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First published online February 15, 2006
Journal of Experimental Biology 209, 810-816 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02081
Pseudodiarrhoea in zebra mussels Dreissena polymorpha (Pallas) exposed to microcystins
1 Department of Zoology, Ecology and Plant Science, and Environmental
Research Institute, University College Cork, Lee Maltings, Prospect Row, Cork,
Irelan
2 PROTEOBIO, Mass Spectrometry Centre for Proteomics and Biotoxin Research,
Department of Chemistry, Cork Institute of Technology, Cork,
Ireland
* Author for correspondence (e-mail: g.juhel{at}mars.ucc.ie)
Accepted 9 January 2006
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Summary |
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The observed acute irritant response to the toxin represents the first demonstration of an adverse sublethal effect of microcystins on invertebrate ecophysiology. Our results also suggest that it could be a specific response to microcystin-LF, a little studied toxin variant.
Key words: zebra mussel, Microcystis aeruginosa, microcystins, pseudofaeces, ecophysiology, feeding behaviour
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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).
Cyanobacteria are considered as a nuisance because they form harmful algal
blooms (HABs) in freshwater bodies subject to eutrophication
(Codd, 1992;
Nicholls et al., 2002;
Mur et al., 1999).
Microcystins are hepatotoxic, tumour promoting
(Falconer, 1991) and induce
liver cell apoptosis (Chen et al.,
2005). They therefore cause serious, often lethal, health effects
on fish, domestic animals and humans
(World Health Organisation,
2003; Azevedo et al.,
2002; Carmichael,
2001; Chorus and Bartram,
1999).
The freshwater zebra mussel Dreissena polymorpha (Pallas) is
invasive and established in water bodies throughout Europe and North America
and has recently colonised Ireland. As they reproduce rapidly and foul a wide
range of structures, they are of serious concern to industry and environmental
managers. Efficient suspension feeders, they occur in extremely high densities
and cause considerable changes in ecosystem composition/function such as local
extirpation of native mussel populations
(Strayer et al., 1999),
increases in water clarity (Budd et al.,
2001) and the removal of microalgae from water columns
(Raikow et al., 2004), hence
influencing HABs (Reeders et al.,
1989; Roditi et al.,
1996).
One of the most common species responsible for HABs is Microcystis
aeruginosa (Kützing). The relationship between this cyanobacterium
and the zebra mussel has already been studied but with conflicting results.
Laboratory experiments have shown a decline in Microcystis aeruginosa
abundance because mussels preferentially ingested cyanobacteria over diatoms
(Baker et al., 1998), while
others have reported enhanced intake of green algae in the presence of
cyanobacteria (Dionisio Pires et al.,
2004). Field studies have shown that, in the North American Great
Lakes, mussels were capable of selective rejection of toxic Microcystis
aeruginosa in pseudofaeces, promoting cyanobacterial HABs
(Vanderploeg et al., 1996;
Vanderploeg et al., 2001).
Dionisio Pires and Van Donk (Dionisio
Pires and Van Donk, 2002) found that lower clearance rates of
phytoplankton by Dreissena were obtained with a mixture of toxic
cyanobacteria and Chlamydomonas reinhardtii (Dangeard) than with a
mixture containing non-toxic cyanobacteria. Their results also showed that
mussels might finally promote a dominance of Chlamydomonas over
Microcystis, especially when the cyanobacterial strain used was
toxic.
Detailed knowledge of the capture and sorting of particles by the gills and
labial palps of the zebra mussel (Baker et
al., 1998; Baker et al.,
2000) is available, but very little information has been collected
concerning the effects of cyanobacterial toxins on food selection processes.
Furthermore microcystins belong to a family of endotoxins that comprises
different variants. Microcystin-LR (MC-LR) occurs most frequently
(Dawson, 1998) and is
considered the most toxic (Imanishi et
al., 2005) but few data are available concerning the toxicity of
the other variants. Our experiments were therefore designed to provide greater
insight regarding the toxicity of microcystins by comparing the effects of
Microcystis aeruginosa strains, of different toxicity levels and
different toxic profiles, on the ecophysiology of zebra mussels.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Toxic profile of the toxic strains of Microcystis aeruginosa
To obtain toxic profiles, the general procedure of Ortea et al.
(Ortea et al., 2004) was
followed. Briefly, algal samples (50 ml) were freeze-thawed and sonicated to
burst the cells so that all of the toxin would be released. The samples were
then filtered through GFB filter papers by vacuum filtration. The filtrates
were then applied to optimised solid-phase extraction (SPE) columns (Bakerbond
C18 Polarplus cartridge; Phillipsburg, NJ, USA) using the method
based on that developed by Lawton et al.
(Lawton et al., 1994). The SPE
cartridge was conditioned with methanol and water. The filtered algal sample
was applied and the cartridge was washed with 10 ml portions of 25%
methanol/water. Toxins were then eluted using methanol (6 ml) containing 0.1%
trifluoroacetic acid (TFA) and the eluent was evaporated to dryness using a
Turbo Vap LV Evaporator, and reconstituted in water (1 ml) for analysis.
Liquid chromatography–tandem mass spectrometry (LC-MS/MS) analyses of microcystins were carried out using a HP100 series LC system with an ultraviolet-photodiode array (UV-PDA) detector (Agilent, Ipswich, UK) linked with an LCQ ion-trap mass spectrometer (ThermoFinnegan, San Jose, USA). The mass spectrometer was equipped with an electrospray ionisation (ESI) interface. Using a flow injection rate of 3 µl min–1, the mass spectrometer was tuned using MC-LR; the optimised temperature was 220°C with a voltage of 3.0 V. The optimum relative collision energy (% RCE) was determined for each of the four toxic variants studied: MC-LR, MC-RR, MC-YR and MC-LF. Separation of the microcystins was achieved using a Luna (2) (5 µm, 2.0x150 mm, Phenomenex, Macclesfield, UK) column at 40°C (5 µl injection). A gradient elution of acetonitrile (with 0.05% TFA) over 42 min was used at a flow rate of 0.2 ml min–1.
Mussel collection and handling
Thirty mussels were collected from the submerged area of a quay in Ballina
Marina, Killaloe, Tipperary, Ireland, in March 2004. Only adult mussels
between 20 and 24 mm shell length were used to minimize size-related
variation. They were brought back to the laboratory in lake water and
acclimated to standard filtered (0.45 µm) freshwater maintained at
20±1°C for 48 h prior to the feeding experiments. Only active
individuals showing valve and siphon movements were used in the
experiments.
Diets offered to the mussels
Each cultured strain was used in single cell suspensions to feed the
mussels, corresponding to three separate diets. They were diluted in standard
filtered (0.45 µm) freshwater to adjust each diet to comparable mass of
suspended matter. Standard freshwater was prepared according to Sprung
(Sprung, 1987). The fourth
diet consisted of a mixture of the diatom Asterionella formosa and
the toxic cyanobacterium Microcystis aeruginosa CCAP 1450/10. This
was made up so that each of the two strains represented 50% of the total
biomass of cells present in the mixture. The total cell mass per unit of
volume was similar to that employed in the other three diets. Each diet was
supplied to the mussels at bloom concentration (106 cell
ml–1 for the two cyanobacterial strains and the mixed diet
and 104 cell ml–1 for the non-toxic diatom). All
algal cell concentrations were measured by Coulter Counter after determining
their equivalent spherical diameter (ESD).
Experimental setup
An experimental Perspex flow-through system, consisting of a chamber with
baffles, was designed to ensure constant unidirectional flow at a steady
microalgal concentration, as described
(Barillé et al., 2003)
(Fig. 1). The system was
supplied with the algal diets from an agitated tank through a Masterflex L/S
Economy Drive peristaltic pump (Cole Parmer Instrument Company, Vernon Hills,
IL, USA) at a flow rate of around 100 ml h–1.
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The system was particularly designed to separate physically pseudofaeces from faeces produced by the mussels (Fig. 1). The mussels were placed close to the outflow and the baffle acted as a separation; the inhalant siphon opened in the middle part of the chamber (between the two baffles) and the exhalant siphon in the right hand part of the chamber (between the right baffle and the outflow). Pseudofaeces were consequently expelled in the middle part of the chamber and the faeces in the right hand section of the system, facilitating separate collection using a Pasteur pipette (Fig. 1).
Feeding trial
Feeding experiments consisted of 90 min trials, performed for each diet
with six individual replicates for the single cell suspensions diets and ten
for the mixture trial. Individuals were filmed at 25 fields
s–1 from the side of the chamber, or from below as required.
Video analysis was performed for two diets: Asterionella formosa and
Microcystis aeruginosa CCAP 1450/10. For these diets, the mussels'
movements were deconstructed into different actions and the frequency of each
action evaluated (see Results for details). For the other diets, videos were
screened to evaluate the general behaviour of the mussels.
Analysis of pseudofaecal ejecta
At the end of 90 min trials with the mixture of non-toxic diatoms and
highly toxic cyanobacteria, pseudofaecal ejecta were collected using a Pasteur
pipette. Subsamples (each 1 ml) were analysed with a Coulter Counter to
determine concentrations of the two cell types, following resuspension of
ejecta in 10 ml of standard freshwater. The rest of the sample was
volumetrically measured, then filtered and dried to determine dry weight. From
the algal cultures, the individual dry weights of each of the two cell types
were determined. These were then used to calculate the weight of each of the
algal types present in the pseudofaecal materials from the cell
concentrations. Assuming that the pseudofaecal ejecta are composed only of
cells and mucus, we calculated the percentage of mucus by mass, by
subtraction.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Video analysis of the feeding behaviour of zebra mussels
Analysis of videos showed that all six individuals tested per given diet
showed the same feeding behavioural patterns in response to that diet. When
fed the non-toxic diatom Asterionella formosa, all mussels behaved
`normally' with expulsion of pseudofaeces through their inhalant siphons
(Fig. 3A; see movie 1 in
supplementary material) and ejection of faeces through their exhalant siphons
(Fig. 3B; see movie 2 in
supplementary material); both types of ejecta being produced in small
quantities. We also observed that during `normal' behaviour, mussels
periodically closed their shell valves and siphons (not illustrated).
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The same phenomenon was observed when we gave a mixture of the non-toxic Asterionella formosa and highly toxic Microcystis aeruginosa CCAP 1450/10 to mussels (not illustrated). However, when mussels were fed with low-toxicity cyanobacteria Microcystis aeruginosa strain CCAP 1450/06, only `normal' feeding behaviour (not illustrated) was observed, with small quantities of pseudofaeces being expelled through the inhalant siphon, faeces expelled intermittently through the exhalant siphon and mussels closing their shell valves and siphons periodically.
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Concerning pseudofaeces production, no statistical difference could be observed (Student's t-test; P=0.510) between the two diets even though the frequency of pseudofaecal expulsions was 10.4±1.5 h–1 with mussels fed the diatom against 8.9±1.7 h–1 when the mussels were fed the toxic cyanobacteria (Fig. 4). The same pattern was observed for faeces production (Mann–Whitney Rank Sum test, P=0.818) between the two diets even if the frequency of faeces production was 7.3±4.0 h–1 for mussels fed Asterionella against 2.3±0.8 h–1 when offered Microcystis aeruginosa CCAP 1450/10. However, significantly more valve closure events were observed in mussels fed the toxic cyanobacteria compared with those fed the non-toxic diatom (Student's t-test; P=0.008; 22.4±3.3 h–1 and 10.3±1.9 h–1, respectively; Fig. 4).
Composition of pseudodiarrhoea/pseudofaeces
Pseudofaecal and pseudodiarrhoeal samples were analysed for algal type,
algal concentration and mucus content when mussels were offered the mixture
diet (Fig. 5). As shown
earlier, Microcystis aeruginosa CCAP 1450/10 and Asterionella
formosa cells did not overlap in size (no overlap in their ESD). It was
therefore possible to determine their concentration within the same sample
with the Coulter Counter. From the culture we determine that the specific mass
of Microcystis aeruginosa CCAP 1450/10 cells was
1.4x10–8 mg cell–1. Asterionella
formosa cells had a specific mass of 2.57x10–7 mg
cell–1.
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Back calculations from the cell densities showed that the two materials differed slightly in composition. Pseudofaeces expelled by the inhalant siphon were composed of 46.1±3.2% M. aeruginosa, 24.5±2.4% Asterionella formosa and 29.4±5.2% mucus by dry mass (mean ± s.e.m.). Pseudodiarrhoea expelled through the pedal gape was 40.7±6.6% Microcystis aeruginosa, 14.0±1.04% Asterionella formosa and 45.2±7.00% mucus by mass (mean ± s.e.m.). Statistical analysis showed no significant differences in the proportion of Microcystis aeruginosa between pseudofaeces and pseudodiarrhoea (one-way ANOVA on arcsine transformed data; P=0.558; N=10; data normally distributed). However, pseudodiarrhoeal material had significantly less Asterionella formosa than pseudofaeces (ANOVA on ranks on arcsine transformed data; P=0.002; N=10; data not normally distributed). Although pseudodiarrhoea appeared to contain more mucus than pseudofaeces, the difference was not statistically significant (one-way ANOVA on arcsine transformed data; P=0.078; N=10; data normally distributed).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). Particles are generally filtered and captured
through the mussels' inhalant siphons and sorted on the gills and labial palps
(Baker et al., 2000). Unwanted
particles are embedded in strings of mucus and transported to the inhalant
siphon for rejection as pseudofaeces, whereas preferred particles are carried
to the mouth for ingestion and digestion. They are ultimately ejected as
faeces through the exhalant siphon of the bivalve
(Baker et al., 1998;
Baker et al., 2000). The
mechanisms underlying food selection are not well known but variations in
particle clearance rates have been attributed to differences in food quality
[related to size, polyunsaturated fatty acid (PUFAs) content or toxic content]
(Dioniso Pires and Van Donk, 2002;
Dionisio Pires et al.,
2004).
Our study demonstrates that toxic strains of Microcystis
aeruginosa have a dramatic effect on processing of microalgae by zebra
mussels, whereas nontoxic strains do not. Our data document the first
sublethal adverse effect of microcystins on the ecophysiology of an
invertebrate species; an acute irritant response to highly toxic
Microcystis aeruginosa. This response could be considered as
analogous to the acute diarrhoeal symptoms of microcystin toxicity in humans
(World Health Organisation,
2003; Dillenberg and Dehnel,
1960) in that it causes substantial shedding of Microcystis
aeruginosa in highly mucous pseudofaeces and pseudodiarrhoea.
Furthermore, we noted that, in the presence of the very toxic cyanobacteria,
mussels closed their shell valves and siphons significantly more often than
they did when fed a non-toxic diatom species. Though mussels normally
punctuate their active filtering sessions with periods of quiescence during
which the valves close and the siphons withdraw
(Morton, 1969;
Horgan and Mills, 1997), these
marked differences in valve closure rhythm are another sign of the mussels'
irritation due to the toxicity of microcystins.
Analysis of the toxic profiles of the two cyanobacteria showed that the
most abundant microcystins variant was MC-LF in the very toxic cyanobacterial
strain whereas only a small amount of MC-LR was present in that same strain
and in the low-toxicity strain. Previous studies investigating zebra mussels
feeding on toxic and non-toxic Microcystis aeruginosa
(Vanderploeg et al., 2001;
Dionisio Pires and Van Donk,
2002) were performed with strains containing only the most
abundant variant in nature [MC-LR (Dawson,
1998)]. MC-LR is also considered to be the most toxic variant
among microcystins (Imanishi et al.,
2005). However, no information is available on the relative
toxicity of MC-LF, but we suggest that, the reaction of the mussels,
manifested as the production of copious `pseudodiarrhoea', indicates that
MC-LF is a highly toxic microcystins variant that merits further studies.
Analysis of the two types of pseudofaecal ejecta corresponding to the
mixture diet showed that they were mostly composed of toxic cyanobacteria,
particularly the `pseudodiarrhoea'. This confirms that Microcystis
aeruginosa was preferentially being rejected in comparison with
Asterionella formosa, since proportions of the two species in the
diet were equal, a process being greatly enhanced by production of
`pseudodiarrhoea'. Earlier work in the Great Lakes of Canada
(Vanderploeg et al., 1996;
Vanderploeg et al., 2001)
demonstrated that zebra mussels could distinguish between toxic
Microcystis aeruginosa and desirable food algae
(Cryptomonas), removing the former in pseudofaeces released into the
environment, and hence encouraging blooms of the toxic species. This response
does not occur in the presence of low toxicity Microcystis
aeruginosa, which are ingested. Furthermore, we noted that the
pseudodiarrhoeal material was easily resuspended in water after collection
with the Pasteur pipette, indicating that it could potentially enhance algal
blooms depending on the water mixing regime. Microscopic observations of the
`pseudodiarrhoea' stained with Trypan Blue also showed mucus aggregations
(blue staining) and Microcystis cells that appeared green, therefore
still viable (not illustrated). Selective rejection, accentuated by the
pseudodiarrhoeal response, will therefore tend to enhance the presence of
toxic Microcystis aeruginosa in mixed Microcystis aeruginosa
cyanobacterial blooms, as well as transferring toxins from the water column to
the benthos. These results also imply that zebra mussels can distinguish
between cyanobacterial strains even though the organisms are of
indistinguishable size and morphology but of different toxic content.
The long-term effects of microcystins have been studied on zebra mussel
larvae (Dionisio Pires et al.,
2003) and other zooplanktonic species
(DeMott, 1999;
Lampert, 1981). These studies
all showed that microcystins had an inhibitory effect, mostly on growth,
feeding and generally survival of the animals. However, the impact of
pseudodiarrhoea on zebra mussels exposed to high levels of microcystins for
long periods is not known, but at the very least the response is likely to be
energetically costly, since molluscan mucus is known to be expensive to
produce (Davies and Hawkins,
1998). Further investigations are therefore needed to evaluate the
impact of microcystins on the physiological energetics of the zebra
mussel.
As mentioned previously, microcystins are considered to have generally negative effects on aquatic animals but no detrimental effects have so far been observed in adult zebra mussels. The expulsion of toxic Microcystis aeruginosa in mucous pseudodiarrhoea (rather than their ingestion), may therefore perhaps be a positive resistance factor that contributes to the successful spread of zebra mussels throughout water bodies subject to eutrophication.
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Acknowledgments |
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Footnotes |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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