A Historical Perspective on Cycads from Antiquity to the Present
by Paolo De Luca

Abstract. DE LUCA. P. (Dipartimento di Biologia vegetale and Orto Botanico, Universita di Napoli, via Foria 223, 80139 Napoli, Italia). A historical perspective on cycads from antiquity to the present. Memoirs of the New York Botanical Garden 57: 1-7. 1990.—A brief survey of the history of cycads in various cultures is given beginning with the Etruscans. Their use in the religious practices of several cultures is also reviewed. The early exploration for cycads by naturalists and horticulturalists is discussed with particular reference to the discoveries and expeditions that led to the descriptions of the cycad genera. The historical aspects of the acquisitions of the more important large living collections in botanical gardens are outlined.

Key words: Cycads; living collections; exploration; cultural uses.
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Historical Survey

CLASSICAL TIMES AND PLACES

In Western classical literature cycads are not reported because these plants were extinct before man arrived in the Mediterranean and surrounding regions. Thus, cycads are not mentioned by Theophrastus, the Greek botanical student of Aristotle; nor by Dioscorides, the Greek botanist from Cilicia in the 1st century A.D.; nor by Pliny, the noted Roman botanist also of the 1st century A.D.

It is understandable that in Greek and Roman times African cycads were not known, because the most northern species of this group occur only to the south of the areas known at the time as "Hic sunt leones." However, it is strange that Asian species (viz., Cycas spp.), were not known, as most of them are distributed in the Indian sub-continent, which Alexander the Great had already arrived at, and from which, in the next century, were brought several exotic plants to Europe for the gardens of Patricians. Among these exotic Asians we should note citrus plants, of which a painting is still present in a Pompeian villa covered in the Vesuvian eruption of 79 A.D. and discovered at the end of the last century.

Some authors have recognized a plant de scribed by Theophrastus and named(xuxas), as a species of cycad referable to the genus Cycas. However, a particular passage from Theophrastus leads us to understand that this plant was an Ethiopian palm, probably Hyphaene thebaica ().
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EXTRA-EUROPEAN CULTURES

So, while the European people did not have contact with cycads, the same is not the case for people of other continents, where cycads are present. People from America, central and southern Africa, Asia, and Oceania have had a good knowledge of these plants and often used their seeds and/or stems to prepare a flour for bread making. Some natives of South Africa, for example, named a local species of cycad "bread tree."

But the interest of man for this plant has been often stimulated by their particularly primitive features and perhaps by the difference in appearance which they show, in contrast to the other plants amongst which they live.

In many localities. cycads have even acquired a sacred significance. Indian people, before con version to Christianity, used to decorate their temples with fronds of Cycas for festivals; this tradition continued after their conversion and Cycas became known as the "Church palm." The phenomenon of sacredness of cycads from non- Christian cultures is also present in Mexico, where Dioon fronds are still used to decorate churches, to the point that campesinos named Dioon "Pal ma de la Virgen."

The austere appearance of cycads is probably the reason for which these plants were considered the symbol of veneration of the dead in many parts of the world. People of Java used to plant Cycas around tombs. Dioon plants in Mexico, besides being the "Palma de la Virgen," are also known as "Palma de Dolores," because of their use at funerals. A species of this genus, Dioon merolae, was reported for the first time from plants cultivated near a funeral chapel in the state of Chiapas in southern Mexico (De Luca et al., 1981). An African Encephalartos, E. hidebrandtii var. dentatus, was found for the first time planted near the Muslim cemetery in Dares Salaam, Tanzania (Melville, 1957; Heenan, 1977).

In Europe, as we have already said, cycads are not present: even though we know of a case of interest by ancient Italian people in a group related to these plants, the Cycadeoidales. More than four thousand years ago, ancient Etruscans found a fossil trunk of a member of the Cycadeoidales, previously used by Neolithic people as a sharpening stone. Probably they understood that they had found something of interest, and they put this trunk in a tomb of the Marzabotto necropolis. This fossil, that has the longest known history of any fossil, is the specimen from which the species Cycadeoidea etrusca was established and is today in the Museo Cappelli in Bologna (Wieland, 1916).

The above, not strictly pertinent to the study of cycads, pertains rather to that series of ap proaches that man has made to plant study and represents the beginning of that scientific interest which became botany.
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BEGINNINGS OF MODERN KNOWLEDGE

The first new report of Cycadales to the Western world was of the genus Cycas, and was due to two Arabian naturalists of the 9th century who, upon returning from travels to India, referred to some plants of this genus as being utilized as a source of flour. Later, we have reports by Antonio Pigafetta and Fernao Lopez de Castanheda, in the 16th century, with further particulars by Francis Drake, who found Cycas plants in the Moluccas, where Indians used to eat the seeds. With regard to American cycads, certainly the first report in the West is that of Giovanni Lerio, whose report of his trip to Brazil in 1576 contains his observations of a plant named Ayrius, which certainly refers to the genus Zamia.

With the beginning of exploration of our world. many naturalist voyagers made notes in their diaries of news and paintings of various cycads which they came across. They introduced living plants to European botanical gardens and, for the first time, took care to collect dried specimens which they deposited in various herbaria, from that moment leaving material help for botanists who study the systematics of cycads. There are a notable number of explorers, but I would like to confine myself to explorers of the Americas.

The first of these were Humboldt and Bonpland. who collected valuable material in the course of their explorations in tropical America from 1799-1804. Later, Poeppig. in the 1830's, collected cycad samples in Peru and Bolivia.

Of particular interest is the work of Liebmann, a Danish naturalist explorer, who in 1840 collected material in Mexico which later was to be attributed to the new genera Dioon and Ceratozamia.

Karwinski, a Russian baron, explored Mexico for a long time in the first half of the last century and transported to the St. Petersburg (now Leningrad) Botanical Gardens live material on which a new species was later described.

At the same time, C. d'Orbigny explored, on behalf of the Paris Science Museum, in the Mato Grosso of Bolivia, collecting samples from which a new species was described.

Von Warsewicz, a Polish traveler, in the middle of the last century, explored Colombia and Central America, and Seemann, an English traveler of the same period, explored the Choco in Colombia, both finding new species of cycads.

In the second half of the last century Roezl and Wallis traveled to South America, finding new species of cycads described later by botanists, who named two of these species after the two discoverers.

All these naturalist travelers increased the collected material of both botanical gardens and private collections, as seen in the very long list published by Wendland (1854).
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EARLY PRIVATE COLLECTIONS

Among the private collections, we note that of James Yates in England. An amateur botanist, he had a deep knowledge of cycads, and had continuous scientific relationships with the botanists of the time. His herbarium material was donated to the British Museum in London.

Numerous other amateur students of cycads, at great personal sacrifice, built up very important living collections. To many of them we owe our thanks, because they donated their collections to botanical gardens, offering researchers precious study material.

While not wishing to present another list, I must mention Garbari, a physician in Trento in North Italy, whose cycad collection was donated to the botanical garden of Florence in 1907. Nor can I omit to mention Professor Luigi Califano, an internationally famous pathologist and a large scale collector and scholar of cycads, who bequeathed his collection, upon his death in 1976, to the Naples Botanical Garden.
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Scientific History of Cycads

DESCRIPTIONS OF NEW GENERA

It is now opportune to move to the scientific history of cycads. The first botanical description of a plant belonging to the order Cycadales is that of the pre-Linnean botanist Rheede Tot Draakestein, who described a cycad by the name of Todda panna in 1682. Linneaus, in 1753, us ing the illustrations of this botanist, named the genus Cycas, the first cycad genus of modern botany. Linneaus probably thought that the plant described by Rheede and classified by him was the same one described by Theophrastus as(xuxas). On the basis of this erroneous interpretation, he named the genus, Cycas, a Latinization of the word used by Theophrastus.

The second genus of cycads described by bot anists is American. Again Linneaus described it, in 1763, and called it Zamia. The origin of this name is obscure and its derivation from the writ ings of Pliny, as claimed by Schuster (1932), is erroneous.

The third genus described (by Lehmann. 1834) is African, with the name Encephalartos. As stat ed above, the natives produced flour from the seeds of the strobili which are at the top of the trunk of this plant. Lehmann formed the genus name from the Greek words en-cephali-artos () which mean bread on the head.

In 1842, Miquel described the first Australian genus, which he called Macrozamia, by adding the prefix macro (large) to Linneaus' name Zamia. The following year Lindley described a new North American genus which he named Dioon from the two Greek words(dis) and(oon), which loosely means twice ovulate with reference to the two seeds on each megasporophyll. In 1846, Brongniart described a new North American genus which he named Ceratozamia, again by pre fixing to the name Zamia a word,(xeras = horn), to note the presence of two small horns on the sporophylls.

In 1853, Moore described a small South African genus which he named Stangeria in honor of Dr. Stanger, general superintendent of Natal, who in 1851 had sent the plant to him in England from Port Natal. The genus Stangeria was originally attributed by Kunze to the fern genus Lomaria and only later, with Moore's description of the strobili, was it correctly attributed to the Cycadales.

In 1857, Regel described a new Australian genus to which he gave the name Lepidozamia, by prefixing to the name Zamia the Greek name(lepis = scale), because the leaf scars on the trunk of this plant resemble the scales of a snake.

Later, in 1863, Joseph Hooker described a new Australian genus, Bowenia, in honor of Sir George F. Bowen, a botanist and the first governor of Queensland.

De Candolle (1868) described the genus Microcycas, a Cuban endemic, by adding the word micro (= small) to the name Cycas, although this is certainly a misnomer, because Microcycas is often larger in size than Cycas.

As exploration for new cycads continues to day, it perhaps is not surprising that recently Dennis Stevenson and Knut Norstog have discovered a new and very locally endemic genus in Northern South America, which is described in this volume. This genus, named Chigua after the name for cycads used by the indigenous people of this region, is the only cycad genus endemic to South America.

Above, in my description of the eleven genera of Cycadales, while it was superfluous to mention the new species attributed to known genera. I cannot forbear mentioning that many botanists have described new species on the basis of a single herbarium specimen or a single living plant, without a sound knowledge of previously de scribed species. Consequently, several species al ready described were re-described as new, and this has led to great confusion in the systematics and nomenclature of the Cycadales.
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SYSTEMATIC REVISIONS

Of great help in rectifying this inconvenience were the large systematic revisions of the order, the first by Miquel, the Dutch botanist mentioned earlier. His first major cycad work, pub lished in 1842, is exemplary for its scientific rigor and quantity of information. In 1861, Miquel published the Prodromus Systematis Cycadea rum and, in 1868 and 1870, "Nouveaux materiaux pour servir a la connaissance des Cyca dees," a work in which he reported everything then known on the biology and systematics of these plants.

Of equal importance is the "Cycadearum generum specierumque revisio" by Regel (1876), a work done with an acute systematic sense, the crowning glory of the research activity of that Russian botanist.

Another excellent monograph on cycads was published by de Candolle (his Prodromus Sys tematis Cycadearum of 1868). Also important is the 1884 monograph of American cycads published by Thiselton-Dyer, then Director of Kew Gardens, in "Biologia centrali-americana."

Among others who have worked in the present century, of particularly important relevance was C. J. Chamberlain, noted American botanist, both for the quantity of data and the novelty of his approach to the study of cycads. He was the first to understand the importance of field studies with the purpose of evaluating the extreme morphological variability in the distinctive characters of these plants during the course of their life; and therefore, he traveled for 15 years in America, Africa, and Australia to observe cycads in their habitat. In 1919, he published The living cycads, a flowing volume, rich in data, still current for its synthesis of the taxonomy, morphology, and reproductive biology of these plants, containing most of the data from his original research.

In 1932, the German paleobotanist Schuster published the volume "Cycadaceae" as part of the important work Des Pflanzenreich edited by Engler. This monograph was intended to be a complete synthesis of what was known up to that time and is valuable for the richness of the bibliographic citations. Unfortunately, Schuster had no familiarity with living cycads, consulted few herbaria (among them Berlin, later destroyed in the Second World War), and was superficial with regards to nomenclature. Moreover, he did not understand the nomenclatural type concept in the modern sense and never annotated the specimens cited as types in his work, creating great confusion and instability in the nomenclature of cycads. All these deficiencies constrain and con found the contemporary botanist, complicating nomenclatural revisions.

At the beginning of the 1940's, Chamberlain wrote an excellent monographic work on Cycadales in which he reported the mistakes and con fusions of all earlier studies of this group. For example, he strongly criticizes the practice of de scribing new species from a single herbarium specimen or living plant of dubious origin with out understanding the great variability of these plants during their life cycle. Unfortunately, this work was never published, probably due to his death. and thus botanists could not use this fundamental contribution to the knowledge of cy cads. Copies of the Chamberlain manuscript are stored at the Fairchild Tropical Garden of Miami, the New York Botanical Garden, and the Botanical Garden of Naples. From his writings, it is possible to see the very high number of correct intuitions by Chamberlain.

In the last decade there has been a growing interest in the biosystematics, chemosystematics, comparative morphology, ecology, physiology, karyology, and reproductive biology of Cycadales, as reported in this volume on the present state of research in these fields by the most qualified researchers in the world. It is not possible to discuss them all individually, but I must mention Professor Knut Norstog, the leader in the study of the reproductive biology of this group.
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LIVING COLLECTIONS IN BOTANICAL GARDENS

All the research reported in this volume could only take place thanks to the existence of collections of cycads in botanical gardens. In the field, these plants are distributed in areas very distant from one another, and often they are found in areas of difficult access. Only in botanical gardens is it possible to obtain an overall view and have access to the material to undertake comparative research among families and genera.

As an example, let me relate the history of the cycad collection of the Naples Botanical Garden, with which I have some familiarity. The Botanical Garden of Naples has a priceless collection of Cycadales, notable for both the number of specimens and the number of species. All ten known genera are represented. This collection was started in 1809, two years after the foundation of the Botanical Garden, with the acquisition of a specimen Encephalartos altensteinii. In that year, a Neapolitan noble (and plant collector), gave to the Botanical Garden a specimen of this species started at the end of the 18th century from seed collected in the wild. This plant, still present in the collection today, became re productive for the first time in 1864 and formed two magnificent male cones.

This first donation was followed by a second, in 1813, given by the queen of Naples, Maria Carolina Bonaparte, the wife of King Giacchino Murat. She imported from Japan two large specimens of Cycas revoluta and gave one to the Naples Botanical Garden; this plant lived until 1905. The following years saw new acquisitions, but they were not recorded.

Michele Tenore's 1845 catalogue of plants cultivated in the botanical garden shows that, at that time, there were grown outside specimens of Cycadales belonging to three genera (Cycas, Encephalartos, and Zamia), with a total of nine species.

In the 1867 catalogue of the "Royal Botanical Garden" of Naples, prepared by Giuseppe Antonio Pasquale, the list of cycads was brought up to date. It included a specimen of Dioon edule. There is no further mention of the collection for about fifty years.

In 1913, Fridiano Cavara in a note of the Roy al Botanical Garden writes: "in (cultivation) in open ground are specimens of Cycadales, including Dioon edule, Cycas revoluta, Encephalartos altensteinii, E. horridus, Zarnia muricata...." These plants were grown outside and during the winters they were protected by simple reed-matting. They were transplanted from the open ground into pots a little after 1929.

In 1934, the collection was enlarged with a pseudobulb of a male Cycas revoluta from the Botanical Garden of Pisa, in Central Italy, which periodically produced fertile pollen, used for pollination and production of seeds.

In 1966, the Cycadales were exhibited in the area occupied by Gymnosperms and at this time an inventory listed the following specimens: Ceratozamnia mexicana male and female, Cycas circinalis female, C. revoluta male and female, Dioon edule female, Encephalartos altensteinii male, E. horridus male, E. longifolius female and Macrozamia communis.

At the end of the 1960's interest in the Cycadales underwent a notable expansion and the collection was notably increased, with the idea of protecting. conserving, multiplying and spreading these plants. The Naples Botanical Garden has been a leader in this cultural operation. Our collection has increased in three different ways: acquisition of specimens, donations and field collections.

Between 1966 and the present day, we have acquired from South Africa 193 specimens of 32 species of Encephalartos and 15 specimens of Stangeria eriopus collected from their original localities. From 1974 to the present day, we have acquired from Australia 83 specimens of all the known species of Macrozamia, 25 specimens of the two species of Bowenia, 12 specimens of the two species of Lepidozamia and also 50 specimens of the nine species of Australian Cycas. We also acquired cultivated specimens of unknown origin. From 1966 to the present day in this manner, we have obtained 34 specimens belonging to the genera Cvcas, Dioon, Encephalartos, and Macrozamia.

The collection of Cycadales of the Botanical Garden has also notably increased thanks to do nations from private collections and scientific institutions.

In 1973, a Catholic missionary sent two specimens of Encephalartos laurentianus collected in the wild on the border of Zaire and Angola. In 1974, the Singapore Botanical Garden donated plants of Cycas rumphii. In 1976, Professor Muniz of the Havana Botanical Garden (Cuba) visited Naples, bringing as a gift a magnificent specimen of Microcycas calocoma.

On the 14th of January 1976, the death of the earlier mentioned Professor Luigi Califano occurred. His family, respecting the wishes of the deceased, gave to the Botanical Garden his entire collection of plants, which consisted of a precious and useful group of Cycadales. In this way we had the honor and the fortune to inherit 102 specimens of 59 species belonging to 8 genera.

In 1977 and 1978 Professor Viviani of the Botanical Garden of Puerto Rico sent specimens of Zamia latifoliolata, Z. media, Z. portoricensis, and Z. pumila.

In the years 1978-1980, our collection was enriched by some specimens of Ceratozamia. Stangeria, and Macrozamia donated by the estate of Professor Angelo Verga, a lawyer by profession and an enlightened collector of plants. The donations from Professor Verga included a priceless specimen of Encephalartos woodii. Two specimens of Cycas thouarsii, collected in Madagascar, were donated by him in 1980 and 1981.

The collection has been enriched with inter esting specimens by exchange with the Fairchild Tropical Garden in Miami. From 1980 to this day Fairchild Tropical Garden has sent specimens of Zamia floridana, Z. chiqua, Z. manicata, Z. pseudoparasitica and Microcycas calo coma.

From 1969 onwards, there was a notable growth of the collection thanks to a number of botanical expeditions. The first expeditions took place in 1969, 1971, and 1974 and were organized on behalf of the Accademia Nazionale dei Lincei by Professors Luigi Califano, Aldo Merola (the late director of the Naples Botanical Garden) and Ruggero Tomaselli (the late director of the Botanical Garden of Pavia). Professor Sergio Sa bato and myself also participated in these expeditions.

In the course of these botanical expeditions we collected numerous specimens of Dioon edule, D. mejiae, D. spinulosum and specimens of an unknown species of Dioon, numerous species of Zamia and Ceratozamia, as well as seeds of many species.

In 1975, on a research trip in the east with Professor Aldo Merola, I collected specimens of Cycas rumphii in Indonesia and C. siamensis in Thailand.

From 1980 to the present day, there have been seven botanical expeditions to Latin America. These expeditions, led by Professor Sergio Sabato with the help of Professors Aldo Moretti and Gesualdo Siniscalco Gigliano of the Department of Plant Biology in Naples, led to the acquisition of numerous specimens of Dioon, Ceratozamia, and Zamia. Most of these expeditions were made in collaboration with Profes sors Mario Vazquez Torres, Dennis Wm. Stevenson, and Knut Norstog. This material has been used for phytochemical, systematic, embryological and other studies. In this regard I would like to mention our contribution to the knowledge of the systematics of the genus Dioon. On the basis of the specimens collected in the wild and cultivated in the botanical garden, six new species and one new variety were described, adding to the four species known in 1980.

The collection at the Botanical Garden of the University of Naples is, therefore, one of the most important in the world today, consisting of 570 adult specimens and numerous seedlings be longing to 111 species of all 10 known genera. Of these specimens, 95% are classified with certainty and about 80% are of known collection locality.

This collection is of notable scientific importance, not only for the number of specimens, but because of the number of species and genera rep resented and for the presence of the frequently reproductive male and female specimens. Other important living collections for both scientific and conservation purposes are to be found at Kew Gardens; Fairchild Tropical Garden, which has the most extensive collection of cycads with respect to both the number of plants and number of taxa; New York Botanical Garden; Hortus Amsterdam; and Leiden Botanical Garden. The latter two are notable because they have living plants which are the types of many of the species described by Miquel in his 36 years of work on cycad systematics.

To conclude my introduction, I hope that this volume will lead to further scientific meetings on cycads with the aim of the exchange and comparison of both ideas and plant material. Such living material is invaluable for studies on each field of cycad research.

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