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Impact of the invasive parasitic copepod Mytilicola orientalis on native blue mussels Mytilus edulis in the western European Wadden Sea

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Invasive species can indirectly affect native species by modifying parasite–host dynamics and disease occurrence. This scenario applies to European coastal waters where the invasive Pacific oyster (Magallana gigas) co-introduced the parasitic copepod Mytilicola orientalis that spills over to native blue mussels (Mytilus edulis) and other native bivalves. In this study, we investigated the impact of M. orientalis infections on blue mussels by conducting laboratory experiments using controlled infections with larval stages of the parasitic copepod. As the impact of infections is likely to depend on the mussels’ food availability, we also tested whether potential adverse effects of infection on mussels intensify under low food conditions. Blue mussels that were experimentally infected with juvenile M. orientalis had a significantly lower body condition (11–13%) compared with uninfected mussels after nine weeks of infection. However, naturally infected mussels from a mixed mussel and oyster bed did not significantly differ in body condition compared with uninfected mussels. Contrary to effects on mussel condition, we did not find an effect of experimental infections on clearance rates, shell growth or survival of blue mussels and no clear sign of exacerbating effects of food limitation. Our study illustrates that invasive species can indirectly affect native species via parasite co-introductions and parasite spillover. The results of this study call for the integration of such parasite-mediated indirect effects of invasions in impact assessments of invasive species.
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Impact of the invasive parasitic copepod Mytilicola
orientalis on native blue mussels Mytilus edulis in
the western European Wadden Sea
M. Anouk Goedknegt, Sarah Bedolfe, Jan Drent, Jaap van der Meer & David
W. Thieltges
To cite this article: M. Anouk Goedknegt, Sarah Bedolfe, Jan Drent, Jaap van der Meer & David
W. Thieltges (2018): Impact of the invasive parasitic copepod Mytilicola orientalis on native blue
mussels Mytilus edulis in the western European Wadden Sea, Marine Biology Research, DOI:
10.1080/17451000.2018.1442579
To link to this article: https://doi.org/10.1080/17451000.2018.1442579
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ORIGINAL ARTICLE
Impact of the invasive parasitic copepod Mytilicola orientalis on native blue
mussels Mytilus edulis in the western European Wadden Sea
M. Anouk Goedknegt , Sarah Bedolfe, Jan Drent , Jaap van der Meer and David W. Thieltges
Department of Coastal Systems, NIOZ Royal Netherlands Institute for Sea Research, and Utrecht University, P.O. Box 59, 1790 AB Den Burg,
The Netherlands
ABSTRACT
Invasive species can indirectly affect native species by modifying parasitehost dynamics and
disease occurrence. This scenario applies to European coastal waters where the invasive
Pacific oyster (Magallana gigas) co-introduced the parasitic copepod Mytilicola orientalis that
spills over to native blue mussels (Mytilus edulis) and other native bivalves. In this study, we
investigated the impact of M. orientalis infections on blue mussels by conducting laboratory
experiments using controlled infections with larval stages of the parasitic copepod. As the
impact of infections is likely to depend on the musselsfood availability, we also tested
whether potential adverse effects of infection on mussels intensify under low food
conditions. Blue mussels that were experimentally infected with juvenile M. orientalis had a
significantly lower body condition (1113%) compared with uninfected mussels after nine
weeks of infection. However, naturally infected mussels from a mixed mussel and oyster bed
did not significantly differ in body condition compared with uninfected mussels. Contrary to
effects on mussel condition, we did not find an effect of experimental infections on
clearance rates, shell growth or survival of blue mussels and no clear sign of exacerbating
effects of food limitation. Our study illustrates that invasive species can indirectly affect
native species via parasite co-introductions and parasite spillover. The results of this study
call for the integration of such parasite-mediated indirect effects of invasions in impact
assessments of invasive species.
ARTICLE HISTORY
Received 18 December 2016
Accepted 14 February 2018
SUBJECT EDITOR
Roy Kropp
KEYWORDS
Invasive species; parasite co-
introduction; parasite
spillover; controlled
infections; Pacific oyster;
Magallana gigas
Introduction
Invasive species affect native species, communities and
ecosystems worldwide (Davies 2009; McGeoch et al.
2010; Lockwood et al. 2013), often directly via preda-
tion and competition (Parker et al. 1999; Simberloff
et al. 2013). However, invasive species can also exert
indirect effects, for example by changing habitat struc-
ture or modifying parasitehost dynamics. Parasite-
mediated indirect effects of invasive species can take
place via several mechanisms, including the co-intro-
duction of a parasite with an invasive host species
(parasite co-introduction; Lymbery et al. 2014). Conse-
quently, in the invaded range, a co-introduced parasite
might spill over from its invasive host to novel native
host species (parasite spillover; Prenter et al. 2004;
Kelly et al. 2009). Such parasite spillover events also
occur in marine ecosystems and can lead to emerging
diseases and subsequent mass mortalities of native
hosts with, in several cases, knock-on effects on
native communities and ecosystems (Goedknegt et al.
2016).
Parasite co-introduction and spillover have also
occurred with the introduction of the Pacific oyster,
Magallana (previously Crassostrea)gigas (Thunberg,
1793) to European coastal waters for aquaculture pur-
poses (Troost 2010). With the initial oyster imports in
the 1960s and 70s, the intestinal parasitic copepod
Mytilicola orientalis Mori, 1935 was co-introduced to
Europe (His 1977). The parasites native range is in Japa-
nese waters, and it has a direct life cycle with a free-
living larval dispersal stage, after which it resides in
the digestive tract of molluscs (Mori 1935). After its
co-introduction to Europe, the parasite spread first via
its principal host, the Pacific oyster, but was later
additionally found in wild native blue mussels (Mytilus
edulis Linnaeus, 1758), common cockles (Cerastoderma
edule (Linnaeus, 1758)), Baltic tellins (Limecola (formerly
Macoma)balthica (Linnaeus, 1758)) and European flat
oysters (Ostrea edulis Linnaeus, 1758), indicating
© 2018 Informa UK Limited, trading as Taylor & Francis Group
CONTACT M. Anouk Goedknegt Anouk.Goedknegt@nioz.nl Department of Coastal Systems, NIOZ Royal Netherlands Institute for Sea Research, and
Utrecht University, P.O. Box 59, Den Burg Texel 1790 AB, The Netherlands
Supplemental data for this article can be accessed https://doi.org/10.1080/17451000.2018.1442579. The underlying research materials for this article can
be accessed at https://doi.org/10.4121/uuid:7a4d46a5-048d-4ecc-a8c7-2de3b78d122e
MARINE BIOLOGY RESEARCH, 2018
https://doi.org/10.1080/17451000.2018.1442579
Published online 29 Mar 2018
several spillover events (His 1977; Stock 1993; Pogoda
et al. 2012; Goedknegt et al. 2017a). In particular,
native blue mussels are increasingly serving as new
hosts, with infection prevalences being similar to or
even exceeding those in Pacific oysters in some areas
(Pogoda et al. 2012; Goedknegt et al. 2017a). Native
blue mussels are also infected by Mytilicola intestinalis
Steuer, 1902, a related parasite species described
from the Mediterranean Sea (Steuer 1902), which has
a similar direct life cycle to M. orientalis (Caspers
1939; Grainger 1951; Dethlefsen 1985; Gee and Davey
1986), and was first found in the Wadden Sea in 1938
(Caspers 1939). Mytilicola intestinalis became infamous
as the red worm disease, because it was thought to
be the causative agent of mass mortalities of blue
mussels in the North Sea in the 1950s and 60s (Korringa
1968; Blateau et al. 1992). However, so far experimental
evidence to support this hypothesis is scarce. Histori-
cally, especially juvenile stages of M. intestinalis were
held responsible for mortalities of mussels (Korringa
1950; Dethlefsen 1985) because of their presence in
the ramifications of the digestive gland (Campbell
1970). In addition, the energy demand of young infec-
tive stages is expected to be high after exploiting their
egg yolk, the only food source available during the
pelagic larval phase (Grainger 1951). This increases
the chance for mussels to be negatively affected by
juvenile parasites. For mature M. intestinalis, lethal and
sublethal effects on important host fitness components
such as body condition, filtration rate and reproduction
do not seem to be unidirectional and have been contro-
versially discussed (Lauckner 1983). Only recently, con-
trolled infection experiments have been conducted
with M. intestinalis and blue mussels, in which a
reduction in blue mussel dry weight was found as a
result of infection by the parasite in sympatric para-
sitehost populations (Feis et al. 2016). Similarly,
although M. orientalis is generally considered a serious
pest (Holmes and Minchin 1995) and is registered on
the list of 100 worst invaders of the Mediterranean
Sea (Streftaris and Zenetos 2012), studies on its lethal
and sublethal effects on M. gigas (Katkansky et al.
1967; Deslous-Paoli 1981; De Grave et al. 1995;Steele
and Mulcahy 2001)andOstrea lurida Carpenter, 1864
(Odlaug 1946) have been inconclusive and they have
generally lacked an experimental approach. The
effects of M. orientalis on its new host, the blue
mussel, have not been studied to date. A potential
effect of M. orientalis on native blue mussels is likely to
be modified by environmental factors and species inter-
actions (Hepper 1953; Campbell 1970; Lauckner 1983;
Troost 2010). For example, seasonal cycles, extreme
temperatures and inter- and intraspecific competition
may lead to food limiting conditions that can either alle-
viate or intensify the adverse effects of infection by the
parasitic copepod. Along these lines, Moore et al. (1977)
postulated that M. intestinalis actually lives in a com-
mensal relationship with their host, but that this
relationship can turn into a negative interaction in
times of serious food limitation. However, experimental
evidence for an augmented effect of Mytilicola spp.
infections on hosts at low food levels is lacking.
In this study, we investigated the effects of
M. orientalis infection on the native blue mussel
M. edulis by conducting two laboratory experiments
that used controlled infections of mussels with larval
stages of the copepod.Following the hypothesis of
Moore et al. (1977), we also tested whether the poten-
tial adverse effects of infection on survival, clearance
rate, body condition and shell growth of blue mussels
intensified under low food conditions. In addition, we
collected mussels in the field to determine natural
infection levels and to investigate the effect of Mytili-
cola infections on mussel body condition in a natural
environment. This combination of lab and field investi-
gations allowed us to assess the impact of the spillover
of the invasive parasite M. orientalis from invasive
Pacific oysters on native blue mussels.
Materials and methods
Field survey
To determine the natural prevalence (the proportion of
infected individuals) and mean infection intensity
(mean number of parasites in infected mussels) of Myti-
licola orientalis in blue mussels (Mytilus edulis) in the
wild, we collected 30 mussels of 3050 mm length
from a mixed bed of Pacific oysters (Magallana gigas)
and blue mussels located on the Vlakte van Kerken, a
tidal flat on the east coast of the island of Texel
(Figure 1) in the western European Wadden Sea
(southern North Sea) on 11 June 2014. Additionally,
we collected from this bed another 39 mussels (34
54 mm) to analyse the effect of infection status
(infected/uninfected) on mussel body condition.
Experimental infections
Uninfected mussels (3035 mm; n= 150) for the exper-
iments were haphazardly collected from basalt groynes
on the north-west shore of the Dutch mainland (Julia-
nadorp, Figure 1) on 11 September 2014. Previous
explorations by M. A. Goedknegt had shown that Myti-
licola spp. does not occur at this location, which was
verified by haphazardly sampling and screening 30
2M. A. GOEDKNEGT ET AL.
additional mussels, which were all found to be free of
infection. Any epifauna (mostly barnacles) on the
mussels was carefully removed from the shells to
ensure that copepod larvae could infect mussels
without being eaten or physically obstructed during
experimental infections (Johnson and Thieltges 2010).
Until the infection procedure, collected mussels were
maintained in 75-l flow-through tanks at 18°C under a
24-hour light cycle (12 h light and 12 h dark) and fed
three times per week with fresh Isochrysis galbana
Parke, 1949 culture, or alternatively with Phyto-Feast®
when fresh culture was unavailable (on average once
a week).
To acquire a source for M. orientalis larvae, mussels (n
= 140) were haphazardly collected from a mixed bed
with known Mytilicola infections located on a tidal flat
on the east coast of the island of Texel (Figure 1)on
22 August 2014. Within two days of collection, mussels
were dissected and gravid M. orientalis females
extracted, which were identified and distinguished
from M. intestinalis based on descriptions of Mori
(1935) and Elsner et al. (2011). The egg sacs were separ-
ated from the female and placed in individual petri
dishes (Ø 60 mm) filled with seawater. They were incu-
bated at approximately 30°C to expedite the larval
development time (based on results of a pilot study)
and were monitored daily. Larval stages were identified
based on descriptions of M. intestinalis larvae by Gee and
Davey (1986). When larvae had developed into the infec-
tive copepod I stage (Gee and Davey 1986), uninfected
mussels (n= 74) were exposed to the larvae.
Before exposure to infective larvae, the shell length
(maximum anteroposterior axis) of each mussel was
measured with callipers to the nearest mm. Because
of variation in larval hatching and development time,
insufficient larvae were available to infect all mussels
at once, ultimately resulting in two temporal exper-
iments with infected mussels. Individual mussels in
the first experiment (n= 34 mussels) were exposed to
parasites in a 100-ml cup and after 24 h, mussels and
filtered seawater were transferred to a 1000-ml con-
tainer for the following eight weeks of the experiment.
For individual mussels in the second experiment (n=
30), exposure was carried out directly in the 1000-ml
container, where they remained for the entire nine
weeks of this study.
Exposure of mussels to infective larvae was done by
carefully pipetting (200-μl pipette) 25 larvae from the
Petri dish (by the use of a stereo microscope) and
depositing them into the container with an uninfected
mussel and filtered seawater. To promote filtration and
uptake of infective larvae, small amounts of algal
culture (I. galbana) were added to the seawater
during exposure of mussels of the second experiment.
Five extra mussels for each of the two experiments
were artificially infected and sacrificed for examination
of larval development at mid-way points during the
experiments. Control (uninfected) mussels (Experiment
1: n= 34, Experiment 2: n= 30) were treated identically
to exposed mussels within each experiment (including
the transfer of filtered seawater and addition of small
amounts of algal culture) but without the addition of
copepodites.
Experimental set-up
The experiment was set up immediately after exposing
the mussels to the parasite larvae, which was for the
first experiment on 10 September 2014 and the
second experiment on 7 October 2014. The experiment
was run in a two-factorial design with M. orientalis
infection (infected/uninfected) and food level (high/
low) as fixed factors and set up in blocks of four
1000-ml containers each containing one individual
mussel. Thus, each block contained a replicate of the
following treatments: uninfected mussel low food
level, infected mussel low food level, uninfected
mussel high food level, and infected mussel high
food level. The first experiment contained 17 of these
replicated blocks (n= 68 mussels in total), while the
second experiment contained 15 replicated blocks (n
= 60 mussels in total). The containers were kept in a
climate-controlled room at 18°C and seawater was
replaced weekly. All mussels were fed three times per
week, with mussels in the high food treatment receiv-
ing 50 ml algae mixture and mussels in the low food
Figure 1. Sampling locations of wild blue mussels (Mytilus
edulis) (squares; n= 30 and n= 39), blue mussels as a source
for gravid Mytilicola orientalis females (circles; n= 140) and
naturally uninfected blue mussels (triangles; n= 150).
MARINE BIOLOGY RESEARCH 3
treatment receiving half that quantity. When fresh
algae culture was unavailable, on average once per
week, 0.1 ml of PhytoFeast® per mussel was provided
in the high food treatment, while 0.05 ml was provided
to mussels in the low food treatment. Only fresh algal
culture was provided on days when clearance rates
were measured.
After dissections at the end of the experiment, we
found that some experimental blocks contained
mussels with failed infections (exposed to larvae but
not found to be infected at the end of the experiment),
or unanticipated infections (found to be infected
despite not having been exposed to larvae). In these
cases, affected blocks were excluded from the analysis
to preserve a balanced design with a complete dataset.
In the first experiment, four mussels (out of 34 mussels
exposed to larvae) remained uninfected and one
mussel was unintentionally infected, while in the
second experiment infection success was lower and
seven (out of 30) mussels were uninfected. After
removing all blocks with failed and unanticipated infec-
tions, 12 blocks were left for the first experiment (n=48
mussels) and 10 blocks for the second experiment (n=
40 mussels).
Measurement of clearance rate, body condition
and shell growth
Clearance rate
We conducted the first clearance rate measurements of
the mussels of the first experiment one week after
exposure to M. orientalis larvae, while the clearance
rate of mussels of the second experiment was measured
immediately (one day) after exposure. We continued to
measure the clearance rate of each mussel once per
week, to assess if and when larval maturation affected
the clearance rate of mussels.
Clearance rate was assessed by means of the indirect
clearance method (Riisgård 2001;Petersenetal.2004).
One day prior to the measurement, all containers were
refreshed with filtered seawater and mussels were
checked for survival (severely gaping mussels in smelly
water were assigned as dead). In the morning before
the test, we made dilutions of live algal (I. galbana)
culture and analysed its density using a CASY® Cell
Counter and Analyser System Model TT (Schärfe
System GmbH). The algal dilutions were calibrated to
Relative Fluorescence Units (RFU) using a Trilogy® Lab-
oratory Fluorometer (Turner Designs), which allowed
us to measure a large number of samples in a short
period of time. Fluorometer measurements required
1.5 ml of water that we obtained from each experimen-
tal container with a 2-ml pipette.
We measured background fluorescence levels (RFU)
immediately before the test and created a calibration
curve to calculate the amount of algal culture needed
to create an initial starting concentration of 13 × 10
3
14 × 10
3
algal cells per ml in each experimental con-
tainer. This level was chosen to avoid very high or
very low algal densities, which are known to hamper fil-
tration by mussels (Clausen and Riisgård 1996) and
because it falls in the middle of the range in which
mussel filtration rate is independent of food density
(Riisgård and Randløv 1981). Algal culture of the calcu-
lated quantity was added once to all experimental con-
tainers and fluorescence was measured immediately
after addition (t
0
) and again after one (t
1
) and two
hours (t
2
). The measured RFU values at these measure-
ment intervals were corrected for background fluor-
escence after which these values were transformed to
number of algal cells by the use of the calibration
curve. Subsequently, the decrease in algal cells over
two hours was estimated by calculating the slope of
the regression line of the ln-transformed cell numbers
as a function of time (in min; after Stier et al. 2015).
Finally, to assess the clearance rate in ml min
1
we mul-
tiplied the slope of each individual regression by
1000, to account for the 1000 ml volume of water in
which the mussels were kept during the measure-
ments. Some mussels did not filter at all during the
measurements and therefore a separate category (suc-
cessful filtration: yes/no) was used as a random effect in
the clearance rate mixed model to take this variation
into account.
Body condition and shell growth
The experiments ran for eight (Experiment 1) and nine
weeks (Experiment 2) and immediately after termin-
ation of the experiments all mussels were measured,
screened for presence of M. orientalis larvae, frozen,
freeze-dried and weighed to assess body condition.
We separated the shells from the mussel tissue and
extracted adult copepods from the intestines. Larvae
were left in the tissue, as these were too small to
handle without disturbing the mussel flesh. Mussel
tissue was compressed between glass slides and exam-
ined under a stereo microscope (magnification 10
80×) to account for all parasitic copepods, including
larvae and juveniles (Gee and Davey 1986). We then
carefully removed the mussel tissue from the plates,
deposited it in glass vials, froze (20°C for at least 24
hours) and freeze-dried it (48 hours) to ultimately
measure the dry weight of the tissue. Condition index
was determined as CI = DW L
3
, where DW is the dry
weight (mg) of the tissue and L is the final shell
length (cm, after Petersen et al. 2004). At termination
4M. A. GOEDKNEGT ET AL.
of the experiment, the length of each individual mussel
shell was measured to the nearest mm with callipers.
Shell growth was then calculated by extracting initial
length from the final length of each mussel.
Statistical analysis
All statistical analyses were performed using the stat-
istical software environment R (R Development Core
Team 2015) and model assumptions were confirmed
using qq plots and histograms (Zuur et al. 2010).
When data were not normally distributed, we applied
appropriate transformations. Pvalues of < 0.05 were
considered significant.
The condition index of wild mussels was log
10
-trans-
formed, before the difference in naturally infected and
uninfected mussels was analysed with a Studentst-
test. The results of the two laboratory experiments
were analysed separately, but using similar models.
To test for effects of the parasite on clearance rate of
the mussels, we applied a square-root transformation
and used a linear mixed model (lmm; lmer function
from the package lme4; Bates et al. 2015) with infection
status, food level, time, the interaction between these
three variables and experimental block as fixed
factors. Individual mussels and successful filtration
were included as random effects. We used a similar
model to investigate the effect of infection intensity
(number of M. orientalis individuals per infected
mussel) on clearance rate of infected mussels, with
the number of M. orientalis individuals as predictor vari-
able in the model. For all these mixed models, Pvalues
were obtained by comparing the full model (with all
fixed effects) against a reduced model (without the
fixed effect in question) with a likelihood ratio test.
Condition index was log
10
-transformed to improve
normality of the data. To test for effects of the parasites
on the condition of blue mussels, we applied a general
linear model (glm) with infection status, food level,
their interaction and the blocking factor as explanatory
variables. Again, we used a similar model to investigate
the effect of infection intensity on the condition index
of infected mussels, but we replaced infection status
with M. orientalis intensity.
Finally, to test for the effects of the parasite on mussel
shell growth, we first modelled shell growth against
mussel shell length at the start of the experiment with
a linear model. We took the residuals from this model
as a proxy for shell growth (corrected for initial length)
and subsequently used a general linear model to test
for the effects of infection status, food level, their inter-
action, and experimental blocking as explanatory vari-
ables. Finally, we tested the effect of intensity of
infection on (corrected) shell growth of infected
mussels, by using a similar linear model where we
replaced the infection category by numbers of
M. orientalis.
Results
Natural infections
Mytilicola orientalis prevalence in blue mussels (Mytilus
edulis,n= 30, 3050 mm) in a mixed mussel (M. edulis)
and Pacific oyster (Magallana gigas) bed on a tidal flat
on the east coast of Texel was 53% with a mean (± SE)
intensity of 1.8 (± 0.3) individuals per infected host.
From this sample batch, 10 mussels had the same
size class as the mussels used in our experiment (30
35 mm) and this group had a prevalence of 50% and
mean intensity SE) of 3.0 ± 0.7. Naturally infected
mussels (n= 18) tended to have 20% lower condition
indices than uninfected mussels (n= 21), however the
difference was not statistically significant (t= 8.880, P
= 0.068; Figure 2; for raw data see Goedknegt et al.
2018)).
Figure 2. Condition index (log
10
-transformed) of uninfected
blue mussels (Mytilus edulis)(n= 21) and mussels infected
with Mytilicola orientalis (n= 18) collected on a mixed blue
mussel (M. edulis) and Pacific oyster (Magallana gigas) bed
on a tidal flat on the east coast of Texel (Vlakte van Kerken,
Texel, The Netherlands; see Figure 1). The boxes represent
the interquartile range, the whiskers denote the lowest and
highest values within the 1.5 interquartile range, the black
line in each box denotes the median and the black dots rep-
resent the mean condition indices of each group. Note the
truncated y-axis.
MARINE BIOLOGY RESEARCH 5
Success of controlled infections
Hatching success
Dissection of 140 source mussels from a mixed blue
mussel and Pacific oyster bed on the east coast of
Texel (Vlakte van Kerken) produced 60 egg sacs (preva-
lence of gravid females was 43%). The time from egg
sac extraction to hatching of copepod larvae was
highly variable and ranged from immediate hatching
to 8 d after extraction, with an average of 4.4 d. At
early phases the eggs were opaque (Figure 3a), but
when close to hatching, the eggs became transparent
and the red eye spots of the larvae became visible
through the egg case (Figure 3b). All eggs within an
individual egg sac developed at similar rates. The nau-
plius phase (Figure 3c) lasted a maximum of 1 d, and
infective copepodite I larvae (Figure 3d) appeared on
average 4.8 d after egg extraction, though the earliest
larvae metamorphosed within two days. After eight
days, larval survival declined, and the collection
period was terminated. The nauplii were 200220 μm
in length and the copepodite I (infective) stages were
240290 μm long. An average of 50 copepodite
larvae successfully emerged from a single females
egg sac pair, although the maximum recorded was
more than 200 copepodites in a pair. Hatching
success ranged from 0 to 100%, and overall, 26.1% of
the eggs failed to hatch.
Infection success
In the first experiment, mussels had a higher infection
success rate (88%) than in the second experiment
(76%). The maximum number of individual
M. orientalis found in a single mussel was 12. Average
intensities of controlled infections in both experiments
were comparable to those of similar-sized mussels in
the field (mean ± standard deviation, SD; Experiment
1: 3.0 ± 2.4, Experiment 2: 3.5 ± 3.2). Like adults, juvenile
copepods were found in the digestive tract near the
stomach of blue mussels and were approximately
2 mm long at termination of the experiment (Figure
4). Therefore, the copepodites had increased about
10 times in size, growing at a rate of about 30 μm
day
1
after infecting their hosts. As the copepods
were not yet grown to mature size, it was impossible
to determine their sex. The uninfected control
mussels were confirmed to be free of infection,
except for one mussel in the first experiment that
was infected with two adult female M. orientalis.
Effects on mussel clearance rate
No mortality occurred in either infected or uninfected
mussels in either of the two experiments. In both
experiments, 13% of the mussels did not filter during
the experimental period, and non-filtering mussels
occurred across all treatments. We did not find signifi-
cant overall effects of infection status or food limitation
on mussel clearance rates (Supplementary Table SI),
but clearance rate significantly differed over time in
the second (lmm; P= 0.150 * 10
13
;Figure 5b) but
not in the first experiment (P= 0.722; Figure 5a; for
raw data see Goedknegt et al. 2018). This difference
probably results from the relatively high clearance
rates in the first week and relatively lower clearance
rates in week 7 of Experiment 2 in comparison to Exper-
iment 1 (Figure 5). When testing for the effects of
M. orientalis intensity upon infected mussels, we
found no significant results for any of the factors in
the first experiment and no significant interaction
between food level and infection intensity, but a sig-
nificant effect of time (P= 0.261 * 10
6
; Table SI) in
the second experiment.
Effects on mussel body condition
Experimentally infected mussels had significantly lower
body condition indices compared with uninfected
Figure 3. Developmental phases of Mytilicola orientalis: (a) a pair of egg sacs, (b) eggs about to hatch (note the red eye spots), (c)
nauplius and (d) infective copepodite I larva. The white scale bars denote 200 μm.
6M. A. GOEDKNEGT ET AL.
mussels (mean ± standard error, SE: Experiment 1:
infected mussels 0.74 ± 0.03, uninfected mussels 0.81
± 0.01; Experiment 2: infected mussels 0.68 ± 0.02,
uninfected mussels 0.75 ± 0.02; Figure 6; Supplemen-
tary Table SII; for raw data see Goedknegt et al. 2018).
Furthermore, infected mussels kept under low food
levels had the tendency to have lower condition
indices, whereas uninfected mussels had slightly
increased condition indices (Figure 6). However, in
both experiments, the effect of food level and the inter-
action between infection status and food level was not
significant (Table SII).
In additional analyses, where we tested for an effect
of M. orientalis intensity and food limitation on the con-
dition index of infected mussels, we found different
results for both experiments. In the first experiment,
we found a positive relationship between M. orientalis
intensity and body condition of mussels (P= 0.046),
but this result was not significant in the second exper-
iment (Table SII). Additionally, the block factor was sig-
nificant in the first experiment (P= 0.013), but not
Figure 4. Developmental status of Mytilicola orientalis infections in blue mussels (Mytilus edulis) after approximately (a) 5.5 weeks
(scale bar denotes 1000 μm) and (b) 8 weeks (scale bar denotes 500 μm) after exposure to infective larvae.
Figure 5. Mean clearance rate (± SE) of uninfected blue
mussels (Mytilus edulis) (grey) and mussels infected with Myti-
licola orientalis (black) fed under high (circles) and low (tri-
angles) food levels. Clearance rates were measured weekly
after exposure to infective larvae for each of the four treatment
groups in the first (a) and second (b) experiment.
Figure 6. Boxplots of the condition index (log
10
-transformed)
of blue mussels (Mytilus edulis) in the first (a) and second (b)
experiment that were either infected (grey) or uninfected
(white) and kept under high or low food level conditions
during the nine weeks of the experiment. The boxes represent
the interquartile range, the whiskers denote the lowest and
highest values within the 1.5 interquartile range, the black
line in each box denotes the median, the large black dots rep-
resent the mean condition indices of each group and the
smaller dots outside the boxes are outliers. Note the truncated
y-axis.
MARINE BIOLOGY RESEARCH 7
significant in the second experiment (Table SII). Finally,
we did not find any significant effects of food level or
an interaction between intensity and food level in
both experiments (Table SII).
Effects on mussel shell growth
Mean mussel shell growth ± SE was 0.56 ± 0.05 mm in
the first experiment and 0.49 ± 0.07 mm in the second
experiment, which is an average of about 0.01 mm
day
1
. In both experiments, mussel shell growth (cor-
rected for initial shell length) was not significantly
affected by M. orientalis infection status, food level,
the interaction between those variables or the blocking
factor (Supplementary Table SIII; for raw data see Goed-
knegt et al. 2018). Furthermore, among only the
infected mussels we did not detect any significant
effect of infection intensity, food level, an interaction
between those terms or an effect of experimental
blocking on the shell growth of infected mussels in
either experiment (Table SIII).
Discussion
This study experimentally tested for the effects of the
invasive parasitic copepod Mytilicola orientalis (which
has recently spilled over from invasive Pacific oysters
(Magallana gigas)) on native blue mussels (Mytilus
edulis).In laboratory experiments, we found significant
negative effects of infection with (juvenile stages of)
the invasive parasite on the body condition of
mussels, although the feeding, growth and survival
were not affected.
The detrimental effect of early developmental
stages of Mytilicola infection has been previously
suggested for the congeneric M. intestinalis (Korringa
1950; Dethlefsen 1985) because of their presence in
the ramifications of the digestive gland (Campbell
1970). This is the digestive organ in molluscs, and infec-
tions may compromise its functioning. As stable
isotope analyses suggest that Mytilicola feeds on host
tissue (Gresty and Quarmby 1991; Goedknegt et al.
2017b), the energy demand of the growing copepods
can be expected to lead to a significant loss of tissue,
ultimately resulting in a potential lower host condition
(1113% reduction in our experiments). Moreover,
when Mytilicola feeds on host tissue, the resulting
metaplasia of the host gut epithelium (Moore et al.
1977) needs to be repaired, which is an energetically
demanding process for the host and likely to reduce
host condition. When Mytilicola matures, the effects
of the parasite may become less severe as the cope-
pods move away from the digestive gland and
migrate further down the digestive tract (Grainger
1951; Gee and Davey 1986). A decrease in harmfulness
with parasite age may also explain why we did not find
significant difference in condition between infected
and uninfected mussels in the field, as those infections
consisted of a mix of juvenile and adult stages of
M. orientalis. Generally, adverse effects of M. orientalis
on host condition have also been reported for
oysters, Ostrea lurida (Odlaug 1946) and M. gigas (Kat-
kansky et al. 1967) and are known to increase with
infection intensity (Katkansky et al. 1967). Similarly,
for the congeneric species M. intestinalis reductions in
dry weight of its blue mussel host are more severe
when the parasite occurs in higher numbers in sympa-
tric parasitehost populations (Feis et al. 2016).
However, in our experiments we could not find a
general trend of declining mussel condition with
M. orientalis intensity, as the two experiments gave
contrary results in this respect. Nevertheless, the
general negative effect of infections with early stages
of M. orientalis on mussel body condition suggests
that native mussels may experience negative effects
from the spillover of this invasive parasite. The exact
mechanism behind the loss in body condition and
the effect of the parasite on the energy budgets
(lipids/glycogen content) of mussels, are a topic for
future studies.
In contrast to the adverse effects of juvenile
M. orientalis on mussel condition, we found no evi-
dence that M. orientalis infection impacted the clear-
ance rates of mussels. Previous work has observed a
reduced filtration capacity in mussels infected with tre-
matode metacercariae, which encyst in mussel gills and
palps and interfere with filtration (Stier et al. 2015).
However, as Mytilicola resides in the musselsintestines
it may not directly affect gill function in the same way
as trematode metacercariae. Instead, Mytilicola infec-
tions may only indirectly affect filtration by influencing
host energy requirements and expenditure. Alterna-
tively, mussels could intensify their filter activity when
infected with M. orientalis to counterbalance the
higher energy demand caused by the parasite.
However, we did not observe any significant effects
of parasite infection on mussel clearance rates. We
acknowledge that our inference in this respect might
have been hampered due to the variation in clearance
rates we observed over time, especially in the second
experiment. Part of this variation is explained by the
mussels that did not filter during our experiments,
which we therefore included as a random effect in
the model. Overall, observed clearance rates were rela-
tively low and in many cases dropped to less than
10 ml min
1
, which is lower than filtration rates
8M. A. GOEDKNEGT ET AL.
previously reported for mussels under comparable
algal concentrations (Clausen and Riisgård 1996; Stier
et al. 2015). The underlying reasons for these low
values are not known, but may explain the limited
shell growth of all mussels (on average 0.01 mm
day
1
). The absence of any effect of M. orientalis on
mussel shell growth may also be related to the low
growth, but this result also corresponds with observa-
tional studies of Pacific oysters which did not detect
negative effects of infections on growth (Katkansky
et al. 1967; Steele and Mulcahy 2001). Finally, a nega-
tive effect of the parasite on mussel survival could
have been expected given that its congeneric
M. intestinalis has been considered to be the causative
agent of mussel mass mortalities in the past (Korringa
1968; Blateau et al. 1992). However, in our experiments
there was no mortality of mussels among treatments,
illustrating the sub-lethality of the parasite that has
also previously been shown for Pacific oysters (Kat-
kansky et al. 1967).
In contrast to our expectation, we did not find clear
evidence that food shortage exacerbated the effects of
Mytilicola infections at the food levels applied, which
were chosen to lie within the range of concentration
where mussels actually filter. It may well be that
adverse effects of infections under even more
extreme scenarios, such as severe starvation, may
occur and future studies could investigate the effects
of the parasite under more extreme food conditions.
In general, controlled infections of hosts with Mytili-
cola infective larval stages proved to be an effective
method to study effects of the parasite on blue
mussel hosts, which can be applied in subsequent
studies with other host species as they would help to
overcome the lack of strong inference in earlier corre-
lative studies on both Mytilicola species. Here, we
have developed a successful technique to harvest the
invasive parasite M. orientalis and to infect its new
blue mussel host under laboratory conditions. The
lack of mortality of mussels among treatments during
the experiments, suggests that only sublethal effects
of the parasite occurred, and that our experimental
procedures were non-lethal. Furthermore, we have
documented the maturation of M. orientalis larval
stages from the moment of hatching to the develop-
ment of the infective stage (see also Pogoda et al.
2012), which typically took less than one week under
the relatively high temperatures used to increase
development speed (i.e., the planktonic phase is likely
to be longer in natural populations). Our infection
methods were successful (success rate 7188%), and
we achieved mean intensities (about 3 copepods per
infected host) that were similar to intensities observed
in natural populations of similar-sized infected mussels.
As the results of our varying infection techniques only
marginally differed between experiments, the addition
of food during parasite exposure and the size of the
infection containers do not appear to drastically
affect the outcome of laboratory infections. Given
that Gee and Davey (1986) estimated a maturation
period of 70.8 (± 16.6, 95% confidence interval) days
at 1418°C and just 8.3 (± 4.1) days at 1822°C for
M. intestinalis, we expected our experiments to
provide ample time for the parasites to achieve matur-
ity. However, our screenings unexpectedly revealed
almost exclusively juvenile M. orientalis after nine
weeks in the experiment, carried out at 18°C. This
may indicate that M. orientalis maturation times are sig-
nificantly longer than M. intestinalis because of a lower
tolerance for cool temperatures and further studies will
be needed to determine developmental times of the
parasite at various temperatures.
In conclusion, this is the first study in which con-
trolled laboratory infections with the invasive
copepod M. orientalis were performed on its new
native blue mussel host. We discovered that infections
with early stages of the copepod (up to nine weeks)
lead to lower condition of infected mussels. As our
study was performed with juvenile stages of the para-
sitic copepod, potential impacts of adult parasites
remain to be investigated. In our experimental study,
we challenged the mussels with only two stressors
(infection with M. orientalis and limiting food con-
ditions). However, for mussels living on natural
mussel beds, stressors may be more diverse and
severe (e.g., extreme temperatures, infections with
multiple parasite species, resource competition with
other species), opening perspectives for future
studies. Such studies will be important to identify the
full range of indirect effects of invasive oysters and
other invasive species on native biota via parasite co-
introductions and subsequent indirect parasite-
mediated effects via parasite spillover.
Acknowledgements
We are grateful to Jarco Havermans for help in the field and
laboratory, Josje Snoek and Kirsten Scholten for maintaining
the algae cultures and Rob Dekker for pointing out unin-
fected mussel populations on basalt groins near Julianadorp.
We also thank three anonymous reviewers and Subject Editor
Dr Roy Kropp for their useful comments on earlier drafts of
this manuscript.
Disclosure statement
No potential conflict of interest was reported by the authors.
MARINE BIOLOGY RESEARCH 9
Funding
This work was supported by the Nederlandse Organisatie
voor Wetenschappelijk Onderzoek (NWO) and the German
Bundesministerium für Bildung und Forschung (BMBF)
[grant number 839.11.002].
ORCID
M. Anouk Goedknegt http://orcid.org/0000-0002-8637-0779
Jan Drent http://orcid.org/0000-0003-1277-5957
Jaap van der Meer http://orcid.org/0000-0003-4818-2408
David W. Thieltges http://orcid.org/0000-0003-0602-0101
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MARINE BIOLOGY RESEARCH 11
... Another closely related invasive parasitic copepod, Mytilicola orientalis Mori, 1935, arrived in the Wadden Sea with its original host, the Pacific oyster (Magallana gigas), on the first decade of the twenty-first century (Feis et al. 2019). Like M. intestinalis, also M. orientalis lowers mussel condition at 18 °C but it has not been reported to cause mortality in native mussels (Goedknegt et al. 2018). Mussel condition is a proxy for reproduction, because in preparation for spawning up to 59% of adult mussel soft tissue weight consists of reproductive tissue (Duinker et al. 2008), and it can also be considered as a proxy for energy reserves in general. ...
... Interestingly, our only mussel mortalities at lower temperatures (14 °C and 18 °C) occurred in parasite exposure groups, one with M. orientalis and three with M. intestinalis exposure. That observation, combined with the survival curve of parasite exposed mussels staying below the control mussel curve at 26 °C until late in the experiment, could point to early stages of infection with juvenile parasites possibly compromising mussel survival, as a larger impact on hosts by M. intestinalis juveniles compared to adult parasites has been suggested before (reviewed by Goedknegt et al. 2018). ...
... Mytilicola orientalis had a negative effect on mussel growth and M. intestinalis on mussel condition. In previous laboratory studies conducted at 18 °C, infections with both parasite species had negative effects on mussel condition and infection with M. orientalis did not affect mussel growth (Feis et al. 2016;Goedknegt et al. 2018). Interestingly, in our study neither of the two parasite species influenced mussel condition at 18 °C; the negative effect by M. intestinalis on mussel condition was clearest at 10-14 °C (Fig. 5), and M. orientalis affected only mussel growth across the whole range of temperatures. ...
Article
Full-text available
An increase in temperature due to climate change may affect the geographic ranges of invasive parasites and alter their impact on native hosts. Our goal was to determine if the effects of infection by two species of invasive endoparasitic copepods on native blue mussel hosts (Mytilus edulis) change with increasing temperatures. We investigated this with a laboratory experiment using temperatures that represent annual mean and mean summer water temperatures of past observations and future predictions for the study area, the European Wadden Sea (10–26 °C). Over a period of 8–20 weeks, infection with Mytilicola intestinalis lowered mussel condition and infection with Mytilicola orientalis decreased mussel shell growth. High temperatures decreased mussel growth and condition in general, but only at low temperatures (10–14 °C) the parasite-induced loss of condition was evident compared to uninfected mussels. Mussel mortality and reproductive activity were not affected by parasite infection, although both were impacted by temperature: the highest temperature (26 °C) increased mussel mortality, and gamete ripening only occurred at lower temperatures (10–18 °C). Taken together, these results suggest that both infection and high temperatures have independent negative effects. However, an increase in temperature does not worsen the effect of infection on individual mussel hosts, and neither does infection decrease host tolerance for long-term exposure to high temperatures. These findings add to our understanding of the interplay between increasing temperature and the interaction between invasive parasites and native hosts, and help predicting host and parasite dynamics in systems affected by species invasions and climate change.
... Spatially both parasites use the same niche and infest intestines of mollusks (Goedknegt et al., 2018b), where they attach with hooklike structures to the intestinal wall (Figueras et al., 1991;Bignell et al., 2008). Parasite attachment causes lesions and inflammations (Watermann et al., 2008) that invoke a costly immune response (Santarem et al., 1994) and can lead to reduced body condition (Goedknegt et al., 2018a). Relative to their intestinal habitat both parasites can reach considerable sizes (up to 12 mm (Goedknegt et al., 2018a)). ...
... Parasite attachment causes lesions and inflammations (Watermann et al., 2008) that invoke a costly immune response (Santarem et al., 1994) and can lead to reduced body condition (Goedknegt et al., 2018a). Relative to their intestinal habitat both parasites can reach considerable sizes (up to 12 mm (Goedknegt et al., 2018a)). Their large size and high infection prevalences and intensities spatially restrict niche availability, leading to competition between individuals (Feis et al., 2016). ...
... Interestingly, the overall prevalence of both parasites combined in mussel hosts also dropped since M. orientalis invaded ( Figure 1B). Since infection by both parasites leads to similar energetic costs and lowered body condition of the mussel host (Feis et al., 2016;Goedknegt et al., 2018a), mussels might have actually profited from the invasion of M. orientalis due to lower infection rates. ...
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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.
... Jellyfish blooms lead to reduced tourism at coastal areas (Kontogianni and Emmanouilides, 2014;Ghermandi et al., 2015;Nunes et al., 2015;Vandendriessche et al., 2016;Vasslides et al., 2018) (Graham et al., 2003;Goedknegt et al., 2018;Seregin and Popova, 2020) ...
... Invasive species can affect native species and ecosystems directly via competition and predation therefore impacting the local biodiversity. The parasitic copepod Mytilicola orientalis was co-introduced with Pacific oysters to Europe and is now found to parasitise native bivalves including blue mussels (Goedknegt et al., 2018). In 2001 a bloom of invasive Phyllorhiza punctata jellyfish likely caused millions of dollars of damage to shrimp nets and untold damage via predation on fish eggs and larvae (Graham et al., 2003). ...
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Zooplankton are a key group of organisms at the base of the marine food web and are fundamental to providing a broad range of societal and economic benefits which have previously remained poorly defined. This research addresses this knowledge gap through the provision of a first full assessment of zooplankton ecosystem services and disservices. Anthropogenic stressors such as microplastic pollution, climate change, and fisheries, could negatively affect the marine ecosystem services provided to humans and therefore have a negative impact on human well-being through reduction in food security, livelihoods, income, and good health. Deploying a mixed methodology approach including a semi-systematic literature review and ecological impact assessment, we provide novel evidence of the effects of microplastic pollution (high and low concentrations), fisheries, and climate change on the ecosystem services of three important zooplankton groups (copepods, jellyfish, and krill). We show that the majority of impacts on ecosystem services are negative, with the exception of climate change on jellyfish ecosystem services. Climate change and high microplastic concentration are evidenced to have the most substantial negative impacts on copepods and krill, with accompanying implications for the ecosystem services of climate regulation, water conditions, other materials, science, and entertainment. High microplastic concentration also depressed ecosystem service provision for jellyfish, impacting the services of genetic materials , climate regulation, water conditions, education, and entertainment. Fisheries are also evidenced to have negative impacts on all three zooplankton groups. In the case of jellyfish, climate change is evidenced to have a positive impact on the group's ecosystem service provision in every category except experiential experiences, which is inversely related to increasing population, owing to their negative perception due to sting injuries. The evidence presented in this study shows that by maintaining sustainable fisheries, reducing plastic pollution, and minimising climate change, we will be actively investing in the current and future provision of marine ecosystem services and the human well-being benefits that they provide.
... The models were forced to cross the y-axis on day 0 at the length of an infectious copepodite 1. This length (intercept) was the midpoint of a range given in the literature; 0.47 mm (0.4-0.54 mm) for M. intestinalis and 0.27 mm (0.24-0.29 mm) for M. orientalis (Gee & Davey, 1986;Goedknegt, Bedolfe, et al., 2018). ...
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Climate change may exacerbate the impact of invasive parasites from warmer climates through pre‐existing temperature adaptations. We investigated temperature impacts on two closely related marine parasitic copepod species that share the blue mussel (Mytilus edulis) as host: Mytilicola orientalis has invaded the system from a warmer climate <20 years ago, whereas its established congener Mytilicola intestinalis has had >90 years to adapt. In laboratory experiments with temperatures 10–26°C, covering current and future temperatures as well as heat waves, the development of both life cycle stages of both species accelerated with increasing temperature. In the parasitic stages, the growth of the established invader increased evenly from 10°C to 22°C, whereas the recent invader barely grew at all at 10°C and grew faster already at 18°C. In contrast, temperature had little effect on the transition success between life cycle stages. However, the highest temperature (26°C) limited the egg development success of the established invader and the host entry success of both species, whereas the infection success of the established invader increased at 18°C and 22°C. In general, our experiments indicate that the main effect of temperature on both species is through development speed and not life cycle stage transition success. Based on regional long‐term temperature data and predictions, the numbers of completed life cycles per year will increase for both parasites. The established invader seems better adapted for low current temperatures (around 10°C), whereas the more recent invader barely develops at these temperatures but can cope in high temperatures (around 26°C). Hence, pre‐existing temperature adaptations of the recent invader may allow the species to better cope with heat waves.
... Pacific oysters co-introduced the invasive parasitic copepod Mytilicola orientalis that was likely co-introduced in large numbers or via multiple introductions and followed a similar invasion route as oysters (Feis 2018) and subsequently spilled over to native blue mussels (Pogoda et al. 2012;Goedknegt et al. 2017). This copepod has a direct life cycle and inhabits the intestines of its host, causing reductions in the condition of mussels (Goedknegt et al. 2018a), but not in oysters (Katkansky et al. 1967;Steele and Mulcahy 2001). A congeneric parasitic copepod species, Mytilicola intestinalis, has been infecting native mussels since its introduction to the region 80 years ago (Caspers 1939;Hockley 1951;Korringa 1968). ...
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There are surprisingly few field studies on the role of invasive species on parasite infection patterns in native hosts. We investigated the role of invasive Pacific oysters (Magallana gigas) in determining parasite infection levels in native blue mussels (Mytilus edulis) in relation to other environmental and biotic factors. Using hierarchical field sampling covering three spatial scales along a large intertidal ecosystem (European Wadden Sea), we found strong spatial differences in infection levels of five parasite species associated with mussels and oysters. We applied mixed models to analyse the associations between parasite prevalence and abundance in mussels and oysters, and 12 biological and environmental factors. For each parasite–host relationship, an optimal model (either a null, one-factor or two-factor model) was selected based on AIC scores. We found that the density of invasive oysters contributed to three of the 12 models. Other biological factors such as host size (six models), and the density of target or alternative host species (five models) contributed more frequently to the best models. Furthermore, for parasite species infecting both mussels and oysters, parasite population densities were higher in native mussels, attributed to the higher densities of mussels. Our results indicate that invasive species can affect parasite infection patterns in native species in the field, but that their relative contribution may be further mediated by other biological and environmental parameters. These results stress the usefulness of large-scale field studies for detailed assessments of the mechanisms underlying the impacts of invasive species on native host communities.
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Parasites can alter the traits or densities of mutualistic partners, potentially destabilizing mutualistic associations that underpin the structure, functioning, and stability of entire ecosystems. Despite the potentially wide‐ranging consequences of such disruptions, no studies have directly manipulated parasite prevalence and/or intensity in a mutualistic partner, nor quantified the resulting community‐level effects. Here, we investigated the effects of a common trematode parasite (Cercaria opaca) on the strength of a keystone facultative mutualism in western Atlantic salt marshes between the foundational marsh cordgrass, Spartina alterniflora, and the ribbed mussel, Geukensia demissa. Cordgrass increases mussel survivorship and growth through shading, while mussels enhance cordgrass growth by producing nutrient‐rich biodeposits. This mutualistic association also creates conditions that enhance biodiversity and ecosystem functioning, and mediates the ability of foundational plants to resist and recover from extreme drought. We used lab and field assays to show how increasing infection with trematode metacercariae negatively influenced mussel biodeposit production, as well as the strength of mussel shells and byssal attachments. By conducting a field manipulation using experimentally infected mussels, we demonstrated that the mutualistic benefits of mussels to cordgrass growth decreased with increasing trematode infection intensity—a pattern likely generated by reduced mussel biodeposition and enhanced mortality. Additionally, increasing parasite loads in mussels led to predictable decreases in the abundances of benthic invertebrates, as well as in key ecosystem characteristics and process rates (i.e., redox potential and sediment accretion). Finally, a survey of five North Carolina salt marshes demonstrated that infection with C. opaca was most common in mussels in areas experiencing cordgrass die‐off due to drought, and that infection intensity decreased with distance from die‐off areas. Because the mussel–cordgrass mutualism underpins marsh ecosystem resilience to drought‐associated die‐off, our results suggest that parasitism may depress recovery from these disturbances. Although this is the first experimental demonstration of parasites indirectly altering community structure and functioning by undermining an ecologically influential mutualism, this type of relationship could be common in nature, given that parasites frequently infect influential mutualists.
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Planktonic invasive species cause adverse effects on aquatic biodiversity and ecosystem services. However, these impacts are often underestimated because of unresolved taxonomic issues and limited biogeographic knowledge. Thus, it is pivotal to start a rigorous quantification of impacts undertaken by planktonic invasive species on global economies. We used the InvaCost database, the most up-to-date database of economic cost estimates of biological invasions worldwide, to produce the first critical assessment of the economic dimension of biological invasions caused by planktonic taxa. We found that in period spanning from 1960 to 2021, the cumulative global cost of plankton invasions was US5.8billionforpermanentplankton(holoplankton)ofwhichvirusesencompassednearly93 5.8 billion for permanent plankton (holoplankton) of which viruses encompassed nearly 93%. Apart from viruses, we found more costs related to zooplankton (US 297 million) than to the other groups summed, including myco- (US73million),phyto(43million),andbacterioplankton(US 73 million), phyto- (43 million), and bacterioplankton (US 0.7 million). Strikingly, harmful and potentially toxic cyanobacteria and dinoflagellates are completely absent from the database. Furthermore, the data base showed a decrease in costs over time, which is probably an artifact as a sharp rise of novel planktonic alien species has gained international attention. Also, assessments of the costs of larval meroplanktonic stages of littoral and benthic invasive invertebrates are lacking whereas cumulative global cost of their adult stages is high up to US$ 98 billion billion and increasing. Considering the challenges and perspectives of increasing but unnoticed or neglected impacts by plankton invasions, the assessment of their ecological and economic impacts should be of high priority.
Technical Report
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Special volume (1991): Proceedings of the Fourth International Conference on Copepoda, in the Bulletin of the Plankton Society of Japan. Mytilicola intestinalis inhabits the digestive tract of the commercially important European blue mussel Mytilus edulis. Early researchers believed that Mytilicola damaged the host by feeding directly upon the epithelial lining of the host intestine, whilst more recent work indicated that it does not seriously affect the host and feeds upon excess food (phytoplankton and detritus) which passes through the mussel intestine. Comparative analysis of the stable isotope 15N shows that it is 2.8 ppt higher in whole Mytilicola than in mussel intestine, suggesting that Mytilicola occupies a higher a trophic level than Mytilus and therefore is unlikely to use the same food source. Whilst the limitations and pitfalls of this method are recognised and discussed, it is concluded from these observations (and from evidence provided by other techniques) that Mytilicola utilizes mussel breakdown products such as mucus and sloughed-off cells as its major food source and thus feeds indirectly upon the host.
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Invasive parasites can spill over to new hosts in invaded ecosystems with often unpredictable trophic relationships in the newly arising parasite-host interactions. In European seas, the intestinal copepod Mytilicola orientalis was co-introduced with Pacific oysters ( Magallana gigas ) and spilled over to native blue mussels ( Mytilus edulis ), with negative impacts on the condition of infected mussels. However, whether the parasite feeds on host tissue and/or stomach contents is yet unknown. To answer this question, we performed a stable isotope analysis in which we included mussel host tissue and the primary food sources of the mussels, microphytobenthos (MPB) and particulate organic matter (POM). The copepods were slightly enriched in δ¹⁵ N (mean Δ ¹⁵ N ± s.d. ; 1·22 ± 0·58‰) and δ¹³ C (Δ ¹³ C 0·25 ± 0·32‰) with respect to their host. Stable isotope mixing models using a range of trophic fractionation factors indicated that host tissue was the main food resource with consistent additional contributions of MPB and POM. These results suggest that the trophic relationship of the invasive copepod with its mussel host is parasitic as well as commensalistic. Stable isotope studies such as this one may be a useful tool to unravel trophic relationships in new parasite-host associations in the course of invasions.
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Invasive species can cause indirect effects on native biota by modifying parasite-host interactions and disease occurrence in native species. This study investigated the role of the invasive Pacific oyster (Crassostrea gigas) in potential spillover (co-introduced parasites infect native hosts) and spillback (native or established parasites infect invasive hosts and re-infect native hosts) scenarios of recently introduced (Mytilicola orientalis) and previously established (Mytilicola intestinalis) marine parasitic copepods in two regions in northern Europe, the Dutch Delta and the Wadden Sea. By examining 3416 individuals of 11 potential host species from sympatric host populations, we found that the recently introduced parasite M. orientalis does not only infect its principal host, the invasive Pacific oyster (prevalence at infected sites 2–43 %, mean intensity 4.1 ± 0.6 SE), but also native blue mussels (Mytilus edulis; 3–63 %, 2.1 ± 0.2), common cockles (Cerastoderma edule; 2–13 %, 1.2 ± 0.3) and Baltic tellins (Macoma balthica; 6–7 %, 1.0 ± 0), confirming a spillover effect. Spillback effects were not observed as the previously established M. intestinalis was exclusively found in blue mussels (prevalence at infected locations 3–72 %, mean intensity 2.4 ± 0.3 SE). The high frequency of M. orientalis spillover, in particular to native mussels, suggests that Pacific oysters may cause strong parasite-mediated indirect impacts on native bivalve populations.
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Host–parasite coevolution has rarely been observed in natural systems. Its study often relies on microparasitic infections introducing a potential bias in the estimation of the evolutionary change of host and parasite traits. Using biological invasions as a tool to study host–parasite coevolution in nature can overcome these biases. We demonstrate this with a cross-infection experiment in the invasive macroparasite Mytilicola intestinalis and its bivalve host, the blue mussel Mytilus edulis. The invasion history of the parasite is well known for the southeastern North Sea and is characterised by two separate invasion fronts that reached opposite ends of the Wadden Sea (i.e. Texel, The Netherlands and Sylt, Germany) in a similar time frame. The species’ natural history thus makes this invasion an ideal natural experiment to study host–parasite coevolution in nature. We infected hosts from Texel, Sylt and Kiel (Baltic Sea, where the parasite is absent) with parasites from Texel and Sylt, to form sympatric, allopatric and naïve infestation combinations, respectively. We measured infection rate, host condition and parasite growth to show that sympatric host–parasite combinations diverged in terms of pre- and post-infection traits within <100 generations since their introduction. Texel parasites were more infective and more efficient at exploiting the host’s resources. Hosts on Texel, on the other hand, evolved resistance to infection, whereas hosts on Sylt may have evolved tolerance. This illustrates that different coevolutionary trajectories can evolve along separate invasion fronts of the parasite, highlighting the use of biological invasions in studies of host–parasite coevolution in nature.
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Six species of Copepoda Poecilostomatoida of the families Myicolidae, Sabelliphilidae, Lichomolgidae, and Mytilicolidae are recorded from six different species of intertidal bivalves in the East Scheldt (The Netherlands), a branch of the southern bight of the North Sea. One bivalve species may harbour more than one species of copepod, and one copepod species may use more than one species of bivalves as host.