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New Zealam{{ournaloJBotany, 1979, Vol. 17:431-40

Anthecology: Old Testament, New Testament, Apocrypha (Banquet Address, 8 February 1979) HERBERT G. BAKER

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Department of Botany, University of Califomi a, Berkeley, CA 94720, U.S.A. Abstract The development of anthecology, with an emphasis on pollination ecology. is surveyed. using less-often cited literature. The Old Testament of anthecology was written at the end of the nineteenth century; the New Testament began to be assembled after the rise of the Synthetic Theory of Evolution ("Neo-darwinism") in the 1940s. Differences between the Old and the New anthecology are discussed and particular attention is given to the new emphasis on tropical anthecology. Apocryphal writings are to be found in all the literature periods; some of them have led to important developments and others may do so. Particularly with the prospect of serious development of the anthecology of ecosystems. it is suggested that amateur botanists can make a contribution to the New anthecology comparable to their influence on the Old.

INTRODUCTION In 1977. Dr Eric Godley asked me ifI would speak to you about reproductive biology as I have seen it "throUgh several decades". That reference to "several decades" shook me but, after I calmed down. this began to seem like a good opportunity to look back even farther into history than several decades, and to make some comments upon changes in the aims and methods of reproductive biology. with special emphasis on pollination biology. This will take me back through several incarnations, not merely several decades! I chose a title for my talk that was intended to be only slightly irreverent (and not at all irrelevant). And the first word in the title is anthecology. which may be less familiar to you than the other words. In my opinion this term deserves to become standard. to encompass the various ecological aspects of pollination (and seed-dispersal) biology. It was introduced over 70 years ago by Charles Robertson (1904). an American biologist whose work and writings have had less recognition generally than they deserve. mSTORY Sex in flowering plants

Any careful observer of natural pollination can qualify as an anthecologist. and this habit probably goes back a very long way in human history. Before there was agriculture. and certainly soon after its appearance on the world scene. it is probable that

mankind was more aware of the processes of plant reproduction than we tend to assume. The naturally observant gatherer of wild seeds for food must soon have become aware that in wet weather some of. them sprouted to produce seedlings. And. as suggested by the famous Mesopotamian bas-relief. from the ninth century B.C .• that is nicely pictured on page 9 of Baastian Meeuse's (1961) book on pollination. where men are shown shaking branches from a staminate date palm over the flowers of a pistillate palm. it was probably dioecious species that gave the clue that flowering plants have sex. The analogy with the two sexes of human beings and domesticated animals would have seen to that. In their book. "The Pollination of Flowers". Michael Proctor & Peter Yeo (1973) give a clear summary of the development of European thinking and understanding of the pollination biology of flowering plants. A detailed account of those aspects that refer to the relation between nectar production and insect pollination is provided by Jacob Lorch (1978). Also my colleague Rudolf Schmid. in a recent article in "The Biologist" gives an excellent bibliography (Schmid 1975). Conseqently. I need not traverse all that ground again. but I should like to draw your attention to some pieces of literature that the historians of anthecology often miss. In the year 1700. a Dutchman named Willem Bosman visited the Guinea Coast of West Africa. and he wrote to a friend back in Holland. "There grow multitudes of papay-trees all along the Coast;

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New Zealand Journal of Botany, 1979, Vol. 17

and these are of two sorts, viz. the male and female nourish it till it becomes a perfect seed". (Smith or at least they are here so called, on account that 1841,p.3) those named males bear no fruit but are continually In a few lines, he not only demonstrated apofull of blossoms, consisting of long white flowers; mixis but also dealt a death blow to the once widely the female also bears the same blossom, though not held belief about the parentage of embryos, both so long, nor so numerous". those of plants and, by extrapolation, those of "Some have observed that the females produce animals and human beings, too. their fruits in greatest abundance when the males It was goodbye to the homunculus in the sperm! grow near them; you may, Sir, believe what you please: but if you do not, I shall not charge you with Self- and cross-pollination heresy." (W. Bosman, in translation in Pinkerton But most flowering plants are hermaphrodite, and it (1814).) was hard for the eighteenth and early nineteenth The really interesting fact is that the West century pollination biologists to see how this could Africans had recognised sex in their plants at a time promote anything but self-fertilisation. when Rudolf Camerarius (1694), in Germany, and Consequently, in the mid-eighteenth century, Nehemiah Grew (1682), in England, the protagonists when Joseph Kolreuter made systematic observaof the idea that flowering plants have sex, were sub- tions of pollination, and carried out experiments to jected to scornful denunciation by the great French show that, even in some hermaphrodite flowers, botanist Joseph Tournefort. insect visits were necessary for seed-setting, he was Tournefort believed (and I quote from a trans- inclined to attribute this to self-pollination brought lation in Proctor & Yeo (1973» that the stamens about by the insects (Kolreuter 1761, 1763). merely serve to " ... excrete unwanted portions of When Christian Konrad Sprengel published his the sap in the form of pollen" . A sort of solid trans- pioneering work "Oas entdeckte Geheimniss der piration, if you like! Natur im Bau und in der Befruchtung der Blumen" Of course, things improved from then on, and in 1793, he presented plenty of evidence that flowers many botanists contributed to our understanding of attract and reward insects with nectar. He also how, even in those flowers that contain both showed that wind-pollination occurs, demanding, in stamens and carpels, there is sexual reproduction. that case a plentiful supply of pollen. Whatever the And, in 1735, Carolus Linnaeus produced his mode of pollination, he wrote, "It seems that nature "sexual system of plant classification" (Linnaeus is unwilling that any flower should be fertilized by its 1735) that gave special attention to the androecium own pollen" (translation in Lovell 1918, p. 12). But, and the gynoecium. did he appreciate the biological significance of this cross-pollination? Apomixis Sprengel's work lay almost unnoticed or unapIt may be appropriate, at this moment, to point out preciated for over 50 years, and Herman Miiller, that a dioecious taxon also provided an early- himself a great anthecologist, pointed out a reason probably even the first - demonstration of the for this (Muller 1883, p. 3) - "It is remarkable in absence of sex in some flowering plants. The dis- how many cases Sprengel recognized that the pollen covery was made by John Smith, and presented to a is carried of necessity to the stigmas of other flowers meeting of the Linnean Society, in London, in 1839. by the insect-visitors, without suspecting that John Smith (it was his real name) was first employed therein lies the value of insect visits to the plant". in the Edinburgh Botanic Garden, but moved to the Muller blamed Sprengel's failure to show an Royal Botanic Gardens, Kew in 1822. He is best advantage to the plants in cross-pollination for the known for his work with ferns but he was interested neglect of his work in subsequent years. How much better it might have been ifSprenge1 and his contemin a wider botanical range. At Kew, Smith received a shipment of five poraries had been able to attend an international· plants of what we should now call Alchornea symposium on the reproduction of plants, as we are ilicifolia Muell. Arg., in the Euphorbiaceae. These doing now? I say this because, in 1799, Thomas plants came from Moreton Bay, in Queensland, Knight, President of the Horticultural Society of Australia. He noted that all five of them were pistil- London, reported in print on many crosses that he late plants, with no sign of an androecium. Neverthe- had made between varieties of garden peas and less, he observed them to set full crops of germinable showed that cross-fertilisation had rather surprising seed at Kew, and raised plants from them that he results: "Among the progeny of my hybridizations, I used as a demonstration to the Linnean Society. At found a numerous variety of new kinds produced, the end of a beautiful three-page paper, he wrote, "I many of which were in size and in every other resshall conclude by merely observing that the absence pect, much superior to the original white kind, and of pollen in this instance is irreconcilable with the grew with excessive luxuriance" (Knight 1799). And theory that every grain of pollen furnishes a germ, Knight then made his famous dogmatic statement and that the ovulum is merely a matrix to receive and that "No plant self-fertilizes itself for a perpetuity of

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generations" - a non-testable proposition that would be frowned upon by scientific purists at the present day. Similar experiments were made later by Carl Friedrich von Gartner (1844, 1849), by William Herbert (1837), by Friederich Hildebrand (1867) and, of course, by Charles Darwin (especially Darwin 1876; "The Effects of Cross and Self Fertilisation in the Vegetable Kingdom"). This, in turn, led toa vast amount of data-collecting by naturalists intent on demonstrating the operation of outcrossing mechanisms. I believe that, in New Zealand, these included notable contributions from T. F. Cheeseman (1872, et seq.) and George Malcolm Thomson (1878, et seq.). So, the Old Testament of Anthecology was being assembled. Heresies All of us are familiar to some extent with this story, but what is not so generally realised is that there were a number of biologists who were unconvinced of the truth of this alleged advantage of cross-pollination. Thus, in England, the Reverend George Henslow, after originally agreeing with Darwin, objected strongly (Henslow 1876, et seq.) that some of the world's most successful species are weeds that have penetrated the farthest corners of the world. These plants, for example, Poa annua. Oxalis cornicutata, Stellaria media, and Anagallis arvensis, are usually self-pollinated. Henslow believed that flower shapes and colors were caused by the "irritation" of the insects that visited the flowers. Twelve years after his first protest, he wrote: ". . . our previous ideas were all wrong and we must reverse them. The most conspicuous flowers ... fertilized by insects are not the best off; but they cannot help themselves. Whatever an insect does to them, they must yield to it and grow in adaptation to it; but while they are thus stimulated to become what we may choose to call finer flowers, ... all this is secured at a sacrifice of fertility. They neither set seed in anything like the proportion that "weedy" plants produce, nor can they hold their own so well when they find themselves transported to distant countries . . . . Those [plants] which cannot have plenty of well-nourished seeds, and are dependent on insects, - perhaps one or two kinds only - will ultimately die out and disappear altogether" (Henslow 1891, pp. 147-8). There is so much that is nearly true in what Henslow wrote, but also so much that is egregiously wrong, that it is hard to judge his many contributions to anthecology appropriately (Baker 1965). In North America, Thomas Meehan took the same line as Henslow, and a rather similar line was taken in the early twentieth century by a Dutchman, W. Burck (1909).

433 Now - George Henslow was the son of John Stevens Henslow, the man who had inspired Charles Darwin when he was a Cambridge undergraduate, and who had strong influence in getting Darwin on to the voyage of H.M.S. Beagle. Also, Joseph Dalton Hooker, Darwin's botanical right-hand man, had married George Henslow's sister. Consequently, in the British social system of the Victorians, these two facts alone would have been enough to enable George Henslow to escape criticism from Darwin's camp. So, he was just ignored - and his many writings became part of the Apocrypha of anthecology. Incidentally, Thomas Meehan was not so fortunate - at Darwin's instigation, he received a smart dressing-down from Asa Gray (Baker 1965). However, I think it is important to keep Henslow's championship of the seifers in mind, for it was subsequently realised, in the twentieth century, that the breeding mechanisms of flowering plants are often flexible and adaptable to environmental circumstances, and cross-pollination is not always advantageous. Less well-known is the heresy of the great French botanist, Gaston Bonnier. Bonnier, who published a big study of floral nectaries and nectar in 1879, along with some other papers on pollination, decided that the function of nectar, often from glands in the vicinity of the ovary, is to be re-absorbed as nourishment for the developing seeds, provided that it is not "stolen" by insects. He denied that its presence in flowers was a result of selective pressure for cross-pollination. But what Bonnier never explained was why nectar could also be found in purely staminate flowers (Linnaeus (1751) had already pointed out that staminate flowers of Salix produce nectar). This idea, that the exudation of nectar from a nectary is just a means of getting sugar and water out of the way temporarily, has, to this day, not lost all its adherents, but, mostly they are plant physiologists rather than ecologists. However, the idea can be traced back to Giulio Pontedera, in 1720, and was espoused by several botanists subsequently (listed in Lorch 1978). I have found it in slightly different form in a remarkable book by a very remarkable man, Erasmus Darwin, the grandfather of Charles Darwin. His book, "Phytologia", was published in 1800. Erasmus Darwin believed that plant parts could be compared with animal organs. He believed that the leaves of a plant and the petals of its flowers functioned as lungs for the oxygenation of the vegetable blood (its sap); the veins of the leaves corresponded to the arterial and venous systems of an animal, while he even suggested that the soft pith in the middle of a stem might be brain tissue. The following quotation sums up his opinion of nectar exudation, " ... honey ... is secreted by an appro-

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priate gland from the blood after its oxygenation in the corol ... , and is absorbed for nutriment by the sexual parts of the flower" (E. Darwin 1800, p. 109). By "sexual parts" he meant ovary and the stamens because he was well aware of the existence of nectarproducing staminate as well as pistillate flowers. However, I think we can say "Here is another contribution to the Apocrypha!" Later, in 1907, Burck statedjustthe opposite. In his opinion the exudation of nectar is a kind ofleakage in the flower during the process of withdrawing water from the anthers, causing them to dehisce. After that, he thOUght that the nectar WOUld, in some way, serve to protect the ovary from desiccation (Burck 1909). A somewhat similar suggestion, that unneeded water (with contained excreta) is removed from the tissues as nectar, was put forward in 1832 by A. P. de Candolle. Even earlier, J. G. Kriinitz ( 1773) had claimed that nectar is a harmful substance to the flower and that insects help the plant by removing it.

New Zealand Journal of Botany, 1979, Vol. I7

descriptive information, but is remarkable, also, for some ideas that were ahead of their time. Thus, there is a very modem ring about this statement by Hermann Miiller, in his account of Lythrum salicaria and its pollination, "The loosestrife is visited by a number of long-tongued flies, especially Rhingia rostrata. This fly, standing on o:te or more of the petals ... stretches its proboscis out to a length of II to 12 millimetres, and thrusts it down into the flower, letting it remain there from six to ten seconds. Immediately after withdrawing it from the tube, it usually manipulates one of the anthers with its labellae for a short time (one to two seconds) in order to add to the liquid nonnitrogenous food some solid nitrogenous matter in the shape of pollen grains." (H. Miiller 1883, pp. 259-60). My only criticism of that account must be that the nectar of Lythrum species is not completely lacking in nitrogenous substances (Baker & Baker 1975)! But although he contributed so much material to it, Hermann MiilIer did not write what I really conThe Old Testament of anthecology Despite some contrary views, the Darwinian sider to be the Old Testament of anthecology. This (Charles Darwinian) theory of evolution by natural was contributed by a lesser scientist, Paul Knuth, selection caught on in the second half of the nine- who brought virtually everything that was known at teenth century, and there was great enthusiasm the end of the nineteenth century together in his among naturalists to elucidate the selective advan- "Handbuch der Bliitenbiologie", published in three tage, in promoting cross-pollination, of every floral volumes from 1898 to 1905. His compendium was preceded chronologically by a similar two-part work character. Careful studies of the morphology and by Ernst Loew (1895) and by a notable handbook by behaviour of floral parts were made. Long lists of Anton Kerner (1878), but it is Knuth's book that has insect visitors to flowers were compiled, often with- become a classic. Knuth dedicated his volumes to out much concern to see whether all of these insects Sprengel and to Hermann Miiller, truthfully indicatwere effective and frequent carriers of pollen ing whence came the inspiration for his largely compilatory work. between plants. Two of Knuth's three volumes were translated Sometimes the rationalisation was not completely convincing. An example is the pollen into English by J. Ainsworth Davis, and published in dimorphism that Fritz Miiller described in a hetero- Oxford in 1906 to 1909. Interestingly indicative of the stylous Brazilian species of Rubiaceae that he attri- parochialism of scientific attitudes at the time, was buted to the genus Faramea (but which is really a the failure of the English version's publishers to have species of Rudgea - Baker 1956). Fritz Miiller's the third German volume, dealing largely with nonsuggestion was that the spiny pollen grains from the European items, translated and, for many botanists, exserted anthers of the short-styled form needed it has been as if the third volume had never been their spines to stick together on windy days and to written (see Schmid & Schmid 1970). But this was the end of an era. hang on to a pollinator that might brush against them. It is possible that the publication of this On the other hand, smooth pollen would be adequate for the long-styled form because this produces its apparently comprehensive survey may have directly pollen in the shelter of the corolla tube (see Darwin inhibited work on pollination biology, for many publishers may have felt that "the job was done". 1877, pp. 129-30). But the greatest contribution of all was probably Notably, when Charles Robertson (1928) wrote a that made by Fritz Miiller's brother, Hermann book that listed mid-western North American Miiller, in 1873, in his book "Die Befruchtung der flowers and their pollinators, he published it himself. However, there must have been other reasons Blumen durch Insekten". It was translated into English and published in London in 1883. for the apparent diminution in the amount of active Incidentally, Charles Darwin wrote a "Prefatory research that occurred in the first four decades of the Notice" for the English edition, one of the last twentieth century. Actually, the tum of the century was a time of crisis for any kind of biology with an writings that he made before his death in 1882. This book contained an enormous amount of evolutionary emphasis. The rediscovery of

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Mendelism tended to put a damper on over-enthusiastic Darwinism, with its ascription of easily appreciated selective advantage to every morphological feature. Also, the rise of physics, chemistry, and other indoor sciences tended to promote laboratory study rather than field natural history as the thing to do to win acclaim. The taxonomists, who were active, made little use of floral junction, even though they were giving close attention to floral structures, and making use of them in classification Even outdoors, the new discipline of ecology was in a phase where the description of vegetation took most of the time of its exponents. Anthecology went into a decline, although it certainly was not dead. Some well-written books were published, such as those by Oskar von Kirchner (1911) and H. Cammerloher (1931). One of the nicest books of this period was the unfortunately titled' 'The Flower and the Bee" , by John H. Lovell (1918). This dealt with North American flowers and their insect visitors (not just bees), and is beautifully illustrated by photographs. In some ways, this book, which partly redressed the European imbalance of Knuth's Handbook, contained a look into the future by its entomological as well as botanical concern and by the stress that it put on floral biology on a community basis, as well as dealing with individual species. Also, during this period, there were substantial studies of an experimental sort (again presaging an emphasis that was to come to anthecology later) by F. Knoll (1921, etc.), Frederick E. Clements & F. L. Long (1923), E. Daumann (1932, etc.), and the great studies with honey bees by Karl von Frisch (1950, etc.). In the tropics, and elsewhere, Otto Porsch (1909, etc.) was travelling and observing pollination mechanisms, especially those involving birds (Porsch 1924, et seq.). Porsch seems to have been the first to give serious consideration to bat-pollination (and pollination by some other mammals) as a significant feature of tropical anthecology (Porsch 1931). The New Testament of anthecology It took the rise of the Synthetic Study of Evolution - Neo-darwinism, as some people called it just before and during World War II, to bring anthecology back into importance. Palaeontologists, morphologists, taxonomists, ecologists, geneticists, and practitioners of some other disciplines saw the value of inter-disciplinary synthesis in the solution of evolutionary problems. Ifgene-flow, or the lack ofit, is important evolutionarily, then knowledge of breeding systems and anthecology are needed. And to be able to provide something that is needed is a great human stimulus to work. It would be invidious to point to the leaders in the assemblage of information and ideas from which the New Testament of anthecology will be com-

435 posed. Most of them, young and old, are working actively now. And there is no need to go into detail about what kinds of information will go into the New Testament, because that is what this symposium is all about. Nevertheless, it might be useful to point to a few of the differences between the New anthecology and the Old. When the New anthecology began, the reaction against the old, long lists of flower visitors was immediate. Syndromes of characters were drawn up whereby any flower could be identified as a "butterfly flower", a "hawkmoth flower", a "beetle flower" , and so on. An illustration would be a species of Aloe from South Africa. Red, scentless, broadly tubular flowers with exserted stamens and styles, a plentiful supply of only slightly viscous nectar at the base of the corolla tube, and a standing place on the inflorescence for a nectar-taker who will contact anthers and stigmas all add up to a "sunbird pollination syndrome". But honey bees visit these flowers to collect pollen, and they must play some role in the pollination process, too. Syndromes are described particularly in the works of L. van der Pijl (1960-61), Faegri & van der Pijl (1966), and Baker & Hurd (1968). But, still more recently, I think the pendulum, having swung to both extremes, is back in a central position, for it is now realised that complete dependence on a single kind of pollinator is a rare phenomenon. Even the classic case of strict mutualism of the Yuccas and the Yucca moths (Tegeticula) is being modified to some extent. Looking at cultivated material of Yucca aloifolia, Jacob Galil (1973) has discovered that this species produces floral nectar and is visited - and occasionally pollinated - by bees. Tropical studies The Old anthecology was largely made up from temperate zone studies, and most of these were made in Europe. But, now, there is a growing emphasis on tropical studies and I should like to give special attention to work in the tropics. The foraging patterns of diurnal bees, birds, and butterflies, and of nocturnal moths and bats are often more easily studied in tropical forests and savannas, and such phenomena as "trap-lining" by some of these animals have come to light there (cf. Janzen 1971, Baker 1973, etc.). Some bats forage singly, others do so in groups (Heithaus et al. 1974; Sazima & Sazima 1977, 1978), and more is being found out about these patterns of behaviour by the use of nightviewing devices (Ayensu 1974) and radio telemetry (Fleming et al. 1977, Heithaus & Fleming 1978). Even the photography of bats at work is much more sophisticated now than it was when Brian Harris and I attempted it in West Africa some 25 years ago (Baker & Harris 1957, etc.). Operating in the dark, we could only see dimly what was going on

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436 and the pollination story had to be largely built up from the pictures that were taken. Now, with excellent electronic equipment, much more can be learned in the field. A. N. Start & A. G. Marshall (1976) and Edwin Gould (1978), in Malaya, and Ray Heithaus & Theodore Fleming (1978) and Donna Howell (1978), in Central America, have shown that bats may forage at trees many kilometres away from their roosts, and these same workers are developing some ideas, as yet apocryphal, I suppose, about the communication of foraging information between these bats in their communal roosts. Robert Sussmann & Peter Raven (1978) have developed a theory, still apocryphal until more hard data can be acquired, that before flower-visiting bats inhabited the Palaeotropics, non-volant mammals performed pollinatory functions, but have now largely been replaced by the bats. Lemurs may still do the job in Madagascar. Delbert Wiens & J. P. Rourke (1978) have studied the pollination of Proteaceae that produce their flowers at ground-level by rodents in South Africa. And it has been pointed out to us at this meeting by James Armstrong and Hugh Ford that some of the ground-level flowering Australian Fabaceae are pollinated by ground-foraging birds of the Meliphagidae. I confess that this disappoints me, for I have long nourished a secret belief that the knob on a Sturt's Desert Pea (Clianthus formosus) is punched by the tapering snouts of bandicoots in need of a refreshing drink Gust as we do to a soft-drink machine). So - bandicoot pollination may be apocryphal, but, of course, other marsupial pollination offlowers has been photographed beautifully for woody plants in Australia by Michael Morcombe (1968, etc.). A very important development in anthecology is that close attention is being given to the comparative anthecology of some of the larger tropical families (following the example set for the largely temperate family Polemoniaceae by Grant & Grant (1965». A case in point is the close study of the Bignoniaceae by Alwyn Gentry (1974, etc.). Another is the beautiful work on the Lecythidaceae of tropical America by Ghillean Prance and his collaborators (Prance 1976, etc.), where the large and elaborately structured flowers are related to the various kinds of bees that are involved in their pollination. Perhaps we shall get, from studies like these, an answer to another minor problem that has always worried me - why should Rafflesia (Ratllesiaceae) in south-east Asia produce a flower a metre across just to be pollinated by flies? Can some other pollinator be, or have been, involved in its floral evolution? Experimental work Experimental and analytical studies on the breeding systems of tropical trees, especially those made in

New Zealand Journal of Botany, 1979, Vol. 17 Central America by Kamaljit Bawa (1974, et seq.) and Paul Opler, in South America by Thirza Ruiz Zapata & Mary Arroyo (1978), and in the Palaeotropics by Brian Styles (1972, et seq.) as well as by Peter Ashton and his Malayan collaborators (Ashton 1977, etc.), have revealed unusually high proportions of dioecious and monoecious species amongst .tropical forest trees. The dioecism and monoecism had often escaped notice before because the staminate and pistillate flowers look so much alike. Undoubtedly, this is due to the necessity of attracting animal pollinators to both kinds of flower - a difference from the situation in trees in temperate regions, where the two kinds of flower are very different because of their adaptation to wind-pollination. Recently, it has been shown (Baker 1976) that, in some cases, rewards to visitors are not made by pistillate flowers but only by staminate ones (nectar and pollen in the dioecious Caricaceae, for example, and pollen only in such monoecious species as Stelechocarpus burakol, in the Annonaceae). In these cases, I have called the visits of animals to the pistillate flowers' 'mistake pollination" , and this may not be uncommon in tropical ecosystems. Still more recently, investigators led by Peter Ashton (Kaur et al. 1978, Ashton 1977), in Malaya, have begun to demonstrate apomixis as a possibly frequent breeding system in climax forest trees, freezing the heterozygosity (and, possibly, heterosis) produced by the cross-pollination of their sexual ancestors. In the New anthecology, the chemistry of pollen and nectar rewards to animal pollinators of flowers is getting attention. Both pollen and nectar have been revealed to be much more complex chemically than had been recognised previously. Nectar cannot be regarded as just sugar-water any more. Lipids, proteins, amino acids, other organic acids, phenolics, alkaloids, and other substances may occur in greater or lesser amounts (Baker & Baker 1975, 1977; Baker 1977, 1978). Lipids have been found to be quite common nectar constituents (mostly in emulsion form in the aqueous nectar) (Baker & Baker 1975, Baker 1978, etc.), and they may be part of the energy provision by the flowering plant that is used by the visitors. Floral gland exudates that are almost completely lipid have been found in tropical and subtropical Malpighiaceae, Krameriaceae, Scrophulariaceae, and Orchidaceae (Vogel 1974, Simpson et al. 1977) as well as in the Melastomataceae (Buchmann 1979) and these exudates are collected by bees, especially of the genus Centris, that appear to use them to feed their larvae. In north temperate Lysimachia (Primulaceae), a similar exudation of lipids occurs (Vogel 1976). Even the sugars of nectar pose some problems. Take bird-pollination for an example. Hummingbird

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flowers tend to produce sucrose-rich nectar. On the other hand, flowers pollinated by passerine (perching) birds tend to be rich in hexoses (Baker & Baker 1980). This can be illustrated by two species of Campsis (Bignoniaceae). Campsis radicans. from North America, is pollinated by hummingbirds, and has sucrose-rich nectar. Campsis grandiflora, from China, the only other species in the genus, has a hexose-rich nectar that fits with its availability to passerine birds in its native area (Baker & Baker 1980). Presumably the offerings are matching the preferences of the birds, but to find out why there should be such different preferences, more work by ornithologist/physiologists is needed. Quantitative studies Quantitative study of the energetics ofnectar-collecting by flower visiting animals is one of the outstanding attributes of the New anthecology. The energy supply, based upon the rate of exudation of nectar and its sugar concentration, is being linked to the foraging behaviour of these animals and to the breeding systems of plants. The seminal paper in this area was published by Bernd Heinrich & Peter Raven, in 1972, and a good review of the subject was written by Heinrich (1975). Nowadays, all aspects of the New anthecology are quantitative - this is its most distinctive feature. And new techniques have been introduced to make it possible to follow pollen dispersal in quantitative fashion. Thus, the old method of dusting a powdered dyestuff in flowers and locating the stain it produces when carried to other flowers is still used (e.g., Linhart 1973), but potentially more accurate methods, such as the neutron activation technique developed by Steven Handel (1976), are becoming available to investigators with the necessary technological backing. Ecosystem anthecology With this increase of attention to the fine details of flower-visitation has come a realisation that the pollination-requirements of widespread flowering plant species may be satisfied differently, by different pollinators, in different habitats, and that there are floral differences that can be related to this. Verne Grant (see Grant & Grant 1965, pp. 69-73) pioneered what we may call "pollination ecotype" study with his investigation of populations of Gilia splendens in California. This has been followed by other studies by several investigators and now some Berkeley students are making such studies on other genera in temperate and tropical regions. This serious concern with the needs and behaviour of the pollinators - and with pollen and nectar "thieves" as well - suggests that we are gradually moving toward looking at anthecology on an ecosystem basis. To do this, we have to return to

437 the Old Testament practice of looking at all kinds of visitors to a plant's flowers, but distinguishing between those that are relevant to pollination in that species and those that are not. We did this a dozen years ago for Ceiba acuminata (Bombacaceae) in the thorn scrub of northwestern Mexico (Baker et al. 1971). The large flowers of this tree open just after dusk, and are pollinated during the night by bats (Leptonycteris sanborn i) and in the morning by hummingbirds. However, there is nectar left over from these visits and this is taken in the morning by several kinds of bee, a wasp, and skippers. The pollen remaining in the anthers is removed by halictid bees. None of these Hymenoptera or Lepidoptera contact the stigma, so they are not pollinators of Ceiba acuminata, but this tree feeds them at a time when there are few other trees, shrubs, or herbs flowering in the thorn scrub, and they are thus kept available for other species when these do come into flower. Of course, such behaviour is not altruism; it represents successful minor parasitism by the insects, but it surely plays a part in the evolved organisation of the thorn-scrub ecosystem. The same sort of tallying, on a much more exact and quantified basis, needs to be done with all of the other species in the ecosystem. It will be an enormous task! Andrew Moldenke (1975, 1976) has made comparative studies of the pollinators of plants in several ecosystems in California, and has estimated the roles of "generalists" and "specialists" among the flower visitors in these ecosystems. Earlier, Theodore Mosquin (1971) had described competition for pollinators and its avoidance by differential flowering times in a western Canadian mountain ecosystem. Several recent reports of flowering time difference have implied that adaptive displacement offlowering times have occurred. In Utah, Kent Ostler & Kimball Harper (1978) have used data resulting from earlier ecological surveys to reveal patterns of predominant flower colour variation between ecosystems, an approach which it may be pointed out was pioneered in the European Alps by Hermann Miiller(l873; 1883, pp. 596-7) and also hinted at by Lovell (1918). Even at this level of ecosystem analysis much work is required; for total investigation of flower-pollinator interactions in only one ecosystem, complete dedication by the investigator will be needed. Consequently, we may expect the move towards ecosystem studies to be very gradual. It may start with comparative phenological studies (of which the study in Costa Rican forest regions by Frankie et al. (1974) may be an example), and continue in the style of Heithaus' (1973, 1974) comparative studies of insect-plant relations in a range of Costa Rican ecosystems, noting whether flower visitors are specialists or generalists, whether they

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438

New Zealand Journal of Botany, 1979, Vol. 17

are long-lived or short-lived and, if they have a freeliving larval stage, what its requirements are. This will involve much straightforward observation, and I would like to suggest that, in this, there could be a significant contribution made by amateurs, just as they used to contribute in Old Testament, nineteenth century days. The enormous effiorescence of literature that has enveloped us in the last 30 years, and the utilisation of complicated and expensive equipment in solving anthecological problems, may have suggested to amateurs in many lands that they have no place in biological research today. This is most unfortunate, because there probably has never before been such a large population of biologically rather well-informed amateurs available - with leisure time on their hands. And some of them have skills that can be used to great advantage. For example, photography enthusiasts can try the effects of using different filters and films to provide images that will reveal how flowers actually appear to different kinds of flower visitors (see Kevan 1978). There are really instructive books available now. Thus Baastian Meeuse's delightful book (Meeuse 1%1) has raised the enthusiasm of many a reader for pollination study. And the success of Michael Proctor & Peter Yeo's (1973) book, written primarily for the educated Briton, is part of the success of the "New Naturalist" series of books that began in the 194Os. It shows that there are large numbers of potential amateur enthusiasts out there. They are as anxious as we are that the functioning of ecosystems should be understood before they are imperilled by destructive human intervention. Let us reach out to them! IfI may be irreverent again, I should say that we need missionary zeal!

REFERENCES ASHTON, P. S. 1977: A contribution of rainforest research to evolutionary theory. Annals of the Missouri Botanical Garden 64: 694-705. AYENSU, E. S. 1974: Plant and bat interactions in West Africa. Ibid. 61: 702-27. BAKER, H. G. 1956: Pollen dimorphism in the Rubiaceae. Evolution 10: 23-31. --1%5: Charles Darwin and the perennial flax - a controversy and its implications. Huntia 2: 141-61. --1973: Evolutionary relationships between flowering plants and animals in American and African tropical forests. pp. 145-59 In Meggers, B. J.; Ayensu, E. S.; Duckworth, W. D. (Eds) "Tropical Forest Ecosystems in Africa and South America: A Comparative Review". Smithsonian Institution Press, Washington. --1976: "Mistake" pollination as a reproductive system, with special reference to the Caricaceae. pp. 161-9 In Burley, J.; Styles, B. T. (Eds) "Tropical Trees: Variation, Breeding and Conservation". Academic Press, London. --1977: Non-sugar constituents of nectar. Apidologie 8: 349-56. --1978: Chemical aspects of the pollination of woody plants in the tropics. pp. 57--S2 In Tomlinson, P. B.; Zimmerman, M. (Eds) "Tropical Trees as Living Systems". Cambridge University Press, New York. BAKER, H. G.; BAKER, I. 1975: Studiesofnectar-constitution and pollinator-plant coevolution. pp. 100-40 In Gilbert, L. E.; Raven, P. H. (Eds) "Animal and Plant Coevolution". University of Texas Press, Austin. --1977: Intraspecific constancy of floral nectar amino acid complements. Botanical Gazette 138: 183-91. --1980: Sugar analyses of floral nectar and their significance. (In press). In Elias, T. S.; Bentley, B. L. (Eds) "The Biology of Nectaries". Columbia University Press, New York. BAKER, H. G.; CRUDEN, R. W.; BAKER, I. 1971: Minor parasitism in pollination biology and its community function. The case of Ceiba acuminata. BioScience 21: 1127-9.

CONCLUSION

I have only spoken this evening about some aspects of anthecology, and have said nothing at all about other areas of reproductive biology, but, of course, the contributions of embryogeny, embryology, and studies of seed-dispersal and seedling establishment are equally vitally important. In future symposia they should probably get more emphasis than they have here, so that more inclusive syntheses may be made. There is much to do before the New Testament of anthecology can be written, and even then we shall have to be working on the Newer New Testament - continuing indefinitely the evolution of our favourite subject. Thank you!

BAKER, H. G.; HARRIS, B. J. 1957: The pollination of Parkia by bats and its attendant evolutionary problems. Evolution II: 449-60. BAKER, H. G.; HURD, P. D. 1968: Intrafloral ecology. Annual Review of Entomology 13: 385-414. BAWA, K. 1974: Breeding systems of tree species of a lowland tropical community and their evolutionary significance. Evolution 28: 85-92. BONNIER, G. 1879: Les nectaires. Annales des sciences naturelles (Botanique) 8: 1-213. BUCHMANN, S. L. 1979: Vibratile ("buzz") pollination in angiosperms with poricidally dehiscent anthers. Ph.D. thesis (Entomology), University of California, Davis. BURCK, W. 1907: On the influence of the nectaries and other sugar containing tissues in the flower on the opening of the anthers. Recueil des travaux botaniques neerlandais 3: 163-72. --1909: On the biological significance of the secretion of nectar in the flower. Proceedings of the Section of Sciences, K. akademie van wetenschappen te Amsterdam 2: 445-9.

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Baker -

Banquet address

CAMERARIUS, R. J. 1694: "Epistola de Sexu Plantarum" (Transl.and ed. by Mobius, M. in 1899 and pub\. by W. Engelmann, Leipzig). CAMMERLOHER, H. 1931: "B1iitenbiologie" I. Borntrager, Berlin. CANDOLLE, A. P. DE 1832: "Physiologie Vegetale". Vol. II. Paris. CHEESEMAN, T. F. 1872. On the fertilisation of the New Zealand s~cies of Pterostylis (Orchideae). Transactions of the New Zealand Institute 5: 352-7. CLEMENTS, F. E.; LONG, F. L. 1923: "Experimental Pollination". Carnegie Institution, Washington. DARWIN, C. 1876: "The Effects of Cross and Self Fertilisation in the Vegetable Kingdom". John Murray, London. ---1877: "The Different Forms of Flowers on Plants of the Same Species". John Murray, London. DARWIN, E. 1800: "Phytologia, or the Philosophy of Agriculture and Gardening". J. Johnson, London. DAUMANN, E. 1932: Uber postflorale Nektarabscheidung. Beihe/te zum Botanischen Zentralbatt 49: 720-34. FAEGRI, K.; VAN DER PuL, L. 1966: "The Principles of Pollination Ecology". Pergamon Press, Oxford. FRANKIE, G. W.; BAKER, H. G.; OPLER, P. A. 1974: Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. Journal oJEcology 62: 881-919. FLEMING, T. H.; HEITHAUS, E. R.; SAWYER, W. B. 1977: An experimental analysis of the food location behavior offrugivorous bats. Ecology 58: 619-27. FRISCH, K. VON 1950: "Bees, their Vision, Chemical Senses and Language". Cornell University Press, Ithaca. GAUL, J. 1973: Topocentric and Ethodynamic pollination. pp. 85-100 In Brandtjes, N. B. M.; Linskens, H. F. (Eds) "Pollination and Dispersal". Department of Botany, University of Nijmegen, Nijmegen. GARTNER, C. F. VON 1844: "Beitrage zur Kentniss der Befruchtung". Stuttgart. -1849: "Versiiche iiber die Bastarderzeugung im Pflanzenreich". Stuttgart. GENTRY, A. H. 1974: Coevolutionary patterns in Central American Bignoniaceae. Annals oj the Missouri Botanical Garden 61: 728-59. GOULD, E. 1978: Foraging behavior of Malaysian nectarfeeding bats. Biotropica 10: 184-92. GRANT, V.; GRANT, K. A. 1965: "Flower Pollination in the Phlox Family". Columbia University Press, New York. GREW, N. 1682: "Anatomy of Plants". E. de Rawlins, London. HANDEL, S. N. 1976: Restricted pollen flow oftwo woodland herbs determined by neutron-activation analysis. Nature 260: 422-3. HEINRICH, B. 1975: Energetics of pollination. Annual Review oj Ecology and Systematics 6: 139-70. HEINRICH, B.; RAVEN, P. H. 1972: Energetics and pollination ecology. Science 176: 597-602. HEITHAUS, E. R. 1973: "Species diversity and resource partitioning in four neotropical plant-pollinator communities". Ph.D. thesis, Biology, Stanford University. -1974: On the role of plant-pollinator interactions in determining community structure. Annals oj the Missouri Botanical Garden 61: 675-91. 2

439 HEITHAUS, E. R.; FLEMING, T. H. 1978: Foraging movements of a frugivorous bat Carollia perspicillata (Phyllostomatidae). Ecological Monographs 48: 127-43. HEITHAUS, E. R.; OPLER, P. A.; BAKER, H. G. 1974: Bat activity and pollination of Bauhinia pauletia: plant pollinator coevolution. Ecology 55: 412-9. HENSLOW, G. 1876: Self-fertilisation of plants. Nature 14: 543-4. ---1891: "The Making of Flowers". Society for Promoting Christian Knowledge, London. HERBERT, W. 1837: "Amaryllidaceae, with a treatise on cross-bred vegetables". London. HILDEBRAND, F. H. G. 1867: "Die Geschlechtsverteilung bei den Pflanzen". W. Engelmann, Leipzig. HOWELL, D. J. 1978: Time sharing and body partitioning in bat-plant pollination systems. Nature 270: 509-10. JANZEN, D. H. 1971: Euglossine bees as long-distance pollinators of tropical plants. Science 171: 203-5. KAUR, A.; HA, C. 0.; JONG, K.; SANDS, V. E.; CHAN, H. T.; SOEPADMO, E.; ASHTON, P. S. 1978: Apomixis may be widespread among trees of the climax rain forest. Nature 271: 440-1. KERNER VON MARILAUN, A. 1878: "Flowers and their Unbidden Guests". Kegan Paul, London. KEVAN, P. G. 1978: Floral coloration, its colorimetric analysis and significance in anthecology. pp. 51-78. In Richards, A. J. (Ed.) "The Pollination of Flowers by Insects". Academic Press, London. KIRCHNER, O. VON 1911: "Blumen und Insekten". B. G. Teubner, Leipzig. KNIGHT, T. 1799: Experiments on the fecundation of vegetables. Philosophical Transactions oj the Royal Society (London) 89: 195-204. KNOLL, F. 1921: BombyliusJuliginosus und die Farbe der B1umen. Abhandlungen der Zoologisch-botanischen GesellschaJt in Wien 12: 17-119. KNUTH, P. 1898-1905: "Handbuch der Bliitenbiologie". 3 vols. W. Engelmann, Leipzig. ---1906-1909: "Handbook of Flower Pollination". Trans!. by J. A. Davis. 3 vols. (I, 1906; II, 1908; III, 1909). Clarendon Press, Oxford. KOLREUTER, J. G. 1761: "Vorlaufige Nachricht von einigen das Geschlecht der Pflanzen betreffenden Versuchen und Baobachtung". Leipzig. KRUNITZ, J. G. 1773: Oekonomisch Encyclopadie, vo!' IV. Quoted from Lorch (1978), q.v. LINHART, Y. B. 1973: Ecological and behavioral determinants of pollen dispersal in hummingbird-pollinated Heliconia. American Naturalist 107: 511-23. LINNAEUS, C. 1735: "Systema Naturae". Leyden. ---1751: "Philosophia Botanica". Stockholm. LOEW, E. 1895: "EinfUhrung in die B1iitenbiologie auf historischer Grundlage". F. Diimmler, Berlin. LORCH, J. 1978: On the discovery of nectaries and its relation to views on flowers and insects. Isis 69: 514-33. LOVELL, J. H. 1918: "The Flower and the Bee: Plant Life and Pollination". Scribner's, New York. MEEUSE, B.J. D. 1961: "The Story of Pollination". Ronald Press, New York. MOLDENKE, A. R. 1975: Niche specialization and species diversity along a California transect. Oecologia 21: 219-42.

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5.

SAZIMA, M.: SAZIMA, I. 1978: Bat pollination of the passion flower Passijlora mucronata. in southeastern Brazil. Ibid. 10: 100-8. SCHMID, R. 1975: Two hundred years of pollination biology: An overview. The Biologist 57: 26-35. SCHMID, R.: SCHMID, M. 1970: Knuth's often overlooked "Handbuch del' Bllitenbiologie", III. Band.

Emlogy 51: 357-8. SIMPSON, B. B.: NEFF, J. L.: SEIGLER, D. 1977: Krameria, free fatty acids and oil collecting bees. Nature 267: 150-1. SMITH, J. 1841: Notice of a plant which produces perfect seeds without any apparent action of pollen. Trans-

actions a/the Linnean Society. London 18: 509-12. SPRENGEL, C. K. 1793: "Das Entdeckte Geheimniss der Natur im Bau und in der Befruchtung der Blumen". Friedrich Vieweg, Berlin. START, A. N.; MARSHALL, A. G. 1976: Nectarivorous bats as pollinators of trees in West Malaysia. Pp. 141-50 In Burley, J.: Styles, B. T. (Eds) "Tropical Trees: Variation, Breeding and Conservation". Academic Press, London. STYLES, B. T. 1972: The flower biology of the Meliaceae and its bearing on tree breeding. Silvae Genetic-a

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