The marine food
web has been shown to be severely affected by mixotrophic dinoflagellates, with
microalgal blooms causing the death of fish, copepods and other metazoans. Karlodinium is an example of a genus of
toxic microalgae that form such blooms in eutrophic coastal waters. They work
by releasing neurotoxins that stun their prey before feeding via myzocytosis.
This investigation focused on the species Karlodinium
armiger and Karlodinium veneficum
and their effects on the motility and mortality of the copepod Acartia tonsa and other metazoans. Karlodinium veneficum is a well known
ichtyotoxic bloom, which produces Karlotoxins to stun prey before ingestion. Karlodinium armiger is also believed to
work in a similar manner, however has not been studied as extensively, so the
specific neurotoxin used is currently unknown.
The interactions
between the microalgae and copepods were observed using an inverted microscope.
Immobilisation was characterised by copepods lying on the bottom of the
microwell displaying erratic movements but with gut movements still occurring,
and death was identified when gut movements stopped. Shortly after adding the
copepods to the culture, Karlodinium
armiger was attracted to them and first began to attach to the antennae and
telson. These are important in sensing hydrodynamical disturbances in the
surrounding area, which copepods then use to determine between prey and
predator by size. As Karlodinium armiger
is of a much smaller size in comparison, this suggests it is disguised as prey,
allowing the attack of the copepod to occur whilst remaining unnoticed.
After 135
minutes Karlodinium armiger was shown
to immobilise nearly all the copepods. Within 24 hours all copepods were dead and
surrounded by swarms of Karlodinium
armiger with feeding tubes attached. After 24 hours the copepods with the Karlodinium veneficum strains were alive
and healthy, therefore further experiments used only Karlodinium armiger. The experiment was repeated with adult
nematode, trochophore and late stage polychaete larvae, all of which
experienced immobilisation and mortality, suggesting Karlodinium armiger affects a wide range of metazoans. Further
experiments concerning cell density demonstrated that when Karlodinium armiger was below 1100 cells ml-1 copepods
were unaffected, however at 3500 cells ml-1 they were immobilised
and killed. As field studies have reported densities of Karlodinium armiger and Karlodinium
veneficum between 10,000 and 100,000 cells ml-1 in coastal
areas, this suggests microalgal feeding is likely to have detrimental effects
on metazoans.
Although Karlodinium armiger contains chloroplasts, when relying on only
phototrophic growth, growth rates are very slow. However, feeding on prey such
as copepods provides important growth factors and also stimulates
photosynthesis, meaning consuming even a small amount of prey can result in a
significant increase in growth rate. This was demonstrated in the 3500 cell ml-1
cultures of Karlodinium armiger that
contained copepods by an increase in 85% of the population growth rate in
comparison to those without copepods.
This
investigation has provided valuable insight into the flexibility of feeding exhibited
by Karlodinium armiger. The fact that
this species can consume a wide range of metazoan suggests competition for a
variety of food sources may occur across many trophic levels, which could
result in the disruption of the structure and function of the marine food
web. However, further studies are needed
to establish the specific toxin produced by Karlodinium
armiger and also into the behaviour of other such harmful species in order to
reveal which organisms are most vulnerable.
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The ISME
Journal 6, 1926-1936 (October 2012) | doi:10.1038/ismej.2012.29
Hi Aimee, it is very interesting how these microalgae use a kind of "auxiliary income" to upgrade photosynthesis. However, I am wondering if Karlodinium mainly occurs in eutrophic waters, would it not be cheaper and less risky to invest in the uptake of ambient nutrients rather than producing toxins and attacking metazoans? Also did the authors have any suggestion why the copedpods were not attacked by Karlodinium veneficum, which is known to produce Karlotoxins, or is K. veneficum just specialized on a different type of prey?
ReplyDeleteHey Anna. Yes that's a good point. Although they expend energy to produce toxins and immobilise their prey I think there are many benefits that make it worthwhile. The fact they can feed on so many different metazoans means they can take advantage of the food resources at a range of trophic levels. Also, when feeding on prey this stimulates photosynthetic growth, meaning they only need to consume a small amount of prey to significantly increase their growth rate. The authors said that other studies had also showed Karlodinium veneficum had no effect on different species of copepods, however this did vary depending on the strain. They suggested the lack of effect may have been due to the fact they have quite low mixotrophic tendencies, which vary according to environmental factors including salinity, temperature and limitation of nutrients. Therefore despite the fact Karlodinium veneficum showed no effects in this experiment, they couldn’t rule out the idea that it may be triggered to attack metazoans under certain environmental conditions.
ReplyDeleteHi Aimee,
ReplyDeleteIs there any specific method for targeting the toxin to the copeopod? From reading the article you've written I got the impression that the microalgae secreted the toxin until the concentration was sufficient to kill the copeopod. However in open ocean I don't understand how the concentration or toxin produced by microscopic algae can build up to a significant amount in billions of litres of water!
Hey Harri, the study showed that direct cell to cell contact is required for Karlodinium to have an effect, so they attach directly to the copepod and release neurotoxins that result in immobilisation of the copepod. I can only seem to get the abstract of the paper now, but here’s a link (http://www.sciencedirect.com/science/article/pii/S1568988311001491) to another paper that has some photos of Karlodinium veneficum attaching to a copepod if you want to have a look. It really puts into perspective the size difference between the prey and predator!
DeleteHi Harri, I agree that forming a cloud of toxins would yield poor results. Instead, as I understood from Aimee's post, Karlodinium seems to attach to and attack the copepod directly and cause a fast immobilisation through the transfer of the toxin. Would be interesting to know though whether the microalgae collaborate between each other to coordinate the attack, maybe through quorum sensing signaling to switch to the heterotrophic stage once a certain density/environmental conditions are reached?!
ReplyDeleteHey Anna, yes the study did seem to show the Karlodinium to work via quorum sensing. When the cell density of Karlodinium armiger was below 1000 cells ml-1 the copepods actually grazed them. At 1100 cells ml-1 copepods still consumed Karlodinium armiger and reproduction continued to occur. However, after 40 hours the number of nauplius larvae, eggs and faecal pellets produced by the copepods were recorded as less than the number recorded at 24 hours, suggesting the Karlodinium were feeding on them. When the cell density further increased the prey and predator began to switch roles. At 3500 cell ml-1 Karlodinium armiger immobilised and killed all copepods within 24 hours and could be seen swarming around it with feeding tubes attached.
Delete