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Marine Biology (2004) 144: 747–756
DOI 10.1007/s00227-003-1223-4
R ES E AR C H A RT I C L E
D. J. Ross Æ C. R. Johnson Æ C. L. Hewitt Æ G. M. Ruiz
Interaction and impacts of two introduced species
on a soft-sediment marine assemblage in SE Tasmania
Received: 6 November 2002 / Accepted: 11 September 2003 / Published online: 26 November 2003
Ó Springer-Verlag 2003
Abstract Introduced species are having major impacts in respective ranges expand, suggesting a strong overlap in
terrestrial, freshwater and marine ecosystems world- food resources will result from the shared proclivity for
wide. It is increasingly recognised that effects of multiple bivalve prey. A. amurensis and C. maenas provide good
species often cannot be predicted from the effect of each models to test the interaction between multiple intro-
species alone, due to complex interactions, but most duced predators, because they leave clear predator-spe-
investigations of invasion impacts have examined only cific traces of their predatory activity for a number of
one non-native species at a time and have not addressed common prey taxa (bivalves and gastropods). Our
the interactive effects of multiple species. We conducted experiments demonstrate that both predators had a
a field experiment to compare the individual and com- major effect on the abundance of bivalves, reducing
bined effects of two introduced marine predators, the populations of the commercial bivalves Fulvia tenuicos-
northern Pacific seastar Asterias amurensis and the tata and Katelysia rhytiphora. The interaction between
European green crab Carcinus maenas, on a soft-sedi- C. maenas and A. amurensis appears to be one of re-
ment invertebrate assemblage in Tasmania. Spatial source competition, resulting in partitioning of bivalves
overlap in the distribution of these invaders is just according to size between predators, with A. amurensis
beginning in Tasmania, and appears imminent as their consuming the large and C. maenas the small bivalves.
At a large spatial scale, we predict that the combined
effect on bivalves may be greater than that due to each
Communicated by M.S. Johnson, Crawley
predator alone simply because their combined distribu-
D. J. Ross (&) Æ C. R. Johnson tion is likely to cover a broader range of habitats. At a
School of Zoology and Tasmanian smaller scale, in the shallow subtidal, where spatial
Aquaculture and Fisheries Institute,
overlap is expected to be most extensive, our results
University of Tasmania,
indicate the individual effects of each predator are likely
7000 Sandy Bay, Tasmania,
to be modified in the presence of the other as densities
Australia
E-mail: rossdj@unimelb.edu.au increase. These results further highlight the need to
Fax: +1-3-83447909
consider the interactive effects of introduced species,
D. J. Ross Æ C. L. Hewitt especially with continued increases in the number of
Centre for Research on established invasions.
Introduced Marine Pests,
CSIRO Marine Research,
7001 Hobart, Tasmania,
Australia
G. M. Ruiz
Introduction
Smithsonian Environmental Research Center,
Edgewater, MD 21037, USA
Biological invasions, or the establishment of non-native
Present address: D. J. Ross
species outside their historic range, have become a major
Department of Zoology,
University of Melbourne, force of ecological change throughout the world. Al-
3010 Melbourne, Victoria,
though invasions have occurred for millions of years,
Australia
there has been a rapid increase in the rate of newly de-
Present address: C. L. Hewitt tected invasions over the last two centuries, driven by
Ministry of Fisheries,
human-aided movement across and between continents
PO Box 2526, Wellington,
and oceans (Carlton and Geller 1993; Vitousek 1994;
New Zealand
748
inevitable, and we predict the interaction between
Cohen and Carlton 1998; Hewitt et al. 1999; Ruiz et al.
A. amurensis and C. maenas will modify the effects
2000; Ruiz and Carlton 2003). The magnitude of eco-
resulting from each species individually.
logical effects by invasions has become increasingly
This seastar/crab/bivalve system is an excellent model
evident, resulting in fundamental changes to population,
to explore the interactive effects of multiple introduced
community and ecosystem processes (Cloern 1996;
species, because each predator leaves characteristic pat-
Vitousek et al. 1996; DÕAntonio et al. 1998; Wilcove
terns on shells of their bivalve prey. Predation by sea-
et al. 1998; Strayer 1999; Grosholz et al. 2000). Despite a
stars results in undamaged and empty shells, whereas
growing amount of literature on invasion effects, the
bivalves eaten by crabs are broken by this crushing
impacts of most invasions remain unstudied, and the
predator (i.e. usually hinges with only a fraction of the
interactive effects of multiple species have rarely been
shell remaining). Using this physical evidence of preda-
evaluated (Ruiz et al. 1999; Simberloff and von Holle
tor type, we tested the separate and combined impacts of
1999). The combined effects of several introduced spe-
A. amurensis and C. maenas on a soft-sediment assem-
cies may not be strictly additive, and can result in many
blage, focusing particular attention on bivalves. Because
complex interactions, including accelerated impacts on
there was little information on the distribution and
native communities (Simberloff and von Holle 1999).
abundance of native species prior to the establishment of
Indeed, modification of interactions, whereby the direct
A. amurensis and C. maenas, the study focuses on
interaction between two species is altered by the pres-
experimental manipulations of the two species in a rel-
ence of a third, is thought to be commonplace (Kareiva
atively unimpacted habitat at the interface of their cur-
1994).
rent ranges.
Hundreds of non-native marine species are now
established in the coastal waters of Australia, despite
the relative degree of geographic isolation (Pollard and
Hutchings 1990a, 1990b; Jones 1991; Furlani 1996;
Materials and methods
Hewitt et al. 1999). Among the most conspicuous
introductions are two large, predatory species found in
Collection and maintenance
sheltered, low-energy environments: the northern Pa-
cific seastar Asterias amurensis and the European green A manipulative experiment was undertaken in the sheltered upper
crab Carcinus maenas. The green crab is known to reaches of King George Sound, south-east Tasmania at a depth of
have significant effects on infaunal communities in 2–3 m (Fig. 1). Sediment in the area is composed predominantly of
sandy mud. The habitat type at this site is similar to that present in
many parts of the world (Reise 1985; Grosholz et al.
other bays and estuaries around Tasmania, in terms of depth
2000; Walton 2003). Furthermore, both species are profile, wave exposure and sediment quality. Because the area does
known to have significant effects on native populations not currently support populations of either Asterias amurensis or
in Tasmania (Ross et al. 2002, 2003a; Walton et al. Carcinus maenas, the experiment was conducted in completely en-
closed cages and only male specimens were used to reduce the risk
2002).
of establishing these species.
Both A. amurensis and C. maenas are now common in
The experiment consisted of five treatments, which included all
the coastal waters of Tasmania. A. amurensis was possible combinations of presence (a single animal per cage) and
introduced to south-east Tasmania in the early 1980s, absence of crabs and seastars in cages, and an unmanipulated 1 m2
plot without either cages or added predators. The cages consisted
where it has become a dominant invertebrate predator in
of a rigid (1 m·1 m base·0.7 m high) steel frame with legs (0.5 m
the Derwent Estuary (Grannum et al. 1996). C. maenas is
long) to securely anchor the cage in the sediment. The cage top and
thought to have been introduced to mainland Australia sides (except legs) were completely covered in plastic mesh (6 mm),
in the early 1900s (Fulton and Grant 1900), but it was and the cage legs were driven into the sediment so that 100–
not recorded in Tasmania until 1993, where its range has 150 mm of the cage sides was buried to prevent passage in or out of
large predators or prey by burrowing.
expanded rapidly (Gardner et al. 1994; Thresher et al.
To control for patchiness of infauna in the analysis of treatment
2003). In their native ranges both species are important effects, we used a randomised complete-block design. In a pilot
predators of a wide variety of epifaunal and infaunal study, plots 3–5 m apart were similar in composition, while plots
species (e.g. Hatanaka and Kosaka 1959; Fukuyama and separated by 30–60 m were usually dissimilar. Thus, the experiment
followed a randomised complete-block design, with one replicate of
Oliver 1985; Jensen and Jensen 1985; Sanchez-Salazar
each of the five treatments applied randomly to separate experi-
et al. 1987; Fukuyama 1994). Bivalve populations in
mental units ($5 m apart) in each of three blocks ($30 m apart).
particular appear to be very susceptible to predation by By accounting for the variation between blocks, we hoped to obtain
A. amurensis (Hatanaka and Kosaka 1959; Kim 1969; a smaller experimental error and improve the power to detect
treatment effects (see Newman et al. 1997).
Nojima et al. 1986) and C. maenas (Ropes 1968; Griffiths
The experiment was monitored weekly to check the condition of
et al. 1992; Grosholz and Ruiz 1995; Walton 2003). Al-
the enclosed predators and remove fouling organisms from the
though the distributions of C. maenas and A. amurensis cage. Eight weeks after the commencement of the experiment, cages
in Tasmania do not currently overlap, such sympatry and predators were removed. Two different sampling techniques
appears imminent given the current rate of spread and were employed. First, treatment plots were sampled with cores
(150 mm diameter, 100 mm deep) to estimate the abundance of all
apparent absence of any dispersal barriers for C. maenas.
infaunal and epifaunal organisms (>1 mm). Three replicate cores
Since both species are major predators of bivalves in were taken at random positions in each plot. No samples were
sheltered, low-energy environments, it appears that taken within $0.1 m of the cage perimeter to avoid possible
direct biological interaction between these species is edge effects of the cages. Because it was not anticipated that core
749
Fig. 1 Map of south-east
Tasmania showing study
location, King George Sound
samples would provide precise estimates of the abundance of larger versus block were examined. In cases where an interaction was
and/or rare species that may be important prey, the entire contents clearly evident by visual inspection, the analysis was not con-
of the plots were subsequently sampled to a depth of 0.1 m, using a ducted. Data were checked for normality and homoscedasticity,
diver-operated, air-driven suction device. To do this, an open and transformed as necessary depending on the relationship be-
square frame (1 m·1 m) was inserted into the sediment to isolate tween standard deviations and means of treatment groups
the plot, and all contents vacuumed into a 1-mm-mesh bag. Sam- (ignoring the blocking effect) (Draper and Smith 1981). Trans-
pling in both cores and air-lift samples was to a depth of 0.1 m, formations are expressed in terms of the untransformed variate,
because the vast majority of macroinvertebrate infauna was found Y. Where prey depletion occurred and multiplicative effects were
in this depth range in a pilot study. likely, as was the case for F. tenuicostata and K. rhytiphora, we
Samples were sieved (1.0 mm mesh) prior to fixing in 5–10% tested a multiplicative model by running the ANOVA on log
buffered formalin with Rose Bengal stain, and then rinsed in abundances. The statistical package SAS was used for all uni-
freshwater before storing in 100% ethanol. For core samples, all variate analyses.
infaunal and epifaunal organisms (>1 mm) were sorted and In the absence of significant predation effects by the seastar and
identified to the lowest possible taxon. Suction samples were sieved crab effects, or seastar·crab interactions, the minimum detectable
again (2.0 mm mesh), and all bivalves and the echinoid Echino- effect size (MDES) for a power of 80% was calculated for preda-
cardium cordatum were sorted and identified to species. tion effects. MDES values were calculated as the percentage change
Because both predators leave clear traces of their activities from the mean abundance in treatments in which the predator was
when consuming bivalves, the number of clams (Fulvia tenuicos- absent using the MSblock·seastar and MSblock·crab interaction terms
tata and Katelysia rhytiphora) eaten by each predator was counted from the original ANOVA as the estimate of variation for seastar
in suction samples to examine the potential for interaction effects and crab MDES calculations, respectively. These power calcula-
between predators in more detail. Undamaged, empty shells with tions were done using PiFace, a power analysis add-in for Micro-
gaping valves identified bivalves that were eaten by seastars. Bi- soft Excel (available at: http://www.stat.uiowa.edu/ftp/rlenth/
valve hinges with only a fraction of the shell remaining were PiFace/).
identified as prey eaten by crabs. To test for size selection by To test for size selection by seastars and crabs on the com-
seastars and crabs and whether size selection is altered in the mercial bivalve F. tenuicostata, and whether size selection is altered
presence of the other predator, the lengths of live and undamaged in the presence of the other predator, we compared size-frequency
empty bivalves were measured in all treatments. distributions between treatment groups using the Kolmogorov–
Smirnov (K–S) test. The specific comparisons of size-frequency
distributions for:
Statistical analysis 1. seastar size selection: empty bivalves in the seastar treatment
versus live bivalves in the cage control treatment;
The responses of dominant taxa to experimental treatments were 2. crab size selection: live bivalves in the crab treatment versus live
determined using species abundance data obtained from suction bivalves in the cage control treatment;
samples of 1 m2 plots, with the exception of polychaetes, which 3. effects of crabs on seastar size selection: empty bivalves in the
were counted in cores. For polychaetes we used the arithmetic seastar treatment versus empty bivalves in the seastar+crab
mean of the three replicate cores taken from each plot. Tests for treatment; and
predation effects and cage effects were conducted separately. To 4. effects of seastars on crab size selection: live bivalves in the
test for the possibility of cage effects, a one-way randomised, crab treatment versus empty bivalves in the crab+seastar
complete-block ANOVA, with ‘‘treatment’’ (two levels: cage treatment.
present and cage absent, both without added predators) as a fixed
factor and ‘‘block’’ as a random factor were used. The effects of The sequential Bonferroni procedure for multiple testing was
A. amurensis and C. maenas on prey species were analysed using a used to adjust significance levels (see Quinn and Keough 2003).
two-factor randomised, complete-block ANOVA, with ‘‘A. am- Note that the size-frequency data were pooled across blocks for
urensis’’ (present or absent) and ‘‘C. maenas’’ (present or absent) each treatment to ensure adequate sample sizes for construction of
as fixed factors and ‘‘block’’ as a random factor. Note, that, while size-frequency distributions.
there are no special assumptions required to conduct the tests, To depict the multivariate patterns among blocks and treat-
interpreting the significance of the predator effects requires no, or ments, non-metric multi-dimensional scaling was done on Bray–
a relatively small, predator by block interaction. To assess Curtis distances calculated from fourth-root-transformed data,
treatment by block interactions, plots of dependent variables using the Primer computer program (Clarke 1993).
750
added crabs (Table 1; Fig. 2a). Comparison of the size-
Results frequency distributions of F. tenuicostata between the
cage controls and treatments containing crabs shows
The major groups found in the core samples were that crab predation was largely on small (<25 mm)
polychaetes, bivalves and heart urchins that represented bivalves (Fig. 3a). The size-frequency distributions of F.
37%, 29% and 8%, respectively, of the total numerical tenuicostata remaining in treatments containing crabs
abundance. The bivalves Fulvia tenuicostata and Theora and in the cage control were significantly different
spp.; the polychaetes Simplisetia amphidonta, Lysilla (Fig. 3a, K–S test P>0.05). There was no evidence that
jennacubinae and Glycera spp.; and the echinoid Echi- predation by crabs influenced the abundance of the
nocardium cordatum represented 88%, 86% and 100% other commercial bivalve at this site, K. rhytiphora. It is
of the total abundance of bivalves, polychaetes and noteworthy that the majority of K. rhytiphora in all
echinoids, respectively. The numerically dominant spe- experimental plots exceeded 25 mm in total length.
cies from suction samples were the bivalves F. tenuicos-
tata, Theora spp., Kataleysia rhytiphora, Wallucina
assimilis and the echinoid E. cordatum. Interaction of crabs and seastars
The crab·seastar interaction was not significant for live
Commercial bivalves: F. tenuicostata and K. rhytiphora bivalves or open bivalve shells for eitherF. tenuicostata
or K. rhytiphora. In contrast, the crab·seastar interac-
tion was significant for F. tenuicostata hinges (Table 1).
Effect of cages The number of F. tenuicostata eaten by crabs (hinges) in
the presence of seastars was reduced compared with
There were no significant effects of cage controls on the when the crab was alone, but higher than when preda-
abundance of F. tenuicostata or K. rhytiphora (Table 1). tors were absent (Fig. 2a). However, the size of bivalves
eaten by the crab was not altered in the presence of the
seastar; the size-frequency distribution of bivalves not
Effect of predation by seastars
eaten in the crab treatment was not significantly different
from the size-frequency distribution of bivalves not ea-
There was a major reduction in densities of F. tenui-
ten by the crab in the crab+seastar treatment (Fig. 3,
costata and K. rhytiphora in all treatments containing
K–S test P>0.05). Although seastars consumed similar
Asterias amurensis; however, this difference was only
numbers of F. tenuicostata (open shells) in the presence
significant for F. tenuicostata (Table 1; Fig. 2a). The
of crabs (Fig. 2), there was a significant shift in the size-
abundance of recently opened shells (indicative of se-
frequency distribution of bivalves consumed, with larger
astar predation) of both species was greater in treat-
bivalves consumed in the presence of crabs (Fig. 3, K–S
ments with seastars; however, this difference was only
test P<0.05).
significant for K. rhytiphora (Table 1; Fig. 2a). Where
there were changes in abundance but differences were
not significant for live K. rhytiphora and open F. ten-
uicostata, only changes of >204% and 380%, respec- Other species
tively, of the mean abundance in treatments without
seastars could have been detected with 80% confi- The general pattern described for commercial bivalves
dence. Size selection by seastars was not apparent for is evident in the ordination (MDS) of treatment plots
F. tenuicostata, as the size-frequency distribution of based on abundances of bivalves and echinoids
this species eaten by A. amurensis was not significantly (Fig. 4a) and on those of the whole assemblage
different from the size-frequency distribution of live (Fig. 4b). However, on the basis of individual species,
bivalves in the cage control treatment (Fig. 3, K–S test there were no significant effects of added predators or
P>0.05). cages detected for E. cordatum and the bivalves Theora
spp. and W. assimilis or for the polychaetes S. am-
phidonta, L. jennacubinae and Glycera spp. (Table 1;
Effect of predation by crabs
Fig. 2b, c). Of the species for which there were no
apparent changes in abundance in the presence of ei-
The abundance of F. tenuicostata was reduced in all
ther predator, changes of between 9% and 97% in the
treatments containing Carcinus maenas compared with
presence of either predator could have been detected
the cage control; however, this difference was not sig-
with 80% confidence for the polychaetes and Theora
nificant (Table 1; Fig. 2a). Note that only a change of
spp. For the remaining species for which there were no
>212% could have been detected with 80% confidence
apparent changes in abundance in the presence of ei-
for F. tenuicostata. Although there was a crab·seastar
ther predator, only changes of >100% could have
interaction, the abundance of F. tenuicostata hinges
been detected in the presence of either predator with
(indicative of crab predation) was greater in treatments
80% confidence.
containing crabs compared with treatments with no
Table 1 Analysis of effects of predation and caging on the abundance of numerically abundant taxa. The table shows results of the ANOVA test of predation comparing among
treatments of Asterias amurensis (present or absent) and Carcinus maenas (present or absent) and the ANOVA test of caging comparing among treatments (cage present and cage
absent) with no predators added. Significant P-values (<0.05) are shown in boldface. Note K. rhytiphora hinges were not present in samples. Minimum detectable effect sizes (MDES)
for a power of 0.8 have been calculated for predation effects in the absence of significant predator or predator·predator interactions and are expressed as percent change from the mean
abundance in treatments in which the predator was absent
Predation effects Cage effects
Tranformation MSresid MSseastar·block MScrab·block Pseastar·crab Pseastar MDES (%) Pcrab MDES(%) MSresid Pcage
Degrees of freedom 2 2 2
Denominator used in each F-test MSresid MSseastar·block MScrab·block MSresid
Commercial bivalves
Fulvia tenuicostata
Alive log(x+0.01) 4.350 1.464 5.504 0.711 0.026 0.495 250 247.167 0.611
Empty shell log(x+0.01) 4.006 1.968 5.370 0.336 0.067 204 0.404 212 112.500 0.408
Hinge log(x+0.01) 0.012 0.003 0.595 0.026 0.102 0.144 66.500 0.792
Katelysia rhytiphora
Alive log(x+0.01) 1.578 4.463 2.385 0.323 0.086 380 0.573 1309 3.500 0.580
Empty shell log(x+0.01) 1.330 2.139 3.844 0.558 0.025 0.369 751 1.167 0.742
Other bivalves and echinoids
Echinocardium cordatum x 1160.359 382.443 648.328 0.756 0.324 102 0.612 165 211.211 0.406
x0.5
Theora spp. 16.083 21.583 3.083 0.707 0.812 70 0.665 97 390.167 0.524
Wallucina assimilis x 8.911 3.862 6.742 0.219 0.449 690 0.415 592 4.167 0.251
Polychaetes
Simplisetia amphidonta x 1.590 0.174 1.507 0.507 0.136 9 0.155 21 0.233 0.075
Lysilla jennacubmae x 0.750 0.287 0.731 0.574 0.547 35 0.843 54 1.167 0.529
x
Glycera spp. 1.766 0.488 0.424 0.493 0.126 33 0.845 25 0.056 0.074
751
752
Fig. 2a–c Densities of the most abundant species in each treat- There was no evidence that either predator influenced
ment. Densities of commercial bivalves (a) and other bivalves and abundances of the echinoid Echinocardium cordatum, the
echinoids (b) are means per square meter (+SE) taken from suction
bivalves Theora spp. and Wallucina assimilis, or the
samples to a depth of 100 mm (n=3 plots). Polychaete densities (c)
polychaetes Simplisetia amphidonta, Lysilla jennacubinae
are means per square meter (+SE) scaled from counts in cores
and Glycera spp. However, the tests on unaffected
(n=3 cores pooled, each 150 mm diameter, 100 mm deep) in each
plot (n=3 plots) species varied in power. For species in which variation
between blocks was high (e.g. E. cordatum), or densities
were very low (e.g. W. assimilis), the power to test for
Discussion treatment effects was low and little weight is given to
these non-significant results. Power analysis indicated
The main effect of both predators was on the commercial that only very large changes in abundance (>592% and
bivalves, Fulvia tenuicostata and Katelysia rhytiphora. 165%) could have been detected with 80% confidence
753
Fig. 4 Ordination (MDS) of treatment plots based: a on abun-
dances of bivalves and echinoids and b on the entire assemblage.
Fig. 3 Length-frequency histograms of Fulvia tenuicostata remain- For both ordinations, plots with added seastars separate clearly
ing at the end of the experiment in: a live treatments (uncaged control, from plots with only added crabs, and both are distinct to plots
cage control and treatments with crabs) and b open treatments (with without added predators. These groupings have been outlined with
seastar+crab and seastar). Unshaded and shaded histograms were ellipses for clarity. The grouping is consistent with the general
significantly different in paired Kolmogorov–Smirnov tests pattern described for the commercial bivalves in the univariate
analysis. Note that the mean number per core in each treatment
plot was used to estimate the number per square meter for taxa
when testing for crab effects on W. assimilis and found in cores for this comparison
E. cordatum, respectively. In contrast, for polychaetes,
there was sufficient power to detect much smaller
changes in abundance (between 9% and 54%) with 80% other species including polychaetes when the bivalve
confidence, which is smaller than changes detected for became rare. While the commercial bivalves were clearly
seastar and crab effects in other experiments (Ross et al. preferred over polychaetes in our short-term experiment,
2002, 2003a; Walton et al. 2002). Thus, for polychaetes had the experiment run longer A. amurensis may
we are confident that they were unaffected by preda- have switched to polychaetes when the bivalves were
tors in this experiment. Importantly, it is also possible exhausted.
that not all direct and indirect effects had occurred
before the termination of the experiment given its
relatively short duration (2 months). It is noteworthy Caging effects
that in a short-term study carried out in the Derwent
Estuary, Asterias fed predominately on F. tenuicostata Caging experiments are recognised as a valuable tool in
after its massive settlement, but shifted to feed on examining the effect of predators on marine communities
754
1995; Morrice 1995; L. Turner, personal communica-
(see Peterson 1979; Thrush 1999); however, the potential
tion). The results of the present experiment are consis-
for cage artefacts to confound true treatment effects is
tent with the hypothesis that predation by A. amurensis
well recognised (e.g. Hulberg and Oliver 1980; Under-
is responsible for the rarity of adult F. tenuicostata and
wood 1986). By undertaking the experiment immediately
K. rhytiphora in the Derwent Estuary. Moreover, in a
beyond the current range of the seastar in a similar but
recent study, the seastar was shown to have a major
unimpacted area, the contrast of open plots with empty
impact on the survivorship of juvenile F. tenuicostata in
cages provides a straightforward test for most cage
the Derwent Estuary, effectively arresting a massive
artefacts. In our experiments, there were no significant
settlement event (Ross et al. 2002).
effects detected in making this comparison. However, it
was not possible to control for cage effects on predator
behaviour, and so we must assume that the cage has not
Impacts of Carcinus maenas
greatly affected the behaviour of the predators. In this
context an important point to emphasise is that both
seastar (Nojima et al. 1986; Grannum et al. 1996; Ling Although there was no significant effect of C. maenas on
2000) and crab (Crothers 1968; Jensen and Jensen 1985; F. tenuicostata in the experiment, the pattern of abun-
McKinnon 1997) densities similar to and substantially dance of live F. tenuicostata and hinges remaining after
higher than those we used in the cages have been predation events are consistent with predation by the
recorded in Tasmania and in their native ranges, and crab. The abundance of F. tenuicostata in the presence of
the crab was $50% lower than in the control treatments.
that these high densities have persisted for periods much
longer than our experimental period. Thus, we suggest it Hinges were far more abundant in the presence of crabs
is reasonable to expect similar effects on native species compared with treatments in which the crab was absent,
should the predators attain the densities used in this indicating that crab predation was largely responsible
experiment. for the differences in densities between treatments.
Furthermore, a comparison of the size frequency of
F. tenuicostata in the cage control and crab treatment
indicates that C. maenas consumed the majority of small
Impacts of Asterias amurensis
bivalves (>25 mm). It is likely that C. maenas is unable
to prey on larger bivalves. Comparable size constraints
In this study, densities of the commercial bivalves were
$80 individuals m)2 lower for Fulvia tenuicostata and have been recorded for similar-sized C. maenas feeding
$5 individuals m)2 lower for Katelysia rhytiphora in the on other cockles, such as Mercenaria mercenaria (Walne
presence of seastars at a density of 1 individual m)2 and Dean 1972), Katelysia rhytiphora (McKinnon 1997;
´
Walton et al. 2002) and Cerastoderma edule (Mascaro
compared with the cage control. Recently opened shells
and Seed 2000). Similarly, size constraints in handling
were far more abundant in the presence of seastars
prey explain the absence of a detectable effect on
compared with the cage control for both bivalve species,
K. rhytiphora, given that the majority of K. rhytiphora in
indicating that seastar predation was largely responsible
this experiment were large (>25 mm).
for the differences in densities between treatments. These
In similar short-term experiments in intertidal soft-
results have been supported from feeding observations
sediment habitats, C. maenas predation was shown to
in non-experimental areas both in the Derwent Estuary
significantly reduce the abundance of the bivalves
and in a recently invaded area outside the estuary, where
Paphies erycinaea, K. rhytiphora and K. scalarina in
aggregations of seastars consumed virtually all the
Tasmania (McKinnon 1997; Walton et al. 2002), and the
F. tenuicostata, as anticipated from this and other
bivalves Nutricola confusa and N. tantilla in California
experiments (Ross et al. 2002, 2003a, 2003b).
(Grosholz and Ruiz 1995). These earlier studies indicate
The results of the present study are consistent with
that predation by C. maenas is likely to impact popula-
observations in the native habitat of the seastar, where it
tions of small bivalves in both intertidal and subtidal
is a major predator of bivalves, including cockles, oys-
soft-sediment habitats where it becomes abundant,
ters, scallops and other clams (Hatanaka and Kosaka
including Tasmania. Although our results did not dem-
1959; Kim 1969; Nojima et al. 1986). In the Derwent
onstrate a significant effect of C. maenas predation, de-
Estuary, Grannum et al. (1996) calculated electivity
spite a large decline in bivalve density, we interpret this as
indices based on field data; they found that A. amurensis
a lack of statistical power due to the relatively high
was highly selective for bivalves and concluded that
variation among plots compared to the previous studies.
predation by A. amurensis posed a serious threat to
many bivalve species, particularly the populations of
Chioneryx striatissima and Venerupis spp., within the
Interactions of A. amurensis and C. maenas
estuary. For many bivalve species such as F. tenuicostata
and K. rhytiphora live large adults are rare in the Der-
The presence of C. maenas appeared to have no effect on
went Estuary, despite the presence in the sediments of
K. rhytiphora predation by A. amurensis. This likely
numerous remains (intact shells) of large individuals.
resulted from an absence of small individuals of this
This is disturbing given the high prevalence of juveniles
bivalve and the inability of C. maenas to consume large
in the sediments and the diet of A. amurensis (Lockhart
755
ones. In contrast, the individual effects of each predator R. Thresher and C. Procter. This work was supported by funds
from the CSIRO Marine Research Centre for Research on
on F. tenuicostata were influenced by the presence of the
Introduced Marine Pests (awarded to C.R.J.) and the School of
other species. Fewer F. tenuicostata were consumed by Zoology, University of Tasmania. This work was undertaken as
C. maenas in the presence of the seastar compared part the senior authorÕs Doctor of Philosophy degree at the
with when it was alone. Although similar numbers of University of Tasmania, who was supported by an Australian
Postgraduate Award. The experiments we performed comply with
F. tenuicostata were consumed by A. amurensis in the
the current laws of Australia, conducted on a permit for intro-
presence of C. maenas compared with when it was alone, duced species research issued under section 14 of the Living
the seastar consumed larger bivalves when the crab was Marine Resources Management Act 1995 in Tasmania.
present. Thus, the interaction between C. maenas and
A. amurensis appears to be direct competition for
resources, resulting in the partitioning of bivalves
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DOI 10.1007/s00227-003-1223-4
R ES E AR C H A RT I C L E
D. J. Ross Æ C. R. Johnson Æ C. L. Hewitt Æ G. M. Ruiz
Interaction and impacts of two introduced species
on a soft-sediment marine assemblage in SE Tasmania
Received: 6 November 2002 / Accepted: 11 September 2003 / Published online: 26 November 2003
Ó Springer-Verlag 2003
Abstract Introduced species are having major impacts in respective ranges expand, suggesting a strong overlap in
terrestrial, freshwater and marine ecosystems world- food resources will result from the shared proclivity for
wide. It is increasingly recognised that effects of multiple bivalve prey. A. amurensis and C. maenas provide good
species often cannot be predicted from the effect of each models to test the interaction between multiple intro-
species alone, due to complex interactions, but most duced predators, because they leave clear predator-spe-
investigations of invasion impacts have examined only cific traces of their predatory activity for a number of
one non-native species at a time and have not addressed common prey taxa (bivalves and gastropods). Our
the interactive effects of multiple species. We conducted experiments demonstrate that both predators had a
a field experiment to compare the individual and com- major effect on the abundance of bivalves, reducing
bined effects of two introduced marine predators, the populations of the commercial bivalves Fulvia tenuicos-
northern Pacific seastar Asterias amurensis and the tata and Katelysia rhytiphora. The interaction between
European green crab Carcinus maenas, on a soft-sedi- C. maenas and A. amurensis appears to be one of re-
ment invertebrate assemblage in Tasmania. Spatial source competition, resulting in partitioning of bivalves
overlap in the distribution of these invaders is just according to size between predators, with A. amurensis
beginning in Tasmania, and appears imminent as their consuming the large and C. maenas the small bivalves.
At a large spatial scale, we predict that the combined
effect on bivalves may be greater than that due to each
Communicated by M.S. Johnson, Crawley
predator alone simply because their combined distribu-
D. J. Ross (&) Æ C. R. Johnson tion is likely to cover a broader range of habitats. At a
School of Zoology and Tasmanian smaller scale, in the shallow subtidal, where spatial
Aquaculture and Fisheries Institute,
overlap is expected to be most extensive, our results
University of Tasmania,
indicate the individual effects of each predator are likely
7000 Sandy Bay, Tasmania,
to be modified in the presence of the other as densities
Australia
E-mail: rossdj@unimelb.edu.au increase. These results further highlight the need to
Fax: +1-3-83447909
consider the interactive effects of introduced species,
D. J. Ross Æ C. L. Hewitt especially with continued increases in the number of
Centre for Research on established invasions.
Introduced Marine Pests,
CSIRO Marine Research,
7001 Hobart, Tasmania,
Australia
G. M. Ruiz
Introduction
Smithsonian Environmental Research Center,
Edgewater, MD 21037, USA
Biological invasions, or the establishment of non-native
Present address: D. J. Ross
species outside their historic range, have become a major
Department of Zoology,
University of Melbourne, force of ecological change throughout the world. Al-
3010 Melbourne, Victoria,
though invasions have occurred for millions of years,
Australia
there has been a rapid increase in the rate of newly de-
Present address: C. L. Hewitt tected invasions over the last two centuries, driven by
Ministry of Fisheries,
human-aided movement across and between continents
PO Box 2526, Wellington,
and oceans (Carlton and Geller 1993; Vitousek 1994;
New Zealand
748
inevitable, and we predict the interaction between
Cohen and Carlton 1998; Hewitt et al. 1999; Ruiz et al.
A. amurensis and C. maenas will modify the effects
2000; Ruiz and Carlton 2003). The magnitude of eco-
resulting from each species individually.
logical effects by invasions has become increasingly
This seastar/crab/bivalve system is an excellent model
evident, resulting in fundamental changes to population,
to explore the interactive effects of multiple introduced
community and ecosystem processes (Cloern 1996;
species, because each predator leaves characteristic pat-
Vitousek et al. 1996; DÕAntonio et al. 1998; Wilcove
terns on shells of their bivalve prey. Predation by sea-
et al. 1998; Strayer 1999; Grosholz et al. 2000). Despite a
stars results in undamaged and empty shells, whereas
growing amount of literature on invasion effects, the
bivalves eaten by crabs are broken by this crushing
impacts of most invasions remain unstudied, and the
predator (i.e. usually hinges with only a fraction of the
interactive effects of multiple species have rarely been
shell remaining). Using this physical evidence of preda-
evaluated (Ruiz et al. 1999; Simberloff and von Holle
tor type, we tested the separate and combined impacts of
1999). The combined effects of several introduced spe-
A. amurensis and C. maenas on a soft-sediment assem-
cies may not be strictly additive, and can result in many
blage, focusing particular attention on bivalves. Because
complex interactions, including accelerated impacts on
there was little information on the distribution and
native communities (Simberloff and von Holle 1999).
abundance of native species prior to the establishment of
Indeed, modification of interactions, whereby the direct
A. amurensis and C. maenas, the study focuses on
interaction between two species is altered by the pres-
experimental manipulations of the two species in a rel-
ence of a third, is thought to be commonplace (Kareiva
atively unimpacted habitat at the interface of their cur-
1994).
rent ranges.
Hundreds of non-native marine species are now
established in the coastal waters of Australia, despite
the relative degree of geographic isolation (Pollard and
Hutchings 1990a, 1990b; Jones 1991; Furlani 1996;
Materials and methods
Hewitt et al. 1999). Among the most conspicuous
introductions are two large, predatory species found in
Collection and maintenance
sheltered, low-energy environments: the northern Pa-
cific seastar Asterias amurensis and the European green A manipulative experiment was undertaken in the sheltered upper
crab Carcinus maenas. The green crab is known to reaches of King George Sound, south-east Tasmania at a depth of
have significant effects on infaunal communities in 2–3 m (Fig. 1). Sediment in the area is composed predominantly of
sandy mud. The habitat type at this site is similar to that present in
many parts of the world (Reise 1985; Grosholz et al.
other bays and estuaries around Tasmania, in terms of depth
2000; Walton 2003). Furthermore, both species are profile, wave exposure and sediment quality. Because the area does
known to have significant effects on native populations not currently support populations of either Asterias amurensis or
in Tasmania (Ross et al. 2002, 2003a; Walton et al. Carcinus maenas, the experiment was conducted in completely en-
closed cages and only male specimens were used to reduce the risk
2002).
of establishing these species.
Both A. amurensis and C. maenas are now common in
The experiment consisted of five treatments, which included all
the coastal waters of Tasmania. A. amurensis was possible combinations of presence (a single animal per cage) and
introduced to south-east Tasmania in the early 1980s, absence of crabs and seastars in cages, and an unmanipulated 1 m2
plot without either cages or added predators. The cages consisted
where it has become a dominant invertebrate predator in
of a rigid (1 m·1 m base·0.7 m high) steel frame with legs (0.5 m
the Derwent Estuary (Grannum et al. 1996). C. maenas is
long) to securely anchor the cage in the sediment. The cage top and
thought to have been introduced to mainland Australia sides (except legs) were completely covered in plastic mesh (6 mm),
in the early 1900s (Fulton and Grant 1900), but it was and the cage legs were driven into the sediment so that 100–
not recorded in Tasmania until 1993, where its range has 150 mm of the cage sides was buried to prevent passage in or out of
large predators or prey by burrowing.
expanded rapidly (Gardner et al. 1994; Thresher et al.
To control for patchiness of infauna in the analysis of treatment
2003). In their native ranges both species are important effects, we used a randomised complete-block design. In a pilot
predators of a wide variety of epifaunal and infaunal study, plots 3–5 m apart were similar in composition, while plots
species (e.g. Hatanaka and Kosaka 1959; Fukuyama and separated by 30–60 m were usually dissimilar. Thus, the experiment
followed a randomised complete-block design, with one replicate of
Oliver 1985; Jensen and Jensen 1985; Sanchez-Salazar
each of the five treatments applied randomly to separate experi-
et al. 1987; Fukuyama 1994). Bivalve populations in
mental units ($5 m apart) in each of three blocks ($30 m apart).
particular appear to be very susceptible to predation by By accounting for the variation between blocks, we hoped to obtain
A. amurensis (Hatanaka and Kosaka 1959; Kim 1969; a smaller experimental error and improve the power to detect
treatment effects (see Newman et al. 1997).
Nojima et al. 1986) and C. maenas (Ropes 1968; Griffiths
The experiment was monitored weekly to check the condition of
et al. 1992; Grosholz and Ruiz 1995; Walton 2003). Al-
the enclosed predators and remove fouling organisms from the
though the distributions of C. maenas and A. amurensis cage. Eight weeks after the commencement of the experiment, cages
in Tasmania do not currently overlap, such sympatry and predators were removed. Two different sampling techniques
appears imminent given the current rate of spread and were employed. First, treatment plots were sampled with cores
(150 mm diameter, 100 mm deep) to estimate the abundance of all
apparent absence of any dispersal barriers for C. maenas.
infaunal and epifaunal organisms (>1 mm). Three replicate cores
Since both species are major predators of bivalves in were taken at random positions in each plot. No samples were
sheltered, low-energy environments, it appears that taken within $0.1 m of the cage perimeter to avoid possible
direct biological interaction between these species is edge effects of the cages. Because it was not anticipated that core
749
Fig. 1 Map of south-east
Tasmania showing study
location, King George Sound
samples would provide precise estimates of the abundance of larger versus block were examined. In cases where an interaction was
and/or rare species that may be important prey, the entire contents clearly evident by visual inspection, the analysis was not con-
of the plots were subsequently sampled to a depth of 0.1 m, using a ducted. Data were checked for normality and homoscedasticity,
diver-operated, air-driven suction device. To do this, an open and transformed as necessary depending on the relationship be-
square frame (1 m·1 m) was inserted into the sediment to isolate tween standard deviations and means of treatment groups
the plot, and all contents vacuumed into a 1-mm-mesh bag. Sam- (ignoring the blocking effect) (Draper and Smith 1981). Trans-
pling in both cores and air-lift samples was to a depth of 0.1 m, formations are expressed in terms of the untransformed variate,
because the vast majority of macroinvertebrate infauna was found Y. Where prey depletion occurred and multiplicative effects were
in this depth range in a pilot study. likely, as was the case for F. tenuicostata and K. rhytiphora, we
Samples were sieved (1.0 mm mesh) prior to fixing in 5–10% tested a multiplicative model by running the ANOVA on log
buffered formalin with Rose Bengal stain, and then rinsed in abundances. The statistical package SAS was used for all uni-
freshwater before storing in 100% ethanol. For core samples, all variate analyses.
infaunal and epifaunal organisms (>1 mm) were sorted and In the absence of significant predation effects by the seastar and
identified to the lowest possible taxon. Suction samples were sieved crab effects, or seastar·crab interactions, the minimum detectable
again (2.0 mm mesh), and all bivalves and the echinoid Echino- effect size (MDES) for a power of 80% was calculated for preda-
cardium cordatum were sorted and identified to species. tion effects. MDES values were calculated as the percentage change
Because both predators leave clear traces of their activities from the mean abundance in treatments in which the predator was
when consuming bivalves, the number of clams (Fulvia tenuicos- absent using the MSblock·seastar and MSblock·crab interaction terms
tata and Katelysia rhytiphora) eaten by each predator was counted from the original ANOVA as the estimate of variation for seastar
in suction samples to examine the potential for interaction effects and crab MDES calculations, respectively. These power calcula-
between predators in more detail. Undamaged, empty shells with tions were done using PiFace, a power analysis add-in for Micro-
gaping valves identified bivalves that were eaten by seastars. Bi- soft Excel (available at: http://www.stat.uiowa.edu/ftp/rlenth/
valve hinges with only a fraction of the shell remaining were PiFace/).
identified as prey eaten by crabs. To test for size selection by To test for size selection by seastars and crabs on the com-
seastars and crabs and whether size selection is altered in the mercial bivalve F. tenuicostata, and whether size selection is altered
presence of the other predator, the lengths of live and undamaged in the presence of the other predator, we compared size-frequency
empty bivalves were measured in all treatments. distributions between treatment groups using the Kolmogorov–
Smirnov (K–S) test. The specific comparisons of size-frequency
distributions for:
Statistical analysis 1. seastar size selection: empty bivalves in the seastar treatment
versus live bivalves in the cage control treatment;
The responses of dominant taxa to experimental treatments were 2. crab size selection: live bivalves in the crab treatment versus live
determined using species abundance data obtained from suction bivalves in the cage control treatment;
samples of 1 m2 plots, with the exception of polychaetes, which 3. effects of crabs on seastar size selection: empty bivalves in the
were counted in cores. For polychaetes we used the arithmetic seastar treatment versus empty bivalves in the seastar+crab
mean of the three replicate cores taken from each plot. Tests for treatment; and
predation effects and cage effects were conducted separately. To 4. effects of seastars on crab size selection: live bivalves in the
test for the possibility of cage effects, a one-way randomised, crab treatment versus empty bivalves in the crab+seastar
complete-block ANOVA, with ‘‘treatment’’ (two levels: cage treatment.
present and cage absent, both without added predators) as a fixed
factor and ‘‘block’’ as a random factor were used. The effects of The sequential Bonferroni procedure for multiple testing was
A. amurensis and C. maenas on prey species were analysed using a used to adjust significance levels (see Quinn and Keough 2003).
two-factor randomised, complete-block ANOVA, with ‘‘A. am- Note that the size-frequency data were pooled across blocks for
urensis’’ (present or absent) and ‘‘C. maenas’’ (present or absent) each treatment to ensure adequate sample sizes for construction of
as fixed factors and ‘‘block’’ as a random factor. Note, that, while size-frequency distributions.
there are no special assumptions required to conduct the tests, To depict the multivariate patterns among blocks and treat-
interpreting the significance of the predator effects requires no, or ments, non-metric multi-dimensional scaling was done on Bray–
a relatively small, predator by block interaction. To assess Curtis distances calculated from fourth-root-transformed data,
treatment by block interactions, plots of dependent variables using the Primer computer program (Clarke 1993).
750
added crabs (Table 1; Fig. 2a). Comparison of the size-
Results frequency distributions of F. tenuicostata between the
cage controls and treatments containing crabs shows
The major groups found in the core samples were that crab predation was largely on small (<25 mm)
polychaetes, bivalves and heart urchins that represented bivalves (Fig. 3a). The size-frequency distributions of F.
37%, 29% and 8%, respectively, of the total numerical tenuicostata remaining in treatments containing crabs
abundance. The bivalves Fulvia tenuicostata and Theora and in the cage control were significantly different
spp.; the polychaetes Simplisetia amphidonta, Lysilla (Fig. 3a, K–S test P>0.05). There was no evidence that
jennacubinae and Glycera spp.; and the echinoid Echi- predation by crabs influenced the abundance of the
nocardium cordatum represented 88%, 86% and 100% other commercial bivalve at this site, K. rhytiphora. It is
of the total abundance of bivalves, polychaetes and noteworthy that the majority of K. rhytiphora in all
echinoids, respectively. The numerically dominant spe- experimental plots exceeded 25 mm in total length.
cies from suction samples were the bivalves F. tenuicos-
tata, Theora spp., Kataleysia rhytiphora, Wallucina
assimilis and the echinoid E. cordatum. Interaction of crabs and seastars
The crab·seastar interaction was not significant for live
Commercial bivalves: F. tenuicostata and K. rhytiphora bivalves or open bivalve shells for eitherF. tenuicostata
or K. rhytiphora. In contrast, the crab·seastar interac-
tion was significant for F. tenuicostata hinges (Table 1).
Effect of cages The number of F. tenuicostata eaten by crabs (hinges) in
the presence of seastars was reduced compared with
There were no significant effects of cage controls on the when the crab was alone, but higher than when preda-
abundance of F. tenuicostata or K. rhytiphora (Table 1). tors were absent (Fig. 2a). However, the size of bivalves
eaten by the crab was not altered in the presence of the
seastar; the size-frequency distribution of bivalves not
Effect of predation by seastars
eaten in the crab treatment was not significantly different
from the size-frequency distribution of bivalves not ea-
There was a major reduction in densities of F. tenui-
ten by the crab in the crab+seastar treatment (Fig. 3,
costata and K. rhytiphora in all treatments containing
K–S test P>0.05). Although seastars consumed similar
Asterias amurensis; however, this difference was only
numbers of F. tenuicostata (open shells) in the presence
significant for F. tenuicostata (Table 1; Fig. 2a). The
of crabs (Fig. 2), there was a significant shift in the size-
abundance of recently opened shells (indicative of se-
frequency distribution of bivalves consumed, with larger
astar predation) of both species was greater in treat-
bivalves consumed in the presence of crabs (Fig. 3, K–S
ments with seastars; however, this difference was only
test P<0.05).
significant for K. rhytiphora (Table 1; Fig. 2a). Where
there were changes in abundance but differences were
not significant for live K. rhytiphora and open F. ten-
uicostata, only changes of >204% and 380%, respec- Other species
tively, of the mean abundance in treatments without
seastars could have been detected with 80% confi- The general pattern described for commercial bivalves
dence. Size selection by seastars was not apparent for is evident in the ordination (MDS) of treatment plots
F. tenuicostata, as the size-frequency distribution of based on abundances of bivalves and echinoids
this species eaten by A. amurensis was not significantly (Fig. 4a) and on those of the whole assemblage
different from the size-frequency distribution of live (Fig. 4b). However, on the basis of individual species,
bivalves in the cage control treatment (Fig. 3, K–S test there were no significant effects of added predators or
P>0.05). cages detected for E. cordatum and the bivalves Theora
spp. and W. assimilis or for the polychaetes S. am-
phidonta, L. jennacubinae and Glycera spp. (Table 1;
Effect of predation by crabs
Fig. 2b, c). Of the species for which there were no
apparent changes in abundance in the presence of ei-
The abundance of F. tenuicostata was reduced in all
ther predator, changes of between 9% and 97% in the
treatments containing Carcinus maenas compared with
presence of either predator could have been detected
the cage control; however, this difference was not sig-
with 80% confidence for the polychaetes and Theora
nificant (Table 1; Fig. 2a). Note that only a change of
spp. For the remaining species for which there were no
>212% could have been detected with 80% confidence
apparent changes in abundance in the presence of ei-
for F. tenuicostata. Although there was a crab·seastar
ther predator, only changes of >100% could have
interaction, the abundance of F. tenuicostata hinges
been detected in the presence of either predator with
(indicative of crab predation) was greater in treatments
80% confidence.
containing crabs compared with treatments with no
Table 1 Analysis of effects of predation and caging on the abundance of numerically abundant taxa. The table shows results of the ANOVA test of predation comparing among
treatments of Asterias amurensis (present or absent) and Carcinus maenas (present or absent) and the ANOVA test of caging comparing among treatments (cage present and cage
absent) with no predators added. Significant P-values (<0.05) are shown in boldface. Note K. rhytiphora hinges were not present in samples. Minimum detectable effect sizes (MDES)
for a power of 0.8 have been calculated for predation effects in the absence of significant predator or predator·predator interactions and are expressed as percent change from the mean
abundance in treatments in which the predator was absent
Predation effects Cage effects
Tranformation MSresid MSseastar·block MScrab·block Pseastar·crab Pseastar MDES (%) Pcrab MDES(%) MSresid Pcage
Degrees of freedom 2 2 2
Denominator used in each F-test MSresid MSseastar·block MScrab·block MSresid
Commercial bivalves
Fulvia tenuicostata
Alive log(x+0.01) 4.350 1.464 5.504 0.711 0.026 0.495 250 247.167 0.611
Empty shell log(x+0.01) 4.006 1.968 5.370 0.336 0.067 204 0.404 212 112.500 0.408
Hinge log(x+0.01) 0.012 0.003 0.595 0.026 0.102 0.144 66.500 0.792
Katelysia rhytiphora
Alive log(x+0.01) 1.578 4.463 2.385 0.323 0.086 380 0.573 1309 3.500 0.580
Empty shell log(x+0.01) 1.330 2.139 3.844 0.558 0.025 0.369 751 1.167 0.742
Other bivalves and echinoids
Echinocardium cordatum x 1160.359 382.443 648.328 0.756 0.324 102 0.612 165 211.211 0.406
x0.5
Theora spp. 16.083 21.583 3.083 0.707 0.812 70 0.665 97 390.167 0.524
Wallucina assimilis x 8.911 3.862 6.742 0.219 0.449 690 0.415 592 4.167 0.251
Polychaetes
Simplisetia amphidonta x 1.590 0.174 1.507 0.507 0.136 9 0.155 21 0.233 0.075
Lysilla jennacubmae x 0.750 0.287 0.731 0.574 0.547 35 0.843 54 1.167 0.529
x
Glycera spp. 1.766 0.488 0.424 0.493 0.126 33 0.845 25 0.056 0.074
751
752
Fig. 2a–c Densities of the most abundant species in each treat- There was no evidence that either predator influenced
ment. Densities of commercial bivalves (a) and other bivalves and abundances of the echinoid Echinocardium cordatum, the
echinoids (b) are means per square meter (+SE) taken from suction
bivalves Theora spp. and Wallucina assimilis, or the
samples to a depth of 100 mm (n=3 plots). Polychaete densities (c)
polychaetes Simplisetia amphidonta, Lysilla jennacubinae
are means per square meter (+SE) scaled from counts in cores
and Glycera spp. However, the tests on unaffected
(n=3 cores pooled, each 150 mm diameter, 100 mm deep) in each
plot (n=3 plots) species varied in power. For species in which variation
between blocks was high (e.g. E. cordatum), or densities
were very low (e.g. W. assimilis), the power to test for
Discussion treatment effects was low and little weight is given to
these non-significant results. Power analysis indicated
The main effect of both predators was on the commercial that only very large changes in abundance (>592% and
bivalves, Fulvia tenuicostata and Katelysia rhytiphora. 165%) could have been detected with 80% confidence
753
Fig. 4 Ordination (MDS) of treatment plots based: a on abun-
dances of bivalves and echinoids and b on the entire assemblage.
Fig. 3 Length-frequency histograms of Fulvia tenuicostata remain- For both ordinations, plots with added seastars separate clearly
ing at the end of the experiment in: a live treatments (uncaged control, from plots with only added crabs, and both are distinct to plots
cage control and treatments with crabs) and b open treatments (with without added predators. These groupings have been outlined with
seastar+crab and seastar). Unshaded and shaded histograms were ellipses for clarity. The grouping is consistent with the general
significantly different in paired Kolmogorov–Smirnov tests pattern described for the commercial bivalves in the univariate
analysis. Note that the mean number per core in each treatment
plot was used to estimate the number per square meter for taxa
when testing for crab effects on W. assimilis and found in cores for this comparison
E. cordatum, respectively. In contrast, for polychaetes,
there was sufficient power to detect much smaller
changes in abundance (between 9% and 54%) with 80% other species including polychaetes when the bivalve
confidence, which is smaller than changes detected for became rare. While the commercial bivalves were clearly
seastar and crab effects in other experiments (Ross et al. preferred over polychaetes in our short-term experiment,
2002, 2003a; Walton et al. 2002). Thus, for polychaetes had the experiment run longer A. amurensis may
we are confident that they were unaffected by preda- have switched to polychaetes when the bivalves were
tors in this experiment. Importantly, it is also possible exhausted.
that not all direct and indirect effects had occurred
before the termination of the experiment given its
relatively short duration (2 months). It is noteworthy Caging effects
that in a short-term study carried out in the Derwent
Estuary, Asterias fed predominately on F. tenuicostata Caging experiments are recognised as a valuable tool in
after its massive settlement, but shifted to feed on examining the effect of predators on marine communities
754
1995; Morrice 1995; L. Turner, personal communica-
(see Peterson 1979; Thrush 1999); however, the potential
tion). The results of the present experiment are consis-
for cage artefacts to confound true treatment effects is
tent with the hypothesis that predation by A. amurensis
well recognised (e.g. Hulberg and Oliver 1980; Under-
is responsible for the rarity of adult F. tenuicostata and
wood 1986). By undertaking the experiment immediately
K. rhytiphora in the Derwent Estuary. Moreover, in a
beyond the current range of the seastar in a similar but
recent study, the seastar was shown to have a major
unimpacted area, the contrast of open plots with empty
impact on the survivorship of juvenile F. tenuicostata in
cages provides a straightforward test for most cage
the Derwent Estuary, effectively arresting a massive
artefacts. In our experiments, there were no significant
settlement event (Ross et al. 2002).
effects detected in making this comparison. However, it
was not possible to control for cage effects on predator
behaviour, and so we must assume that the cage has not
Impacts of Carcinus maenas
greatly affected the behaviour of the predators. In this
context an important point to emphasise is that both
seastar (Nojima et al. 1986; Grannum et al. 1996; Ling Although there was no significant effect of C. maenas on
2000) and crab (Crothers 1968; Jensen and Jensen 1985; F. tenuicostata in the experiment, the pattern of abun-
McKinnon 1997) densities similar to and substantially dance of live F. tenuicostata and hinges remaining after
higher than those we used in the cages have been predation events are consistent with predation by the
recorded in Tasmania and in their native ranges, and crab. The abundance of F. tenuicostata in the presence of
the crab was $50% lower than in the control treatments.
that these high densities have persisted for periods much
longer than our experimental period. Thus, we suggest it Hinges were far more abundant in the presence of crabs
is reasonable to expect similar effects on native species compared with treatments in which the crab was absent,
should the predators attain the densities used in this indicating that crab predation was largely responsible
experiment. for the differences in densities between treatments.
Furthermore, a comparison of the size frequency of
F. tenuicostata in the cage control and crab treatment
indicates that C. maenas consumed the majority of small
Impacts of Asterias amurensis
bivalves (>25 mm). It is likely that C. maenas is unable
to prey on larger bivalves. Comparable size constraints
In this study, densities of the commercial bivalves were
$80 individuals m)2 lower for Fulvia tenuicostata and have been recorded for similar-sized C. maenas feeding
$5 individuals m)2 lower for Katelysia rhytiphora in the on other cockles, such as Mercenaria mercenaria (Walne
presence of seastars at a density of 1 individual m)2 and Dean 1972), Katelysia rhytiphora (McKinnon 1997;
´
Walton et al. 2002) and Cerastoderma edule (Mascaro
compared with the cage control. Recently opened shells
and Seed 2000). Similarly, size constraints in handling
were far more abundant in the presence of seastars
prey explain the absence of a detectable effect on
compared with the cage control for both bivalve species,
K. rhytiphora, given that the majority of K. rhytiphora in
indicating that seastar predation was largely responsible
this experiment were large (>25 mm).
for the differences in densities between treatments. These
In similar short-term experiments in intertidal soft-
results have been supported from feeding observations
sediment habitats, C. maenas predation was shown to
in non-experimental areas both in the Derwent Estuary
significantly reduce the abundance of the bivalves
and in a recently invaded area outside the estuary, where
Paphies erycinaea, K. rhytiphora and K. scalarina in
aggregations of seastars consumed virtually all the
Tasmania (McKinnon 1997; Walton et al. 2002), and the
F. tenuicostata, as anticipated from this and other
bivalves Nutricola confusa and N. tantilla in California
experiments (Ross et al. 2002, 2003a, 2003b).
(Grosholz and Ruiz 1995). These earlier studies indicate
The results of the present study are consistent with
that predation by C. maenas is likely to impact popula-
observations in the native habitat of the seastar, where it
tions of small bivalves in both intertidal and subtidal
is a major predator of bivalves, including cockles, oys-
soft-sediment habitats where it becomes abundant,
ters, scallops and other clams (Hatanaka and Kosaka
including Tasmania. Although our results did not dem-
1959; Kim 1969; Nojima et al. 1986). In the Derwent
onstrate a significant effect of C. maenas predation, de-
Estuary, Grannum et al. (1996) calculated electivity
spite a large decline in bivalve density, we interpret this as
indices based on field data; they found that A. amurensis
a lack of statistical power due to the relatively high
was highly selective for bivalves and concluded that
variation among plots compared to the previous studies.
predation by A. amurensis posed a serious threat to
many bivalve species, particularly the populations of
Chioneryx striatissima and Venerupis spp., within the
Interactions of A. amurensis and C. maenas
estuary. For many bivalve species such as F. tenuicostata
and K. rhytiphora live large adults are rare in the Der-
The presence of C. maenas appeared to have no effect on
went Estuary, despite the presence in the sediments of
K. rhytiphora predation by A. amurensis. This likely
numerous remains (intact shells) of large individuals.
resulted from an absence of small individuals of this
This is disturbing given the high prevalence of juveniles
bivalve and the inability of C. maenas to consume large
in the sediments and the diet of A. amurensis (Lockhart
755
ones. In contrast, the individual effects of each predator R. Thresher and C. Procter. This work was supported by funds
from the CSIRO Marine Research Centre for Research on
on F. tenuicostata were influenced by the presence of the
Introduced Marine Pests (awarded to C.R.J.) and the School of
other species. Fewer F. tenuicostata were consumed by Zoology, University of Tasmania. This work was undertaken as
C. maenas in the presence of the seastar compared part the senior authorÕs Doctor of Philosophy degree at the
with when it was alone. Although similar numbers of University of Tasmania, who was supported by an Australian
Postgraduate Award. The experiments we performed comply with
F. tenuicostata were consumed by A. amurensis in the
the current laws of Australia, conducted on a permit for intro-
presence of C. maenas compared with when it was alone, duced species research issued under section 14 of the Living
the seastar consumed larger bivalves when the crab was Marine Resources Management Act 1995 in Tasmania.
present. Thus, the interaction between C. maenas and
A. amurensis appears to be direct competition for
resources, resulting in the partitioning of bivalves
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