Marine fish are wonderful, of course, but the main attraction in a reef aquarium is the diverse assortment of invertebrates that we can now keep with success. This diversity is far greater than what we could keep in freshwater aquaria. Though there are many interesting species of invertebrates in freshwater habitats that could potentially be kept in aquaria, many of them are insects that have the annoying habit of maturing into winged adults that leave the water in search of mates and new places to lay eggs. Needless to say, aquaria filled with aquatic insects do not go over well with most spouses. In contrast, most marine invertebrates are fully aquatic and, furthermore, many of the major marine invertebrate groups are either totally absent in freshwater (e.g. echinoderms and tunicates), or far less diverse than in the ocean (e.g. cnidarians, sponges, and others). Many of these marine invertebrates are strange, indeed bizarre, from our mammalian perspective. For most people, many of the marine invertebrates might as well be aliens from another planet: they are that strange. The same might be said for most of the marine macroalgae.

Many of these marine organisms challenge our conventional notions as to what it is to be an organism. For example, some of the macroalgae, such as various species in the genus Caulerpa, challenge the idea that all cells are small, since a given individual of Caulerpa is not a collection of cells, but one huge cell. Similarly, corals and some of the other invertebrates challenge our notions as to what it is to be an animal. After all, the giant clams and most of the corals we grow have symbiotic dinoflagellate algae (zooxanthellae) living within their tissues, which carry out photosynthesis, using light energy to make food for themselves and their animal hosts. Many sponges also have photosynthetic symbionts living within them (in sponges these are usually cyanobacteria), as do some species of tunicates (sea squirts), and some other invertebrates. Indeed, keeping a coral reef aquarium is more like tending a garden of plants than like caring for animals, and these corals, sponges, and other sessile invertebrates have lifestyles and growth patterns that more closely resemble plants than animals in many ways.

Reef aquarists have become accustomed to strange, plant-like animals such as corals. However, some invertebrates challenge our notions of what it is to be an animal even farther, and at first glance it can sometimes be difficult to tell just what sort of organism you are viewing. For example, consider the following photo:

A close-up of the parapodia of a lettuce sea slug.

The beautiful iridescent ruffles in the photo above might look like the leaves or petals of some exotic plant, but in fact they are the ruffled flaps of tissue (parapodia) that outline each side of the back of a two inch sea slug that lives in the waters of the Caribbean and Florida Keys. This animal, Elysia crispata (formerly known as Tridachia crispata, and still usually sold under that name), is commonly known as the lettuce sea slug, so named because when the animal is at rest the parapodia make this snail without a shell look a lot like a small head of ruffled lettuce.

A wider view of the lettuce sea slug shown above.

The resemblance of the lettuce sea slug's parapodia to leaves is more than just a coincidence, since these structures, and indeed much of the surface of the animal, function somewhat like leaves. In fact, this sea slug carries out photosynthesis within its body. Like some of its relatives, this animal feeds by sucking the cytoplasm (the semi-liquid contents of the cells) from the cells of marine algae, but this species and some other sea slugs don't completely digest what they ingest. The lettuce sea slug keeps the chloroplasts (the structures within the algal cells that carry out photosynthesis) intact, and relocates them close to its skin. There, the stolen chloroplasts continue to function, using energy from sunlight to build energy-rich food molecules from carbon dioxide and water, but rather than feeding the algal cells that produced these chloroplasts, the food molecules that are produced feed the sea slug. Just as the leaves of a plant provide the plant with more surface area for the capture of sunlight, the parapodia of the lettuce sea slug provide more surface area for light capture. These parapodia also increase surface area for gas transfer (oxygen uptake and carbon dioxide release), so they serve double duty, functioning somewhat like gills.

A lettuce sea slug (the same individual as in the other photos) crawling on the glass in Augsburg College's coral reef aquarium (pink Bird's Nest coral in background).

A close-up of a ruffled frill of tissue along the back of a lettuce sea slug.

While at first glance the sea slugs might appear to be doing the same thing as corals, giant clams, and photosynthetic sponges and tunicates, this situation is fundamentally different. First, these photosynthetic sea slugs are not plant-like sessile organisms, but rather active, mobile creatures. Much more importantly, while the corals, clams, sponges, and tunicates house intact algal cells that multiply and maintain more-or-less stable populations within their hosts, the lettuce sea slugs are housing only the chloroplasts. These chloroplasts are not so much symbionts as they are stolen goods - dismembered parts from intact and fully functional cells. Though lettuce sea slugs are remarkably good at keeping the chloroplasts alive and functional, to maintain their solar collector arrays, lettuce sea slugs suck the cytoplasm from algae on a regular basis (www.seaslugforum.net).

The lettuce sea slug's use of stolen chloroplasts is indeed an interesting turn of events, especially when one considers the evolutionary origins of these chloroplasts. These chloroplasts have been engulfed by other organisms before in their evolutionary history, and indeed, some of the most critical moments in the evolution of muticellular life have involved the engulfing of one organism by another.

To understand this story, I need to give a brief lesson in cell biology. The most important thing to be understood is that there are two fundamentally different types of organisms in the world from a cellular structure perspective. Some organisms, called prokaryotes, usually have very tiny cells (frequently as small as a few millionths of a meter in diameter) with little obviously visible internal structure. The incredibly diverse bacteria are prokaryotes, as are the cyanobacteria (which essentially are photosynthetic bacteria), and another group known as the archaebacteria. The rest of life falls into a group called the eukaryotes, which are typified by having much larger cells (there are some exceptions, such as certain of the planktonic marine algae that have very tiny cells despite the fact that they are eukaryotes). Eukaryotes also have extensive internal compartmentalization and chromosomes packaged up inside a special compartment called a nucleus. The eukaryotes include such groups as the protists, fungi, pretty much all of the algae other than the cyanobacteria, the plants, and the animals (including you and me). In short, nearly all of the organisms most folks are familiar with are eukaryotes. The cells of eukaryotes contain many specialized structures called organelles (which means "little organs") that carry out specific functions. Along with the already-mentioned nucleus and a number of other organelles, eukaryotic cells usually also contain some very special organelles called mitochondria and chloroplasts, the latter being present only in plants and eukaryotic algae. Mitochondria play important roles in the breakdown of food molecules to release energy in a form that is useable by the cells, and the chloroplasts give plants and algae the ability to capture energy from sunlight and use it to manufacture energy-rich food molecules.

The really interesting thing about these organelles is that there is abundant evidence that tells us that mitochondria, chloroplasts, and possibly a few other organelles started out as free-living prokaryotes that got engulfed by other larger prokaryotes. These events resulted in the formation of the first eukaryotic cells. Not only are mitochondria and chloroplasts both about the same size and shape as some bacteria, but they have their own small chromosomes carrying a number of genes all their own. Furthermore, the DNA that makes up the chromosome of a mitochondrion or chloroplast is formed into a loop, as is the DNA in a bacterial cell. In contrast, the chromosomes in the nucleus of a eukaryote are in the form of strands. Mitochondria and chloroplasts are also both enclosed in double membranes. The inner membrane represents the original membrane forming the "skin" or outer surface of the original free-living cell. The outer membrane represents a "bubble" of the host cell's membrane turned inside-out that formed around the captured cell when it was engulfed. (To visualize this, imagine you are inside a large very flexible balloon and you pull another, much smaller, balloon inside without breaking the large balloon - the engulfed small balloon would have its own outer covering surrounded by a bubble formed by the outer covering of the larger balloon).

By engulfing cells of other species and keeping them intact and functional as internal symbionts, the first eukaryotic cells gained new functionality. The bacteria that gave rise to the mitochondria characteristic of eukaryotic cells today had unique biochemical capabilities. These ancestors of the mitochondria "invented" the highly efficient oxygen-consuming method of extracting energy from food molecules that we and most other multicellular forms of life use today, and brought these biochemical capabilities with them when they took up residence in their host cells. Similarly, the ability to perform photosynthesis evolved first in free-living prokaryotes, and they brought this capability to their hosts when they were engulfed by the ancestors of today's algae and plants. In time, these internal symbionts, or endosymbionts, lost the ability to live independent lives. They lost many of their genes as they became more and more dependent on their host cells for basic life support, and as they became more specialized and efficient at carrying out their own unique roles. Mitochondria and chloroplasts are now completely dependent upon their host cells, just as their hosts are dependent upon them. You could not live without the unique services provided by your mitochondria, nor could algae or plants live without their mitochondria and chloroplasts.

While the zooxanthellae within corals and giant clams are apparently not well adapted for independent life, they can in fact live on their own, and can be cultured outside of their hosts in the laboratory. This is not the case for mitochondria and chloroplasts, which can only reproduce within their normal host cells. The chloroplasts taken up by the lettuce sea slugs are temporary residents of their new hosts; however, their numbers in the sea slug's tissues are being maintained by regular ingestion of algal cytoplasm by the sea slug.

Lettuce sea slugs are molluscs, belonging to the Class Gastropoda, the most diverse of the molluscan groups. They essentially are snails without shells. Lettuce sea slugs are often erroneously referred to as lettuce nudibranchs, but in fact they belong to a different order of gastropods, the Sacoglossa, than the true nudibranchs, which are in the order Nudibranchia. Unlike the nudibranchs, the sacoglossan sea slugs lack the tufts of external gills that give nudibranchs their name (nudi = naked, branch = gill). Sacoglossans do have radulas, however, and this is something they have in common with all of the other molluscs except for the bivalves (the bivalves, including the clams, oysters, mussels, etc. lack radulas). A radula is essentially a long, slender tooth-studded tongue-like structure that in many snails is used as a rasp to scrape small bits of food into the mouth (See article by Ron Shimek for more information on radula function. Also see photos and diagrams of radulas: diagram of the mouth of a mollusc, diagram of a radula in action, photo of the teeth on a radula). In the sacoglossan sea slugs, the radula is reduced to just a single row of teeth that are used to slit algal cells prior to sucking out the contents (Ruppert and Barnes 1994). Sacoglossans tend to be quite specialized in their diets, often feeding on only certain algal species. In some cases, it appears that different species of algae are fed upon at different stages in the life of a given sea slug (www.seaslugforum.net). Not all sacoglossans retain the algal chloroplasts as do the lettuce sea slugs, but other members of their family (Elysidae) do.

One of these lettuce sea slug relatives has made the news in recent years as a possible solution for the plague of invasive Caulerpa taxifolia that is taking over the Mediterranean seafloor (see article on this problem , and another article: www.seaslugforum.net). Elysia subornata sea slugs, which feed upon Caulerpa taxifolia in its place of origin, have been collected by European researchers and are being evaluated as a potential biological control agent. The proponents of this approach argue that these sea slugs are absolute specialist feeders that would pose no threat to any other organisms in the Mediterranean other than their C. taxifolia hosts. This matter is in hot debate, however, since host switching has been documented in other herbivorous sea slugs, and some sea slug experts are very strongly opposed to any introductions of non-native sea slugs to the wild (www.seaslugforum.net). The danger is that if Elysia subornata were to start feeding on a new algal species in the Mediterranean, it might threaten some native species with extinction, and in so doing it may itself become a major force driving undesirable ecological change. There is abundant precedent for introduced species causing wholesale change in ecosystems, and extreme caution needs to be exercised when any intentional introduction is contemplated. According to Cynthia Towbridge (a sacoglossan sea slug researcher who opposes the release of the sea slugs), as of the time of this writing (April 2002) releases of these sea slugs into the Mediterranean have not yet been made.

The lettuce sea slug and other members of its family are not alone in their habit of gaining extra functionality by using cellular structures stolen from the organisms they eat. Some nudibranchs arm themselves with stolen nematocysts (tiny stinging structures produced by the cells of anemones, hydroids, and their relatives) from the cnidarians they eat. Somehow, they manage to eat their prey without discharging all of the nematocysts, and they relocate some of these nematocysts to certain regions of their skin, where they continue to function. Many would-be predators of the nudibranchs are stung upon contact with the nudibranchs. Also, some nudibranchs store the toxins produced by their prey for self-defense, thus arming themselves with stolen chemical weaponry.

As aquarium residents, sea slugs as a group vary greatly in their suitability for captive life. In most cases, the problem is that sea slugs are typically extremely specialized feeders. Many of the nudibranchs feed only on a particular species of cnidarian, sponge, bryozoan, or tunicate, for example. Berghia verrucicornis, the nudibranch that is now bred in captivity and marketed as a control for Aiptasia anemones in reef tanks, feeds only on this genus, and can only be maintained when this anemone is present in the tank. The specific organisms fed upon by other nudibranchs are often difficult or impossible to raise in captivity. In the case of the sacoglossan sea slugs, the particular algae that a given species of sea slug feeds upon must be present. Different sources cite different algae as the preferred foods of lettuce sea slugs, with various Caulerpa species as well as a number of other species of green algae typically being named (Kaplan 1982, and www.seaslugforum.net). In the aquarium trade, lettuce sea slugs are marketed as control agents for Bryopsis, though Delbeek and Sprung (1994) suggest that only certain color forms will feed on Bryopsis (see www.seaslugforum.net for photos of some of the different color forms).

Though the lettuce sea slug does not appear to be an extreme food specialist, many sea slugs are extremely specialized, and one might well ask why. Without question, at least a portion of the answer is that these animals feed upon sessile organisms that have extensive chemical defense mechanisms. Sessile organisms such as algae, plants, corals, sponges, and tunicates are sitting ducks for herbivores and predators. If an enemy attacks them, they cannot get up and walk, swim, or fly away. Consequently, a variety of other more passive defensive mechanisms have evolved in such organisms. Most corals, sponges, and tunicates, for example, are veritable arsenals of chemical weapons (if you have ever trimmed corals in your reef aquarium, have you ever wondered what the disgusting smells released by damaged Xenia and other corals are all about?) Many of the algae are similarly armed. Such defensive chemicals typically have high biological activity (indeed, there are several research labs at major universities that specialize in "prospecting" for new potential medicinal drugs from marine life such as corals, sponges, and tunicates), and these chemicals dissuade feeding by most animals. Animals that eat these chemically protected sessile invertebrates and algae need to have biochemical mechanisms for dealing with the toxins and other defenses, and this is apparently sufficiently difficult that extreme specialization exists for dealing with a small subset of the possible chemicals.

An analogous situation exists on land in the interactions between terrestrial plants and the herbivorous insects that feed on them. While the vast majority of marine invertebrates have been barely studied or not studied at all, given the great economic importance of plant-feeding insects the interactions between many herbivorous insects and their food plants have been extremely well-studied. These terrestrial systems shed useful insights into the likely interactions taking place between many marine invertebrates and their food organisms. Most plants produce toxins called secondary metabolites that deter most herbivores (though some of these compounds, such as caffeine, or the aromatic oils in culinary herbs are enjoyed by humans!) Consequently, each species or family of plants has its own group of specialist insect herbivores that have evolved mechanisms for dealing with that plant's unique toxins, and these specialists normally don't eat any other plant species. Often, these specialized herbivores even cue in on their host plant's unique toxins, recognizing the plant by its toxins and refusing to eat any plant that lacks the toxins. In some cases, the toxin alone is enough to stimulate feeding. For example, corn rootworm beetles (Diabrotica sp.), which as adults feed extensively on members of the cucurbit family (e.g., squash, cucumbers, etc) will eat paper that has been soaked in a solution of cucurbitacins. Cucurbitacins are compounds that are widespread in plants in the cucurbit family and that sometimes make cucumbers bitter. Similarly, the foul compounds in Xenia probably taste pretty good to the specialist nudibranchs that feed on this soft coral, and the foul toxins in Bryopsis and Caulerpa species probably taste pretty good to the lettuce sea slugs.

My experience with the lettuce sea slug has involved only the green form seen in the photos in this article, as this is the form commonly collected in the Florida Keys and sold by biological supply houses and some aquarium vendors. I have kept these sea slugs several times with varying success.

The first time my lettuce sea slug went into a very simple 20 gallon aquarium in a west-facing window in a lab in which the main algae present were red slime algae (cyanobacteria), Caulerpa paspaloides, and Halimeda opuntia. The tank had two normal output fluorescent bulbs plus natural lighting from the window, but it was winter and overcast most of the time. Within a day or two, the sea slug had taken on a reddish color (presumably from eating cyanobacteria?), and it spent its relatively brief existence in the tank perched atop objects in the best-lit portions of the tank. It lived only a few weeks, but since conditions in this tank were not ideal and I was relatively inexperienced with reef systems at the time, it is hard to say what caused its demise. My strong suspicion though was that inadequate diet and inadequate lighting were likely to blame.

My second set of lettuce sea slugs (3 individuals) went into the seagrass aquarium at Augsburg College (www.augsburg.edu), which at the time had a wide assortment of Caulerpa species (at least 8 species), as well as several species of Halimeda and a number of other green macroalgae. Water quality was good (supporting healthy coral growth) and there was intense lighting from a 400 watt metal halide light, but things did not seem right with these sea slugs. They spent much of their time wandering about, and they weakened and died within a few months. My impression was that they were not finding suitable food (or perhaps they died of old age? See below).

My most recent lettuce sea slug (the one in the photos) has now been living in Augsburg's roughly 70 gallon reef aquarium for 6 months. Two adults were originally purchased, but one disappeared within days of introduction to the tank. The remaining individual has been the picture of health. This tank has good water quality and strong lighting, as well as something that was lacking in my previous trials with this species...the green alga Bryopsis. This reef tank currently has several healthy patches of Bryopsis. Other than coralline algae, diatoms, some Valonia, and miscellaneous turf algae scattered about in fairly inconspicuous growths, these tufts of Bryopsis are about the only algae visible. The sea slug crawls about on occasion, but most of the time it can be found sitting still in a well-lit location (presumably "soaking in the rays" and photosynthesizing), usually atop a patch of Bryopsis. Normally Bryopsis patches are the only places it stays still for any length of time. Though this is circumstantial evidence, it really does appear that the Bryopsis and the good lighting are responsible for this particular sea slug's good health. However, though surely it must be eating, I have seen no obvious signs of its feeding activities.

The above photo shows the lettuce sea slug sitting on a patch of the marine alga Bryopsis, which is one of the sources of the stolen chloroplasts. This sea slug spends much of its time simply sitting like this in a well-lit location, providing the chloroplasts with the light energy necessary for the manufacture of food.

A roughly 6 cm wide tuft of Bryopsis growing on a piece of dead Montipora digitata skeleton. See closer view below.

Though it is sometimes a vexing pest in reef aquaria, Bryopsis is quite beautiful when viewed in closeup.

Though the lettuce sea slug is often cited as a control agent for Bryopsis in reef aquaria, my observations lead me to doubt the general effectiveness of this approach. Despite the fact that my lettuce sea slug surely must have been eating something for the past six months, and it appears to have a great fondness for Bryopsis, I have seen no obvious reduction in the size of the Bryopsis patches where it spends most of its time. My guess is that these sea slugs simply don't eat all that much. Actually, this would make a great deal of sense. While a typical herbivorous snail gets all of its energy from the algae it eats and digests, the lettuce sea slug is supplementing consumed food energy with sunlight energy captured by its stolen chloroplasts, meaning it probably does not need to eat as much as a non-photosynthetic animal would.

Nonetheless, Morgan Lidster of Inland Aquatics in Terre Haute, Indiana has told me of numerous successes in clearing Bryopsis from reef aquaria using lettuce sea slugs. Morgan pointed out that this works best in low flow/low surge tanks. Also, one of his recent success stories involved higher densities of sea slugs than in my tank (3 sea slugs in a 50 gallon tank, which cleared the tank of Bryopsis in about 2 weeks). I would love to hear the details of other Bryopsis control successes using lettuce sea slugs.

Whether or not they cure your Bryopsis problems, lettuce sea slugs are indeed lovely and interesting animals, and a wonderful addition to a tank with adequate lighting and suitable algal species for them to feed upon. Although various species of Caulerpa are often cited as foods, my only real success with this animal has been in a tank with Bryopsis, and Morgan Lidster's experience has been that Bryopsis is the only algae they feed on in his tanks (at least as adults). Also, given the lettuce sea slug's fondness for sitting right beneath metal halide lights, my recommendation would be to only attempt to keep this animal if you have intense lighting on your tank. One word of warning, however, is that most sea slugs have fairly short lives, with lifespans as short as 6 months often cited for these animals (obviously, my current sea slug is older, since it was an adult when I got it 6 months ago). Indeed, it may well be that some of my previous failures with lettuce sea slugs came in part from the slugs being near the end of their life expectancy when I got them.

A tank for lettuce sea slugs should not only be well-lit, but it should also be relatively free of hazards. Though they produce noxious defensive secretions from their skin (www.seaslugforum.net), it would be prudent to avoid housing them with any predators capable of handling an animal of their size. Also, these soft-bodied creatures could easily be sucked into an unprotected powerhead, or could end up slipping through the slots of an overflow box and ending up in the sump where other hazardous pump intakes might await them. Finally, very strong currents can easily dislodge them from the surfaces they are crawling on or sitting on, so the regions of the tank with high light intensities and suitable algae for them to feed on should have relatively calm water currents.

Though lettuce sea slugs are not to my knowledge being captive bred commercially, there are a variety of accounts of young being produced in captivity. Morgan Lidster tells me that lettuce sea slugs usually, if not always, reproduce when placed in the large commercial 1600 gallon systems at Inland Aquatics. Furthermore, the Sea Slug Forum (www.seaslugforum.net) has some terrific photos of juveniles growing up in a person's home aquarium, as well as several other accounts of reproduction in captivity. The larvae do not feed (they are lecithotrophic), and they undergo metamorphosis to the adult body form without an extensive planktonic period. One study demonstrated that the extremely fine-bladed Caulerpa verticillata is the preferred first food immediately following metamorphosis, but it appears that other algae will likely do as well. Thus, it seems likely that this species has potential for captive breeding programs.

If you decide to try keeping lettuce sea slugs in an aquarium, my recommendation would be to not do so simply for Bryopsis control, but also for the intrinsic interest of the sea slugs themselves. They are truly beautiful animals, and the biological stories behind that beauty can hardly be beat.

More information, and many more photos can be found by clicking on the following links:

For further information on the lettuce sea slug, go to: www.seaslugforum.net. This page also has some wonderful photos showing the great variation in color within this species, and some really nice photos of tiny juvenile lettuce sea slugs in an aquarium where reproduction occurred. I highly recommend you take a look at this site, if only to see the beautiful lettuce sea slug photos.

For information on solar powered sea slugs in general, go to: www.seaslugforum.net

For more information on nudibranchs that arm themselves with stolen nematocysts, go to: www.seaslugforum.net

For more information on nematocysts (and the cnidarians that produce them), go to: www.animalnetwork.com

For a great deal more information on sea slugs in general, and many beautiful photos of colorful sea slugs, explore the pages of the Sea Slug Forum: www.seaslugforum.net.

Delbeek JC, and J Sprung. The reef aquarium: a comprehensive guide to the identification and care of tropical marine invertebrates. vol 1. Ricordea. Coconut Grove, Fla. 1994

Kaplan, EH. A Field Guide to Coral Reefs, Caribbean and Florida. Houghton Mifflin. Boston. 1982

Ruppert E, and R Barnes, Invertebrate Zoology. 6th ed. Saunders. New York. 1994

All photos and images courtesy of William Capman.