Chemoecology 5/6,3/4:191-193 (1994/1995)

0937-7409/95/040191-03 $1.50 +0.20 © 1995 Birkh/iuser Verlag, Basel

After Louvain: Thinking about Chemical Ecology Miriam Rothschild Ashton Wold, Peterborough PE8 5LZ, United Kingdom

Jeremiah 1 may or may not have been a distinguished chemical ecologist but he understood one of the essential links between the animal and plant world, • . . And the wild asses did stand in the high places, they snuffed up the wind like dragons; their eyes did fail, because there was no grass.

George Wald 2 understood too, and won a Nobel prize. He pointed out that "throughout their entire range these excitations appear to be derived chemically from a single closely knit family of compounds, the carotenoids. This relationship persists from phototropism in moulds to vision in man." T o m Eisner 3 in his preface to "Chemical Ecology", stresses the fact we live in a world of sight and sound, and tend to be oblivious of the chemical events in our surroundings and in ourselves. Certainly we rarely reflect that without the golden pigments which plants donate so generously to the animal kingdom (about 100 million tons produced annually 4) we would be doomed to live like mole rats, tapping or thumping out information to one another in eternal darkness. On the other hand, on a warm, balmy summer evening we may well be thankful not to be consciously aware of the plethora of chemical messages cris-crossing the air around us - from thousands of sex-starved female insects calling, calling, calling for satisfaction. The hum and ping of their wings is quite enough. Chemical Ecology is a delightful area of investigation since it is relatively 'new', and the weft is dense and provocative, and surprise and discovery inevitable, mainly because the recent improbable advance in technology has 'opened unknown doors'. Sometimes it is Old Testament: Jeremiah 14: vi 2 Wald G (1960) The Distribution and Evolution of Visual Systems in Comparative Biochemistry. Vol I. p. 311 345. New York: Academic Press 3 Eisner T, Meinwald J (eds) (1995) Chemical Ecology. Washington DC: National Academy Press 4 Borenstein B, Bunnell RH (1966) Carotenoids: properties, occurrence and utilization in foods. Adv Food Rep 15:195 276 Bergstr6m G, Rothschild M, Groth I, Crighton C: present volume 6 Rothschild M (1994): unpubl. 7 Rothschild M, Moore BP, Brown VW (1984) Pyrazines as warning odour components in the Monarch Butterfly, Danaus plexippus, and in moths of the genera Zygaena and Amata (Lepidoptera). Biol J Linn Soc 23:375 380 Bopprb M (1977) Pheromonbiologieam Beispiel der Monarchfalter (Danaidae). Biologie in unserer Zeit 7:161-169 9 Malcolm SB: present volume

agreeable to ignore the constraints of philogeny! As I have already pointed out, we share pyrazines - aromatic volatiles - with plants and animals 5 - from passion flowers to nettles, tree trunks to sea anemonies, and rabbits to fish. In man - like in mice - they are found in our urine. Pyrazines stimulate recall in chickens and school children 6 and probably in T-cells; they can regulate ovarian development in mice, signal warnings from toxic plants, enhance the odour of m a n y flowers, and the bouquet of coffee and some white wines• Is their only benefit to man a possible stimulation of T-cells? Is our failure to recall surnames in old age due to a falling off in the production of pyrazines? This is something to think about in traffic jams. If the insect world has really pointed us in the right direction for improving recall we have much to be grateful for especially to Chemical Ecology and the ladybirds. Probably these charming beetles and their evocative odour were the first insects to be tested by GC. As larvae monarch butterflies sequester pyrazines from milkweeds 7 and store them, but if the caterpillars are fed on plants which do not contain any, the butterflies lack them too. Except Danaus megalippe, the Trinidad monarch; these insects secrete pyrazines themselves, if their hosts don't provide them - but they have not learned how to manufacture carotenoids. Ingested pyrrolizidine alkaloids - so elegantly described and with such matchless illustrations, by Michael BopprU - eventually generate sexual arousal in both men and adult danaine butterflies, but this curious and romantic coincidence has not produced a flicker of interest among chemical ecologists• The late Howard Hinton once remarked that the miracle of all time was the green world. Unquestionably - if surprisingly - the plants have won the battle against insects• But how? They are more versatile chemists, but they are static. They use the wind as a pollinator but many of them now depend on insects. How, for instance, can flowering plants protect their pollinators and yet cope with the appetites of hungry herbivores? Do the cardiac glycosides in the latex of Asclepias, which are sequestered by the larvae of danaines, protect these caterpillars from aerial predators and thus preserve the butterfly pollinators? Stephen Malcolm 9 has suggested that these plants produce a substance in the latex which thins out the population of freshly hatched young larvae. This would ensure a negligible sacrifice of foliage - even of seedlings - for the sake of the future invaluable pollinators.

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A glance at the literature concerning the scents produced by flowers indicates that vanilla is their commonest and most persistent odour. It is also recorded as a frequent fragrance on the wings of butterflies and moths. This is a subtle ploy whereby plants attract pollinators and bring the sexes together, offering them simultaneously both food and mates and thus furthering reproduction. The polyphagous garden tiger moth (Arctia caja) and other members of this ravishing genus, apparently do nothing to assist their host plants - for they are tongueless, and cannot function as pollinators. However, in the Valley of the Butterflies their relative, the Jersey tiger (Euplagia quadripunctaria), after their long summer drowse, bejewels the ivy blossom in their thousands and the flowering Ling in Rhodes. According to H a r t m a n ~° the cinnabar (Tyria jacobaea) - another relative - seems to have won this round, for it is no pollinator either, but by means of an insect enzyme "specifically processes a plant derived defence compound" to its own advantage. This discovery emphasises the great advances made in the field of chemical ecology for a mere 27 years ago, when the cinnabar larva was first shown to sequester and store PAs ~, it was only tentatively surmised that these alkaloids might function as part of a defence mechanism. By far the most exciting news of plants response to predators is Marcel Dicke's 12 revelation that by means of volatiles released from damaged foliage, carnivores are attracted to the scene and attack the voracious herbivores. A wonderful new vista now lies spread out before us - but one hopes fervently the elimination of the large white (Pieris brassicae) is not envisaged, although it may now be possible. The Caterpillar on the Leaf Repeats to thee thy mother's grief Kill not the M o t h or Butterfly For the Last Judgement draweth nigh. Fortunately among the Chemical Ecologists we have Ritsuo Nishida 13 - a gifted scientist who loves butterflies. He and his school of thought give us a glimmer of hope for the whites and blues. The plants' response to the presence of insect eggs on their leaves is more subtle - by producing deterrent volatiles further

10 Hartmann T: present volume 11 Aplin RT, Benn MH, Rothschild M (1968) Poisonous alkaloids in the body tissues of the cinnabar moth. Nature 219:747-748 12 Dicke M: present volume 13 Nishida R: present volume 14 Blaakmeer A, Hagenbeek D, van Beek TA, de Groot AS, Schoonhoven LM, van Loon JJA (1994) Plant response to eggs vs host marking pheromone as factors inhibiting oviposition by Pieris brassicae. J Chem Ecol 20:1657-1665 15 Nash R: present volume 16 Sondheimer E, Simeone JB (eds) (1970) Chemical Ecology. New York: Academic Press 17 Zlotkin E (1973) Chemistry of Animal Venoms. Experientia 29:1453-1588 18 Brown KS Jr, Trigo JR (1995) The ecological activity of alkaloids. Pp 227 354 in Cordell GA (ed) The Alkaloids 47. San Diego/CA: Academic Press; and present volume

CHEMOECOLOGY oviposition is inhibited but the eggs are not destroyed 14 - thus preventing excessive predation but allowing for the survival of a few useful pollinators. It is worth recording that if the large white female has access to the nectar of crucifers, she lays more rapidly than without this stimulus. Recently, Robert Nash 15 has identified hitherto undescribed glycosidase inhibiting alkaloids in plants, which are sequestered by various larvae and thus eventually stored by the butterflies. Maybe this endows the insects with indigestible qualities. Tropane alkaloids, one surmises, are present in the nectar of various flowers as well as their foliage. Is this yet another plant ploy for protecting pollinators without the sacrifice of a single leaf?. Chemical Ecology began for me when I heard T o m Eisner and Murray Blum read papers at the Entomological Conference in Vienna in 1960. I felt these two invented chemical ecology. Some ten years later Sondheimer and Simeone's book ~6 appeared and I really abandoned my rabbit fleas at that moment. Eli Zlotkin's fabulous series of publications on animal venoms added flames to the fire. About this time (in the early seventies) it was claimed that 10,000 papers on this topic appeared annually. Zlotkin ~7 pointed out that "one is often obliged to make the choice between a superficial but complete coverage of the whole subject or detailed presentation of only a part of it". This is also true now of Chemical Ecology but fortunately, to begin with, questions and answers were conveniently circumscribed: Do monarch butterflies store cardiac glycosides? Is sinigrin the large white's oviposition cue? Do captive birds reject mimics after experience with models? But these days are nearly over. Now, if you dare look closely at the chemical defences of any insect you are awestruck, almost appalled, by its complexity and variability. What is ACh doing in such quantities in the garden tiger, and pyrazines, PAs, cardiac glycosides, and the lethal protein cajin? Where does the pterobilin in its eggs come from considering the caterpillar exceptionally - has none? Since the eggs contain PAs, why are they not yellow like the cinnabar's eggs? Maybe they only occasionally contain PAs because the larval diet is polyphagous and crypsis is probably a precautionary measure. Variation is the salt of life! Keith Brown now demonstrates how to integrate animal and plant chemistry within natural biological systems. His "Ecological Activity of Alkaloids ''~8 is a stunning contribution. He gives us a good account too, of the magnificent muddle we have to disentangle, which "reveals a confusing variety of diffuse and complex patterns becoming increasingly closer to chaos". Eli Zlotkin's present expansion into genetic engineering and molecular biology may well by-pass us, and will add a bit of Brave New World to the toxin scenario. Meanwhile, we follow Keith Brown into the Brazilian forest or the New Forest (in the U.K.) - while they are still there - and reflect how fortunate we are to have lived in a time while there is still an interface to investigate between the Chemical and Natural Worlds! The monarch butterfly, since it is known to contain cardenolides, PAs, pyrazines, carotenoids and blue bile

Vol. 5/6, 1994/1995 pigments, should be the Chemical Ecologist's logogram - only it is preoccupied. But what can we do about the man-made plight of the millions of monarchs gathering at this moment in Mexico? Today, the hibernating site of

D. plexippus is in great danger due to the logging of the trees in the area where they roost in winter. The situation in Mexico is extremely complex, beset with political and economic crises - very deep water, with multiple undercurrents, inter-departmental conflicts aggravate the situation ... There are five core centres where the monarchs hibernate. One of these is taken over by the Govern-

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meat as a tourist attraction and, since it engenders a lot of money, it will probably survive. The giant spruce fir trees which constitute the remaining four core centres stand on what is common land. The local inhabitants can walk in and fell any tree they fancy. There are now big companies provided with up-to-date machinery which are buying the timber rights from the people who own the common rights. I am very much afraid that one of the most grandiose phenomena of the butterfly world and chemical ecology is doomed to extinction. Can't we do something about it?