Summary:
A common phenomenon seen in insect-plant interactions is the insect herbivore sequestering secondary compounds in order to use the compounds for its own defenses (Harborne, 1993). The marine environment has long been known to harbor a similar chemical arms race among its inhabitants. It is no surprise then to see that the behavior of sequestering secondary compounds from ones host also exists in the marine environment as well.
Nudibranchs, a family of sea slugs has many members that also sequester secondary compounds from their hosts. This behavior has been seen in nudibranchs feeding on sea fans, and sponges (Proksh, 1994; Marin, 1997). The secondary chemicals are used by the hosts to defend themselves against predation. The same effect is also observed for the nudibranchs that sequester the compounds (Proksh, 1994).
This paper reviews what is known about the ability of nudibranchs to sequester secondary metabolites. It covers the basic chemical groups sequestered and how the nudibranchs incorporate them in the defense of themselves and their offspring. The sequestering abilities of these animals in many ways surpasses that of insects. The paper discusses the issue of aposematic coloration which has been a source of recent debate. One feature shared by all of the Opsithobranchs is that the shell has been lost over evolutionary time (Faulkner and Ghiselin, 1983). For most gastropods the shell plays a key role in the defense of the animal. Without a shell, the Opisthobranchs had to resort to a different means of protection. Most species have developed some form of chemical defense (Faulkner and Ghiselin, 1983). Nudibranchs represent a very successful group of opisthobranch. They feed on a variety of sessile marine organisms including, coral, hydrozoans, bryozoans and sponges. They are found in all parts of the ocean from the arctic to the tropics. Many early researchers have noted that despite the lack of shell these organisms rarely were preyed upon (Thompson, 1960; Faulkner and Ghiselin, 1983; Rudman, 1991). This lead to the investigation of the chemical defense in these organisms. In this review I will cover the basics of the defense of sponge eating nudibranchs including: where their chemicals come from, what types of chemicals are used, how these chemicals are used by the nudibranchs and finally the role of coloration in these organisms.
One of the earlier documentations on the nudibranchs ability to thwart predation was by Crozier (1916). He noted that a Chromodoris nudibranch was brightly colored and seemed to be avoided by fish. He collected a few nudibranchs and dropped them in a tank which contained a species of fish. He noted the fish tasted the animal a few time and then gave up. This result was even obtained by using natural blind fish. He concluded that the odor of the nudibranch kept the fish away. Thompson (1960) showed that a Pleurobranchus nudibranch secretes an acidic mucus when disturbed. He and his colleagues tasted several different species of nudibranchs and noted that many of them tasted bitter or were distasteful in other ways. This confirmed indirectly that there is some noxious chemicals in the nudibranch. Russell (1966) repeated this test with four species of fish. He too found that the fish found most of the nudibranchs distasteful. This suggested that this was a realistic defense by the nudibranchs against predation.
The origin of allelochemicals in nudibranchs
Not only did the nudibranchs show chemical defense, they also seemed to display some food preference. In a test arena a nudibranch could be given a choice between a sponge it was found grazing on and another species of sponge. In many cases the nudibranch could distinguish the location of one species of sponge over another (Cook, 1962; Elvin, 1976; Roger et al., 1990). The nudibranchs were placed down stream from a simple "T" design. Currents were run past the test item and the control towards the nudibranch. The nudibranch would follow the chemical scent up stream and then make a choice. In all three experiments, the nudibranchs could locate the food source when the control chamber was empty. This suggested that the nudibranchs are able use chemical cues to locate their prey. There were mixed results when another sponge was placed in the control chamber. Elvin (1976) found that Diaulula sandiegensis did a lot worse in picking out its host sponge when another species was place in the control side then when the control side was empty. On the other hand, Rogers and Paul (1991) found that the Glossodoris nudibranchs were able to select different "races" of sponges within the same species.
The second piece of evidence that nudibranchs are not generalists was found by comparing the radula of the different genera. Bloom (1976) showed the radula of each nudibranch was shaped differently depending on the sponges they ate. Different species of sponges have different ratios of spicules and spongen. The spicules are calcarous or silicon based spines while spongin is flexible proteins. The nudibranchs that ate spicule filled sponges also had a ceacum while those that ate sponges with high percentages of spongin had reduced ceacums. The main question is why specialize?
In terrestrial environments, herbacious insects will specialize on a certain species or genus of plants and sequester the secondary chemicals the plants produce for defense. The insects will then use these chemicals to defend themselves as well. These insects are selective about their food source and many can use chemical cues to find the host plant (Harborne, 1984). Marine nudibranchs seem to show similar behavior patterns in terms of selectivity which might indicate sequestering as well. Observations in the field have shown that the nudibranch will lose their defensive chemicals after several discharges. If kept from their natural food they are unable to replace their defense chemicals (Thompson, 1960). Many studies have showed that nudibranchs indeed share the same allelochemicals as their host sponges Table 1. lists some of the major studies in this area. In most of these cases the researchers used chromatography and NMR techniques to separate chemicals from the sponge and the nudibranchs found feeding on it. They then compared the secondary chemicals of the sponge with the nudibranch and found many were identical. The actual proof that nudibranchs do indeed sequester the chemicals from their host was from a radiolabling experiment done by Oakes (1979). This experiment was done on a cnidarian feeding nudibranch, Hermissenda crassicornis and compared to a shelled gastropod Tegula funebalis. Placida dendritica was fed C-14 labeled food. This was found to spread through the cnidarian in 60min. The nudibranch was allowed to feed on the hydroids and the C- 14 was transported to the cerata situated on the back of the animal in 30 min. The Tegula was fed labeled food and the C-14 remained in the digestive tract for 22 hrs. It never was moved to the rest of the body. This suggests that the nudibranch was sacrificing digestive efficiency in order to gain the secondary metabolites (Oaks, 1979).
The chemicals sequestered
Sponges face a variety of dangers in their environment. They compete with other sponges and sessile organisms for space (Proksch, 1994). Many species of fish and arthropods could potentially feed on these sessile organisms. In addition sponges also can be settle upon by small microorganisms that tend to clog the sponges' ostiums (where they take in water and food). In order to prevent predation and fouling sponges produce a variety of secondary metabolites which either deter feeding or kill off any potentially harmful microorganisms (Proksch, 1994). This is analogous to the plant-herbivore and plant-microbe interactions that occur in terrestrial environments (Proksch, 1994).
Nudibranchs face similar predators as the sponges. By using the toxins taken from the sponges, nudibranchs acquire the same protection. Thus, the variety of possible chemicals the nudibranchs can contain is as vast as the sponges' arsenal. When examining Table 1., one pattern emerges from the data. Each genus of Nudibranch seems to deal with particular types of chemicals. For example the Chromodoris nudibranchs all sequester diterpenes from the sponges they feed on. The sequestering of terpenes seems true from a lot of the family Chromodoridae. Hypselodoris tend to sequester furanoterpenes and Cadlilina margunata takes in both sesquiterpens (Burgyone et al., 1993) and diterpenes (Tischler and Andresen, 1989). The family Chrochidorididae is not as consistent as Chromodoridae. Archidoris tends to sequester Diterpenoid acid glycerides (Faulkner et al., 1990) Discodoris take in sesquiterpenes, and Petodoris atromaculata were found to use large polyacetlynenes. Notodoris nudibranchs were found to sequester alkaloids.
In addition to the variety of chemicals sequestered within a genus, each species was found to sequester multiple chemicals. For example Chromodoris youngbleuthei can sequester different deacetylscalaradals (1-3)( Terem and Paul, 1986). P. pustulosa was found to sequester 4a- isocyanogorgon (4), 4a-formamidogorgon (5), 4a-isothiocyanatogorgon (6) and 3- isocyanobisabolane-8,10-diene(7) (Kassuhlke et al,1991). The first three have a similar skeleton with a small change but the final one is different. These are but a few cases where this has occurred. This suggests that the nudibranchs are able to handle a variety of chemicals.
This chemical variation turns out to go even further then just a few chemicals. Avila et al. (1994) compared the chemical composition in Hypselodoris webb and Hypselodoris villafranca from the Italian coast and Spanish coast. They found that the chemicals sequestered by the nudibranchs differed from each area. H. webb for example sequestered longifolin (8) from Castellammare (Italian Mediterranean coast), longifolin and nakafuran-9 (9) from Taranto (Italy) and longifolin and isotavacfuran (10) from Blanes (Spain). All of these chemicals came from the same species of sponge Dysidae fragilis (Avila et al, 1994). This means that in order to survive in different areas the nudibranchs have to be able to deal with a diverse set of chemicals. One species of nudibranch, Cadlina marginata feeds on 19 genera of sponges (McDonald and Nybakkan, 1997). It has already been documented as sequestering chemicals from several species of these sponges (Burgoyne et al, 1993; Tischler and Andersen, 1989; Faulkner et al, 1990). The list of chemical groups sequestered by these animals includes: Sesquiterpenes, sesquiterpenes furans, diterpenes, sesquiterpene isonitriles, sesquiterpene isothiocyanates, and norsesterpenes. This is an impressive list especially when compared to the insect examples which generally sequester only a single type of chemicals (Harborne, 1993). In fact the average number of genera fed on by the species of nudibranchs listed in Table 1 is about 4 (McDonald and Nybakkan, 1997). This may explain the earlier results which showed that some nudibranchs have a hard time distinguishing one sponge from another. How can a single species deal with this type of variation? One possibility is that the chemicals are transported through the body of the animal to the mantle without actually moving through the animals body. In a cnidarian eating nudibranch, the nematocystes are transported through the organism to the mantle without firing them off. The nudibranch then uses these cells for its own protection (Brusca and Brusca, 1990). Perhaps the sponge eating nudibranchs are somehow using the same mechanism and thus never actually having to deal with the toxicity.
The toxins are indeed stored in only certain areas in the nudibranch The chemicals in Glossodoris pallida store the chemicals in special mantle dorsal formations (MDFs) which fall along the border of the mantle (Avile and Paul, 1997). Chromodoris on the other hand store the chemicals in sacs on the mantle (Rudman, 1991). Avile et al (1997) tested the Glossodoris nudibranch on fish with mantles and without mantles. The fish were repelled by the nudibranchs with mantles but would eat those nudibranchs where the mantle was removed. This showed that the mantle was the key storage area fro the nudibranch. In a mollusk the vital organs are all located in the viseral mass beneath the mantle. In most molluscs the mantle secretes the shell perhaps the function of the nudibranch mantle has become a storage place for toxic materials and provide a thick shield between the stored chemicals and the body. One morphological feature of the nudibranch is the branched midgut gland (liver). This digestive organ actually extends into the mantle (Figure 1) of the nudibranch (Hyman, 1978) This seems like an ideal setup for transporting chemicals from the digestive tract to the mantle without allowing the chemicals to enter the rest of the body. Indeed, in dissections of nudibranchs the mantle and digestive tracts are the only two areas where the chemicals are reported in abundance (Oaks, 1976; Avila et al, 1991; Avila et al., 1997).
Chemical production in nudibranchs
In a few cases certain chemicals are actually modified by the nudibranchs. In Glossodoris the terpene scaradial (11) was found to be very abundant in the nudibranchs. Deoxoscalarin (12) was found in the nudibranch and its egg masses but not in the sponge (Avila et al, 1997). This suggests that the nudibranch is modifying the scaradial into a new chemical. This same reaction was found in Hypselodoris orsini (Cimino et al, 1993). Hypselodoris zebra had euryfuran (13) which was not in the sponge food (Grode and Cardellina, 1984). Terem and Sheuer (1986) found two deacytelscaradials in Chromodoris youngbleuthi that were not in the sponge Spongia oceania. It is possible that these nudibranchs also modify the secondary metabolites they sequester.
This ability to sequester chemicals appears to be an evolutionary step beyond what is seen in the insect-plant interactions. There is few if any cases where the insects sequester a chemical from a plant and then modify it for their own defense (Harborne, 1993).
The dorid Dendrodoris limbataand D. grandflora both sequester sequiterpenoids and in addition produce their own defensive chemical Polygodial (14) (Cimino et al, 1983; Cimino et al., 1985). To determine this Cimino et al (1983) radiolabled mevalonic acid which they felt would be a suitable precursor to polygodial. They found that the mevalonic acid was indeed incorporated into the polygodial showing that the nudibranchs are capable of synthesizing the molecule on their own. The same process is assumed in D grandflora because they too contain polygodial and their sponge prey did not (Cimino et al. 1985).
The uses of the allelochemicals
One of the major uses implied so far is that the secondary chemicals are able to deter fish from feeding on them. Most of the papers cited in Table 1 also include a test where the nudibranch is offered to the fish. In man cases the fish would bite at the food and then spit it out. Food laced with the separated chemicals were also tried. Similar behavior was observed from most chemicals separated by the researchers. In the case of Phyllida varicosa the chemicals actually killed the fish (Sheuer, 1977). Glossodoris pallida also was able to deter crabs. (Avila et al, 1997).
As I mentioned most of the chemicals were effective but there were a few that did not affect fish. What about the exceptions? Matsunaga et al. (1986) separated a macrolide called Kabiramide C (15) from the egg mass of a unknown nudibranch. This chemical was not found to deter fish however it did have an important property. They tested Kabiramide C against fungi and found that it will kill many different species of fungi. Pawlik et al (1988) found that the Spanish dancer, Hexabranchus sanguineus, put macrolides such as Kabiramide B into its eggmasses. It was also found to be an antifungal agent. Nudibranchs generally lay a string of eggs and then leave them (Edmunds, 1991). By placing these toxins in the eggs they could prevent any microorganisms from eating the eggs. As mentioned above the modi fied deoxosaralin in Glossodoris was placed in the egg masses (Avila et al., 1997). Perhaps this is the reason some of these nudibranchs alter the sequestered chemicals to protect the eggs. Many insects also protect their eggs with sequestered chemicals (Harborne, 1993 ). This is actually important for the nudibranchs, not only do they have to protect themselves but they have to protect their young. The chemicals in the egg masses may insure the young are protected in the future. It may be that the young eating their way out of the eggs may also sequester some of the compounds to protect them in their early life.
The last type of chemical sequestered inadvertently protects the nudibranch. In a few cases the nudibranchs the color pigments of their prey. Marin et al (1997) found that in addition to the ichthyotoxins acquired the Discodoris also sequester the color pigments of their host sponge. This allows them to blend into their host. This is a cheap way of ensuring you match the color of your host.
Is the color of nudibranchs aposematic?
The mention of color brings us to a large debate in the nudibranch literature, why are nudibranchs colorful (Edmunds, 1991)? The most obvious explanation for color would be aposematic coloration. Edmunds (1991) puts forth four criteria in order for aposematic coloration to be true.
1) the organism is noxious enough so that predators
don't eat it
2) It is conspicuously advertised (colored)
3) Predators avoid attacking it because of the colors
4) This protection is more effective then being
cryptic
We've already established that the nudibranchs are indeed noxious to a variety of fish. Whether or not the fish learn the colors is a different question. Color in the ocean is more difficult to deal with then the colors on land. On land the colors are generally constant while in water the reds and oranges get filtered out near the surface of the ocean. In deeper areas reds would be seen as blacks and browns (Edmunds, 1991). As Just and Tendal (1983) pointed out however, nudibranchs can be found at a variety of depths. Secondly in some areas the colors penetrate deeper then others. Nudibranchs are usually patterned (Rudman, 1991) as well which could create another clue for a naive fish to learn. I think it would be safe to assume then that the nudibranchs are indeed conspicuous.
One additional argument put forth by the authors on this subject is how to classify the colorful nudibranchs that match their sponges. They seem to indicate that these individuals are being cryptic and are vulnerable when they move to a new host (Faulkner, 1983; Rudman, 1991; Edmunds, 1991). One answer to this debate is that the nudibranchs are aposematic and that their host is also aposematically colored. They already match the hosts chemistry so why not match the color? This way if a fish learns that red is distasteful from a sponge they will learn to avoid red. Fish are also able to readily learn odors of distasteful food and avoid the food by smell (Crozier, 1916). If you combine the two the fish have multiple signals to identify a distasteful food source and will avoid the animal quicker. In this sense the sponge could benefit this relationship as well. Although this hardly balances the cost of being eaten.
The fourth point presented by Edmunds (1991) has not been looked at to this author's knowledge. An ideal experiment would be to somehow remove the coloration on a nudibranch and compare its survival to unchanged nudibranchs. This would possibly demonstrate the effectiveness of the coloration to the survivorship of the nudibranch.
Rudman (1991) suggested that if aposematic coloration is indeed effective then mimicry should occur. He looked at this in Australian Chromodoris nudibranchs. He compared the species in the area with the colors and patterns they have. What he found was that different areas around Australia are dominated by particular color patterns. Although in most cases a single species is found in multiple areas, the colors of the individuals in a particular area match that of the nudibranchs in that area. In a sense many of the nudibranchs in an area converge on a particular color pattern. This is classic Mullarian mimicry. It appears that aposematic coloration could explain the coloration of most of the nudibranchs. They are either matching their host species or other species in the area.
Conclusions:
Nudibranchs are extremely efficient at utilizing their food sources. Not only do they acquire nutrition but defense chemicals as well. These chemicals can then be used for the defense of the animal and its eggs as well. The sponge eating nudibranchs are in some ways more advanced then the terrestrial herbivores. They are able to sequester broad ranges of chemicals from their host sponges. They are not generally limited to single hosts (McDonald and Nybakken, 1997) as seen by the traditional plant eating utilizers. In addition some nudibranchs are able to modify the chemicals they sequester and in a few cases produce their own. The ability to sequester a large range of chemicals, their ability to use many hosts, and their coloration probably accounts for the incredible success of this group.
Acknowledgements
Thanks to Gary McDonald for his help.
References
Avila, C., G. Cimino, A. Fontana, M. Gavagnin, J. Ortea, E. Trivellone. 1991. Defensive strategy of two Hypselodoris nudibranchs from Italian and Spanish coasts. Journal of Chemical Ecology 17(3):625-636.
Avila, C., G. Cimino, A. Crispino, and A. Spinella. 1991. Drimane sesquiterpenoids in Mediterranean Dendrodoris nudibranchs: Anatomical distribution and biological role. Experientia. 47:306-310.
Alvi, K. A., B. M. Peters, L. M. Hunter, and P. Crews. 1993. 2-Aminoimidazoles and their znc complexes from Indo-Pacific Leucetta sponges and Notodoris nudibranchs. Tetrahedron. 49(2):329-336.
Avila, C., V. J. Paul. 1997. Chemical ecology of the nudibranch Glossodoris pallida: is the location of diet-derived metabolites important for defense? Marine Ecology Progress Series 150:171-180.
Bloom, S. A. 1976. Morphological correlations between dorid nudibranch predators and sponge prey. Veliger 18(3):289-301.
Bobzin, S. C., D. J. Faulkner. 1989. Diterpenes from the marine sponge Aplysilla polyrhaphis and the dorid nudibranch Chromodoris norrisi. Journal of Organic Chemistry 54(16):3902-3907.
Brusca, R. C., and G. J. Brusca. 1990. Invertebrates. Sinauer Associates, Inc.: Mass.
Burgoyne, D. L., E. J. Dumdei, R. J. Andersen. 1993. Acanthene- a to acanthene-c - a-chloro, isothiocyanate, formamide sesquiterpene triad isolated from the northeastern Pacific marine sponge Acanthella sp. and the dorid nudibranch Cadlina luteomarginata. Tetrahedron 49(21):4503-4510
Carmely, S., M. Ilan, Y. Kashman. 1989. 2-amino imidazole alkaloids from the marine sponge Leucetta chagosensis. Tetrahedron 45(7):2193-2200.
Carroll, Anthony R., Bruce F. Bowden, John C. Coll. 1993. New imidazole alkaloids from the sponge Leucetta sp. and the associated predatory nudibranch Notodoris gardineri. Australian Journal of Chemistry 46(8):1229- 1234.
Carte, B., D. J. Faulkner. 1986. Role of secondary metabolites in feeding associations between a predatory nudibranch, two grazing nudibranchs, and a bryozoan. Journal of Chemical Ecology 12(3):795-804.
Castiello, D., G. Cimino, S. De Rosa, S. De Stefano, G. Sodano. 1980. High molecular weight polyacetylenes from the nudibranch Peltodoris atromaculata and the sponge Petrosia ficiformis. Tetrahedron Letters 21(52):5047-5050.
Cimino, G., S. De Rosa, S. De Stefano, G. Sodano. 1982. The chemical defense of four Mediterranean nudibranchs. Comparative Biochemistry Physiology, B--Comparative Biochemistry 73(3):471-474.
Cimino, G., S. De Rosa, S. De Stefano, G. Sodano G. Villani. 1983. Dorid nudibranch elaborates its own chemical defense. Science 219(4589):1237- 1238.
Cimino, G., S. De Rosa, S. De Stefano, G. Sodano. 1985. Observations on the toxicity and metabolic relationships of polygodial, the chemical defense of the nudibranch Dendrodoris limbata. Experientia 41(10):1335-1336.
Cimino, G., S. De Rosa, S. De Stefano, R. Morrone, G.Sodano. 1985. The chemical defense of nudibranch molluscs. Structure, biosynthetic origin and defensive properties of terpenoids from the dorid nudibranch Dendrodoris grandiflora. Tetrahedron 41(6):1093-1100.
Cook, E. F. 1962 A study of food choice of two opisthobranchs, Rostanga pulchra McFarland and Archidoris montereyensis (Cooper). Veliger 4(4):194-197.
Corley, D. G., R. Herb, R. E. Moore, P. J. Scheuer, V. J. Paul. 1988. Laulimalides: new potent cytotoxic macrolides from a marine sponge and a nudibranch predator. Journal of Organic Chemistry 53(15):3644-3646.
Crozier, W. J. 1916. On the immunity coloration of some nudibranchs. Proceedings from the National Acadamy of Sciences.
de Silva,E. D., S. A. Morris, S. Miao, E. Dumdei, and R. J. Andersen. 1991. Terpenoid metabolites from skin extracts of four Sri Lankan nudibranchs in the genus Chromodoris. Journal of Natural Products. 54(4):993-997.
Edmunds M. 1991. Does warning coloration occur in nudibranchs. Malacologia. 32(2):241-255.
Elvin, D. W. 1976. Feeding of a dorid nudibranch, Diaulula sandiegensis, on the sponge Haliclona permollis. Veliger. 19(2):194-198.
Faulkner, D. J., M. T. Ghiselin. 1983. Chemical defense and evolutionary ecology of dorid nudibranchs and some other opisthobranch gastropods. Marine Ecology, Progress Series 13(2- 3):295-301.
Faulkner, D. J., T. F. Molinski, R. J. Anderson, E. J. Dumdei, and E, D. de Silva. 1990. Geographical variation in defensive chemicals from pacific coast dorid nudibranchs and some related marine mulluscs. Comparative Biochemistry and Physiology. 97C(2):233-240.
Fontana, A., C. Avila, E. Martinez, J. A. Ortea, E. Trivellone, G. Cimino. 1993. Defensive allomones in three species of Hypselodoris (Gastropoda, Nudibranchia) from the Cantabrian Sea. Journal of Chemical Ecology 19(2):339-356.
Fontana, A., E. Trivellone, E. Mollo, G. Cimino, C. Avila, E. Martinez, J. Ortea. 1994. Further chemical studies of Mediterranean and Atlantic Hypselodoris nudibranchs -- a new furanosesquiterpenoid from Hypselodoris webbi. Journal of Natural Products, Lloydia 57(4):510- 513.
Fontana, A. E. Mollo, D. Ricciardi, I. Fakhr, G. Cimino. 1997. Chemical studies of Egyptian opisthobranchs: spongian diterpeniods from Glossodoris atromarginata. Journal of Natural Products 60(5):444-448.
Fusetani, N., H. J. Wolstenholme, K. Shinoda, N. Asai, S. Matsunaga, H. Onuki, H. Hirota. 1992. Two sesquiterpene isocyanides and a sesquiterpene thiocyanate from the marine sponge Acanthella cf. cavernosa and the nudibranch Phyllidia ocellata. Tetrahedron Letters 33(45):6823- 6826.
Grode, S. H., J. H. Cardellina II. 1984. Sesquiterpenes from the sponge Dysidea etheria and the nudibranch Hypselodoris zebra. Journal of Natural Products 47(1):76-83.
Gustafson, K. R. J. Andersen. 1985. Chemical studies of British Columbia nudibranchs. Tetrahedron 41(6):1101-1108.
Harborne, J. B. 1993. Introduction to Ecological Biochemistry 4th ed. Academic Press: London. Hellou, J. E., R. J. Andersen, and J. E. Thompson. 1982. Terpenoids from the dorid nudibranch Cadlina luteomarginata. Tetrahedron. 38(13): 1875-1879.
Hyman, L. H. 1967. The Invertebrates Vol. VI. Mollusca I. McGraw Hill Book Co. New York.
Just, H., O. S. Tendal. 1983. On the sponge diet of Archidoris pseudargus (Rapp, 1827). Veliger 25(4):403-404.
Kakou, Y., P. Crews, G. J. Bakus. 1987. Dendrolasin and latrunculin A from the Fijian sponge Spongia mycofijiensis and anassociated nudibranch Chromodoris lochi. Journal of Natural Products (Lloydia) 50(3):482-484.
Kassuhlke, Katharina E., Barbara C. M. Potts, D. John Faulkner. 1991. New nitrogenous sesquiterpenes from two Philippine nudibranchs, Phyllidia pustulosa and P. varicosa, and from a Palauan sponge, Halichondria cf. lendenfeldi. Journal of Organic Chemistry 56(11):3747-3750.
Kubo, A., Y. Kitahara, S. Nakahara. 1989. Synthesis of new isoquinolinequinone metabolites of a marine sponge, Xestospongia sp., and the nudibranch Jorunna funebris.Chemical Pharmaceutical Bulletin 37(5):1384-1386.
Marin, A., M. D. Lopez Belluga, G. Scognamiglio, G. Cimino. 1997. Morphological and chemical camouflage of the Mediterranean nudibranch Discodoris indecora on the sponges Ircinia variabilis and Ircinia fasciculata. Journal of Molluscan Studies 63(3):431-439.
Matsunaga, S., N. Fusetani, K. Hashimoto, K. Koseki, M. Noma. 1986. Kabiramide C, a novel antifungalmacroclide from nudibranch eggmasses. Journal of the American Chemical Society 108(4):847-849.
McDonald, G. J. Nybakken. 1997. A world-wide review of the food of nudibranchs. Veliger 40: Supplement 1-000 [www2.uscs.edu/people/mcduck/nudifood.htm]
Oakes, J. V. 1979. Distribution of 14C-labeled food material through the bodies of various gastropods. Wasmann Journal of Biology 37(1/2):27-29.
Pawlik, J. R., M. R. Kernan, T. F. Molinski, M. K. Harper, D. J. Faulkner. 1988. Defense chemicals of the Spanish dancer nudibranch Hexabranchus sanguineus and its egg ribbons: macrolides derived from a sponge diet. Journal of Experimental Marine Biology Ecology 119(2):99-109.
Proksch, P. 1994. Defensive roles for secondary metabolites from marine sponges and sponge- feeding nudibranchs. Toxicon 32(6):639-655.
Rogers, S. D., V. J. Paul. 1991. Chemical defenses of three Glossodoris nudibranchs and their dietary Hyrtios sponges. Marine Ecology Progress Series 77(2-3):221-232.
Rudman, W B. 1991. Purpose in pattern: the evolution of colour in chromodorid nudibranchs. Journal of Molluscan Studies. 57:5-21.
Russell, E. 1966. An investigation of the palatability of some marine invertebrates to four species of fish. Pacific Science 20(4):452-460.
Scheuer, P. J. 1977. Chemical communication of marine invertebrates. Bioscience 27(10):664- 668.
Schulte, G., P. J. Scheuer. 1982. Defense allomones of some marine mollusks. Tetrahedron 38(13):1857-1863.
Terem, B., P. J. Scheuer. 1986. Scalaradial derivatives from the nudibranch Chromodoris youngbleuthi and the sponge Spongia oceania. Tetrahedron 42(16):4409-4412.
Thompson, T E. 1960. Defensive adaptations in Opisthobranchs. Journal of Marine Biology. 39: 123-134.
Tischler, M. R. J. Andersen. 1989. Glaciolide, a degraded diterpenoid with a new carbon skeleton from the nudibranch Cadlina luteomarginata and the sponge Aplysilla glacialis. Tetrahedron Letters 30(42):5717-5720.
Tischler, M. R. J. Andersen, M. Iqbal Choudhary, Jon Clardy. 1991. Terpenoids from the sponge Aplysilla glacialis and specimens of the nudibranch Cadlina luteomarginata found on the sponge. Journal of Organic Chemistry 56(1):42-47.