Dear Mihir,

As you will see on the solar power Page, there are two major groups of solar-powered slugs. One group, the sacoglossans, are essentially herbivores who remove intact plastids from the plants and keep them alive and functioning in their own bodies. The second group are essentially carnivores, or related to carnivores, and they nurture single-celled plants [zooxanthellae] in their bodies. In most cases they have 'stolen' the zooxanthellae from their original cnidarian hosts [such as sea anemones or soft corals].

Quite different procedures are needed to keep these two types of animal - and their food - in aquaria. As far as I know only the first group have been successfully kept and studied in the lab. If you go to the Elysia chlorotica and Elysia clarki Fact Sheets and look at the attached messages you will find addresses of a number of researchers working in this field.

Concerning the second group, Ingo Burghardt [ingo.burghardt@rub.de] may be able to offer some suggestions,

Best wishes,
Bill Rudman

Dear Sam,
When I suddenly get 5 or 6 messages all asking much the same question, I think it is fair to suspect that a teacher has asked a class to answer a question. So this answer is for all of your class mates as well.

The ability of some animals, such as solar-powered sea slugs to remove functioning plastids from plants and keep them alive in their own bodies [sacoglossans] or to keep whole plant cells alive in their bodies [nudibranchs], is fascinating for many reasons and is fertile ground for opisthobranch workers, physiologists, botanists, geneticists etc. I think it will be many years before we can say just how the symbiosis works. I think Kerry Clark coined the term kleptoplasty, or at least popularised it, for the phenomenon of 'stealing' plastids. It is from the same Ancient Greek word which gives us the word kleptomania - [compulsive stealing] an affliction which seems to infect American filmstars with monotonous regularity.

And now to your question about whether this is a tertiary symbiosis. I guess we have to define what a plastid is and what its origin is. This is, I am afraid, getting a little outside my field of expertise. What I can say is that you should have a look at some of Lynn Margulis's publications. I have a very thumbed copy of her 1981 book Symbiosis in Cell Evolution but I am sure you can find more up to date editions to have a look at. She clearly stated the hypothesis that eucaryotic cells evolved from bacteral ancestors by a series of symbioses. Many cell organelles are considered to be symbiotic organisms which 'invaded' protoorganisms in the early stages of the evolution of life on this planet. Plastids, like mitochondria, have their own genome, and at cell division act as though they are symbionts. I don't know if we gain much in our understanding of their biology by trying to number their 'grade' of symbiosis.

As I said above, their are two types of 'solar powered slugs. If we first consider the sacoglossans. In plants, the plastids could be considered primary symbionts. When they are removed by sacoglossans to their own cells, the plastids still occupy the same position in relation to the cell, as a primary symbiont. However if we look at the plastid in the sacoglossan we could say that this is its second primary symbiosis.

If we look at the solar-powered nudibranchs, the situation is a bit more complex. They remove whole single-celled plants [zooxanthellae] from the primary host (usually a cnidarian) and re-use them in their own tissue. In this case the plastid is a symbiont of the zooxanthella which is the symbiont of an animal. I guess you could call this a secondary symbiosis but it all becomes quite confusing if you want to record that it has been moved from its first host to a second host. In fact I once described the removal of zooxanthellae from cnidarians to nudibranchs as a 'secondary symbiosis' but I was describing the transfer of the zooxanthella from its primary host to a secondary host. You, on the other hand, are trying to number how many steps we can go back until we get to the first symbiont. I think its all a bit confusing and doesn't really enlighten us very much.

• Margulis, L. 1981. Symbiosis in Cell Evolution W.H.Freeman & Co.: San Francisco. 1-419.

I hope my answer is not too confusing,
Best wishes,
Bill Rudman

Dear Caroline,
I guess you have found the Solar-powered Sea Slug Page where there is a lot of introductory information.

It's a bit hard to answer your question about 'what benefits' the algae receives from its relationship with sea slugs. Asking about benefits suggests that there is an accountant sitting there balancing expenditure against income. I'm afraid nature doesn't really work that way. These systems have evolved over millions of years and don't necessarily utilise the most cost efficient methods of operation. The important thing is that the whole system works as a single unit and the organisms involved survive to reproduce and pass on the system to the next generation of participants.

We are not even sure that the one-celled algae (zooxanthellae) can survive outside the slug. The zooxanthellae are related to free-living algae called dinoflagellates, but I don't think there is any research that has shown that they can complete their life-cycle as free living plants. Asking about the benefits of living in the slugs suggests there is an alternative, when in fact there probably is not. The symbiosis between zooxanthellae and animal is now an integral part of the life of both the plant and the animal. We might feel inclined to say that the plant benefits from a stable protected environment in the animal, but that doesn't mean very much because the plant probably hasn't any alternative.

You must also realise that in the case of the sacoglossan sea slugs it is not a whole plant that is kept alive in the slug's tissues, but just the chloroplasts, which are the organelles found in green plant cells which photosynthesise. In the case of chloroplast symbiosis, the chloroplast is either a 'slave' of the plant or a 'slave' of the sea slug, without one or the other it will die.
Best wishes,
Bill Rudman

Dear Tom,
One of the main differences between plants and animals is that plants produce their own food by chemical reactions while animals obtain their nutrients by eating existing organic matter. Sea Slugs are a specialised group of snails (Phylum Mollusca), and are definitely animals. Some are herbivores (plant-eaters) while others are carnivores, often eating only a very specialised group of animals.

There are two fascinating groups of sea slugs, which I have called 'Solar Powered' because they have become very plant-like in their behaviour. Have a look at the Solar Powered Slugs Page for some background information on these animals. Perhaps they are what made you wonder whether they are in fact plants?

Have a look also at the messages below yours on this page as there is more information with each message. If you click on any underlined word it will take you to another relevant page.
Best wishes,
Bill Rudman

Daniel sent this request to me personally and with his permission I have posted it on the Forum. If anyone would like an assistant or could suggest someone he should contact, perhaps they could email Daniel directly.
Thanks,
Bill Rudman.

Dear Liz,
Congratulations to you and your colleagues on this publication. It is nice to have a Sea Slug as the 'covergirl' on any journal and it is certainly a bonus to have it on a plant journal!

This is a very useful review of our knowledge of the physiology and evolution of the slug - chloroplast symbiosis. Although, as you say, it is from the chloroplast's point of view, it will definitely be required reading for anyone wishing to understand the significance of the symbiosis.

It also has a very interesting summary of the life history of Elysia chlorotica, and also has some useful recent references which I will need to add to my list of references on the topic.

Bill Rudman.

Dear Mark,
To my knowledge there are no dorid nudibranchs with an algal symbiosis. The closest relatives - and they are not very close - would be the aeolids and arminoideans I discuss on the "Solar-powered sea slugs" Page.

If you know of any dorids, or have suspicions about possible symbionts, I would like to hear about them.

Bill Rudman.

Dear Molly,
I guess the 'Ruffled Sea Slug' is Tridachia crispata, which is found in the Caribbean. It is quite similar in shape to species such as Elysia ornata to which it is closely related. Tridachia and Elysia are sacoglossans, a group of herbivorous sea slugs, which suck the cell contents from the algae they feed on. Some have developed the means to keep the photosynthetic plastids from the plant tissue alive in their bodies where they are able to photosynthesise and provide extra nutrients for the animal. There are a number of families of nudibranch sea slugs which do something similar, keeping whole one-celled plant alive in their bodies. Have a look at the page on Solar-powered sea slugs for further information, and be sure to look at the messages and answers below yours on this page.

Best wishes,
Bill Rudman.

PS: Unfortunately I don't have a photo of Tridachia. If anyone out there can oblige I would be grateful.

Dear Jennifer,
If you look at the page on 'solar-powered' Sea Slugs you will see that there are two quite different processes at work.

The herbivorous sacoglossan Sea Slugs, suck the cell contents from the sea weeds they feed on. From this cell sap, they keep alive and functioning the plastids (those parts of the plant cell which convert the sun's energy into sugars). The conversion of the sun's light energy into food for the plant is called photosynthesis. In green plants the plastids are green, and are called chloroplasts. Most sacoglossans are coloured by the plant pigments they retain in their bodies.

Amongst the nudibranch Sea Slugs, which are all carnivores, a number of different families have evolved ways of keeping microscopic single-celled plants alive in their bodies. These single-celled plants are called zooxanthellae, and although they have free-living relatives in the plankton, they are adapted to living within the tissues of animals. The most spectacular zooxanthellae are the species which live in the tissues of coral animals. Without their symbiotic zooxanthellae, the tiny coral polyps would be unable to produce the calcium carbonate skeleton, which is the building material for the great coral reefs of the world.

Now to your question about what benefit the plant gets from the association. I guess your question refers to the Sea Slugs with zooxanthellae. I'm afraid applying cost-benefit analysis questions, which are the joy of accountants, probably doesn't have much meaning in the natural world. In the real world the only reward is survival and the ability to produce a new generation to carry on your genes. I guess being a microscopic free-living cell, floating around in the plankton, has its risks. There are many filter feeders waiting to eat you and you are at the mercy of the currents and tides. Despite this, free-living phytoplankton are clearly a very successful life form. From all accounts, living in an animal which has evolved special anatomical features and behaviour patterns, for your comfort, has its benefits, much like a plant being cared for in a greenhouse.
Ove Hoegh-Guldberg's studies on Pteraeolidia ianthina showed that zooxanthellae within its body, breed very rapidly, and at the same time produce nutrients, far in excess of their own requirements. This suggests that the zooxanthellae are living in a very healthy, protected environment.

The zooxanthellae are specially adapted for this symbiotic life and although we are not 100% sure, it seems they do not have the ability to live free. There is therefore not much point in listing the good and bad aspects of this life in some sort of balance sheet. This is the only life possible to them, they do not have the alternative of a free-living existence.

Best wishes,
Bill Rudman.

Dear Derek,
I am not sure what level you are at in your studies so its a little hard to know at what level to answer your question. If you are at university, I would suggest you look at some of the references I have just posted on chloroplast symbiosis. Also look at the information at the top of this page above your message, and also at some of the correspondence you will find below your message. You will also find some information on the Flatworm Page about Convoluta roscoffensis which is a flatworm with symbiotic chloroplasts.

Best wishes,
Bill Rudman.

Dear Jussi,

There are sacoglossans in quite northern latitudes with symbiotic chloroplasts. For example Elysia chlorotica in Nova Scotia and Elysia viridis in England. Also the photosynthetic flatworm Convoluta roscoffensis lives in the North Atlantic.

I have posted a list of publications on chloroplast symbiosis which may be useful. Any updates would be welcome.

One active research worker in the field, who could give you up to date advice is Cynthia Trowbridge whose address is:

Dr. Cynthia D. Trowbridge
Research Assistant Professor,
Oregon State University
Department of Zoology/Hatfield Marine Science Center
Newport, OR 97365
USA
fax 541-867-0105
trowbric@ucs.orst.edu

Best wishes,
Bill Rudman.

Dear Michael,
I am not an expert in plastid physiology so I have sent copies of your message to a few colleagues who hopefully are more able to answer your question intelligently.

There are however a number of general points.
You say there are a number of genes in the Elysia which match the genes in the Vaucheria it feeds on. The obvious question to ask is how did you ensure that the Vaucheria-like genes were not contaminants from its food?

The other point is what got me interested in these symbioses in the first place, and that is the morphological adaptations that the "host" has undergone to become an efficient plastid or zooxanthellae "farmer". All these animals are related to animals which don't have symbiotic relationships and we can see how in certain phylogenetic lines of animals species have modified their anatomy, (finely branched gut, branches into the epithelial layer, flattened cerata, transparent bodies etc) all to better enable them to keep their plant tissues in an optimum environment for photosynthesising. A good example is shown in the aeolid genus Phyllodesmium where in one genus we can see major morphological changes which are correlated with the varying ability between species to grow zooxanthellae in their bodies (Rudman, 1991 - see references at top of page).

All things being equal, if gene transfer is the key - and possible, - then I suspect the experiment would only work in animals that had by chance a morphology which would provide an hospitable "nursery" for plant tissue. For example, the skin of most vertebrates, I would think, would block out sunlight and so prevent photosynthesis.

If you have any photos of Elysia chlorotica either on or off its food, or some photos of the plastids, it would be nice to put them up on the Sea Slug Forum.

With luck, one of the people I sent copies of your message to, will reply.
Best wishes,
Bill Rudman.

Dear Tammy,

I know teachers often like to pigeon-hole nature into convenient categories but I'm afraid the relationships that organisms form with one another forms a continuum which defies our best attempts at dividing into suitable categories. In the Middle Ages, theologians used to discuss in great seriousness how many angels could fit on to the head of a pin. I suspect attempts at categorising relationships between organisms is of similar value.

In this case, the plant involved is a dinoflagellate algae belonging to the genus Symbiodinium or Gymnodinium. These dinoflagellates are known as "zooxanthellae" and are commonly found living in the tissues of cnidarians. Without them the polyps of the tropical hard corals would be unable to build the huge coral reefs of tropical waters. Other invertebrates also harbour zooxanthellae, including the Giant Clams (Tridacna spp). The relationship is usually described as an "endosymbiosis" and as I said above, in the case of reef-forming corals, seems to be essential for the coral's well-being. The increased incidence of coral-reef "bleaching", where the coral colonies over large areas eject their zooxanthellae, is causing grave concern amongst reef ecologists.

There is also debate over how many species of zooxanthellae there are. Some say there are only a few species, others that each 'host' has its own species of zooxanthellae especially adapted for that 'host'. The zooxanthellae in nudibranchs are particularly interesting in that debate because they are zooxanthellae which have been removed from their initial host, a cnidarian, and transplanted to a second host, a mollusc, in a completely unrelated phylum. If a zooxanthella can survive in two quite distinct phyla then it would tend to support the argument that there are a few widely distributed species of zooxanthellae.

The other point to realise is that the ability to "house" and "farm" zooxanthellae in nudibranchs has evolved independently a number of times and not all "hosts" are equally proficient in doing so. Some species seem to do no more than temporarily retain zooxanthellae until the zooxanthellae die. In these cases they are probably only useful as colour camouflage as they help to colour the slug and so camouflage it on its similarly coloured cnidarian food. From such simple beginnings we can find all stages to the "ultimate" stage where zooxanthellae are successfully farmed and bred within the nudibranch's body and the nudibranch gains a significant proportion of its nutrient requirement from the zooxanthellae.

If you are thinking of sea slugs as a whole rather then just nudibranchs, then a few words about the sacoglossans. They have a remarkably similar story. Instead of removing whole plants from their food animals, like the aeolid nudibranchs, they are herbivores which remove the plastids from the plants they feed on intact. Again I guess this is a "symbiosis" though the plastids are hardly a potentially "free-living" partner.

Plastids are considered cell organelles. If you have time a fascinating book to look at is:
Margulis, L. (1981). Symbiosis in Cell Evolution. Life and its Environment on the early Earth. W.H.Freeman & Co: San Francisco.
In it she discusses her ideas about the evolution of life and how plastids and other cell organelles such as mitochondria possibly evolved as endosymbiotic organisms in early protozoa.

Hope this of some help,
Best wishes,
Bill Rudman.

Dear "j.e.",
Your obviously have been doing some thinking and reading! Sorry I can't answer all your questions at once, but in the hope someone out there has something to say on any of your points I am posting your questions unanswered. .. and will get to them in the next few days.

I hope you find some some animals in the Sargassum. If you have the facilities to photograph anything you find, including Hypselodoris zebra, I would love to post them on the Slug Forum. If you can't provide scans that is no problem. Just send photos or slides to me at:
The Australian Museum,
6 College St
Sydney, NSW 2000
Australia.

I will scan them here and return the photos to you.

Best wishes,
Bill Rudman.

Dear Amanda,
Your question inspired me to put some more examples of "solar-powered" sea slugs on the Slug Forum. Have a look at the examples I have mentioned above on this page.

I'm afraid your proposed experiment is doomed to failure I would think. The process of photosynthesis involves a series of complicated chemical reactions. Chlorophyll is involved, at least in green plants. It is a molecule which traps light. For anything to then happen needs the combined activity of the other molecules and membranes that make up the chloroplast or plastid within the plant cell. Have a look at a text book on photosynthesis to see the wonderful series of chemical reactions that need to occur before the conversion of light to sugars and starches takes place.

That is why the sea slugs can only act like plants by either farming small plants in their bodies (as in the case of the nudibranchs with zooxanthellae), or by keeping the plastids, which are the little photosynthetic factories in plant cells alive, (in the case of the sacoglossans).

I'm sorry if this is not good news for your experiment but I hope it will give you some ideas.

Best wishes,
Bill Rudman

You ask quite a few questions so I'll answer them in order.
1. A good source of information on mollusc phylogeny. The most comprehensive and up to date work would be:
Beesley,P.L., Ross,G.J.B. & Wells,A (eds) 1998. Mollusca: The Southern Synthesis. Fauna of Australia Vol 5.. CSIRO Publishing : Melbourne. Part A pp1-563. Part b pp 564-1234.
I must declare I was involved in writing parts of it but it is generally accepted as the best around at the moment.

2.re photosynthate release. Have a look at

Hoegh-Guldberg,I.O. & Hinde, R.,1986. Proceedings of the Royal Society of London, Series B, 228:493-509.

Hoegh-Guldberg,I.O., Hinde, R. & Muscatine,L., 1986. Proceedings of the Royal Society of London, Series B, 228:511-521.

3. Are the zooxanthellae in special vacuoles? They seem to be in modified ducts of the digestive gland in most but not all the species. sometimes they sem yo be loose in the ducts and in other species they seem to be in subepithelial cells. I have described the position of the zooxanthellae in the various papers I cite at the top of this Solar-powered page.

4. The anemone that Aeolidiella foulisi is feeding on in the photo is Anthothoe albocincta.

5. And lastly, yes I can give you Terry Gosliner's email address. It is
tgosliner@casnotes1.calacademy.org

Good luck with your research and please let us know of any interesting discoveries you make. .... Bill Rudman.