Molluscan resources: their past, present and future value

Kirsten Benkendorff 'Department of Biological Sciences, University of Wollongong, New South Wales 2522

The resource potential of most molluscs is likely to be underestimated. One mollusc, Dicathais orbita, produces a number of potential resources, including pharmaceuticals and materials, from both the adults and egg masses. The value of natural resources can change over time and one resource can have multiple uses. The resource potential of molluscs increases with greater biological diversity. Molluscs from different phylogenetic backgrounds and habitats produce a range of different metabolites and mineralized structures. Ultimately, a wealth of potential resources remains to be discovered among the molluscs and this should

provide an incentive for their conservation. Downloaded from http://meridian.allenpress.com/rzsnsw-other-books/book/chapter-pdf/2643141/rzsnsw_1999_049.pdf by guest on 27 September 2021

INTRODUCTION and other molluscs, I test the assumption that chemical diversity is related to biological Throughout history, in all parts of the diversity. In addition, the value to be gained world, molluscs have provided a diverse from studying a greater variety of species, range of resources, such as food, pearls, with different phylogenetic backgrounds shell grit, ornaments, jewellery, utensils and and divergent environmental adaptations, will musical instruments. Shells have been used be demonstrated by looking at some new as a commercial currency, traded and offered materials that have been developed from as gifts to emperors and Gods (Stix et al. molluscs. 1978; Wye 1996). The asthetic qualities of shells have inspired artists and architects Tyrian Purple — the past, present and future (Stix et al. 1978) and more recently the value of a molluscan resource opisthobranchs, largely shell-less molluscs, have provided a favourite subject for under- Tyrian Purple is most probably the first water photography. Nevertheless, human needs secondary metabolite to be isolated from and values change and as a consequence many a marine mollusc. As early as 1600 BC the species that were once highly treasured may people of Crete found a way to extract a become seemingly superfluous. However, our purple dye from muricids (Baker 1974). In general perception of what constitutes a Roman times Tyrian Purple was worth as resource may be too narrow. All species are a much as 10-20 times its weight in gold potential source of information and could (Baker 1974; McGovern and Michel 1990). therefore enable the discovery and develop- By 300 AD purple dyed material became ment of new resources. protected by laws and reserved for the Gods and Roman Emperors (Baker 1974; The actual discovery of new biological Hoffmann 1990). The Bible prescribes the use resources will essentially be influenced by the of royal purple for colouring tabernacle current needs of the human population. For curtains and priests' vestiments (Exodus example, the recent problem of wide-spread 26:1;28; Numbers 15:38). The purple colour resistance to antibiotics has triggered an is still used, although it is now of synthetic increased effort to screen biological organisms origin. for useful drugs (Beattie 1994, 1996). The large returns from the sale of naturally The commercial use of Tyrian Purple as a derived pharmaceuticals has provided an dye ceased in 1453. A few centuries later incentive for some companies to channel Tyrian Purple was rediscovered and its money back towards the conservation of chemical composition was elucidated by biodiversity (Roberts 1992; Carte 1996). Friedlander in 1909, but by this time there Thus, within the pharmaceutical industry were already cheaper forms of synthetic purple there has been some recognition of the fact available (Hoffmann 1990). Nevertheless, that the continued discovery of new chemical Tyrian Purple was one of the first discoveries products depends on the maintenance of in the emerging field of archaeological biological diversity. chemistry (McGovern and Michel 1990). Knowledge of the structure and spectroscopic The value of certain molluscs and their properties of Tyrian Purple has facilitated associated resources has changed over time. historical research into the significance of the By exploring some biologically active, dye industry in early civilizations (Eisner and secondary metabolites produced by muricids. Spanier 1985; McGovern and Michel 1990).

Pp. 316-21 in The Other 99%. The Conservation and Biodiversity of Invertebrates ed by Winston Ponder and Daniel Lunney, 1999. Transactions of the Royal Zoological Society of New South Wales, Mosman 2088. In the last two decades Tyrian Purple has in the hypobranchial gland (Fig. 1). An also been used as a teaching material in enzyme capable of hydrolysing the salt to organic and natural products chemistry form Tyrian Purple was also found in the (Pinkney and Chalmers 1979; Hiyoshi and hypobranchial glands (Baker and Sutherland Fujise 1996; Torimoto et al. 1996). Its 1968). Nevertheless, the natural function of synthesis illustrates some interesting aspects Tyrian Purple precursors in muricids has of classical and mechanistic organic chemistry, remained unknown (Prota 1980; Ziderman as well as producing an attractive dye (Pinkney 1990). and Chalmers 1979). The continuing value of Tyrian Purple has led to a German patent Recently, in the search for new antibiotics, on the one-step synthesis of the compound I isolated Tyrian Purple and several of its (Gerlach 1991). precursors from the egg capsules of Dicathais orbita (refer to Fig. 1). Tyrindoleninone In the 1960s work carried out on the (III) and Tyriverdin (IV) were both found to Australian muricid, Dicathais orbita, demon- have antimicrobial activity against a range

strated that Tyrian Purple is not present of human pathogens. The activity exhibited Downloaded from http://meridian.allenpress.com/rzsnsw-other-books/book/chapter-pdf/2643141/rzsnsw_1999_049.pdf by guest on 27 September 2021 in living molluscs (Baker and Sutherland by Tyriverdin, along with its structural 1968). Instead it is formed by a series of composition, is interesting enough to warrant reactions beginning with a salt (I) contained further research into its potential use as a

SCH

Sulfatase ^^ ^ Tyrindoxyl sulphate salt

[Purpurase] [O] SCH3 ^ SCH

Br II Tyrindoxyl III Tyrindoleninone

0

IV Tyriverdii?

V Tyrian Purple (6,6' dibromoindigotin)

Figure 1. The production of Tyrian Purple (V) from a precursor salt found in the hypobranchial glands of muricids (adapted from Christophersen et al. 1978). The glands of Dicathais orbita contain the absolute precursor, the salt of Tyrindoxyl sulphate (I), as well as the sulfatase enzyme. Tyrian Purple (V) and the three intermediate precursors (II, III and IV) are not present in the adults but have been found in the egg masses oi Dicathais orbita.

June 1999 The Other 99%. The Consen/ation and Biodiversity of Invertebrates 317 drug. This demonstrates that new uses can be I have tested the egg masses of 31 different found for redundant natural resources. species from two classes ( and Cephalopoda), including 17 families of Molluscan medicines — links between biological Gastropoda. In total, 28 species showed and chemical diversity antimicrobial activity (Table 1). Brominated The egg masses from a number of different compounds (such as the Tyrian Purple species of muricids also show antimicrobial precursors) were not found in the egg masses activity. To determine if the same compounds of any species other than muricids. The were responsible for the observed activity in compounds responsible for the antimicrobial different species, I used Gas Chromatography activity in the other species are not presently Mass Spectroscopy to compare the volatile known, although previous studies have organic compounds present in the egg masses isolated novel antif^ungal and antitumour (Fig. 2). While the fresh eggs of Dicathais compounds from the egg masses of several orbita were found to contain one major opisthobranchs (Yamazaki et al. 1984; brominated compound (tyrindoleninone), a Roesener and Scheuer 1986; Kisugi et al. Downloaded from http://meridian.allenpress.com/rzsnsw-other-books/book/chapter-pdf/2643141/rzsnsw_1999_049.pdf by guest on 27 September 2021 much greater range of brominated com- 1987; Matsunaga et al. 1986; lijima et al. pounds was found in the eggs of the 1995). These compounds come from two Mediterranean species, e.g., Trunculariopsis completely different molecular classes; glyco- trunculus (Fig. 2). Several of these brominated proteins from Aplysia and macrolides from compounds could not be identified on the nudibranchs, providing preliminary evidence mass spectrum library suggesting they may that chemical diversity increases with be novel. Therefore, molluscs from just one biological diversity. family, the , elaborate a variety of Biologically active compounds in molluscs related compounds, which provide a range are not restricted to the egg stage. Previous of structural leads for drug development. studies have demonstrated the potent anti- My research actually suggests that anti- cancer activity of a number of metabolites microbial activity is a wide-spread phenom- from soft bodied molluscs (e.g., Pettit et al. enon in the egg masses of marine molluscs. 1989). Toxic peptides produced by predatory

10 20

a uu^ ii •JluiMI 10 20 30 40 50 Figure 2. Volatile organic components from the egg masses of two muricid molluscs separated by Gas Chromatography a) extractives from the egg mass of the Australian muricid, Dicathais orbita, b) extractives from the egg mass of the Mediterranean muricid, Trunculariopsis trunculus. Brominated compounds were designated according to the presence of characteristic doublets in the mass spectrum. The known brominated compounds (A) were successfully matched to compounds m the mass spectrum library, whereas the mass spectrum of the unidentified brominated compounds (•) did not match any known compounds in the library.

318 The Other 99%. The Conservation and Biodiversity of Invertebrates June 1999 the egg masses.

CLASS/ Order Family Proportion Subclass (Taxon) active GASTROPODA Prosobranchia Mesogastropoda Littorinidae 1/1 Naticidae 1/1 Ranellidae 1/1 Muricidae 4/4 Mitridae 1/1 Conidae 1/1 Opisthobranchia Anaspidea Aplysiidae 6/6 Cephalaspidea Philinidae 1/1 Notaspidea Pleurobranchidae 1/2 Saccoglossa Oxynoidae 1/1 Nudibranchia Dendrodorididae 2/2 Goniodorididae 0/1 Polyceridae 0/1 Downloaded from http://meridian.allenpress.com/rzsnsw-other-books/book/chapter-pdf/2643141/rzsnsw_1999_049.pdf by guest on 27 September 2021 Glaucidae 1/1 Pulmonata Basommatophora Amphibolidae 2/2 Siphonariidae 2/2 (Fresh water) Planorbidae 2/2 CEPHALOPODA Diabranchiata Loliginidae 1/1 TOTAL 28/31 snails in the Conus also provide a of environmental conditions and this is valuable resource. These toxins have been reflected in differences in their mineralized developed as tools for neurological research structures, for example shell morphology. (Carte 1996) and are being trialled as The structural architecture within molluscan strong pain killers and potential drugs shells has recently inspired the development against epilepsy, depression and schizo- of macrodefect (or flexible) concrete (Webb phrenia (Concar 1996). Interestingly, a et al. 1991). Similarly, the highly mineralized different class of toxins has been isolated of chitons are being used to develop from several muricids, including Dicathais new designs for dredging machinery (Webb orbita (Whitaker 1959; Welsh 1964; Roseghini et al. 1991). 1971). While some of these toxins have Other potentially useful materials from been tested and shown to possess pharmaco- molluscs include adhesives. Some molluscan logical activity (Whitaker 1960), their glues have the remarkable features of potential use as muscle relaxants, or tools corrosion resistance and the ability to stick for exploring cellular processes, have not under water. Medicine may also find a use been followed up. for the glues, by sealing wounds in internal Overall, molluscs have evolved a wide range organs (Young 1994). The chemistry of of biologically active compounds. These adhesives with these properties has been compounds span a diversity of chemical investigated in oysters and (Olivieri classes and appear to be more similar within et al. 1992; Young 1994) but the adhesives a family than across families. Species from used to attach egg masses to the substratum one family, such as the muricids, can also might also be of considerable interest. The produce different classes of biologically active deposition of attached spawn has evolved compounds. These may be used for different independently in at least three groups of purposes, such as defence and predation. All marine molluscs (Ponder and Lindberg 1997) these intrinsically toxic compounds are of and molluscan egg masses show great variety potential use in the medical industry. of form (Smith et al. 1989). A variety of glues may be obtainable depending on the species Molluscan materials — adaptations to the and/or the type of egg mass. environment The material of which the actual egg In the building industry the sculptural form capsules of some molluscs are composed may of shells has influenced architecture since also be worthy of investigation. The capsules the time of the Romans (Stix et al. 1978) of Dicathais orbita, for example, have a leathery but in recent times molluscs have had a or plastic-like texture. These capsules can hold more functional role in materials science by water and are soft and pliable when wet. The providing models for building materials and capsules are also biodegradable but will tools. Molluscs have adapted to a wide variety remain intact for many months (pers. obs.).

June 1999 Thie Other 99%. The Conservation and Biodiversity of invertebrates 319 Ultimately, the commodity value of bio- diversity will be much greater than is generally realized. Molluscs, for example, have adapted to a wide variety of life situations and the loss of any diversity will mean the loss of a library of adaptive information and potential resources. The preservation of molluscan biodiversity can therefore be argued on utilitarian grounds alone, although clearly there are also moral and ethical reasons for their conservation.

ACKNOWLEDGEMENTS ; .rl^r^j I am grateful to Dr Andrew Davis and

Professor John Bremner from Wollongong Downloaded from http://meridian.allenpress.com/rzsnsw-other-books/book/chapter-pdf/2643141/rzsnsw_1999_049.pdf by guest on 27 September 2021 University for guidance and assistance. I would also like to thank Dr Andrew Davis for helpful advice on the manuscript. Professor Andrew Beattie from the Centre for Biodiversity and Bioresources, Macquarie Dicathais orbita amongst a well developed egg mass. University, has greatly assisted my under- standing of how bioresources can be used as an argument for conservation. Hence the potential for the development of completely new materials from molluscs is REFERENCES also available. Beattie, A., 1994. Conservation, evolutionary biology Overall, molluscs have evolved a range of and the discovery of future biological resources. In materials to adapt to a variety of environ- Conservation Biology in Australia and Oceania ed mental conditions. The resource base of by C. Moritz and J. Kikkavt^a. Surrey Beatty & Sons: molluscs is increased by the fact that some Chipping Norton. species use different materials at different Beattie, A., 1996. Putting biodiversity to work. Search stages of their life history. Any of these 27(4): 111-13. molluscan materials could provide the key Baker, J. T, 1974. Tyrian Purple: Ancient dye, a modern to the development of a new resource. problem. Endeavour 33: 11-17. Variations in the mineralized structures of Baker, J. T. and Sutherland, M. D., 1968. Pigments related molluscs may also occur due to of marine VIII. Precursors of 6,6'- differences in their environment. Studies dibromoindigotin (Tyrian Purple) from the marine on these differences could facilitate the mollusc Dicathais orbita Gmelin. Tetrahedron Letters development of the optimal product or a 1: 43-46. . range of related products with important but Carte, B. K., 1996. Biomedical potential of marine subtle differences. natural products. Bioscience 46(4): 271-86. Christophersen, C., Watjen, Buchardt, O. and Anthoni, U., 1978. A revised structure of tyriverdin the DISCUSSION precursor of Tyrian Purple. Tetrahedron 34: 2779-781. Molluscs are the second largest Concar, D., 1996. Doctor Snail. New Scientist 152(2052): phylum and have provided a huge range of 26-28. actual and potential resources. Recently, the Eisner, O. and Spanier, E., 1985. The dyeing with Murex provision of resources from invertebrates and extracts, an unusual dyeing method of wool to the other biota has been used as an argument biblical sky blue. Proceedings of the 7" International Wool Textile Research Conference Tokyo 5: 118-30. for conservation (Roberts 1992; Beattie 1996). However, there has been some concern Friedlander, P, 1909. Ueber den Farbstoff des antiken Purpura aus Murex brandaris. Chemische Berichte 42: within the conservation movement that 765-70. only a small proportion of species will turn out to be useful. These concerns should Gerlach, H, J., 1991. Manufacture of 2 nitrobromo- benzaldehydes for the one-step manufacture of 6,6' be reduced as it becomes recognized that dibromoindigo. Ger Ojfen, DE 3,910,648, in Chemical the potential for resource development and Abstracts 114(2): 75. discovery is limited only by our imagination Hiyoshi, Y. and Fujise, Y, 1996. Tyrian Purple as a and knowledge. Furthermore, without knowing learnmg tool for natural products chemistry. Kagaku the needs and values of future generations, to Kyoiku 40(6): 390-93. it is impossible to assess the true value of Hoffmann, R., 1990. Blue as the Sea. American Scientist any given species. 78: 308-09.

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