A Spineless Column by Ronald L. Shimek, Ph.D.

Beautiful, but Unwelcome; Aeolid Nudibranchs
in the Reef Aquarium

"A thing of beauty is a joy forever: its loveliness increases; it will never pass into nothingness."
John Keats

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Figure 1. A colorful and truly beautiful temperate aeolid nudibranch, Phidiana crassicornis. As with all mortal things, unlike the beauty of Keats, it will eventually die and pass into nothingness.

To Send a Message

One of the eternal questions that has transfixed humans, probably since they could think of such things, is, "What is beauty?" We all "know" what beauty is, but it is really impossible to come up with a definition that satisfies everyone. Perhaps a more interesting question is, "Why is beauty?" There are all sorts of reasons that we might perceive something as being beautiful. Setting aside the biological reasons for the perception of beauty within our species, people generally define beauty as a combination of attributes that elicits a pleasurable response. From the aspect of an evolutionary biologist, many of the reasons given for the perception of beauty devolve into the mechanical and, sometimes, arcane world of perception of signals given by one species to another. Individuals within one species often wish to send signals to individuals of other species or just to the world in general. Perhaps the easiest of these signals to understand are those sent by one species to enlist the aid of another. We are all familiar with the beautiful color of many flowers, but many people don't realize that these colors are the plant's way of sending a message to some animal to come and help the plant reproduce.

Flowers' colors are often specific messages to particular groups of animals to tell them that the animals can get a reward, generally food in the form of nectar (sugar water) or pollen (rich in proteins), by visiting that flower. When the pollinator visits successive flowers, it can transfer pollen from one plant to another, thereby helping the plant reproduce. Neither the plant nor the pollinator "thinks" of this process in this way, of course. Plants have no nervous system and can't think, and all the pollinator is after is food. However, the transfer of pollen is not incidental. As the plant with the best signals gets the most visits from pollinators, and this can lead to more offspring, the whole system forms a positive feedback loop under the control of natural selection. Once the system gets going, it can get fine-tuned for specific pollinators; and if the signal for a specific pollinator is sufficiently common, some plants may develop a way to cheat. They give the signal to the pollinator, but don't offer the reward. Pollinators may still visit these plants and transfer pollen, but the plant doesn't have to expend the energy to produce the reward.

Figure 2. Similar signals, different rewards.
Left: The fairy slipper orchid, Calypso bulbosa, rewards pollinators, such as bumblebees, with pollen. Right: The color pattern and shape of the lady slipper orchid, Cypripedium parviflorum, seem to promise a reward; instead, the flower traps pollinators in its pouchlike "lip." When they crawl out they get dusted with pollen. If they are then tricked into another lady slipper, the pollen is transferred.

Not all signals are rewards, either; in our terrestrial environment we are all aware of the way certain animals signal to other species to tell them to avoid attacking or even getting close. Some animal signals are active, such as the facial expressions of a dog that feels threatened and cornered; but many are also passive, such as the coloration of patterns of Pepe Le Pew and his handsome, but malodorous, kin, and those of the yellow jacket wasps. I would bet that very few people who read this have ever been tempted to reach out and grab a large wasp. The avoidance of such patterns is instinctual in many animals and probably is in humans as well; but in addition, if someone does reach out to hassle said flying insect, he is liable to discover just how intensely certain insects can activate parts of the mammalian nervous system devoted to signaling pain. The learning experience that accrues from such an initial miscommunication ensures that henceforth the insect's message of, "I am dangerous, leave me alone!" is well and clearly understood.

Unlike many other terrestrial ethological situations, this type of signaling has exact analogues in the marine realm. In fact, as animals in the seas are much more diverse in body form, and have been evolving for much longer, than those on the land, many more examples of these behaviors exist in the oceans. The use of color or color patterns to signal or warn of an interaction's potentially unpleasant outcome is found throughout marine environments where there is enough light to see the colors. Coloring to signal potential danger is referred to as aposematic coloration and is almost ubiquitous.

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Figure 3. Warning coloration in dorid nudibranchs.
Left: An individual of Phyllidia varicosa, a coral reef nudibranch that is so toxic that the death of a single individual in an aquarium has caused fish mortalities. Right: Triopha catalinae, a toxic temperate nudibranch that lives in turbid waters. The brilliant white and contrasting orange coloration ensures a visible warning signal even in murky seas.

Having a color pattern of any sort implies the production, utilization and storage of pigments. Pigments are often complicated chemicals that may be metabolically "expensive" to produce and maintain. Thus, there is a cost of having "color" of any sort, but having a protective coloration is better than being dinner. Consequently, animals without a way of deterring their potential predators are often camouflaged. Another obvious, but oft forgotten, implication of either a warning or camouflage coloration are that the predator can see. As a corollary of these factors, animals that are preyed upon by predators that don't have eyes, such as those eaten by sea stars, are not aposematically colored, but might possess tactile camouflage, such as the covering of shells and debris that many sea urchins "wear."

Most predators are not indiscriminate in their choice of prey, and as a result, warning colors are often tailored to specific predators; we humans tend to forget that most animals are not as visually well-endowed as we are. While many animals can detect changes in light intensity, relatively few of these animals can detect images. Most animals with eyes have simple eyecup photoreceptors that can detect only changes in light intensity or direction. Visually capable predators in the marine environment are limited to four animal groups: the annelid worms, the cephalopod mollusks, the crustaceans and the vertebrates.

If I define "good vision" as the ability to form and process images, then good vision is not widespread in the annelids; only a few of the polychaetes have well-developed eyes, but those that do have them, such as some pelagic swimming predators, have excellent vision. Good vision is obviously found in the octopods and squids, but their distant cousins, the chambered nautiluses, have only "pinhole" camera eyes that are not very good visual organs. Many crustaceans have compound eyes, which may be very good image forming eyes, albeit with a different type of image than we would see. Within the marine vertebrates virtually all animals have relatively good vision, and virtually all of them are predatory, if not on animals then on various algae and protists. Some people may think that predators eat only animals, but this is, of course, poppycock. Predator-prey interactions as a subset of ecology or ethology encompass all potential predators along with all potential prey.

As I have described, visual predators and their prey are often involved in a co-evolutionary dance. Natural selection fine-tunes predators by promoting attributes such as more visual acuity and interpretative capability. An interesting corollary to this is, all other things being equal, predators are usually more intelligent than their prey. As a professor of mine once put it, rephrased so that the censors won't bleep it out, all a prey animal has to do to be successful is "breed like a bunny" and run like hell. That is an over simplification, of course, to make a point. But, dogs and cats make far more interactive pets than do rabbits or sheep. In aquaria, predatory animals such as fishes have a whale of a lot more personality than do their prey such as sponges, algae, or corals; this even may be said for fishes that eat other fishes, for example, lion fishes are often more interesting animals than are the fish that they may eat. The co-evolutionary dance works on the prey as well, though. They can develop means of hiding in plain sight, such as camouflage, or by behavioral attributes such as nocturnal foraging. Or… they may become dangerous to eat.

Nudibranchs = Mobile Poison Packages

All aquarists are familiar, in some regards, with snails. Snails are mollusks with a very peculiar internal anatomy; their guts are twisted 180º in relation to their head/foot region relative to all other mollusks. This means that in most snails, their anus opens not at the animals' rear, but rather just behind their head on what would be their right shoulder, if they had shoulders. This internal anatomical twist, and nothing else, defines what a snail is. Shelled snails are rather well-protected from predation. The molluscan shell probably evolved as a protective covering of some ancient worm, and it is supremely well-adapted for its function. One of the more interesting aspects of snail biology is that most snails can live quite well if their shell is removed. It happens occasionally even in nature. During the course of my doctoral research I collected and examined a skosh over 15,000 individual snails from subtidal and intertidal environments. Two of them were effectively naked. They had just a small remnant of their shell remaining, having lost the majority of the shell to breakage or erosion. Other researchers have noticed the same thing. In nature these snails eventually perish from predation or simple mechanical damage to their unprotected tissues, but until that happens they can live an effectively normal life.

If such naked animals had a way to protect themselves, they presumably could live and persist. Many snails and other marine animals accumulate materials from their foods in their tissues. This is particularly true of toxic materials. Indigestible toxic materials often are "physically sequestered," that is, enclosed in some sort of protective container, often membrane bound vesicles, which effectively seals them off from the body's metabolism. These materials, such as the heavy metals laughingly known in the aquarium hobby as "beneficial trace elements," are generally so poisonous that the animal can't excrete them without destroying its kidneys Both organic and inorganic poisons may be found in many marine animals, including snails, either enclosed in vesicles, or maintained in an insoluble and therefore non-toxic form, or incorporated in tissues in vacuoles wherein the internal conditions alter the toxic chemical to make it non-toxic. These various forms of detoxification are common in today's mollusks, and given the antiquity of the group, were probably also found in at least some of the ancient forms. Knowing that, it is not too hard to envision a scenario in which some particular ancient snail lost its shell, through some sort of genetic mutation. All of the animals in the taxonomic order Nudibranchia develop a shell during their larval growth. And all of them drop the shell from their bodies when they metamorphose from the larval phase to the juvenile form. Given that all nudibranchs do this, and given that they all do it in the same manner at the same time in their lives, it is likely that such a property was inherited from a common ancestor.

This "shell shedding" could be the result of a single mutation that happened in the ancient seas. It appears that the nudibranchs separated from their shells and in doing so, from their ancestral group of snails sometime in the middle Paleozoic era, probably around 350 million years ago. The common ancestor to all of today's nudibranchs was likely a shelled animal not terribly dissimilar to some of the grazing snails found in today's reef aquaria. This animal was carnivorous, and probably grazed on some sort of sponge or other toxic animal and in some manner it probably sequestered the poisons from its food in its tissues.

Once the nudibranchs separated from the main line of shelled snail evolution, they also diversified. Such small animals must have appeared as a snack to the predators of the time, and there were some fearsome benthic marine predators during that period. If the ancestral nudibranchs were toxic, it would be to their distinct advantage to be aposematically colored. This would drastically reduce their mortality as predators could learn to avoid them. The more distinctively colored, the more rapidly would the predators learn to snack elsewhere. It appears that being toxic and advertising that fact became a generalized nudibranch characteristic; today very few nudibranchs appear to be palatable to any other marine predators. Interestingly, those that are palatable are almost always camouflaged.

Spicy Slugs

During the winter, the native inhabitants of St. Lawrence Island, one of the Pribilof Islands in the Bering Sea, sometimes collect, chop up and eat pieces of the large plumose anemone, Metridium giganteum, which can be found in the lower intertidal zones of that area. Whilst teaching in Alaska eons ago, one of my students from that area told me that it tastes "spicy, kind of like hot peppers." This "spiciness" was, of course, due to the stinging capsules or nematocysts found in the anemones' epidermis. These nematocysts were discharging into the tongue's epithelia, giving the feeling of spiciness (and adding a note, with thanks, from Mr. Borneman when he reviewed this article, "Capsicum, or the chemical found in hot peppers, incidentally, fits almost perfectly into pain receptors.") Interesting the things we humans eat for "spice." Metridium is an anemone that feeds on planktonic particulate materials and doesn't have particularly venomous nematocysts, fortunately. Other common anemones in the area do have much more potent nematocysts, but the natives of the region didn't eat those, probably because they learned long ago that their "spiciness" could be extremely unpleasant or even lethal. Such experiences are lost in antiquity, but the spiciness of the anemone gives an indication of the effects of nematocysts on a predator, albeit a most unlikely one. If the predator were far smaller, the nematocysts' effects would be more extreme and dangerous.

Somewhere very far back in time, however, some small predatory sea slug developed a way to eat some of the cnidarians of its time. The snail gut is not like that of a human. Snails typically eat food by rasping it into very small pieces and ingesting them. Once the food has been eaten and is in the stomach, the fine food particles are sorted by weight, density and size. My guess is that some snails that ate cnidarians managed to have the right combination of gut chemistry and prey items so that most of the nematocysts were not discharged during feeding. Snails also do not digest food the way that vertebrates do, in the gut cavity. Instead, the fine - microscopically fine - particles that constitute the snail's ingested food are only sorted in the gut and those that fall into the right range of size and density are moved into some large glandular structures on either side of the gut. These are called "digestive glands" or sometimes - and very inappropriately - livers. These glands are a collection of very small tubules surrounded by masses of digestive cells. The cells individually ingest food particles and digest them internally. Excess nutrients are liberated to the blood, bathing these cells, and are then transported to the rest of the animal. Indigestible particles are moved out of the digestive gland back to the stomach where they are shunted to ciliary tracts that take them to the intestine and then out of the animal.

Digestion of a nematocyst or something similar would be dangerous, and the ancestral nudibranch probably simply held these for a brief period, a few minutes to a couple of hours, in its digestive gland and then moved them back to the stomach to be excreted as feces. However, over time and in some particular species, the nematocysts were probably maintained for some longer period in the digestive gland. If such an animal were to be eaten by a predator, these nematocysts would be prepositioned to discharge if the nudibranch's tissues were damaged. Depending upon the prey initially eaten by the slug, such a nematocyst discharge could give the predator a really unpleasant sensation. If that particular species of slug was distinctively marked, the predator could easily learn to avoid such a nasty-tasting food item. This could have been the beginning of the coevolution of the predator and its prey, as the distinctive coloration could easily change to become aposematic coloration.

Today, many people find nudibranchs of all types to be among the most beautiful of all animals. They are often vividly and brilliantly colored with striking color patterns that we find aesthetically pleasing; color patterns that many marine animals note as a warning to avoid. While the most colorful nudibranchs are those in the suborder Doridacea, which eat toxic sponges and bryozoans and use striking colors and color patterns as warning signals, many nudibranchs, particularly the larger ones in the suborder Aeolidacea are also considered to be very beautiful. These animals, the aeolids, are specialized to eat cnidarians. They store the eaten, but undigested, nematocysts of their prey in pouches extending up from their backs, presumably as predator deterrence.

Aeolids, the Prey that Bites Back

Figure 4. A small Flabellina showing the type of warning coloration typical
of aeolid nudibranchs.

Most snails are fairly small animals and many aeolid nudibranchs epitomize this. It is a really large aeolid that is over a couple of centimeters long, and many of them reach adulthood while still less than a centimeter long. Aquarists and the general public often seem to conceptually link small size with simplicity of design. That is a mistake with these slugs, however, as they have a complexity of internal structure that is truly impressive. There are probably less than a thousand scientifically described species of aeolids, although it is highly likely that a great many more remain to be described.

Aeolids are nudibranchs, which means that they are snails that have lost the shell they had as larvae. Once they pass out of the larval stage they have no shell or remnant of one. Being snails, they have, for the most part, a rather straightforward internal morphology. They have a typical snail's nervous system consisting of several ganglia surrounding the throat. This ring of ganglia constitutes a reasonably large brain, relative to the size of the animal. Nerve tracts or cords run posteriorly through the body, and there may also be subsidiary nerve cell aggregations in the posterior part of the body. Their sensory structures are a bit odd. Unlike most snails, they lack eyes on the surface of the body, but their eyespots are well developed. These sit right on the dorsal-most ganglia that surround the foregut under several layers of tissues. All nudibranchs have a pair of sensory tentacles that arise from the region of the body that would be the top of the head, if they had a distinct head, which they don't. These tentacles are called "rhinophores," and they contain sensory structures sensitive to current flows, dissolved chemicals, and touch. Sort of "all purpose sensors," these structures have been referred to as "world sensors."

Figure 5. An adult individual of a species of Eubranchus.
The animal was about 3 mm (1/8th inch) long. This small
nudibranch eats hydroids.

They have a well-developed heart consisting of one auricle and one ventricle. Blood, containing hemocyanin, a copper-based respiratory pigment, is pumped from the heart through vessels toward a couple of bodily regions. These vessels soon end, and the blood flows throughout the body, bathing the internal organs. This type of circulatory system, lacking most arteries, capillaries or veins is called an "open" system. Although it lacks vessels, the blood flow is neither indiscriminate nor haphazard; the blood flows through gaps in the tissues that direct it in a precise pattern. Eventually the blood passes through a kidney and then to the heart to complete the circuit. Gas exchange in aeolids takes place over their body's whole surface, but especially in the frill-like extensions, called cerata (singular = ceras), which extend up from the animal's back.

They are simultaneous hermaphrodites and their reproductive system's structure varies significantly among the various subgroups of aeolids. Some species' reproductive plumbing is among the most complex, if not the most complex, in the animal kingdom, containing a male system, a female system, and a tertiary system designed to store and hold sperm, often for several days to a week between copulation and spawning. Even though they are hermaphrodites, they are not self-fertile, so two animals are needed to create viable offspring. Unlike the dorid nudibranchs, which will copulate for hours on end, many aeolids have very short copulatory periods; Phidiana (=Hermissenda) crassicornis, a common temperate species used in neurobiological research, can complete simultaneous and reciprocal (remember, they are hermaphrodites) copulation in under one second. After copulation, sometimes weeks after, aeolids typically deposit a gelatinous egg mass containing "eggs," which actually are developing embryos. These typically hatch from the egg mass and spend from a week to a few months in the plankton, feeding and growing. During this period, they have a typical larval snail shell. When they have developed sufficiently, they settle from the plankton, shed the shell and start crawling around looking for food. If this were the only developmental pattern, these animals would not be any real problem for aquarists, as the larvae would seldom survive their larval period due to the scarcity of plankton upon which to feed. However, a few species - and perhaps more than a few species - have a rapid, totally benthic development that occurs in the egg capsule mass or, alternatively, have a larval period of a day or less. These species can complete their life cycle in aquaria, and some of them can become quite serious nuisances.

In addition to their complex reproductive systems, they have a gut system that has some of the strangest modifications seen in any gut in any animal. The front end of the gut is normal; for all intents and purposes it is indistinguishable from any other small snail's gut. As is the norm for snails, they have a well-developed radula. In this case, it is not a rasping organ and the number of radular teeth has been reduced to only a few, sometimes only a single tooth in each row. Aeolids typically also have jaws that help in slicing off prey. Aeolids are generally specialized to eat cnidarians such as corals, sea anemones and hydroids, although a few oddballs eat other things.

Figure 6. The same Eubranchus individual as in Figure 5, showing the relationship
of some gut structures, cerata and cnidosac.

During feeding the prey tissues are cut into small pieces and swallowed. They then pass into the stomach through a short esophagus. So far, so good; everything is "up to the molluscan standard." Once in the stomach, the food is sorted and digestible foods are sent to parts of the digestive gland where cells lining the tubules ingest and digest them. With nematocysts, however, a different set of events takes place. They are sent into finger-shaped, blind-end tubules which extend up into the cerata. Each ceras contains one digestive gland duct. At the end of each of these tubules is a specialized sac or pouch, called a "cnidosac." This is often highly pigmented; generally, it is colored with brilliant white pigment. Presumably, secretions from the inner walls of the cnidosac maintain the nematocysts in a fully functional condition. Other nudibranchs, such as the dendronotids, also eat cnidarians, but only the aeolids keep the nematocysts within their bodies as functional structures. Aeolids are not toxic in the classic sense. They don't have chemicals in their bodies that deter predation. However, their defenses are also effective. They take internal structures from their prey and use those as defenses against their predators. If something like this existed on land, it would be as if a coyote ate a porcupine, quills and all, and then its digestive system deposited the quills in intestinal pouches growing out of its back to protect it against wolves. Needless to say, this whimsical terrestrial example doesn't occur. But, the marine version does, and it is found in all seas, as aeolid nudibranchs are common in most shallow water marine environments. Although this seems to be an arcane and very unlikely way to protect against predation, the sting of these nematocysts may be very serious. Human injuries from contact with aeolid cerata are not uncommon. Instances of very serious injuries resulting from contact with the nematocysts concentrated in aeolids have been recorded from aquaria.

Figure 7. Nematocysts in the cnidosac of the Eubranchus individual pictured previously.

Aeolid coloration is somewhat related to size. Large species are often brightly colored with aposematic coloration. Smaller ones tend to have color patterns that result in aposematic contrast patterns dominated by dark lines on a white background. Even the most colorful patterns are difficult for us to interpret, though. Not all marine visual predators see colors, and those that do may not see colors the same as we do. Nevertheless, the larger aeolids seem to use a larger palette of colors for their patterns, while the smaller ones are more "black and white."

Aeolids in Aquaria

With only a couple of exceptions, aeolids should not be welcomed with open arms by aquarists. They all eat cnidarians, and many of them are specialized to eat some species of the decorative livestock that aquarists keep. Numerous species have found their way into aquaria from time to time. Generally, the solution to maintaining these animals is simply to remove them. Solitary hitchhikers are seldom able to set up or maintain a breeding population. However, there are some exceptions. Some, typically small, species can pass through their entire life cycle in a reef tank. These particular nudibranchs pass through most or the entire larval period within the egg mass, and do not need to feed in the plankton. Consequently, they can proliferate in an aquarium. As these nudibranchs are specialized in diet, they have picked up the common names of "Montipora-eating nudibranch" or "zoanthid-eating nudibranch." It is likely that there are several species in each group, and controlling them is difficult. Being aeolids, few animals will eat them, and being small and mobile they can spread throughout a tank and infest it before being noticed. Among their few predators are some other slugs (see here for some movies of them being eaten; note how well the cerata repel the potential predator, Pleurobranchaea, and are ineffective against the other, Navanax). Interestingly enough, these other slugs lack eyes, so any aposematic coloration is "wasted" on them. Dips of various sorts may be used to control them in aquaria, but these vary in efficacy. As the converse of these problem aeolids are several other small species, all sold under the "umbrella" name of "Berghia." These nudibranchs are bred and sold specifically to prey upon the pest anemone species in the genus Aiptasia. Large aeolids are often strikingly beautiful animals, but they are not reef aquarium safe. Smaller aeolids tend not to be as highly colored, and some of them are useful in aquaria, but the majority of these are also not animals most hobbyists would want to try to maintain in their aquaria. As with numerous other highly colored marine animals, one might wish to recall the aphorism that "Beauty is in the eye of the beholder."

If you have any questions about this article, please visit my author forum on Reef Central.

Useful References:

Longley, R.D. & Longley, A.J. (1981) Hermissenda: agonistic behaviour or mating behaviour? The Veliger 24: 230-231.

Mauch, S. and J. Elliott. 1997. Protection of the nudibranch Aeolidia papillosa from nematocyst discharge of the sea anemone Anthopleura elegantissima. The Veliger. 40:148-151.

Ruppert, E. E, R. S. Fox, and R. D. Barnes. 2003. Invertebrate Zoology, A Functional Evolutionary Approach. 7th Ed. Brooks/Cole-Thomson Learning. Belmont, CA. xvii +963 pp.+ I1-I26pp.

Rutowski, R.L. (1983): Mating and egg mass production in the aeolid nudibranch Hermissenda crassicornis (Gastropoda: Opisthobranchia). Biological Bulletin, 165: 276-285.

Salvini-Plawen, L. 1988. The structure and function of molluscan digestive systems. In: Trueman, E. R. and M. R. Clarke (Eds): The Mollusca, Volume 11, Form and Function. Academic Press, New York, 301-379.

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Beautiful, but Unwelcome; Aeolid Nudibranchs in the Reef Aquarium by Ronald L. Shimek, Ph.D. - Reefkeeping.com