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The introduction of species is of increasing 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 experimentally demonstrate that two invasive molluscan filter-feeders of European coastal waters interfere with the transmission of free-living infective trematode larval stages and hereby mitigate the parasite burden of native mussels (Mytilus edulis). In laboratory 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 introduced 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.
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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
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,
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
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.
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
˚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
each and enclosed bare sandy
areas of 3 m
. 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
(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
(n=40–90) in 1995 and 2001–2002 and of
0.04 m
(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
(n=10–76) in August/September 2000 and
of 0.04 m
(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.
Both introduced species strongly reduced the infection
success of cercariae in the blue mussels (M. edulis)in
the lab (ANOVA; F
=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
=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
=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
Mussels +
Mussels +
Mussels +
Mussels +
oysters +
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.
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
=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).
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
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 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
Filtration capacity in mussel units
Recovery relative to control (%)
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
=1.0) as expected
from their filtration capacity (grey line, y=141.4 e
=0.96). Oysters (black long-dashed line, y=267595.3
=0.94) and slipper limpets (black short-dashed
line, y=267.9 e
=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
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
1995 2001 2002 2003 2004 2005 2006 2007
No. oysters m-2
No. slipper limpets m-2
Fig. 6 Abundances (m
) 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.
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
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
(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
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
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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Invaders interfere with native parasite–host interactions 1429
... If a non-competent host invades a community of competent, native hosts then there is potential for a dilution effect that could have significant consequences for native symbiont populations and communities (Creed et al., 2022;Kopp & Jokela, 2007;Thieltges et al., 2009). If native symbionts frequently encounter these non-competent hosts when dispersing from one host to another, then there is an increased probability that these symbionts will be lost from the community. ...
... Over time, symbiont abundance and diversity on native hosts is predicted to decline as the non-competent host will function as a sink for native symbionts. Dilution effects are considered positive effects of increased host diversity with respect to parasite and disease transmission and could result in the decline of native parasites and pathogens (Johnson et al., 2013;Keesing et al., 2006;Kopp & Jokela, 2007;Thieltges et al., 2009). However, host dilution will also lead to declines in both mutualist and commensal symbionts. ...
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Symbionts, including parasites, pathogens and mutualists, can play important roles in determining whether or not invasions by host species will be successful. Loss of enemies from the native habitat, such as parasites and pathogens, can allow for higher invader fitness in the invaded habitat. The presence of mutualists (e.g., pollinators, seed dispersers, mycorrhizae and rhizobial bacteria) in the invaded habitat can facilitate invasion success. While there has been a great deal of research focusing on how invading hosts may benefit from enemy losses or mutualist gains, far less attention has focused on how native symbiont populations and communities respond to invasion by non‐indigenous hosts and symbionts. In this paper, we present a conceptual framework examining how symbionts such as parasites, pathogens, commensals and mutualists can influence invader success and whether these native symbionts will benefit or decline during invasion. The first major factor in this framework is the competence of the invading host relative to the native hosts. Low‐ or non‐competent hosts that support few if any native symbionts could cause declines in native symbiont taxa. Competent invading hosts could potentially support native parasites, pathogens, commensals and mutualists, especially if there is a closely related or similar host in the invaded range. These symbionts could inhibit or facilitate invasion or have no discernable effect on the invading host. An understanding of how native symbionts interact with competent vs non‐competent invading hosts as well as various invading symbionts is critical to our understanding of invasion success, its consequences for invaded communities and how native symbionts in these communities will fare in the face of invasion.
... 2). This probability is based on the biogeographic dissimilarity between the 149 receiving and donor communities, and is assumed to increase sigmoidally with the geographic 150 distance dij between sites i and j (Thieltges et al. 2009). ...
... INNS can also affect native host-pathogen relationships, altering population dynamics and disease transmission. Thieltges et al. (2008) demonstrated that the presence of invasive Crepidula fornicata and Crassostrea gigas significantly reduced the trematode parasite burden of native Mytilis edulis, by interfering with the transmission of freeliving infective trematode larval stages and therefore reducing infection of M. edulis. Host-pathogen ecosystem interactions prove complex, creating challenges for the prediction of invasion success at different locations. ...
Invasive Non-Native Species (INNS) can co-transport externally and internally other organisms including viruses, bacteria and other eukaryotes (including metazoan parasites), collectively referred to as the symbiome. These symbiotic organisms include pathogens, a small minority of which are subject to surveillance and regulatory control, but most of which are currently unscrutinised and/or unknown. The (putatively) pathogenic symbionts co-transported by an INNS host may be latent or associated with asymptomatic infection and unable to cause disease in the INNS, but may be opportunistic pathogens of other hosts, causing impact to one or more hosts in their new range. These pathogens potentially pose diverse risks to other species, with implications for increased epidemiological risk to agriculture and aquaculture, wildlife/ecosystems, and human health (zoonotic diseases). Aquatic INNS and their symbionts have many introduction pathways, including commodity and trade (releases, escapes, contaminant), transport (stowaway), and dispersal (corridor, unaided). The risks and impacts arising from co-transported pathogens, including other symbionts of unknown pathogenic virulence, remain largely unexplored, unlegislated, and difficult to identify and quantify. Here, we propose a workflow to determine any known and potential pathogens of aquatic INNS. This workflow acts as a prerequisite for assessing the nature and risk posed by co-transported symbionts of INNS. A better understanding of co-transported organisms, the risks they pose and their impact, is necessary to inform policy and INNS risk assessments. This leap in evidence will be instrumental to devise an appropriate set of statutory responsibilities with respect to these symbionts, and to underpin new and more effective legislative processes relating to the disease screening and risk assessment of INNS.
... Invasive species can also become in fected by resident parasites, amplifying existing endemic diseases in other hosts. Finally, invasive species can dilute the native parasite populations (termed parasite dilution) by acting as sinks, and thereby reduce the risk of infection for the natural hosts (Thieltges et al. 2009, Poulin et al. 2011, Goedknegt et al. 2016. ...
Two populations of the invasive slipper limpet Crepidula fornicata were sampled in Swansea Bay and Milford Haven, Wales, U.K., to determine the presence of putative pathogens and parasites known to affect co-located commercially important shellfish (e.g., oysters). A multi-resource screen, including molecular and histological diagnoses were used to assess 1,800 individuals over 12 months for microparasites, notably haplosporidians, microsporidians, and paramyxids. Although initial PCR-based methods suggested the presence of these microparasites, there was no evidence of infection when assessed histologically, or when all PCR amplicons (n = 294) were sequenced. Whole tissue histology of 305 individuals revealed turbellarians in the lumen of the alimentary canal, in addition to unusual cells of unknown origin in the epithelial lining. In total, 6% of C. fornicata screened histologically harboured turbellarians, and ~33% contained the abnormal cells – so named due to their altered cytoplasm and condensed chromatin. A small number of limpets (~1%) also had pathologies in the digestive gland including tubule necrosis, haemocytic infiltration and sloughed cells in the tubule lumen. Overall, these data suggest that C. fornicata are not susceptible to substantive infections by microparasites outside of their native range, which may contribute in part to their invasion success.
... Causes for this parasite release are small founder populations of hosts as well as the requirement of a specific sequence of hosts by these parasites (Torchin et al. 2003;Goedknegt et al. 2016). On the other hand, introduced suspension feeders may intercept parasite transmissions to resident hosts (Thieltges et al. 2009). In an experiment, American slipper limpets and Pacific oysters consumed trematode cercariae which otherwise would have infected resident mussels. ...
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For about a century, biodiversity in the tidal Wadden Sea (North Sea, European Atlantic) has increased by more than one hundred introduced species from overseas. Most originate from warmer waters and could facilitate the transformation of this coastal ecosystem to comply with climate warming. Some introduced species promote sediment stabilization and mud accretion. This could help tidal flats to keep up with sea level rise. Although some introduced species also entail negative effects, introductions have diversified lower food web levels, and may benefit foraging birds. So far, no resident populations have gone extinct because an introduced species had established. Rather than degrading the ecosystem, the establishment of introduced species seems to have raised the capacity to follow environmental change. We support increasing efforts against introductions to avoid risk. However, once species are integrated, the common condemnation attitude against “non-natives” or “aliens” ought to be reconsidered for tidal ecosystems of low biodiversity.
... Following host establishment, a series of possible changes to host−parasite communities could theoretically occur (Thieltges et al. 2009, Goedknegt et al. 2017). One scenario is that an introduced host leaves behind its parasites ('parasite escape'), providing the non-native host with possible fitness benefits and competitive advantages over native competitors ('parasite release') (Torchin et al. 2001, 2002, Ross et al. 2010. ...
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Biological invasions influence species interactions around the globe, including host and parasite communities. We evaluated trematode parasite diversity and the potential for host-switching of parasites in 3 co-occurring crabs in the Northeast USA, including 1 native species (Cancer irroratus) and 2 non-natives (Carcinus maenas , Hemigrapsus sanguineus) , of which the former represents a historical and the latter a contemporary invader. At 7 sites from Maine to Rhode Island, we surveyed crabs for trematode infection prevalence and abundance, and the influence of parasitism on host body condition. We also conducted DNA sequencing using the 18S rRNA barcoding marker to determine species composition, diversity, and gene flow of trematode lineages among the co-occurring hosts. While the native host, C. irroratus , and the historical invader, C. maenas , exhibited no statistical difference in trematode prevalence, we found that C. maenas had a greater abundance of metacercarial cysts than the other 2 hosts, and the contemporary invader, H. sanguineus , was rarely infected. Crab condition did not vary with infection abundance, although infected females of all species had higher reproductive investment than other groups. Genetic analyses revealed that the microphallid trematodes consisted of 3 main clades, representing over 50 haplotypes, with evidence of host-switching by native parasites utilizing the non-native hosts. Given the importance of crustaceans to parasite life cycles, the introduction of novel hosts to these systems alters both free-living and host-parasite community interactions and could ultimately affect community structure and function. Future studies should continue to investigate host-parasite diversity and demographics following invasions to better understand impacts on native marine communities.
... Infection intensities, on the other hand, always remained higher in oysters, suggesting that an increasing number of mussels got infected from oyster reservoir hosts where high infection intensities produced a large number of infective offspring with higher transmission probability ( Figure 5). Furthermore, dilution effects, i.e. the loss of infective stages by ending up in the wrong host species (Thieltges et al., 2008), are asymmetric between both Mytilicola species and their hosts . The lower transmissibility of M. orientalis originating from mussels can be considered as a minor dilution for M. orientalis epidemiology. ...
Full-text available
In species introductions, non-native species are often confronted with new niches occupied by more specialized natives, and for introduced parasites this conflict can be amplified because they also face novel hosts. Despite these obstacles, invasions of introduced parasites occur frequently, but the mechanisms that facilitate parasite invasion success are only rarely explored. Here, we investigated how the parasitic copepod Mytilicola orientalis, that recently spilled over from its principal host - the Pacific oyster Crassostrea gigas, managed to invade the niche of blue mussel Mytilus edulis intestines, which is densely occupied by its specialist congener, Mytilicola intestinalis. From field observations demonstrating invasion dynamics in nature, we designed a series of experiments addressing potential mechanisms facilitating a successful occupation of the new niche. As expected the specialist M. intestinalis can only infect mussel hosts, but displayed higher infection success there than M. orientalis in both principal host species combined. In the absence of direct competitive interactions M. orientalis compensated its lower infection success (1) by recurrent spill-over from its high-fitness reservoir oyster host, and (2) by active aggregation interference enhancing its own mating success while limiting that of M. intestinalis. The introduced parasite could thus avoid direct competition by changing its own epidemiology and indirectly decreasing the reproductive success of its competitor in the new host. Such mechanisms outside of direct competition have seldom been considered, but are crucial to understand invasion success, parasite host range and community assembly in the context of species introductions.
... This predation effect can strongly influence parasite population dynamics by interfering with transmission pathways because parasites are removed from the system preventing successful host infection. This process has been termed the 'dilution effect', and can result in a reduced infection risk in host species populations (Keesing et al., 2006;Prinz et al., 2009;Thieltges et al., 2009;Johnson & Thieltges, 2010;Goedknegt et al., 2016). In marine systems, dilution effects have been intensively investigated in trematode parasites. ...
Full-text available
The introduction of Pacific oysters to the sedimentary south-eastern North Sea coast and their establishment on intertidal native blue mussel beds has caused the development of mixed reefs of mussels and oysters with extensive tidepools. Tidepools have been intensively studied at rocky shores where they show community structures, which usually differ from that of the surrounding emerging substrates. Tidepools at sedimentary coasts, however, have received less attention. We compared the community structure and species interactions inside and outside tidepools in oyster reefs by determining densities of snails, barnacles and amphipods. Snail densities were similar in and outside tidepools. Barnacle coverage on bivalve shells, however, was lower inside tidepools, which may be caused by higher predation pressure and increased snail grazing under permanently submerged conditions, as was revealed by field and laboratory experiments. Additionally, we studied the occurrence of copepod and trematode parasites in blue mussels inside and outside tidepools. Prevalence and intensity of parasitic copepods was higher in mussels inside tidepools. Trematode parasites, by contrast, showed a lower intensity in mussels inside tidepools. This can be explained by high amphipod densities found inside tidepools because trematode larvae represent a food source of amphipods. Our study suggests that the community structure of oyster reefs within tidepools is not a submerged equivalent to that of intertidal reefs. As their counterparts at rocky shores, they show their own species distribution patterns with particular species interactions and only provide refuge for specific species such as parasitic copepods.
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Cryptic species of coquina clams Donax fossor and D. variabilis carry the hydroid epibiont Lovenella gracilis and are infected with metacercariae of the monorchiid parasites Lasiotocus trachinoti and L. choanura . The associations among this host–epibiont–parasite system were investigated. Fifty clams were collected at low tide over 3 days in June 2020 in South Carolina from each of three groups: clams with no hydroid from the upper intertidal zone and clams with and without hydroids from the swash zone. Clams were measured, identified using a newly developed PCR‐RFLP, and examined for infection by metacercariae. Parasites were identified based on cercarial morphology and on metacercariae habitat in the clams. D. fossor was most often found in the swash zone and D. variabilis in the upper intertidal zone. The hydroid was most often associated with D. fossor , which was more infected by both digeneans than D. variabilis . Mean abundance of metacercariae of L. choanura was higher than that of L. trachinoti in both clams and increased over time for both parasites, because higher infection was correlated with larger clams. Greater time spent in the water by individuals of D. fossor appears to best explain these results, with the presence of the hydroids also being associated with higher infection by metacercariae in this coquina. Integration of D. variabilis in both digenean life cycles appears to lead to a positive outcome for the parasites as prevalence and abundance of infection were high; however, because D. variabilis is most frequent in the upper intertidal, more emersed, zone, it is likely deleterious to the epibiont to establish on this clam.
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Given their sheer cumulative biomass and ubiquitous presence, parasites are increasingly recognized as essential components of most food webs. Beyond their influence as consumers of host tissue, many parasites also have free-living infectious stages that may be ingested by non-host organisms, with implications for energy and nutrient transfer, as well as for pathogen transmission and infectious disease dynamics. This has been particularly well-documented for the cercaria free-living stage of digenean trematode parasites within the Phylum Platyhelminthes. Here, we aim to synthesize the current state of knowledge regarding cercariae consumption by examining: (a) approaches for studying cercariae consumption; (b) the range of consumers and trematode prey documented thus far; (c) factors influencing the likelihood of cercariae consumption; (d) consequences of cercariae consumption for individual predators (e.g. their viability as a food source); and (e) implications of cercariae consumption for entire communities and ecosystems (e.g. transmission, nutrient cycling and influences on other prey). We detected 121 unique consumer-by-cercaria combinations that spanned 60 species of consumer and 35 trematode species. Meaningful reductions in transmission were seen for 31 of 36 combinations that considered this; however, separate studies with the same cercaria and consumer sometimes showed different results. Along with addressing knowledge gaps and suggesting future research directions, we highlight how the conceptual and empirical approaches discussed here for consumption of cercariae are relevant for the infectious stages of other parasites and pathogens, illustrating the use of cercariae as a model system to help advance our knowledge regarding the general importance of parasite consumption.
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Utilitarian arguments concerning the value of biodiversity often include the benefits of animals, plants, and microbes as sources of medicines and as laboratory models of disease. The concept that species diversity per se may influence risk of exposure to disease has not been well developed, however. We present a conceptual model of how high species richness and evenness in communities of terrestrial vertebrates may reduce risk of exposure to Lyme disease, a spirochetal ( Borrelia burgdorferi) disease transmitted by ixodid tick vectors. Many ticks never become infected because some hosts are highly inefficient at transmitting spirochete infections to feeding ticks. In North America, the most competent reservoir host for the Lyme disease agent is the white-footed mouse ( Peromyscus leucopus), a species that is widespread and locally abundant. We suggest that increases in species diversity within host communities may dilute the power of white-footed mice to infect ticks by causing more ticks to feed on inefficient disease reservoirs. High species diversity therefore is expected to result in lower prevalence of infection in ticks and consequently in lower risk of human exposure to Lyme disease. Analyses of states and multistate regions along the east coast of the United States demonstrated significant negative correlations between species richness of terrestrial small mammals (orders Rodentia, Insectivora, and Lagomorpha), a key group of hosts for ticks, and per capita numbers of reported Lyme disease cases, which supports our “dilution effect” hypothesis. We contrasted these findings to what might be expected when vectors acquire disease agents efficiently from many hosts, in which case infection prevalence of ticks may increase with increasing diversity hosts. A positive correlation between per capita Lyme disease cases and species richness of ground-dwelling birds supported this hypothesis, which we call the “rescue effect.” The reservoir competence of hosts within vertebrate communities and the degree of specialization by ticks on particular hosts will strongly influence the relationship between species diversity and the risk of exposure to the many vector-borne diseases that plague humans. Resumen: Argumentos utilitarios relacionados con el valor de la biodiversidad frecuentemente incluyen los beneficios de animales, plantas y microbios como recursos para medicinas y como modelos de enfermedades en laboratorio. Sin embargo, la idea de que la diversidad de especies por sí misma puede influenciar el riesgo de exposición a enfermedades no ha sido bien desarrollada. Presentamos un modelo conceptual de cómo la riqueza de especies y la uniformidad en comunidades de vertebrados terrestres puede reducir el riesgo de exposición a la enfermedad de Lyme, una enfermedad causada por una espiroqueta ( Borrelia burgdorferi) y transmitida por una garrapata ixódida. Muchas garrapatas nunca son infectadas debido a que los huéspedes son altamente ineficientes en la transmisión de espiroquetas a las garrapatas que se alimentan de ellos. En Norte América, el huésped reservorio más competente del agente de la enfermedad de Lyme es el ratón de patas blancas ( Peromyscus leucopus), una especie de amplia dispersión y localmente abundante. Sugerimos que los incrementos en la diversidad de especies dentro de las comunidades de huéspedes pueden diluir el potencial de infección de las garrapatas por el ratón de patas blancas al ocasionar que más garrapatas se alimenten de reservorios ineficientes en la transmisión de la enfermedad. Por lo tanto, se esperaría que una alta diversidad de especies resulte en una prevalencia de infección de garrapatas reducida y, por lo tanto, en una disminución del riesgo de exposición de humanos a la enfermedad de Lyme. Un análisis por estado y de varios estados a lo largo de la costa este de los Estados Unidos demostró correlaciones significativamente negativas entre la riqueza de especies de mamíferos terrestres pequeños (órdenes Rodentia, Insectivora, y Lagomorfa), un grupo clave de huéspedes para garrapatas, y los números per capita de casos de la enfermedad de Lyme reportados, lo cual apoya nuestra hipótesis de efecto de dilución. Contrastamos estos resultados con lo que se podría esperar cuando los vectores adquieren eficientemente agentes de la enfermedad de muchos huéspedes, caso en el cual, una alta diversidad causaría la prevalencia de infección de garrapatas permaneciendo alta aún cuando la diversidad de huéspedes disminuyera. Una correlación positiva entre los casos de la enfermedad de Lyme per capita y la riqueza de especies de aves residentes del suelo apoya esta hipótesis, que hemos llamado efecto de rescate. La capacidad de reservorio de huéspedes dentro de las comunidades de vertebrados y el grado de especialización de las garrapatas en huéspedes particulares, influenciaría fuertemente la relación entre la diversidad de especies y el riesgo de exposición a muchas de las enfermedades transmitidas por vectores que infectan a humanos.
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The filtration rate of Mytilus edulis as a function of acute change in temperature was measured by means of the clearance method in a group of mussels seasonally acclimated to 18 degrees C. This was done by stepwise changes in temperature in order to both determine the temperature-tolerance interval within which the mussels were fully open, and to ensure that the acute effects were reversible. The filtration rate (F, ml min(-1) ind.(-1)) as a function of temperature (T, degrees C) could be expressed by a regression line with the equation: F = 3.27 T + 38.2 in the temperature-tolerance interval between 8.3 and 20 degrees C. A reduction in temperature to below 8.3 degrees C initiated valve closure, and at 6.1 degrees C all mussels were completely closed, The same group of mussels was then acclimated to 11 degrees C over a period of 5 d before the measurements were repeated, and the filtration rate as a function of temperature was subsequently found to be: F = 3.27 T + 38.1 in the temperature-tolerance interval which had extended down to 4.1.degrees C. Next, a group of mussels seasonally acclimated to about 15 degrees C was split up into 3 subgroups which were exposed to 10.2, 15.6 and 20.3 degrees C over the following 23 d. During the acclimation period, the filtration rate of fully open mussels was measured every 3 to 4 d in the 3 groups. Because none of the slopes of the 3 regression lines appreciably differed from 0, it is concluded that the acute effect of a change in temperature is not modified in M. edulis over a 3 wk acclimation period; i.e., there is no evidence for temperature compensation.
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Worldwide introductions of species have raised concern about ecological and economic impacts. However, research on actual impacts of introduced species on native biota is rare. The American slipper limpet Crepidula fornicata (L.) was unintentionally introduced to Europe in the 1870s with oysters imported for farming purposes. Since C. fornicata is a filter-feeder, trophic competition and associated negative effects when epizootic on bivalves have been assumed. This study is the first to experimentally test in the field effects of the epizootic C. fornicata on survival and growth of its major basibiont in northern Europe, the blue mussel Mytilus edulis L. In 2 field experiments of 12 wk each, epigrowth by C. fornicata resulted in a 4- to 8-fold reduction in survival of mussels, equivalent to a mortality of 28 and 30%, respectively. Shell growth in surviving mussels with attached C. fornicata was 3 to 5 times lower compared to unfouled mussels, but similar to that with artificial limpets. As a causative agent, interference competition in the form of changes in small-scale hydrodynamics due to C. fornicata stacks is suggested. This may result in a high energy expenditure for byssus production of mussels. Trophic exploitation competition does not seem to be relevant. In general, interference and not exploitation competition is suggested to be the major impact of epizootic C. fornicata on its basibionts in Europe. However, the generality of this assumption has to be verified by investigating different C. fornicata-basibiont associations. This stresses the need for a species-by-species approach under diverse environmental settings in assessing impacts of introduced species. In the case of M edulis, this study shows that C. fornicata has the potential to act as an important mortality factor.
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The recently introduced invasive tropical seaweed Caulerpa taxifolia has by now invaded large areas of the western Mediterranean coast between Nice (France) and Imperia (Italy). The labrid fish Symphodus ocellatus, which usually inhabits Posidonia oceanica meadows or lives among photophilic algae growing on rocky substrates, is also present in areas which are thickly covered with C. taxifolia. This fish is territorial and sedentary, and its life span is never more than 3 yr. Since C, taxifolia has been present since 1987 in the areas studied, the S, ocellatus individuals living there can be assumed to have probably spent their whole post-larval Lives in the vicinity of the seaweed. At the colonized sites, the invertebrate benthic prey of S. ocellatus have undergone both quantitative and qualitative changes. The effects of these changes on the transmission of parasites were studied using the digeneans of the digestive tract of S. ocellatus as a model. At the control sites, 6 digenean species were identified: Helicometra fasciata, Macvicaria alacris, Proctoeces maculatus, Holorchis pycnoporus, Lecithaster stellatus and Genitocotyle mediterranea (cumulative prevalence of all species = 46.3%; cumulative abundance of all species = 0.95). At the sites colonized by C. taxifolia, only 2 digenean species were present: H, fasciata and L. stellatus (cumulative prevalence = 1.5%; cumulative abundance = 0.02). Among the possible reasons explaining the nearly complete absence of digeneans parasitizing S. ocellatus, the rarefaction of intermediate hosts in the invaded areas can probably be ruled out, at least in the case of 2 digenean species. Secondary metabolites (caulerpenyne and other terpenes) synthesized by C, taxifolia, and then released into the environment or transmmitted along the food web, might be responsible for the near-complete disappearance of the digeneans of S. ocellatus.
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The clearance rate of natural planktonic assemblages was measured for the blue mussel Mytilus edulis (L.) and a co-occurring fouling community from mussel rope cultures using flow cytometry. Blue mussels had significantly higher clearance rates for all particle types and size classes. In addition, blue mussels showed selective feeding in favor of small phytoplankton (3–5 μm), whereas the solitary ascidian Ciona intestinalis (L.) and the suspension-feeding gastropod Crepidula fornicata (L.) showed preferential selection for large phytoplankton (> 16 μm). Clearance rates for large phytoplankton by these members of the fouling community were, however, always lower than blue mussels. Under conditions where food is not a limiting factor, interspecific competition for food by the associated fouling community should not significantly limit the yield of mussels.
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Trematode parasites can affect the molluscan hosts serving as first intermediate hosts in their complex life-cycles in manifold ways, but little is known about trematode-induced effects in second intermediate mollusc hosts. In 2 field experiments in 2 habitats and at 2 tidal heights (low and mid intertidal), controlled infection of blue mussels Mytilus edulis serving as second intermediate hosts for larval stages (metacercariae) of the trematode Renicola roscovita resulted in significant lower growth of parasitized compared to non-parasitized individuals. However, tidal height had a stronger effect on mussel growth than parasitism, without any interaction between the 2 factors. The negative effect of R. roscovita metacercarial infections on mussel growth is thought to result from direct tissue disruptions, interference of metacercariae (located in palps and visceral mass) with food intake ability, and growth of metacercarial cysts within the host. Mussel growth was negatively correlated with the number of metacercariae, but this relation was significant only at the mid and not at the low intertidal sites. This may indicate that parasites act as background stressors that affect their hosts depending on additional environmental stress such as (e.g.) food shortage, desiccation and heat, which all increase with the increasing aerial exposure. The results of this study show that trematode infections can be an important determinant of bivalve growth, with potential economic implications for mussel cultivation.
Most parasites are disseminated by movements of infected hosts. The increasing extent and rapidity of anthropochore fish movements are causing increased concern related to awareness of their potential and known capacity for disseminating parasites. This paper puts these data in perspective by examining examples of actual and potential translocations of fish helminths and crustaceans by anthropochore movements of fish into and throughout the British Isles, and by distinguishing the processes of dissemination and invasiveness from those of colonization and establishment. An investigation of the British fish and helminth parasite fauna suggests that: (1) the range of many species is not well known, many are local in distribution and appearances beyond the range may reflect detection and patchiness, not translocation; (2) taxonomic problems in many groups hinder detection and determination of range; (3) most parasites possess the attributes of good colonizers so the natural expansion and contraction of ranges are often not noticed or recognized as such and the importance of parasite introductions by natural movements of fish or avian hosts is generally underestimated; (4) invasions are far commoner than colonizations, since conditions for establishment may be very restricted and transmission windows very narrow in time and space; (5) successful colonizations and translocations tend to be documented and attract attention whereas invasions resulting in failed colonizations are seldom observed and more seldom documented, thus biasing our perception. Given the extensive history of fish introductions to, and translocations within, the British Isles it is surprising how few fish helminths and crustaceans have invaded the country successfully (16 species: 11·4%) and how many still show restricted distributions. The majority (68·7%) of introduced helminths are associated with fish having ornamental varieties. Barriers of colonization are more effective than those to invasion and it is clear that most translocations and invasions fail. It is right to be concerned about the dangers, but it is also important to put anthropochore factors in perspective.
Pacific oysters (Crassostrea gigas Thunberg 1793) have been introduced into the Wadden Sea (North Sea), where they settle on native mussel beds (Mytilus edulis L.), which represent the only extensive insular hard substrata in this soft-sediment environment. As abundances of C. gigas rose, some mussel beds became increasingly overgrown with oysters, whereas others did not. Field experiments revealed that recruitment of C. gigas was higher in the lower intertidal than in the upper subtidal zone, that it was higher on conspecifics than on mussels, and that it was not affected by barnacle epigrowth except when settling on mussels. Mussel recruitment is known from inter- and subtidal zones. It occurred equally on oyster and mussel shells but showed a clear preference for barnacle epigrowth over clean shells. Assuming that settlement and recruitment are key processes for species abundances on the North Sea coast, it is predicted that the positive feedback in oyster settlement will lead to rapid reef formation of this invader at the expense of mussel beds. Mussels, however, may escape competitive exclusion by settling between or on the larger oysters especially when barnacles are abundant. Experimental patches with mussels were more often covered by fucoid algae (Fucus vesiculosus forma mytili Nienburg) than patches with oysters, and oyster recruitment was poor underneath such algal canopies. Thus, fucoids may provide the native mussels with a refuge from the invading oysters and the two bivalves may coexist, provided food is not limiting.
To understand prevalence patterns of parasites in marine host populations experimental infection studies are required. Bivalves are important host organisms to a variety of trematodes species and in our study area (Wadden Sea) three different Himasthla species co-occur in cockle populations. These species are morphologically very similar but differ with respect to various morphometric dimensions. To study the possible functional importance of differences between Himasthla cercariae (the free-living stage shed from prosobranch snails and encysting as metacercariae in bivalves), we experimentally measured the infectivity of the three congeners in regard to different size groups of juvenile cockles. The smallest species, H. interrupta, has a high infectivity in small cockles (optimum around 4 mm), whereas the two other congeners H. continua and H. elongata exhibit low infection efficiencies in cockles less than 6 mm and higher efficiencies in larger cockles. Behavioural experiments were performed to identify proximate causes underlying the observed infection patterns. Parasite avoidance behaviour of the cockle varies in a host–parasite size-dependent manner so that a large cercaria tend to provoke an avoidance response in a small cockle. The possible consequences of the observed host size preferences in relation to definitive host species (waterbirds) are discussed and it is suggested that one or more of the parasite species are adapted to other host species and that their sympatric occurrence in cockles in our study area is a result of a spinoff from their main cycle mediated through migratory birds.
Pacific oysters (Crassostrea gigas) were fed a mixed diet of algae and silt over a range of concentrations from 0.8 to 637 mg l-1, and an organic content ranging from 0.7% to 78%. These data were used to parameterise a set of functions describing the physiological response of oysters in varying environmental conditions. All parameters were standardised to body length. There was greater variation of size specific clearance rate (CR) standardised into dry tissue weight than length. CR increased hyperbolically with temperature with a maximum rate (0.24 l h-1 cm-1) at 20.7 oC, but further increase in temperature resulted in a negative effect on CR. Most feeding experiments were carried out at 10-13 oC, except for the measurements of temperature effect. CR consistently decreases with high seston concentration, which was modelled as a function of pumping rate of water and extraction efficiency of particles from water. The filtration rate was found to be a Type 2 hyperbolic function of seston concentration with the range tested. Ingestion rate was described as a function of food quantity, quality and selective ingestion on organic particles. A positive effect of organic content on absorption efficiency was found only at very low organic content of less than 5%, while above this level, absorption efficiency was constant at 86%. Oxygen consumption rate had an allometric relationship to body size and increased over the range of experimental temperatures.