AUSTRALIAN FRONTIERS OF SCIENCE, 2008

The Shine Dome, Canberra, 21-22 February

Microscopic algae: Taste-testers and commentators of Southern Ocean environmental states
by Dr Leanne Armand

 

Leanne Armand is the recipient of the 2005–07 European Union Marie Curie Fellowship for her comprehensive taxonomic treatment of Southern Ocean diatoms. She has added rigour to the study of diatoms by applying statistical analysis, increasing the degree of confidence in the reconstruction of sea water temperatures of the past. This has particularly enhanced the value in reconstructing environments during the late Quaternary. The relevance of this type of work is increasing as questions of evolution of our modern environment become more important. Leanne has recently returned to the Antarctic Climate and Ecosystem CRC and CSIRO Marine and Atmospheric Research in Hobart, where she is continuing her research on the modern distribution of diatoms in context to oceanic chemistry, the silica cycle and the effects of climate change in the subantarctic zone.

I am currently working at ACE CRC, the Antarctic Climate and Ecosystems CRC, in Hobart, and my current position is jointly funded by CSIRO Atmospheric and Marine Research as well. The research that I am going to talk to you about today is also funded through the Marie Curie Fellowship.

What are diatoms and why are they useful? What do we know about their distributions? And how are they linked to climate changes and the understanding of ecosystem function? In a sense, a lot of people like to categorise me as a palaeontologist or occasionally as a biologist or a geologist, and in fact I actually cross all themes and disciplines, which is sometimes crazy for me but being cross-disciplinary is a very interesting way to study things.

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First of all, what are diatoms? They are microscopic, unicellular algae. There are over 12,000 species currently identified and there are probably many more of them, and 1400 to 1800 are marine phytoplankton. They photosynthesise, producing the oxygen for the Earth, essentially, and they reproduce on average five times a day, but anything from 0.1 to eight times a day. They are found in any water environment, so from polar regions where water gets down to -2°C to hot water springs where I have seen them in up to 40°C still surviving, chugging away.

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In terms of their size, they range from about 2 microns up to 2 millimetres. The smallest one I have ever seen is the little fellow shown here, Fragilariopsis pseudonana. He is approximately 10 μm in length and 5 μm in width. The image shown beside that is of a group, a huge community of one species. They are all joined together at a foot pole and they have strands going up as a little colony. They are about 2 mm in length. You can actually see them with your eye, and when you get them in a net they completely clog it up and you don't see anything but a mass of green fibrous strands.

Regarding productivity, here we have a picture of the chlorophyll viewed from satellite on an annual scale. As you can see, most of the chlorophyll is either on coastal areas or in the polar regions. This chlorophyll is an indication in the upper surface waters of where there are the dominant phytoplankton, and diatoms generally constitute around 75 per cent of the primary producers in the areas in green and red, In the areas where there is blue they constitute about 35 per cent.

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To look at why they are important: we like to think of the Antarctic region at least, or the marine region, as all these lovely iconic species that we adore – penguins, whales and seals – but really the bottom line is that they don't actually contribute much. They are at the top end of the food chain. The values shown here are wet weight tonnage in terms of how much carbon the various creatures contribute or take up. We have our fish and krill; bacteria are shown at 800 million in the water; the protozoa – all the zooplankton that eat the phytoplankton – at 1500 million; but phytoplankton and diatoms make up most of it, and there are up to 6000 million tonnes of them in the oceans. These are really what we should be studying, because this is what is going on at the bottom of the food chain, which then influences everything that goes up to the top.

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Diatoms are actually quite diverse, and this is why they are an excellent tool for us to study as scientists. They come in a variety of forms – tubes; ribbons which are made up of single cells but all join together, being quite sticky; single solitary 'rockets'; discs; other types of rockets, with branches that will join them to another one so they can actually make chains – this is a whole colony here all together, with individual cells joined together; other big huge discs; and other chains. You even see the alphabet occasionally, with Hs joining up. (The one shown here at the bottom left is in division.) So they are very, very useful.

Each one of them is a species. Even if you have got a discoid species, it has an individual pattern and they are very simple to identify.

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The sea-floor is actually littered with diatoms. You see here an image of the remains. They are made of silica, which is, if you like, glass opal. These remains make up the majority of the sea-floor around Antarctica. We call the blue region, circling Antarctica, the Antarctic Opal Belt. (On this map, PF stands for Polar Front, and SAF for Sub-Antarctic Front.)

They are actually very useful. They constitute the majority of sediments reaching the sea-floor.

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We took all the sea-floor specimens that we could find and we identified them down. We actually ended up picking about 32 species that were very characteristic, very dominant, in those sediments.

We can divide them up by environmental preferences. Their closest relationship is, in fact, to sea surface temperature. They need to be at the surface of the water to photosynthesise, so this is where their no.1 physical relationship is.

Another relationship that we will see in a minute is also sea-ice cover. The closer you are to Antarctic sea-ice, the more the relationship changes.

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So what we end up having is this blue 'doughnut' around Antarctica, with small pennate species – like the one shown here, Fragilariopsis curta – which love very cold waters and love sea-ice at least nine months of the year.

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We get the open ocean species that generally take up the circumpolar distribution, shown here in green. Fragilariopsis kerguelensis is the most dominant phytoplankton in the Southern Ocean. And again this one is very eurythermal: it loves a wide range of temperatures, in fact, from about 2°C to about 12°C. It doesn't particularly like sea-ice.

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As we get away from Antarctica, we get the warm-water diatom species Azpeitia tabularis as shown here, and again most of the abundances are where there is no sea-ice and where temperatures are at least getting over 10°C.

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We use this information, then, to say that the sedimentary record is actually a very good indicator for past sea surface temperature and sea-ice conditions. But really, how is this useful in understanding the past?

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Let's take a step back and look at how we would understand the past if we wanted to understand about sea-ice cover around Antarctica.

Captain Cook was the first one to actually document sea-ice around Antarctica, so he gave us our first record. But his navigation skills, even though they were brilliant for the time, really only give us a one-pin-point place in the South Atlantic and a couple of bits where he tried to find that Great Southern Land. So the records are quite patchy. A couple of others, Wilkes and Dumont, also came through and gave us a few records.

The scientific researchers, which were really associated with the Discovery series, came through from the early 20th century, as shown here in purple. Sealing and whaling also gave us quite a few records about sea-ice in the past. But again they are all patchy, and they are generally in the South Atlantic region.

Satellites have bopped in from around 1975, so we have got records continuously, at least, and at a very high resolution, in the period since then.

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If we want to go back further in time, with the purple blip here representing our satellites, we can use ice cores from Antarctica, either along the Antarctic margin or coastal area. With the Law Dome ice core record they are thinking that they can get back to 100,000 years, but generally speaking they go back to about 20,000 years. We really need to look at fossil ice algae to go all the way back to 200,000 years ago, and perhaps a little bit further beyond, because we know that sea-ice has been around a little bit longer than that as well.

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So we will go off in our ship, the Aurora Australis, generally, or else the Marion Dufresne, which is a French ship. We go out and take ourselves a core. These cores are the deposition record, basically, through time. What we are getting around the Antarctic continent is where there are sea-ice diatoms, represented by these yellow circles here, such as the ones shown at the right of this slide, they will die, their silica remains then constitute the sediments indicated in yellow here, and these contrast with what we would have got from the open-ocean species, shown here in green. And we get this story of time through the core, which we then date.

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Some poor soul, usually me, has to count every centimetre down that core, or every 10 cm or 5 cm, and we produce a list of who appeared when, for each species. Shown here is a typical data series.

You begin to see trends. For example, towards the right-hand end of this figure, you get our sea-ice diatom Fragilariopsis curta quite a lot in one period, then none for a while and up again later on. And then you will get others that are warm-water species, such as Azpeitia tabularis, popping up all over the place as well. So you will get this sort of record that you will get some sorts of trends in and that you can draw lines on, in relation to the isotopic events and isotopic records that we would take. And we get some sort of age scale going as well.

We then apply these, usually through various statistical methods, to try and marry up what we view today at the surface with what we then see when we look at the past.

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There are statistical methods very well established now for sea surface temperature; we have a very good way of indicating sea surface temperature back in time – all that record with all those species ends up giving us a sea surface temperature record back through time. So we know that sea surface temperature for this particular core has varied from today, at around 4°C, to back in time when the sea surface really did get quite cold.

We try and marry these up with sea-ice estimations. Sea-ice estimations statistically at the moment are very contorted, and we are looking at ways of putting a new methodology together to solve the problems. But essentially the gist is that there are three models at the moment, and that you will get sea-ice predicted in some cases, or estimated, and then not, in certain periods. They pretty much all show reasonably the same record, but we are trying to tighten that up. So that is where that science is going at the moment.

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How do we then apply those core records? For instance, shown here are today's conditions around Antarctica. We have summer sea-ice (SSI) shown in green, and the winter sea-ice (WSI) extent in blue. We have all the different oceanographic frontal regions – this is all work done by Steve Rintoul, at CSIRO in Hobart, where they are able now to pick up all the different types of fronts that actually occur between Tasmania and Antarctica, at least. And we have got all these little yellow spots and these stars – the stars are the ones with the diatom records that we have, and the yellow spots are more that are derived from foraminifera and other microscopic organisms for palaeo records.

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Then when we plot up a time slice – you could take whichever time interval you are interested in – here is the last glacial maximum at 20,000 years ago, and we know from the cores that there has been winter sea-ice at least out to the points on the edge of the blue area. By using the temperature also, these records reconcile with the fact that we have sea-ice, and there are indications that the oceanic fronts did actually move northwards as well.

So we can look at the records that we get from the cores, and slowly piece together what happened in the past.

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Now we want to ask how diatoms can indicate changing nutrients in the ocean.

Diatoms are not directly affected by changes in CO2 levels, because they are relying mostly on the fact that their skeletons are actually made of biogenic silica, rather than the organisms that we mentioned before, the calcium carbonate ones that are going to be affected most significantly by the acidification of the ocean. But indirectly these diatoms are going to be affected through that acidification by changes in the ecosystem itself. If the other organisms don't exist any more, whoever ate them, what are they going to eat now? They are probably going to eat these guys, I don't know. They might not taste good.

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To look at nutrients I am going to take you to another study site that I worked on in the last few years. This is on Kerguelen Island, where we did a big study on the influence of iron off the island and the plateau, to see why this area blooms. (This is the chlorophyll concentration annually in this region. As you can see, there is very high chlorophyll along the coast and also in the region that is indicated.) We wanted to understand what were the inputs then of iron to the actual community here, and also the biogeochemical processes. I won't talk about those today, but I will talk about what I found.

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To set the scene, we have here a couple of sample sites where I took sea-floor sediments. This is to just to give you an indication, if we draw a line through, of what it looks like. The Kerguelen Plateau is at 500 metres depth, there are a couple of ridges and troughs, and then it jumps straight down and we hit the sea-floor, where we get Antarctic Bottom Water actually hitting the side, the second polar deep waters, and the influence of the Antarctic winter water going over the top. So that gives you a general idea of what is happening there.

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We then plot up those samples. We already have a sample database with the French, the Crosta et al. database, which provides all the black dots that you see here. And we have some in white that we added in just to see what was going on on the plateau itself.

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What we found – but were not expecting, since there was this huge production happening – was that there was actually a lower abundance of diatoms on the plateau than there was in the deeper oceans, the sea-floor sediments. That was quite a surprise.

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What we wanted to do was to find out whether there were certain diatoms that were actually indicating productivity events. And we did find some.

We found the Chaetoceros species that make big heavy spores which do fall out; they were in the hot-spotted area at the top right here. We found a couple of others, again hot-spotted on the plateau for different reasons.

And then the open-ocean ones, which generally are ubiquitous, found everywhere, these guys we mostly didn't find on the plateau. They were there, but they were in much decreased amounts compared with elsewhere.

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This information is interesting, but in terms of understanding what was going on up at the surface, versus what was actually getting down to the sea-floor, there is still a gap that has got to be bridged. It is very nice to find out that we have got nutrient highs and lows, and these can be revealed by indicator species, but we have now got to go back up to the surface and work out why these indicator species are here, because of the iron et cetera. So that is another work in progress.

We really do want to work out who is doing what, and what the nutrient levels actually do to the community there.

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Over that plateau we had a lot of silica depletion because of the high productivity of the community there. What happened was that we actually went to one site, in the middle of the map shown here, about four times. When we first got there, there was one diatom in particular that was quite prevalent, Eucampia antarctica, which made lovely long chains full of lots of organic material. They were doing quite happily, thank you very much.

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But as the bloom progressed over time, these fellows broke up their chains and became doublets, and then started doing something very strange with their frustules. By the end of the whole period, when we had been out there for just on a month, they looked like the photographs here dated February 12th.

I looked at one of these samples first before I actually found the other one, and I didn't know what it was. I had never seen this before. So we went out there and realised, afterwards, when we were piecing this together, that as silica depletion went along, with the bloom taking up all the nutrients, we suddenly got these funny species doing funny things which we hadn't seen before. This signal won't get down to the sediments, of course, but the doublet dated February 4th does – when we actually looked in the sediment trap material, we found that it was getting down to the sea-floor, so we could see that the change in the nutrient content was sort of getting down to the sea-floor. And again this is just little jigsaw puzzle pieces getting put together.

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In a current study off Tasmania that I did in January this year – we move around a lot on boats – we did the SAZ-SENSE mission. This was a biogeochemistry mission that I participated in, and I work with a huge group of French and Belgian people who are all doing the biogeochemistry. I am just looking at all the diatoms themselves.

We did three process stations here. P3 is in the subtropical waters, which are naturally extremely depleted in silica, so we are not really expecting to find diatoms at all. The area labelled P2, in the polar frontal region, has a lot of silica and has a huge amount of productivity with the diatoms.

What we wanted to do was to introduce a marker by which we could start understanding the silica cycle. We put in a fluorescent marker. When we went to these sites, we put the fluorescent marker in, left it for 24 hours, pulled some diatoms out, killed them off, and put them under fluorescence microscopy to see what was going on.

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This is what happens. The red here is the chlorophyll of the organism, and all the bits that you see fluorescing here are where the biogenic silica has been taken up in the 24-hour period. You might think, 'Oh, that looks fine, but what are all the little black bits in between?' That is where the old cell was.

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You can't see the old cell, which the diatoms are replicating, but all the new stuff you can see. So we are actually starting to get an idea of who is active, who is doing something.

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Here are some others – a big chain of diatoms, Chaetoceros, here. And again the sister cell which would have made the whole unit is in black, so you can't see that. But this one was actively dividing during that 24-hour period.

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This is the tube one here, Dactyliosolen antarctica, with its internal matrix. This one is a ring of crescents, basically, stacked upon each other. As we can see, it was actually adding rings during that 24-hour period to make itself longer.

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Let's look at some of the results. Here is the low biogenic silica (BSi) at depth at the first site, P3, shown in the yellow circle. When we looked at the fluorescence part in the composition of the species, we found that in the Rhizosolenia, another tube forming species, 57 per cent of the actual assemblage was fluorescing – active, doing something. When we did the counts that we would do when we look at them normally, however, we found that that Rhizosolenia only made up 1 per cent of the whole diatom assemblage, and that the Pseudonitzschia, the 62 per cent ones, were actually the most abundant. In the 'olden days', we would have said that Pseudonitzschia was the most active, it was the one doing all the business, but we actually realise now that it was probably in a stage of either senescence or just hanging around – it certainly wasn't doing anything active at that point in time.

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In the Polar Frontal Zone there is actually a lot of silica available, and the drawdown at the top is where all the diatoms are active, taking it up. Again we get the Rhizosolenia, which was going crazy, essentially – 91 per cent there. In terms of its actual contribution to the whole community, it was only 18 per cent. We had another lot of Chaetoceros in the contribution, whereas it showed up as 4 per cent active.

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Finally, the other process station was again in a zone where we did not expect diatoms, and certainly there is no silica available anyway. We have Cylindrotheca – you can barely see the blip in the image to say that something is going on – we had a couple of Thalassiosira species, and we also had Pseudonitzschia at 6 per cent.

When we did the counts, it was the only one that actually matched up. So the abundance in Cylindrotheca – there weren't many diatoms anyway – indicates that it was pretty much the only one that was still actively doing something in the community there.

So we are starting to understand the community processes, linking them in with what is actually available for the diatoms in this area.

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The fluorescent markers really do enable us now to understand more about the community under the nutrient regimes. There is another group in Marseilles, where I have been working, who are now looking at fluorescent markers for calcium carbonate organisms, particularly the coccolithophorids, to see what is going on in those. Again that is a study in process.

So where is the next frontier?

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There are a few frontiers, obviously, but the next frontier for me at least is putting together a new survey off Adélie Land, in Antarctica. This is a huge area of oceanographic and glacial study at present, especially to do with the Mertz Glacier – it has started to crack up, so we don't know where that is going. At the moment this physical extrusion from Antarctica regulates the whole sea-ice area through this region. We have got lots of bergs broken up, and all of the sea ice gets shifted around because all these broken up bergs are stuck here on the contours and push most of the ice past this zone.

This zone is also extremely important because it is the Mertz glacial polynya, and that is the zone where in fact 24 per cent of the Antarctic Bottom Water is formed. It is formed in this area due to the Mertz Glacier itself, so again if this glacier goes, this zone which produces the Antarctic Bottom Water may in fact close down completely. We have no idea at this stage, but it looks as though that will be the indication.

We have from this region two fantastic cores, one from the US area and one from the French. They are between 40 and 30 metres long, and they have fabulous laminations that are 1 millimetre thick. What we see are dark laminations, light laminations, dark laminations, light laminations, all the way down the 40 metres. Those cores have been dated, and they are only 11,000 years old, so we have what appears to be the annual seasonal cycle in the palaeontological record all the way down.

The palaeontologists, not having any information about what lives, breathes and exists in this area, are making huge guesses now to say, 'Oh, the dark lamination. Well, that's when the sea-ice melts, we have the big bloom and there is a bit of IRD input' – ice-rafted debris input – 'and that's coming down and that's why they're dark, and that's that period of time. And that light stuff? Well, that's just before the sea-ice comes in, and we've got lots of sea-ice diatoms in that layer.' So they're starting to make guesses, and there are a couple of layers where there is just a monospecific species and they are saying, 'Oh, that's because there was an autumn ice breakout,' or something or other. So it is really storytelling. (I hate to tell them that!)

My proposal, then, is to bring in the sediment trap now and place this at least 400 metres below sea level, because of icebergs – they all ground before the 400-metre mark. So we are proposing now to put some traps in, to see what is actually coming from the sea surface down to the sea-floor, so we can resolve what these laminations and seasonal signals may be. In doing so, hopefully, we will now be able to marry together the surface, the sediment that is coming down through that twilight zone, and also all those little black spots in the map image at the top of the slide, the samples that were taken just recently, this January. They are all surface samples of the diatoms, which I have got now. We hope to marry them all together and finally make a model that works – with everything.

Where is the use in monitoring the future here? As Malcolm McCulloch pointed out, the warmer waters have started coming. That will mean less sea-ice as well, so the whole ecosystem in this region is going to change, married with the fact that the Mertz Glacier may no longer be there in the future – we don't know. We don't know whether it will just ground off here and the whole region will continue to do the same thing. Nevertheless, we will be able to start seeing that there are warm-water invasions. So by taking some sediment traps now, at least while the system is still quite stable and doing what it has been doing for quite some time, by the sound of things – from the cores – we will be able to benchmark what is living there and why they are doing it and how they are doing it. This is really what is going to be important, to go back and have a look at this area to see what is going on in the future, as climate change continues to increase its effect with warm waters and the increasing pH.

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In summary, diatoms are unique microscopic organisms that enable us to decipher past environments
or oceanographic states, and deciphering their signal from the modern environment via the sediment traps and fluorescent markers will give us a better interpretation of them as a biological indicator of
climate change. And, finally, the new observations will certainly be central to future global warming
impact assessments.