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ORIGINAL PAPER
Invaders interfere with native parasite–host interactions
David W. Thieltges ÆKarsten Reise Æ
Katrin Prinz ÆK. Thomas Jensen
Received: 15 July 2008 / Accepted: 15 August 2008 / Published online: 28 August 2008
ÓSpringer Science+Business Media B.V. 2008
Abstract The introduction of species is of increas-
ing concern as invaders often reduce the abundance of
native species due to a variety of interactions like
habitat engineering, predation and competition. A
more subtle and not recognized effect of invaders on
their recipient biota is their potential interference with
native parasite–host interactions. Here, we experi-
mentally demonstrate that two invasive molluscan
filter-feeders of European coastal waters interfere
with the transmission of free-living infective trema-
tode larval stages and hereby mitigate the parasite
burden of native mussels (Mytilus edulis). In labora-
tory mesocosm experiments, the presence of Pacific
oysters (Crassostrea gigas) and American slipper
limpets (Crepidula fornicata) reduced the parasite
load in mussels by 65–77% and 89% in single and
mixed species treatments, respectively. Both intro-
duced species acted as decoys for the trematodes thus
reducing the risk of hosts to become infected. This
dilution effect was density-dependent with higher
reductions at higher invader densities. Similar effects
in a field experiment with artificial oyster beds suggest
the observed dilution effect to be relevant in the field.
As parasite infections have detrimental effects on the
mussel hosts, the presence of the two invaders may
elicit a beneficial effect on mussels. Our experiments
indicate that introduced species alter native parasite–
hosts systems thus extending the potential impacts of
invaders beyond the usually perceived mechanisms.
Keywords Introduced species Dilution effect
Parasitism Transmission Trematodes
Cercariae
Introduction
Introduced species are an increasing ecological,
conservational and economic problem in ecosystems
around the world (Pimentel 2002; Olden et al. 2004;
Mooney et al. 2005). By imposing new species
interactions and altering existing ones, introduced
species can affect all levels of ecological organisation:
individuals, populations, communities and ecosystems
(Sax et al. 2005). In addition to direct effects on native
species, indirect effects of introduced species may
occur as well. For example, invaders can co-introduce
parasites, especially ones with simple life cycles,
D. W. Thieltges (&)K. T. Jensen
Marine Ecology, Department of Biological Sciences,
University of Aarhus, Finlandsgade 14, 8200 Aarhus,
Denmark
e-mail: David.Thieltges@otago.ac.nz
Present Address:
D. W. Thieltges
Department of Zoology, University of Otago,
P.O. Box 56, Dunedin 9054, New Zealand
K. Reise K. Prinz
Alfred Wegener Institute for Polar and Marine Research,
Wadden Sea Station Sylt, 25992 List, Germany
123
Biol Invasions (2009) 11:1421–1429
DOI 10.1007/s10530-008-9350-y
which can infect naı
¨ve native hosts (Kennedy 1993;
Torchin et al. 2002; Gozlan et al. 2005; Taraschewski
2006). Much less recognized is that invaders may
also interfere with native parasite–host interactions
although they rarely become infected with native
parasites as these are often host specific (Torchin et al.
2003). Most macroparasites depend on free-living
stages to change their hosts during their life cycles.
These free-living stages are vulnerable to a multitude
of environmental conditions. Besides natural abiotic
factors and anthropogenic pollutants (Pietrock and
Marcogliese 2003) the ambient fauna surrounding
infective stages during the transmission process can
affect the infection success (for review, see Thieltges
et al. 2008a). For example, infective stages may fall
prey to a variety of non-hosts as observed in
schistosome trematodes (Chernin and Perlstein 1971;
Upatham and Sturrock 1973; Christensen et al. 1980).
There is evidence that the effect of such interfering
agents is generally density dependent with strongest
effects at high densities of the interfering organisms
(Thieltges et al. 2008a). Similar dilution effects of
ambient fauna have been found to impair the trans-
mission of infectious diseases with incompetent hosts
distracting infectious stages from the ‘‘real’’ hosts,
thus reducing their infection levels (Ostfeld and
Keesing 2000; Keesing et al. 2006). It is likely that
invaders have their share in dilution effects in native
parasite–hosts systems but so far only limited evi-
dence is available (Bartoli and Boudouresque 1997;
Kopp and Jokela 2007).
In this study, we use two prominent invaders of
coastal waters of the northern East Atlantic to test the
hypothesis that invaders can interfere with native
parasite–hosts systems. In the northern part of their
European range, the Pacific oyster (Crassostrea gigas)
and the American slipper limpet (Crepidula fornicata)
became established mainly on native intertidal blue
mussel (Mytilus edulis) beds, and recently proliferated
in the wake of climate change (Thieltges et al. 2003;
Diederich et al. 2005; Nehls et al. 2006). Oysters as
well as slipper limpets not only attach to blue mussel
shells but also occur on their own forming aggregates
besides the mussels (Fig. 1). Slipper limpets assemble
in stacks of several individuals sitting on top of each
other, and oyster larvae preferentially settle upon
oysters. Populations of both invaders are known to be
little or not infected at all by macroparasites (Aguirre-
Macedo and Kennedy 1999; Pechenik et al. 2001;
Thieltges et al. 2004). In contrast, blue mussels are
heavily parasitized by metacercarial stages of dige-
nean trematodes species which use the mussels as their
second intermediate host, with Himasthla elongata
being one of the dominant species (Buck et al. 2005).
This parasite uses the common periwinkle (Littorina
littorea) as first intermediate host and birds as final
hosts. The infective larval stages (cercariae) shed from
the snail hosts enter the mantle cavity of bivalves
through the inhalant current. Inside the mantle cavity
they penetrate the foot of the host and encyst as
metacercariae. Both invaders are not infected by
H. elongata (Thieltges et al. 2003; Krakau et al.
2006). Considering the tight species packing on
mussel beds and that the two invaders are potent
filtrators, we expected an interference with the parasite
transmission process from snails to mussels. By
inhaling cercariae oysters and limpets should reduce
the flux of cercariae to mussels. If this actually
happens, not only consequences for native parasite
population dynamics would arise but also for the
native mussel hosts as digenean parasites generally
have detrimental effects on their mussel hosts (Lauck-
ner 1983; Thieltges 2006). Combining experimental
and observational approaches we test (1) whether the
two introduced species interfere with the transmission
of cercariae and thus reduce parasite loads in the
native blue mussels and (2) whether a potential
dilution effect is density dependent, i.e. increasing
with the density of the two invaders.
Fig. 1 Mixed suspension-feeder beds composed of native
mussels (Mytilus edulis), Pacific oysters (Crassostrea gigas)
and stacks of American slipper limpets (Crepidula fornicata),
and grazing periwinkles (Littorina littorea) in close associa-
tion. Sylt island, October 2007
1422 D. W. Thieltges et al.
123
Materials and methods
Laboratory experiments
Cercariae of H. elongata were obtained from L. litto-
rea collected in the vicinity of the Marine Biological
Station of the University of Aarhus (Ronbjerg, Lim-
fjord, Denmark). After collection, the snails were kept
in bowls filled with sea water and exposed to light for
6 h. Snails shedding H. elongata cercariae were
separated and kept in an aerated flow through aquar-
ium. Cercariae for the experiments were obtained by
exposing a pool of 30–50 snails in bowls filled with sea
water under light for a maximum of 3 h (=max age of
cercariae used in our experiments).
Parasite-free (no first intermediate hosts close by
and checked by dissecting 50 mussels) blue mussels
(M. edulis) (50–60 mm) were obtained from long-line
mussel cultures in the Limfjord (provided by the Danish
Shellfishcentre, Nykøbing Mors, Denmark). Oysters
(C. gigas) (60–110 mm) and slipper limpets (C. forni-
cata) (25–45 mm) were collected by hand in shallow
water (1 m depth) in Klosterfjord, Nykøbing Mors,
Denmark). All organisms were kept in the experimen-
tal set-ups for 1–2 days prior to the experiments. All
experiments were conducted in small mesocosms
consisting of polypropylene buckets (260 9240 mm)
filled with 12 cm of sediment and 6 l of sea water
(salinity approx. 30 psu), and constantly aerated.
In a first experiment we tested whether oysters and
slipper limpets affect parasite loads in mussels using
four treatments: (1) 2 mussels only, (2) 2 mussels plus
4 oysters, (3) 2 mussels plus 16 slipper limpets in 4–5
stacks and (4) 2 mussels plus 2 oysters and 8 slipper
limpets in 2–3 stacks. In addition, we used another
treatment (5) to test whether mussels at high density
also cause a dilution effect by adding 4 mussels to 2
focal mussels. These densities were chosen to roughly
adjust for the differences in filtration rates between the
species according to the literature (1 mussel =1
oyster =4 limpets; Lesser et al. 1992; Ren et al.
2000; Ropert and Goulletquer 2000; Kittner and
Riisga
˚rd 2005). All organisms were randomly placed
in the buckets. Each treatment was replicated four
times in a completely randomized design. Light was
applied from above and water temperature was kept at
room temperature (21°C) during the experiment. To
each treatment, 300 cercariae of H. elongata (counted
under a dissection microscope) were added. After 48 h
all mussels were dissected and the metacercariae of
H. elongata counted using a dissection microscope.
In two additional laboratory experiments we tested
whether the effect of the two invaders on parasite
transmission was density dependent. In both exper-
iments we employed four different treatments. To
investigate the effect of different oyster densities we
added 0, 1, 2 or 3 oysters to 2 mussels in mesocosms
as described above. To investigate the effects of
different slipper limpet densities, we added 0, 5, 10
and 20 slipper limpets to buckets with 2 blue mussels
as described above. In both experiments, all treat-
ments were replicated four times. Duration and
termination procedure for both experiments were
similar to the one described above. The experiments
were conducted at room temperature which resulted
in different water temperatures during the first and
the second experiment (16°C and 19°C, respectively).
Field experiment
To investigate the effect of oyster presence on infection
levels in mussels in the field, we utilized experimental
oyster beds arranged in the lower intertidal zone of
sand flat that were originally constructed for a different
purpose. Rings of 4 m in diameter were constructed by
laying oysters (C. gigas) collected within List tidal
basin (Sylt island, Germany) on the sediment surface
reflecting natural orientation and densities. Rings of
oysters covered 10 m
2
each and enclosed bare sandy
areas of 3 m
2
. Control sites were bare sand, marked as
rings by shells of razor clams stuck into the sediment.
Five rings were constructed per treatment. Mussels
(M. edulis) (15–20 mm) from an uninfected popula-
tion (no first intermediate hosts close by and checked
by dissecting 50 mussels) at the exposed surf zone of
the island were enclosed in meshed bags (15 915 cm)
made of polypropylene with a mesh size of 5 mm. In
each bag, we placed 10 mussels and randomly fixed
one bag on each ring with rods. The experiment started
at the beginning of August and was terminated in mid-
October 2006. Five mussels from each bag were
dissected and the number of metacercariae determined
under a dissection microscope.
Field survey
On mussel beds in the low intertidal zone alongside a
tidal channel in the northern part of Sylt island
Invaders interfere with native parasite–host interactions 1423
123
(Munkmarsch, Germany) the density of C. gigas was
assessed during August/September by counting indi-
viduals ([20 mm max. diameter) in random squares of
0.25 m
2
(n=40–90) in 1995 and 2001–2002 and of
0.04 m
2
(n=30–90) in 2003–2007. Also at the
northern part of Sylt island, eight sites with mussel
beds around spring low tide line were assessed for the
density of C. fornicata by counting individuals
([7 mm max. diameter) on random squares of
0.25 m
2
(n=10–76) in August/September 2000 and
of 0.04 m
2
(n=10) in July 2006.
Statistical analysis
Differences in the no. of metacercariae recovered in the
mussels in the lab experiments were tested with one-
way ANOVA after ln-transformation of the data to
meet the requirements of homogeneity of variance.
Post-hoc comparisons were done with Tukey’s HSD
test (Day and Quinn 1989). For graphical representa-
tions, we calculated recovery rates, being the
proportion of added cercariae recovered as metacer-
cariae in the blue mussels. Differences in parasite loads
in mussels from the field experiment and from the field
survey were tested with t-tests after ln-transformation
of the data to meet the requirement of homogeneity of
variance. In the field experiment, the mean number of
metacercariae per mussels was calculated for each bag
and the values used for further analysis.
Results
Both introduced species strongly reduced the infection
success of cercariae in the blue mussels (M. edulis)in
the lab (ANOVA; F
4,15
=18.1, P\0.001; Table 1);
(Fig. 2). When oysters (C. gigas) or slipper limpets
(C. fornicata) were present, parasite load in the
mussels was 4.5 or 2.8 times lower compared to the
control, respectively. Mussels added to the two focal
mussels had a similar dilution effect with the mussels
harbouring 3.4 times less metacercariae compared to
the control. The dilution effect was strongest in the
mixed oyster and slipper limpet treatment, where
recovery rate was 9.3 times lower than in the control
and 2.7 times lower than in the ‘‘mussels ?mussels’’
treatment (Fig. 2; Table 1).
In both density experiments, parasite load in the
blue mussels decreased with increasing densities of the
introduced species. The number of oysters present in
the mesocosms significantly affected parasite load in
the blue mussels (ANOVA; F
3,12
=28.5, P\0.001)
(Fig. 3). Mussel kept together with a single oyster
acquired already only a third of the numbers of
metacercariae recovered in mussels kept alone at the
end of the experiment. The number of slipper limpets in
the mesocosms also had a significant effect on parasite
loads in mussels (ANOVA; F
3,12
=23.8, P\0.001)
(Fig. 4). Adding five limpets already approximately
halved the parasite load in the mussels.
When the recovery of cercariae in the three
experiments is plotted for each diluting species
(mussels, oysters, limpets) against filtration rates
(transformed into mussel units), recovery declines
exponentially with the potential filtration rate (Fig. 5).
It appears that oysters and limpets have very strong
impacts on cercarial transmission and that their effect
exceeds what could be explained by their potential
filtration rates. In contrast, mussels exhibit a similar
Table 1 Results of post-host tests (Tukey’s HSD) from the
ANOVA analysis of the effects of different organisms added to
mesocosms including two focal mussels (Mytilus edulis).
n=4 replicates each
Control Mussels Oysters Limpets
Mussels 0.0048
Oysters 0.0007 0.7909
Limpets 0.0131 0.9840 0.4931
Oysters and limpets 0.0002 0.0248 0.1877 0.0091
0
10
20
30
40
50
Mussels
only
Mussels +
mussels
Mussels +
oysters
Mussels +
limpets
Mussels +
oysters +
limpets
Recovery (%)
Fig. 2 Percentage recovery (±SD) of added cercariae (as
metacercariae) in mussels (Mytilus edulis) kept alone (mussels
only) and mussels kept with mussels (mussels ?mussels),
oysters (Crassostrea gigas) (mussels ?oysters), slipper lim-
pets (Crepidula fornicata) (mussels ?limpets) and a mix of
mussels and oysters (mussels ?oysters ?limpets) in labora-
tory experiments. n=4
1424 D. W. Thieltges et al.
123
dilution effect as expected from their filtration rates
(Fig. 5). It is possible that some additional density-
dependent effects have impact, though it is important
to stress that the graphs are based on potential rates and
not measurements of actual rates. Differences in water
temperature and species interactions could also be
influential. Nonetheless, our data corroborate the
hypothesis that non-host filtrators may have a negative
effect on transmission of H. elongata to its second
intermediate host through their filtration capacity.
That this also happens in the field is suggested by the
results from the field experiment. Infection levels of
H. elongata in blue mussels were more than three
times lower inside the artificial oyster reef (5.4 ±1.6
metacercariae/mussel) compared to bare sand
(1.6 ±1.3; t-test; F
1,8
=17.0, P\0.01).
After deliberate introduction in 1986 in the north-
ern part of Sylt island, C. gigas was first encountered
on a mussel bed outside an oyster farm in 1991. It
slowly spread and gained in density until 2001 when
regular recruitment commenced, and finally densities
exceeding those of the mussels were attained in 2007
(Fig.6). In the same region, C. fornicata was intro-
duced around 1930, remained at low abundance for
long but then we encountered on mussel beds an
eightfold increase in density between 2000 and 2006
(Fig. 6).
Discussion
Both invaders interfered with cercarial transmission
and reduced parasite loads in the native mussels. A
similar dilution effect could be observed when con-
specific native mussels were added to the mescosoms,
although the effect of the two invaders appeared to be
stronger when compared to mussel filtration rates.
Such a protective effect of con-specifics has also been
investigated in other bivalves and can be ascribed to
the fact that the pool of infective cercarial stages is
spread over the entire host population resulting in
lower infection levels in individual hosts at high
population densities (Mouritsen et al. 2003; Thieltges
and Reise 2007). The two invaders add an additional
dilution effect to the system and thus alter the native
0
2
4
6
8
10
12
0123
No. oysters added
Recovery (%)
Fig. 3 Percentage recovery (±SD) of added cercariae (as
metacercariae) in mussels (Mytilus edulis) kept alone (0) and
kept with increasing numbers of oysters (Crassostrea gigas) (1,
2, 3) in laboratory experiments. n=4
0
10
20
30
40
0 5 10 20
No. limpets added
Recovery (%)
Fig. 4 Percentage recovery (±SD) of added cercariae (as
metacercariae) in mussels (Mytilus edulis) kept alone (0) and
kept with increasing numbers of slipper limpets (Crepidula
fornicata) (5, 10, 20) in laboratory experiments. n=4
0
25
50
75
100
012345678
Filtration capacity in mussel units
Recovery relative to control (%)
Oysters
Limpets
Mussels
Expected dilution
Fig. 5 Percentage recovery of added cercariae (as metacerca-
riae) in mussels relative to the controls in relation of the
filtration capacity of the two invaders and the native mussels
based on potential filtration capacities taken from the literature.
Mussels in the first experiment show a similar exponential
decline (black line, y=183.5 e
-0.3035x
,R
2
=1.0) as expected
from their filtration capacity (grey line, y=141.4 e
-0.2228x
,
R
2
=0.96). Oysters (black long-dashed line, y=267595.3
e
-0.888x
,R
2
=0.94) and slipper limpets (black short-dashed
line, y=267.9 e
-0.5514x
,R
2
=0.99) from the subsequent
density experiments show stronger effects on recovery as
expected from their filtration capacity in mussel units
Invaders interfere with native parasite–host interactions 1425
123
parasite–host interactions. Our lab experiments
showed that the strength of the invader dilution
effect increases with increasing invader density. Any
increase in invader density on the native mussel beds
should thus decrease the parasite burden in the
mussels. That this effect is probably of increasing
relevance in the field is indicated by the strong recent
increase in invader density on the native mussel beds.
Despite this dramatic increase, there is currently no
evidence for competitive exclusion of the native
mussels and both invaders are so far additions to
native mussel beds rather than replacing those (Nehls
et al. 2006). Hence, the current scenario in the field is
similar to our density experiments where increasing
invader densities decreased parasite load in native
mussels when those were kept at constant density.
Unfortunately, long-term data on parasitism on the
local mussel beds are not available and hence we
cannot correlate invader density with parasite load in
the native mussels. Future studies will be valuable in
investigating the long-term effects of the two invad-
ers on parasite loads in the native mussels.
The dilution effect caused by the two invaders has
two important implications. First, the presence of the
two invaders releases the native mussel hosts from
parasite burden. This can be considered to be
beneficial for the mussels as metacercarial infections
have detrimental effects on their hosts. For example,
in mussels they cause reduced growth (Thieltges
2006) and they cause interference with the mussels’
byssus thread production, imposing mussels to the
risk of dislodgment from the bed structure (Lauckner
1983). As the effects of metacercarial infections are
generally density dependent (Fredensborg et al. 2004;
Thieltges 2006), any reduction of parasite load is of
benefit for the hosts. It is an interesting question to
what extent the positive dilution effect of the two
invaders counterbalances potential negative effects
like trophic and interference competition (Diederich
2005; Thieltges 2005). This aspect may deserve more
studies. Second, the dilution effect caused by the two
invaders may also have important long-term conse-
quences for the native parasites, because the dilution
effects may also be regarded as enhanced cercarial
mortality excerted by the invaders. No development
into metacercariae was observed in the invaders and
hence transmission into the final host is blocked. As
transmission between first and second intermediate
hosts is a crucial step in trematode life cycles, failures
of infection may not only affect the population in the
second intermediate host but also in the final hosts. In
the long run, the two invaders may thus decrease the
population size of native parasites not only in the
mussels but subsequently also in the final bird hosts
and in the first intermediate gastropod hosts. It will be
interesting to monitor infection levels of the native
parasites on the mussel beds. We envision a scenario
with a high share of invaders unsuitable as hosts for
trematodes, less native trematodes in mussels, and
this contributes to a higher fitness in the remainder of
the mussels.
Why the two invaders have the observed effect on
H. elongata cercariae is not established. The strong
reduction of the combined treatment of oysters and
slipper limpets which differed from the single treat-
ments suggests that both species are not entirely
complimentary in their effects and the underlying
mechanisms. As the typical second intermediate hosts
for H. elongata (Lauckner 1983) are bivalves, it is not
surprising that we did not find their cysts in slipper
limpets. However, slipper limpets seem to attract
cercariae which were observed to attempt penetrating
the mantle tissue without being successful. They
0
500
1000
1500
2000
1995 2001 2002 2003 2004 2005 2006 2007
No. oysters m-2
0
400
800
1200
1600
2000
2400
60020002
No. slipper limpets m-2
Fig. 6 Abundances (m
-2
) of invading American slipper
limpets Crepidula fornicata (±SD) (above) and Pacific oysters
Crassostrea gigas (below) on mussel beds at low tide line
along the island of Sylt in the North Sea
1426 D. W. Thieltges et al.
123
provoked a response reaction as the slipper limpets
started to withdraw their mantle slightly near the
attack point. Cercariae engaged in such behaviour may
lose energy and be unable to infect mussels at a later
stage. In addition, slipper limpets have an efficient
filter feeding apparatus utilizing a mucus net for
trapping particles (Newell and Kofoed 1977). Cerca-
riae might be trapped and immobilized in the net after
being inhaled by the gastropods. This may not only
extract cercariae from the ambient environment but
also prevent infection of the slipper limpets them-
selves which do not seem to become infected by
trematodes at all (Pechenik et al. 2001; Thieltges et al.
2003). In oysters, the situation is different. Oysters do
not have a foot which is the preferred infection site of
H. elongata in its hosts (Lauckner 1983). This may
explain why they are free of H. elongata infections in
the field (Krakau et al. 2006). Nonetheless, cercariae
enter the oysters via the filtration current. To what
extent cercariae represent a food resource to these non-
host filtrators is presently unknown. Although it
remains to be investigated, it is likely that both
invaders are also capable of interfering with the
transmission of other trematode parasites, given the
rather unspecific mechanisms behind their dilution
effects.
Interestingly, even in the control treatments not all
cercariae added to the mesocosms were recovered.
The pumping capacity of our experimental animals
means that the water (6 l) in each mesocosm
potentially could have passed our organisms several
times during 1 day. Assuming a pumping rate of
6lh
-1
mussel
-1
(Kittner and Riisga
˚rd 2005), the
whole water body could have circulated through the
mussels approximately two times per hour in the
control mussels. Considering that H. elongata will be
infective for a little less than 20 h (at 20°C; own obs.)
there should be a high encounter rate. However, the
maximum recovery rate was only around 35% (the
differences in recovery rates in controls result from
the strong temperature dependence of infection
processes (Thieltges and Rick 2006)). Observational
studies have indicated that host individuals may
manage to reject approaching cercariae and even
remove cercariae attempting to penetrate the foot
(Jensen et al. 1999; Wegeberg et al. 1999). For this
reason, not all cercariae may manage to complete
their mission within time. The two invaders also have
high pumping rates (Lesser et al. 1992; Ren et al.
2000; Ropert and Goulletquer 2000) and thus the
water in each experimental unit probably passed
through the filtrators many times during the experi-
mental period in the lab. However, this is not an
unrealistic scenario in the field. Oysters, slipper
limpets and mussels are tightly connected to each
other in situ (Fig. 1) and during short intervals of
stagnant water they may re-filtrate the same water
body several times. Our results from the field
experiment and field survey suggest that this actually
happens in the field. However, infection levels during
the time of our experiments were unusually low and
hence making the detection of the effect difficult.
The present study demonstrates that two invaders
occurring in the vicinity of a native parasite–host
system can have a strong impact on parasite transmis-
sion and parasite burden in the native hosts. However,
the observed dilution effect is not confined to invaders
but also occurs in native species that do not serve as
hosts themselves. In marine systems, native non-host
anemones, crabs, shrimps and bivalves have been
reported to cause reductions in parasite loads of native
bivalves by preying on the infective cercarial stages
(Mouritsen and Poulin 2003; Thieltges et al. 2008b).
In freshwater systems, several studies have shown that
free-living infective trematode stages are subject to
predation by various organisms associated with the
cercariae shedding host snails (Chernin and Perlstein
1971; Upatham and Sturrock 1973; Christensen et al.
1980). As many parasite–host systems are imbedded
in complex ambient communities, interference from
co-occurring organisms on parasite transmission is
probably a general phenomenon (Morley and Lewis
2004; Thieltges et al. 2008a). However, potential
dilution effects caused by invaders have—with a few
exceptions—largely been neglected. Bartoli and Bou-
douresque (1997) suggested that the invasive alga
Caulerpa taxifolia causes lower parasite infection
levels in fish at invaded sites compared to non-invaded
control sites. This is assumed to result from cercari-
cidal toxins that are released by the algae. Another
laboratory study showed that a resistant non-native
host was shown to cause a reduction of trematode
parasite infection levels in the native first intermediate
snail host, probably by attracting parasite eggs which
failed to infect the new hosts (Kopp and Jokela 2007).
Together with the few available studies our study
indicates that invaders may play an important role in
native parasite–host interactions. Hence, the complex
Invaders interfere with native parasite–host interactions 1427
123
impacts of invaders in their recipient biota may extend
beyond the usually well recognized effects of preda-
tion and competition and may explain the prevailing
pattern of coexistence between invaders and natives.
Acknowledgements We wish to thank Maria Donas-Bo
ˆtto
Bordalo and Alejandro Caballero Herna
´ndez for help with the
experiments. For help with the ring experiment at Sylt we
thank Christian Buschbaum, Patrick Polte and Nils
Volkenborn. This work was supported by a fellowship to
DWT within the Postdoc-Programme of the German Academic
Exchange Service (DAAD).
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