Mortality of post-settlement clams Rangia cuneata (Mactridae, Bivalvia) at an early stage of invasion in the Vistula Lagoon (South Baltic) due to biotic and abiotic factors
Mortality of post-settlement clams Rangia cuneata (Mactridae, Bivalvia) at an early stage of invasion in the Vistula Lagoon (South Baltic) due to biotic and abiotic factors
0 R. Kornijo ?w (&) K. Pawlikowski A. Drgas Department of Fisheries Oceanography and Marine Ecology, National Marine Fisheries Research Institute , Ko??a ?taja 1, 81-332 Gdynia , Poland
1 A. Rychter Institute of Technology, State University of Applied Sciences in Elbla ?g , Wojska Polskiego 1, 82-300 Elbla ?g , Poland
2 L. Rolbiecki Department of Invertebrate Zoology and Parasitology, Faculty of Biology, University of Gdan ?sk , Wita Stwosza 59, 80-308 Gdan ?sk , Poland
The clam Rangia cuneata, originating from the Gulf of Mexico, was recorded in the Vistula Lagoon for the first time in the early 2010s, and quickly became the dominant component of the zoobenthic biomass. To assess mortality as a factor potentially controlling the growth of Rangia population, a year-long field experiment involving marked bivalves placed in sediment-filled trays deployed on the bottom was conducted in 2014 and 2015. Predatorinduced mortality of the clams was low in summer, and very high in the winter-spring period. It was inversely proportional to the size of the clams. Such changes can be partially attributed to predation from at least five fish and three duck species, which contained clams in their digestive tracts. Non-predatory Handling editor: Jonne Kotta mortality particularly affected large individuals, and was highest in spring, several weeks after the end of winter. We hypothesize that it could be caused by persistent low temperatures over several winter months which led to considerable weakening of the condition of clams. A long winter could also reduce their resistance to environmental stress and potential effect of epibionts, as well as increase susceptibility to predation.
Fish; Waterfowl; Predators; Epibionts; Parasites; Food web; Thermal conditions; Survivorship
Invasive alien species are an increasingly serious
ecological and socio-economic issue worldwide
(Williamson & Fitter, 1996; Sala et al., 2000; Katsanevakis
et al., 2014)
, although positive impacts do exist
Charles & Dukes, 2007)
. The determination of when,
where, and why mortality occurs within the inter- and
intra-annual cycles is important for understanding the
invader population dynamics and ecosystem
functioning. This knowledge may be useful in formulating
plans to reduce the negative impact of invaders.
However, research on factors that affect mortality of
non-indigenous species in a natural environment is
very difficult to perform. This particularly applies to
aquatic species, including molluscs. Consequently,
such reports are scarce
(Robinson & Wellborn, 1988;
Reusch, 1998; Hill & Lodge, 1999; Strayer, 1999;
Byers, 2002a; Carlsson et al., 2011; Sousa et al.,
. This scarcity of research also applies to the
clam Rangia cuneata (G. B. Sowerby I), a species
native to the Gulf of Mexico, where it lives in estuaries
at salinities below 19 PSU (LaSalle & de la Cruz,
1985). In Europe, it was first found in Antwerp
harbour, Belgium, in 2005
(Verween et al., 2006)
Since then, it has been recorded in several other
countries, including Poland
(Mo?ller & Kotta, 2017)
Such a fast rate of colonisation is typical of
r-strategists, including R. cuneata, considering features of the
species such as its short life span, small size, high
fecundity, feeding flexibility, and high resistance to
unfavourable environmental conditions
(LaSalle & de
la Cruz, 1985)
In the Vistula Lagoon, R. cuneata was recorded in
the early 2010s
(Rudinskaya & Gusev, 2012;
Warzocha & Drgas, 2013)
. At present, clams reach
abundances of up to 200 ind. m-2, dominating the
zoobenthic biomass (Warzocha et al., 2016). The clam
population fluctuates considerably, with strong
reductions after long and harsh winters in some years. To
highlight the reasons for such fluctuations, we
performed year-long experimental field research with
marked clams placed on trays filled with sediment
which were deployed on the bottom of the lagoon. We
analysed losses of clams caused by predators and
nonpredatory causes that could result from the influence of
abiotic factors (e.g., water oxygenation and salinity,
temperature). We also conducted preliminary analyses
concerning the occurrence of parasites and epibionts
on R. cuneata, whose effect on the host could influence
the magnitude of both predatory and non-predatory
mortality. Mortality was analysed as a function of both
time and clam size. We expected increased clam losses
due to predation pressure in summer, when
ectothermal predators are most active, and increased mortality
caused by abiotic factors in winter, as a result of harsh
conditions. Moreover, considering the fact that R.
cuneata represents an r-reproductive strategy, we
assumed that the greatest losses from both types of
factors would affect young, small clams. This study is
the first to investigate the issue of survivorship of R.
cuneata outside its natural range.
Study site and methods
The Vistula Lagoon is in the south-eastern part of the
Baltic Sea. It is strongly elongated, SW?NE oriented,
and large (838 km2) but shallow (mean depth 2.5 m;
max. depth 5.2 m). The lagoon?s basin is separated
from the Baltic Sea by the Vistula Spit in the north, and
connected with the sea by the Baltiysk Strait. The area
lacks regular tides. Water-level fluctuation with an
amplitude of approximately 1 m is irregular owing to
wind action. Concentrations of nutrients in the lagoon
are high (Ntot. = 1.65?2.31 mg l-1;
Ptot. = 0.089?0.114 mg l-1), favouring the
development of phytoplankton which is dominated by
cyanobacteria, including the potentially toxic
Anabaena and Microcystis
(Nawrocka & Kobos, 2011)
The littoral zone has an intermittent belt of reed
Phragmites australis (Cav.), cattail Typha spp., or
lakeshore bulrush Schoenoplectus lacustris (L.).
Deeper, up to 1.5 m, the bottom is colonised by
scattered patches of submerged vegetation,
particularly by perfoliate pondweed Potamogeton perfoliatus
L. and sago pondweed Stuckenia pectinata (L.).
The study was conducted between 5 June 2014 and
26 May 2015 at a depth of 1.7 m, at a distance of
approximately 800 m from the shore (54 19.8750N,
19 31.9580E) (Fig. 1). The sediment at the
experimental site was sandy, with a slight admixture of mud,
with no submerged vegetation.
Experiment on survivorship/mortality of Rangia
The sediment was collected by means of multiple
Ekman grabs and sieved through 3-mm mesh to
remove clams, shell fragments, and large
invertebrates. The same sediment was used in all trays to
avoid a possible data distortion caused by varying
sediment compositions. After mixing the sediment in a
90-l container, a 0.5-l sediment sample was collected
for chemical and granulometric analyses. A 10-cm
thick layer of sediment was placed in five numbered
plastic trays (length: 49 cm; width: 37 cm; depth:
15 cm; surface area: 0.1813 m2). Then, the trays were
randomly seeded with 20 clams to obtain a number
equivalent to a density of 115 ind. m-2 (which was the
mean value observed in the environment based on 20
samples collected randomly by means of an Ekman
grab with a sampling area of 225 cm2). The clams used
in the experiment had a mean length of 25 mm (range:
9?40 mm, SD standard deviation: ? 5.2). They were
collected near the experimental site by means of a
bottom dredge. The length of each individual was
measured with a caliper with the accuracy of 0.1 mm.
All clams were marked with a number on both sides
of the shell with a water-proof oil marker. Data
concerning each of the clams were entered into a form.
This permitted tracing the history of each individual
On 5 June 2014, the trays with the sediment and
marked clams were submerged to the bottom, in
random order parallel to the shore by lowering them
carefully with a rope with the opposite end attached to
marker buoys. The marker buoys indicated the
position of each of the submerged trays and were removed
after all the trays had been placed on the bottom. A
detailed description of the experimental setup, its
deployment, and retrieval is available in
et al. (2017)
. The trays were left for the following five
periods: 5 June?21 July 2014, 22 July?3 September
2014, 4 September?16 October 2014, 17 October
2014?24 April 2015, and 25 April?26 May 2015. After
each period, the trays were gently lifted from the
lagoon bottom and recovered. In several cases, we
recorded several cm changes in sediment level in the
trays. They involved loss of sediment much more
frequently than an increase in its level. In the latter
case, the level of sediment always remained at least
several cm below the upper edge of the trays. Because
clams do not climb obstacles, but rather hide in
sediments, chances for the clams to leave the trays
were scarce. Due to a considerable thickness and
weight of the shells, it was also improbable for them to
be washed out of the trays as a result of strong wave
action, which was confirmed by observations
performed in the laboratory. Clams placed in Petri dishes
with 2-cm high walls, half-filled with sediment and
placed on the bottom of aquaria for several weeks,
were not able to escape in spite of considerable water
movement caused by an aerator, or by lifting and
dropping the dishes.
After tray removal, the sediment was washed
through a 3-mm sieve. The marked living bivalves,
spent shells (dead bivalves with tissues gone), and
gapers (recently dead shells still containing soft parts)
found in the tray were counted and measured.
Mortality of gapers and spent shells was attributed to
senescence, disease, or limiting physical or chemical
factors (non-predatory mortality), following the
Ford et al. (2006)
. Individuals not found
in the trays (lost clams) were considered eaten by
predators (predator-driven mortality) during a given
time interval, following the approach of
Tenore et al.
. Next, the trays were refilled with sediment and
measured bivalves. The missing and dead bivalves
were replaced with individuals collected in the
environment with the same approximate dimensions,
and the trays were submerged to the bottom again.
Rate of mortality (R) was reported as the combined
percentage of absent/dead animals in the experimental
trays per week during the established time intervals,
calculated according to the following formula:
p? ^ ?1=N?
where R is the rate of mortality in % per week, S is the
number of live individuals at the beginning of each
period, P is the number of lost individuals induced by
predation or by non-predatory mortality, and N is the
length of monitoring period in weeks.
To estimate the size-specific mortality rates, clams
used for the experiment were divided into two length
classes: small (\ 25 mm) and large (C 25 mm).
Temperature, oxygen concentration, and salinity
were measured on each sampling occasion by means
of a WTW probe, model Multi 3110. Continuous
temperature measurements were performed using a
MiniDOT recorder by PME.
The sediment collected for chemical analyses was
dried and manually ground in a mortar, and then
sieved on a set of geological sieves, with meshes of 2,
1, 0.5, 0.25, 0.125, and 0.063 mm. The contribution of
each fraction was determined based on weight. Data
were processed by means of GRADISTAT software
(Blott & Pye, 2001)
. The content of organic matter in
sediment was determined by loss on ignition at a
temperature of 500 C
(Heiri et al., 2001)
Identification of fish and waterfowl predators
The gut contents of potential fish and waterfowl
predators were examined to determine the role of R.
cuneata in their diet. Fish were collected in July,
September, and October 2014, and in May and
October 2015 in the direct vicinity of the experimental
area. In summer, three nets of the Nordic type for
nearshore harvests were applied. Each of the nets was
composed of nine panels with mesh from 15 to 60 mm,
a height of 1.8 m, and a total length of 45 m. In spring
and autumn, the Nordic type net for autumn harvests
was set, composed of 6 panels with mesh from 25 to
60 mm, a height of 3 m, and a total length of 180 m.
Eels caught in fyke nets were obtained from local
fishermen. Nets were set at dusk and collected early in
the morning. In summer, the mean exposure time was
approximately 9 h, in autumn?12 h. Fish were
counted and measured to the nearest 1 mm total
length and weighed to the nearest 1 g. The digestive
tracks of roach Rutilus rutilus (L.), gibel carp
Carassius gibelio (Bloch), white bream Blicca bjoerkna (L.),
European flounder Platichthys flesus (L.), European
perch Perca fluviatilis L., pikeperch Sander
lucioperca (L.), and European eel Anguilla anguilla (L.)
were dissected and preserved in 8% buffered
formaldehyde solution. The digestive contents were
examined for the presence of clams using a
. Dead ducks [tufted duck
Aythya fuligula (L.), greater scaup A. marila (L.), and
velvet scoter Melanita fusca (L.)] were obtained as
bycatch from local fishermen during commercial fishing
in the west part of the Vistula Lagoon, in September
and October 2016. The material contained only seven
individuals because of the difficulty of obtaining dead
ducks. In the laboratory, the ducks were sexed, and
their stomach contents were removed, preserved with
80% ethyl alcohol, and analysed under a
Analyses of parasites and epibionts
Clams for analyses were collected in the area of the
field experiment. A total of 128 clams were collected
in August 2014 with a mean length of 27.7 mm (range:
15.3?46.5 mm, SD: ? 9 mm), and 181 clams in
September 2014 (range: 16.1?33.7 mm,
SD: ? 7.5 mm). The clams were transported to a
laboratory where they were kept in water from the
lagoon at room temperature in plastic containers
(35 9 24 9 13 cm) with aeration. Fifty-to-seventy
clams were placed in each container. After 24 h, the
water was transferred to Petri dishes and analysed for
cercariae. Then, the containers were supplemented
with new water, and after 24 h, the process was
repeated. Next, the clams were subject to standard
parasitological sections. The external and internal
surfaces of the shell and internal organs were
examined under a stereomicroscope. Moreover,
parenchymal organs (digestive gland, gonads) were examined
under a transmission light microscope after being
pressed between glass slides. We used basic
parasitological parameters to determine the level of infection
of the clams: prevalence (percentage of infected
hosts), mean intensity (mean number of parasites or
epibionts in one infected host), and range of intensity
(the lowest and highest number of parasites or
epibionts in the analysed infected infrapopulation).
In the case of ciliates, which develop tree-like
colonies, due to small sizes and difficulty of precise
count, intensity was determined descriptively: single
(up to ten), moderately abundant (from 11 to 50), and
abundant (more than 50).
Due to non-normal distribution of variables (Shapiro?
Wilk test), we used non-parametric statistics. The
Friedman non-parametric ANOVA test was applied in
the analyses of the impact of time and size classes of
clams on their mortality. Analyses of pairs of variables
(small vs. big clams) were performed by means of a
Physical and chemical properties of water
and bottom sediments
The environmental conditions during the experiment
were typical of the Vistula Lagoon, with salinity and
chlorophyll-a concentration fluctuating considerably
(Fig. 2, Table 1).
Water transparency was low, resulting not only
from relatively high chlorophyll-a concentrations and
luxuriant development of phytoplankton, but also
from frequent wind-driven resuspension of suspended
solids. Water oxygenation at the bottom was high,
probably due to low depth and strong mixing.
Continuous measurements of water temperature
suggest a strong temporal pattern (Fig. 3) typical of
the zone of moderate marine climate, with maximum
temperatures in summer and low temperatures from
November to April of the following year. Ice cover
persisted for a relatively short period of slightly more
than 1 week in December 2014.
Sediments from the experimental trays were
finegrained sand (diameter 0.163 mm) with negligible
content of organic matter (1.55%). Such sediment
allows clams to burrow to a depth of 6 cm (Kornijo?w,
Drgas, Pawlikowski, unpubl.).
Temporal changes in mortality of R. cuneata
Time significantly affected both predator-induced
losses [Friedman ANOVA (N = 5, df = 4) = 10.3,
P = 0.035] and non-predatory mortality [Friedman
ANOVA (N = 5, df = 4) = 11.6, P = 0.021] of the
bivalves (Fig. 4). With the exception of the spring and
early summer seasons, mortality from predation was
higher than that caused by abiotic factors, but this
relationship was not statistically significant [Friedman
ANOVA (N = 5, df = 4) = 4.1, P = 0.394],
probably due to the high variance of the data set.
Predatory mortality was not recorded in early
summer (5 June?21 July 2014). It was observed only
between late summer and spring of the following years
(4 September 2014?26 May 2015), with a maximum
between late autumn and early spring (17 October
2014?24 April 2015). Non-predatory mortality was
negligible in summer and early autumn (21 July?16
October), and increased substantially between late
autumn and late spring (17 October 2014?26 May
2015). Mass non-predatory mortality occurred
particularly in spring, as evidenced by a high percentage
(54%) of recently dead individuals with soft tissue
still present in the shells (gapers) among all dead clams
(gapers and spent shells) on 24 April 2015. The
phenomenon was preceded by considerable spikes in
salinity and an increase in water temperature to
approximately 10 C (Figs. 2, 3). A month later, on
26 May 2015, the contribution of gapers was
considerably lower and amounted to 16%. Such a course of
mortality was confirmed by field observations
(sampling from the environment).
Fig. 3 Water temperature
fluctuations at the
experimental site. The dates
of deploying/retrieval of
experimental trays with R.
cuneata are marked with
Higher predatory mortality was observed in the group
of smaller clams, whereas non-predatory mortality
was higher among larger ones (Fig. 5). The
dependence was statistically significant in the case of
predatory mortality (Wilcoxon paired-samples test;
P = 15, P = 11.0, P = 2.8, P = 0.005) but not for
non-predatory mortality (Wilcoxon paired-samples
test; N = 12, T = 16.0, Z = 1.8, P = 0.071).
Rangia cuneata as prey of fish and waterfowl
Rangia cuneata was observed in the guts of five fish
species (Table 2). The contribution of bivalves in the
food of fish was usually low, not exceeding
approximately 10% of its volume. It was difficult to estimate
Fig. 4 Weekly predatory
(percent of absent clams)
and non-predatory mortality
(percent of spent shells and
gapers) of R. cuneata in the
in quantitative terms, because shells found in the gut
content were badly crushed. The eel was an exception.
Entire shells with a length from 7 to 17 mm were
found in their stomachs.
Rutilus rutilus had the highest contribution of
digestive tracts containing clams, and also a
Data from catches taken between July 2014 and October 2015
n number of fish examined
Trella & Horbowy (2014)
substantial share of biomass among clam consumers
(Table 2). Blicca bjoerkna, dominant among the
molluscivores of the lagoon, was represented by a
few individuals with R. cuneata in their guts.
All three examined duck species consumed clams.
Their stomachs contained both crushed and entire
shells with a length of up to 14 mm. The contribution
of clams in the stomach contents varied from several to
100% (Table 3).
We found no internal parasites associated with the
clams. Epibiotic ciliates Sessilida were recorded
around the siphons, and zebra mussels Dreissena
polymorpha (Pallas) on the shell surface. Ciliates were
located on the mucosal excretion directly around the
siphons of R. cuneata, and zebra mussels on the rear
part of the shell near the siphons. Differences in the
occurrence of epibionts were recorded both in
n number of birds examined, im immature, n/a not applicable
particular months and length classes of R. cuneata
No research has been conducted on temporal patterns
of survivorship/mortality of R. cuneata throughout the
year. The literature on the subject provides only data
referring to single findings concerning winter mass
mortality of clams probably caused by factors
unrelated to predation
(Tenore et al., 1968; Gallagher &
Wells, 1969; Hopkins & Andrews, 1970; Gusev &
The results of the experiment carried out in the
Vistula Lagoon suggest considerable natural clam
non-predatory mortality not in winter, as we expected,
but between late autumn and spring of the following
year. Our first hypothesis regarding the effects of
abiotic factors was, therefore, not confirmed. Due to
almost complete lack of ice cover, the lagoon water
must have been well oxygenated, also right above the
sediments, because of low water temperature and,
therefore, high solubility of oxygen and low rate of the
processes of organic matter decomposition. Therefore,
oxygen deficits can be excluded as the cause of
increased mortality. Hypoxic conditions in the bottom
habitats of the Vistula Lagoon and increased mortality
of clams can be expected during persistent ice cover
(Warzocha et al., 2016)
. Notice, however, that R.
cuneata is extremely resistant to oxygen depletion
(Hopkins, 1970; LaSalle & de la Cruz, 1985)
salinity was also unlikely to cause mass mortality
during the experiment. It varied between 2.5 and 5.5
PSU, i.e., in a range well tolerated by the clam
(LaSalle & de la Cruz, 1985; Auil-Marshalleck et al.,
Numerous studies attribute increased mortality of
bivalves to low temperatures. This may act in concert
with other factors in the case of extreme, catastrophic
environmental events, e.g., storms
. Rangia cuneata is a thermophilous
originating from an area with a
subtropical marine climate, where water temperature
is rarely below 10 C. Whereas short-term decreases in
water temperature are not necessarily lethal for the
(Hopkins & Andrews, 1970)
, it is doubtful for
it to have developed adaptations for survival in waters
at a temperature around 4 C for a period of several
months, as was the case in the Vistula Lagoon.
Moreover, low temperature could considerably limit
primary production, and, therefore, negatively affect
food conditions of the filter-feeding R. cuneata. In
consequence, low temperatures persisting for several
months could have both directly and indirectly
weakened the condition of bivalves
(Lane, 1986b; French &
Schloesser, 1991; Werner & Rothhaupt, 2008; Mu?ller
& Baur, 2011)
. Our field observations performed
20.7%, Moderately abundant?abundant/ca 80
24.3%, Moderately abundant?abundant/ca 80
during the experiment and in 2017 (Kornijo? w, Drgas,
Pawlikowski, unpubl.) show that mass mortality does
not occur during and immediately after the end of
winter, but several weeks later, in spring, when water
temperature begins to exceed approximately 10 C.
Mass mortality reaching 51.1% in the period from
April to June 2012 in the Russian part of the Vistula
Lagoon was also recorded by
Gusev & Rudinskaya
Periodic mass mortality of clams undoubtedly has
considerable consequences for the functioning of the
entire ecosystem. The presence of easily available
biomass in the form of dead soft tissue of clams is
equivalent to rapid enrichment of the food base of
microorganisms, invertebrates, and fish. This, in turn,
can have a strong effect on food-web interactions
(Sousa et al., 2012)
. Part of the biomass can enter the
detrital pathway, driving changes in microbial
biomass and nutrient cycles
(Cherry et al., 2005; Sousa
et al., 2014)
. Decomposing tissues must also
negatively affect the sanitary state of waters, although
research on the subject is scarce. Empty shells
accumulated on the surface of sediments are of
habitat-forming importance for many representatives
of benthos, particularly for those which require a hard
bottom (Gutierrez et al., 2003).
In conclusion, the high periodical mortality of R.
cuneata in the Vistula Lagoon might be related to low
temperatures during long winters, leading to the
exhaustion of the organisms. Unfavourable thermal
conditions could further contribute to increased
mortality caused by epibionts and parasites
Ben Abdallah et al., 2012)
Parasites and epibionts associated with R. cuneata
are little known
(Fairbanks, 1963; Wardle, 1983;
Reece et al., 2008)
. Clams from the Vistula Lagoon
proved to be free from parasites. This can result from
several factors, including lack of suitable/specific
intermediate and definitive hosts for potentially
imported parasites, resulting in their disappearance
in new conditions. During their importation, a process
potentially extended in time (e.g., transport in ship
ballast water), ??cleaning?? of hosts from parasites
could also occur. It should be emphasised that our
results are preliminary, because they were based on
only two sets of samples collected in summer and early
autumn. Therefore, the presence of parasites in other
seasons cannot be excluded.
Among epibionts, we recorded ciliates Sessilida on
siphons of R. cuneata and zebra mussels D.
polymorpha on the surface of clam shells. The nature of the
relationships of epibiotic ciliates with their bivalve
hosts is typically not well defined, but appears to range
from commensalism to parasitism. Epibiotic ciliates
are observed in different species of aquatic animals,
among others in crustaceans, bivalves, and even fish,
where in the case of high intensity, and/or under
conditions of intensified environmental stress
et al., 1997)
, they can limit breathing and feeding, and
even damage the tegument/skin and gill epithelium,
additionally, providing conditions for secondary
(Hazen et al., 1978; Colorni, 2008)
Recording D. polymorpha in the Vistula Lagoon only
on large individuals of R. cuneata deserves particular
attention. Apparently, only large clams have a
suitable surface area to be inhabited by D. polymorpha
(Bodis et al., 2014). In addition to the surface area, the
strength/resistance of the clam sufficient to bear the
additional weight can also be an important factor.
Perhaps, smaller clams are also inhabited by zebra
mussels but soon die due to the additional weight.
Moreover, owing to its size (mass), D. polymorpha can
hinder horizontal movement of R. cuneata, and its
burrowing in sediments, which probably constitutes a
method of avoiding predation
(Tenore et al., 1968)
Zebra mussels attached to shells of R. cuneata may
also increase the risk of predation for the latter due to
increased visibility to predators
(Hoppe et al., 1986)
The phenomenon may accelerate the process of
incorporation of R. cuneata in the diet of predators.
It should be considered, however, that in our study,
zebra mussels most frequently inhabited large clams
that were largely unavailable for predators, so this
mechanism probably did not occur.
The fact that small individuals of R. cuneata were
the most susceptible to predation can be related to the
fact that their shell, probably serving as the main line
of anti-predator defence
(Blundon & Kennedy, 1982;
Leonard et al., 1999; Czarno?e?ski et al., 2006; Wilkie
& Bishop, 2012)
, is thin and easy to crush. In addition,
Sylvester et al. (2007)
, studying the effect of fish on
invasive bivalves Limnoperna fortunei (Dunker) in the
Parana River, determined stronger predator pressure
on smaller individuals.
Magoulick & Lewis (2002)
observed an opposite pattern in a reservoir in
Arkansas, where fish preferred larger D. polymorpha.
In that case, however, it could have resulted from the
fact that even large zebra mussels have relatively thin
The literature provides information on cases of both
very strong pressure of native predators on invasive
(Robinson & Wellborn, 1988; Reusch, 1998;
Byers, 2002b; Magoulick & Lewis, 2002; Sylvester
et al., 2007; Watzin et al., 2008; Nakano et al., 2010;
Carlsson et al., 2011; Millane et al., 2012)
(Ilarri et al., 2014; Naddafi & Rudstam,
. According to the literature, post-settlement
individuals of R. cuneata in its native area are eaten by
a variety of predators: crabs, fish, alligators, birds, and
(Darnell, 1958; Perry et al., 2007; Davis,
It is very unlikely that the mortality observed in the
experiment could be attributed to invertebrate
predators. Among them, only the large Chinese mitten crab
Eriocheir sinensis Milne-Edwards could be taken into
consideration. However, its population, consisting of
immigrants from the west Baltic (mitten crabs do not
reproduce in the Vistula Lagoon due to insufficient
salinity), is small
. Moreover, their distribution is
limited to the overgrown shallows, habitats not preferred
by clams, and the analysis of the diets of crabs living in
the natural environment indicates the dominant role of
food of plant origin
(Czerniejewski et al., 2010 and the
As demonstrated by the experiment, the largest
losses in clams due to predation did not occur in
summer, as assumed by the first hypothesis, but in
autumn and winter, perhaps as a result of the structure
of predators. Our study shows that a number of not
only fish but also birds in the lagoon feed on the clam.
For all fish species, it is only a supplement, and not a
dominant food component. The most numerous fish
are potentially of highest importance in reducing the
abundance of clams in the lagoon: roach, gibel carp,
European eel, and European flounder. Among these
species, only roach and European flounder are
commonly known as important consumers of molluscs,
(Specziar et al., 1997; Lappalainen
et al., 2005; Vinagre et al., 2008)
. The aforementioned
species have probably become the greatest
beneficiaries among fish of the presence of the clam in the
environment. The enrichment of their food base can be
expected to translate into the improvement of their
individual condition and growth rate, provided that the
fish become accustomed to a particular type of food.
This usually requires time, because fish often avoid or
reject novel food types
(Warburton, 2003; Carlsson &
Strayer, 2009; Carlsson et al., 2011; Raubenheimer
et al., 2012)
Rangia cuneata seems to play a more important
role as food for the ducks of the Vistula Lagoon. They
predominantly ate small clams with a length of up to
14 mm. According to the literature, however, they can
feed on considerably larger bivalves reaching even
30 mm in length
(Richman & Lovvorn, 2003)
information on the contribution of R. cuneata in the
food of the waterfowl in the Vistula Lagoon has a
signal character, because the sample was relatively
small. In Europe, the potential consumers of clams
also include coot Fulica atra L. and diving ducks, e.g.,
common goldeneye Bucephala clangula (L.)
et al., 1986; Ponyi, 1994; Winfield & Winfield, 1994;
Molloy et al., 1997)
. Their abundance in the Vistula
Lagoon, especially during mild winters when no ice
cover appears, reaches thousands of individuals (Goc
& Mokwa, 2011). During this period, the demand of
birds for food, in contrast to ?cold-blooded?
(ectothermic) fish, strongly increases, and might translate into
more intensive predation. Rangia cuneata is probably
an easy prey. It does not attach to surfaces, and,
although some individuals burrow themselves entirely
in both soft muddy and hard sandy bottom sediments
(approximately 45 and 20%, respectively), others
protrude above the sediment surface (Kornijo?w,
Drgas, Pawlikowski, unpubl.). Due to the shallowness
of the lagoon (not exceeding 3 m over most of its
area), practically its entire surface constitutes feeding
grounds for diving ducks, able to dive and prey in
water up to several meters deep
(Molloy et al., 1997)
Local fishermen also observed other birds (gulls and
crows) preying on R. cuneata in the Vistula Lagoon.
The birds selected clams from exposed sediments (a
result of a seiche), and then dropped them from heights
onto hard surface until the shells cracked and the flesh
could be removed. The phenomenon was also reported
from other areas
(Meire, 1993; Wiese et al., 2016)
Our results show that R. cuneata has become a
substantial part of the local food chain, and predation
seems to be one of the control mechanisms. It seems,
however, that predators alone do not significantly
hinder the growth of the invader population. Similar
conclusions were drawn by
Molloy et al. (1997)
analysing the role of predators as potential factors
eliminating and controlling the invasive zebra mussel.
In conclusion, in the Vistula Lagoon, abiotic factors
had the greatest effect on the mortality not during
winter, as we had assumed, but several weeks later, in
spring. Predation pressure has turned out to be the
highest not in summer, as expected, but in the autumn?
winter period. Therefore, our first hypothesis was not
confirmed. The second hypothesis, assuming higher
mortality among small clams rather than large ones,
cannot be rejected, but only in reference to mortality
caused by predators. Mortality induced by abiotic
factors was higher among big clams.
Acknowledgements The work was conducted as part of
statutory activities of the Department of Fisheries
Oceanography and Marine Ecology of the National Marine
Fisheries Research Institute, project number: Dot17/Rangia.
The authors are grateful to the Institute of Meteorology and
Water Management National Research Institute, Maritime
Branch of Gdynia for providing data concerning water salinity
in the Vistula Lagoon in the period 2014?2015. We also thank
the editor and two anonymous reviewers for their careful
reading and constructive comments, and Dr. David Strayer for
his help with the English language.
Open Access This article is distributed under the terms of the
Creative Commons Attribution 4.0 International License (http://
creativecommons.org/licenses/by/4.0/), which permits
unrestricted use, distribution, and reproduction in any medium,
provided you give appropriate credit to the original
author(s) and the source, provide a link to the Creative
Commons license, and indicate if changes were made.
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