goby consumption rates were significantly
FIG. 5. (a,b) Mean consumption rates (amphipod/g/d ± 1 SE) and (c, d) mean consumed G. fasciatus:E.
ischnus ratios in mussel and macrophyte habitats after three yellow perch were allowed to feed for 24
hours. Error bars that are not apparent are smaller than the symbols.
108
González and Burkart
FIG. 6. (a, b) Mean consumption rates (amphipod/g/d ± 1 SE) and (c, d) mean consumed G. fasciatus:E.
ischnus ratios in mussel and macrophyte habitats after 2 (2000) –3 (2001) round gobies were allowed to
feed for 24 hours. Error bars that are not apparent are smaller than the symbols.
higher in macrophyte treatments than in mussel
treatments in both experiments (t0.05,2 = 7.18, p =
0.02 in 2000; t0.05,6 = 4.34, p = 0.005 in 2001, Fig.
6a and b). The G:E ratio was significantly lower in
the macrophyte treatment than in the mussel treatment only in 2001 (t0.05,6 = 2.87, p = 0.02, Fig. 6c
and d). In macrophyte treatments the G:E ratio was
significantly less than 1 only in 2001 (t0.05,3 = 7.47,
p = 0.002), indicating a higher vulnerability of E.
ischnus to round goby predation. In mussel treatments, the G:E ratios were not significantly different from 1 indicating similar vulnerability of G.
fasciatus and E. ischnus to round goby predation in
this habitat.
DISCUSSION
Our survey results showed inter-habitat differences in the abundance of both amphipod species.
Gammarus fasciatus abundance was consistently
higher in macrophytes than in dreissenid colonies,
while E. ischnus abundance tended to be higher in
dreissenid colonies. Previous studies have also reported higher abundance of E. ischnus in mussel
colonies than in vegetation dominated areas (Witt et
al. 1997, Dermott et al. 1998, Nalepa et al. 2001).
Our results support previous work that suggests
that the exotic E. ischnus may be displacing G. fasciatus on rocky substrate areas in the Great LakesSt. Lawrence system (Dermott et al. 1998). An
earlier study suggested that G. fasciatus was
equally abundant in macrophyte beds and rocky
substrates (Clemens 1950) in Hatchery Bay before
the invasion of Dreissena sp. and E. ischnus. Prior
to the invasion of E. ischnus, G. fasciatus was the
dominant amphipod in mussel colonies, in terms of
numbers and biomass, in Lake Erie including
Hatchery Bay (Dermott et al. 1992, Dermott et al.
1998). However, the higher abundance of G. fasciatus in macrophyte beds suggests that the presence
Amphipod Abundance Patterns in Macrophyte and Dreissenid Habitats
of macrophytes may allow G. fasciatus to coexist
with the exotic species.
The drastic decrease in amphipods between 1996
and 2000-2001 cannot be attributed to differences
in methodology because a similar decrease was observed in the average number of amphipods colonizing experimental cages placed in dreissenid
colonies in 2001 (92 ± 15 (SE) individuals/cage;
González unpublished) compared to 1995–1996
(1630 ± 275 (SE) individuals/cage; González and
Downing 1999). The drastic decrease in the total
number of amphipods in both habitats may be related to the invasion of round goby in the study area
during 1998. Our experimental cages in those experiments excluded predators. However, regular observations by SCUBA divers observed no round
gobies located around the cages in 1995 and 1996,
while the average number of round gobies located
around the cages was 4.45 + 0.9(SE)/cage in 2001
(González unpublished). Kuhns and Berg (1999) reported lower benthic invertebrate abundance in colonization cages where round gobies was allowed to
feed compared to cages excluding round gobies.
Food (Klerks et al. 1996, Stewart et al. 1998) and
shelter (Ricciardi et al. 1997, González and Downing 1999) for benthic invertebrates have increased
since the invasion of Dreissena sp. Although many
researchers have speculated about the potential importance of feces and pseudofeces in the diet of
benthic invertebrates (Klerks et al. 1996, Griffiths
1992, Fisher et al. 1992), ours is the first study to
document the effects of this food on amphipod survivorship and growth. The higher survivorship and
growth of G. fasciatus when fed dreissenid egestion
products provide evidence that the drastic increase
of this amphipod after the Dreissena sp. invasion
was related to increased in food availability in addition to increased habitat complexity.
Our survivorship and growth experiments, however, suggest that differences in the relative abundance of G. fasciatus and E. ischnus cannot be
explained by differences in food quality associated
with each habitat. Based on our intraspecific and interspecific comparisons we would expect the relative abundance of G. fasciatus to be higher in
mussel colonies than in macrophyte beds, because
growth and survivorship of G. fasciatus was significantly greater when fed F+P than when fed M+E.
Although survivorship of both amphipods was similar under F+P diet, G. fasciatus net growth was
higher than E. ischnus. Results for E. ischnus are
more complex. Based on the intraspecific comparisons we would expect similar E. ischnus abun-
109
dance in both habitats. The growth and survivorship
of E. ischnus was similar when fed F+P or M+E.
Our interspecific comparison, however, suggest that
E. ischnus exhibited greater survivorship and
growth than G. fasciatus under M+E diet.
Predation risk is an important factor constraining
the spatial distribution of marine and freshwater organisms (Werner et al. 1983, Duffy and Hay 1991,
González and Tessier 1997). Our results suggest
that differential vulnerability to fish predation between habitats may explain differences in relative
abundance of G. fasciatus and E. ischnus in mussel
colonies and macrophyte beds. The lower relative
abundance of E. ischnus in macrophytes may be
caused by higher vulnerability of this amphipod to
fish predation in this habitat. The G:E ratios were
significantly lower in macrophyte than mussel habitats in three out of four experiments (Figs. 5 and 6)
indicating fish preference for E. ischnus in this
habitat. Also G:E ratios were significantly < 1 in
the same three experiments indicating higher vulnerability of E. ischnus to fish predation than G.
fasciatus. In the mussel habitat fish tended to consume more G. fasciatus than E. ischnus, but G:E ratios were never significantly > 1 indicating similar
vulnerability of the two amphipod species to fish
predation in this habitat. The lack of statistically
significant results in the 2000 round goby experiment was probably related to low statistical power
due to the loss of some replicates. However it is important emphasize that G:E ratio tend to be lower in
macrophyte than mussel habitats, as in the other
three experiments.
The similar trends in consumption patterns between yellow perch and round goby suggest that
predator preferences were related to prey-specific
characteristics mediated by habitat. Differences in
coloration, size, and behavior between G. fasciatus
and E. ischnus may lead to variability in their susceptibility to fish predators between habitats. In
macrophytes the light greenish-gray color and
clinging behavior (“C-shaped posture”) of G. fasciatus (Clemens 1950) may be better camouflage,
whereas the relatively dark reddish color and more
active behavior of E. ischnus (Burkart 1999) may
make it more visible to predators in macrophyte
beds. Active swimming behavior has been documented in E. ischnus (reviewed by Nalepa et al.
2001). Behavioral differences (movement) among
Crangonyx pseudogracilis, G. duebebeni, and G.
pulex was an important factor determining the feeding preference of brown trout on these three amphipod species (MacNeil et al. 1999). Crangonyx
110
González and Burkart
pseudogracilis was preferentially consumed by
brown trout. The most common escape response exhibited by C. pseudogracilis was to swim away,
while both Gammarus species usually adopted a
“C-shaped posture” that make handling by trout difficult.
The lower overall amphipod consumption in
mussel colonies in both round goby experiments
may be related to mussel consumption by round
goby. Stomach content analyses have showed that
round gobies > 7 cm TL rely more on dreissenids,
compared to round gobies < 7 cm TL (Jude et al.
1995, Ray and Corkum 1997, French and Jude
2001). The mean size of round goby in our experiments was 9.8 cm and we observed fragments of
mussel shell in several tanks after the feeding trials.
The similarity in prey preference exhibited by
both fish species, and the drastic decrease in benthic invertebrates after round goby invasion, suggest potential competition between round goby and
yellow perch. Under intense competition for resources during the benthivorous feeding stage,
round goby can create a bottleneck in yellow perch
growth and delay the ontogenetic shift of perch to
piscivory (Olson 1996, Heath and Roff 1996).
Hence yellow perch may be vulnerable to predation
by piscivores for a longer period of time, and high
predator-induced mortality on young yellow perch
may cause poor recruitment (Hartman and Magraf
1993). However, competition may depend on fish
size. In our experiments small yellow perch (6.6 cm
TL) show overall higher consumption rates than
round gobies (9.8 cm TL), while larger yellow
perch (14 cm TL) consumption was considerably
lower than round goby. Studies investigating competition between yellow perch and round goby
should consider size structure of populations.
Intraguild predation has been identified as an important factor determining the establishment of exotic amphipods in streams in Ireland and England
(Dick et al. 1993, 1999). Intraguild predation between G. fasciatus and E. ischnus has recently been
evaluated under laboratory conditions (Kozac
2001). Gammarus fasciatus prey more often on E.
ischnus than vice versa, regardless of whether amphipods are fed M+E or F+P. Based on these findings we would expect G. fasciatus to be the
dominant amphipod in both habitats. Fish predation
may mediate the importance of intraguild predation
on E. ischnus populations differently in mussel and
macrophyte habitats. In mussel colonies higher fish
predation on G. fasciatus may release E. ischnus
from intraguild predation and competition by G.
fasciatus. In macrophyte beds a strong vulnerability
to fish predation and intraguild predation may limit
the abundance of E. ischnus. Future studies should
focus on how fish and intraguild predation mediate
amphipod population distributions in mussel
colonies and macrophyte beds.
In summary, we found differences in the relative
abundance of G. fasciatus and E. ischnus between
mussel and macrophyte beds. Amphipod species
were differentially affected by food resources and
fish predation pressure associated with mussel
colonies and macrophyte beds. However, habitatspecific differences in amphipod relative abundance
seem to be related to differential vulnerability to
fish predation between amphipod species rather
than differences in food availability between habitats. Our results suggest that diversification of the
benthic habitat caused by dreissenid invasion (establisment of mussel colonies and proliferation of
macrophytes) as well as habitat-specific differences
in vulnerability to fish predation seem to mediate
the coexistence of G. fasciatus and E. ischnus in
Lake Erie by allowing the displacement of G. fasciatus by E. ischnus in mussel colonies and minimizing the expansion of E. ischnus into macrophyte
areas. This study also suggests that the establishment of round goby may expand the overall predation pressure on amphipod populations in
macrophytes and mussel colonies causing substantial changes in benthic invertebrates communities in
the Great Lakes. Furthermore, due to the dietary
overlap between round goby and yellow perch, the
drastic decreases in benthic invertebrate abundance
observed in this study after the round goby invasion
may cause a bottleneck effect on growth rate of
benthic yellow perch.
ACKNOWLEDGMENTS
We thank J. Hageman, M. Thomas, and the staff
of F. T. Stone Laboratory for their assistance with
several aspects of the project. We also thank J. Bebout, B. Burkart, E. Croissant, A. Downing, L.
Jeter, L. Knoll, K. Kozac, D. Lavoie, Z. Sutphin, M.
Thomas, and D. Vallance for their field and laboratory assistance. Comments by D. Berg, J. Stoeckel,
M. J. Vanni, and two anonymous reviewers greatly
improved the manuscript. This research was supported by grants from the National Sea Grant College Program, National Oceanic and Atmospheric
Administration, in the U. S. Department of Commerce (R/ER-23-40), Ohio Sea Grant (R/NIS-7),
and Ohio Board of Regents /Research Challenge
Amphipod Abundance Patterns in Macrophyte and Dreissenid Habitats
Grant to M.J.G. and Ohio Sea Grant Seed Funding
to M.J.G. and G.B.
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Submitted: 11 Mach 2003
Accepted: 7 November 2003
Editorial handling: Thomas F. Nalepa