Floral design is an art form like any other. It takes into account a full range of artistic principles, where compositions are thought of in terms of balance, proportion, harmony, and even rhythm. Color, texture, lines and space are all aspects one can contemplate when viewing or creating an arrangement, and like all art, personal taste and school of thought determine its success.

Instead of starting our journey into floral design with the Europeans or the Japanese, we will begin with an interesting, and perhaps unexpected, cast of characters – the ancient “fern allies”. To meet them, we have to go back in time, back to before flowering plants even existed, to the Carboniferous period.

The Carboniferous period was the geological time on Earth that spanned from roughly 360 million years ago to 300 million years ago.  Great spore-bearing forests dominated the forming super-continent Pangaea during this time that, as the name carboniferous suggests, would eventually become great coal fields. Land animals were limited to amphibians, reptiles, and predatory and sap sucking insects[33-35].

Ferns, horsetails, and club mosses were  probably the most familiar flora of the Carboniferous period, although some took on a  larger stature.  Calamites, an extinct cousin of our modern Equisetum, were tree-like horsetails reaching 30 meters tall.

Lepidodendrons, an extinct cousin of our club moss Lycopodium, were no ‘ground pines’, but were towering scale trees, stretching  30 meters above ground with trunks a meter wide.

The late Carboniferous period also saw the rise of the gymnosperms (think conifers).  Gymnosperms differed from much of the plant life of the earlier Carboniferous period in that they produced seeds instead of spores.  Unlike the angiosperms (the flowering plants) that also produce seeds, gymnosperm seeds are “naked” (gymnospermosis “naked seeds” in Greek), meaning that they are not produced within an ovary but instead on the surface of an ovule-bearing scale.  Ovaries (fruit) and flowers come a little later in our story.  It was also this time period that saw the first beetles appear[33-35].

At the end of the Carboniferous period, the Glossopteridales appear in the fossil record. As far back as 299 million years ago, at the start of the Permian period, we find Glossopterids all over what is now the Southern Hemisphere. Originally placed with the ferns, Glossopteris had no spores, and was in fact a seed-bearing gymnosperm. What makes the Glossopterids special from the gymnosperms of the Carboniferous period, is that they had modified leaves that resembled a carpel, the seed producing organ in flowering plants. While not true carpels, the fused leaf structure perhaps provided the forming seed protection against the new beetle threat.  Glossopteris was not flowering, and while it may be an evolutionarily distant cousin of flowering plants, it was no angiosperm “Eve”, despite a passing resemblance[5][7][33-35].

As far back as 280 million years ago, in the Permian period, time of Pangaea and the ancestors of the dinosaurs, something interesting appeared in the fossil record, not flowers but an organic compound called oleanane[16].

The gigantopterids were a family of Permian period plants whose origin is still a little unclear. What makes them of particular importance though, is that unlike the other seed producing plants of the time, the fossil record indicates that they contained oleanane. Oleanane is special because it is produced by many flowering plants today to help protect from fungal and insect invaders, but it doesn’t commonly exist outside of angiosperms[15]. Were gigantopterids the ancestors of flowering plants? Unfortunately, we don’t know, because they disappear from the fossil record after the Permian–Triassic extinction(252.28 million years ago), but that doesn’t mean they vanished, they could have just adapted to the post new, post extinction, conditions on Earth[5][7].

In the Permian period, we see many rather familiar forms, but no flowers.  The Gnetophytes were another early division of Plantae, now considered to be gymnosperms, that possessed angiosperm-like xylem (water-nutrient transport tissue) very similar to that found in modern flowering plants.  Gnetophyta still exists today, including modern members like the well known Ephedra genus, but genetic testing shows that Gnetophytes are not close kin to flowering plants[18][19][20].

Whether the direct ancestors of angiosperms appeared during the Permian period is still debated, but things were clearly moving in that direction.  As the climate and animal life of the Earth changed, new niches needed to be filled and new methods of protecting, and creating, offspring needed to be established.

At the start of the Mesozoic era, the period from 250 to 70 million years ago, we meet another possible angiosperm ancestor, a gymnospermic order known as the Caytoniales. Fossils of Caytoniales show that they contained a modified leaf cupule- cupules are the protective casing around the seeds of some angiosperms, like oaks. This interesting angiosperm characteristic isn’t enough to remove the Caytoniales from the gymnosperms,  but the seeds were not as ‘naked‘ as the other gymnosperms. While not a ‘flowering plant’, the emergence of Caytoniales suggest that flowering plant traits could have been beneficial in light of the changing Earth (a protected seed has a better chance of survival once seed eaters come along)[7].

The bennettitales, another early Mesozoic gymnosperm, possessed the most flower-like form yet, with their reproductive organs surrounded by bracts (almost like a bromeliad). While genetically, the bennettitales are more closely related to the cycads than the angiosperms, they, like the Gigantopteridales, contained oleanane, which hints at an evolutionary link to flowers.  Protecting seeds was clearly becoming more and more important[5][7][17].

The first dinosaurs and the earliest mammals shared the Earth with these flower-like bennettitales. 220 million years ago saw enormous gymnosperm forests dominate the land, a move away from the spore-bearing forests of the Carboniferous period.  The Earth was warmer and far more rich in carbon dioxide than both present day and  the Carboniferous climate, which was perfect for the changing flora and large herbivores[33-35].

It wasn’t until 140 million years ago, during the Cretaceous period, that the fossil record definitively shows ‘flowers’. The Cretaceous period was a time of warm air, high seas, dinosaurs, mammals, bees and angiosperms.

Typically, three early angiosperm families stand out, they are thus labelled the ‘basal angiosperms’ because as far as we know, they were the first. What is exciting is that all three basal angiosperm families still have members that are alive today[25][26].

There is only one species from Amorella still alive today, Amborella trichopoda. A. trichopoda is a rare, understory, evergreen tree, found only on the Pacific island of New Caledonia.  The urbanization of New Caledonia is threatening the home of the last Amborella. Green houses and botanical gardens may be the only way for future generations to see this ‘dinosaur flower’.

The Nymphaeales are a well known order of flowering plants because they contain the water lilies (the Nymphaeaceae family).  In total, there are three living families within the Nymphaeales order, and perhaps 80 extant species total.

The Austrobaileyales order contains possibly three families of woody plants, and perhaps 100 species in all. There is still much debate on the identities of some members here.  The most well known Austrobaileyales is Illicium verum, the plant we get the spice ‘star anise‘ from.

Next came the mesangiosperms.  Shortly after the basal angiosperms appeared in the fossil record, another large grouping of flowering plants diverged, roughly 135 million years ago.  Today, the mesangiosperms make up roughly 99.95% of all flowering plants – that’s around 350,000 known species.

The Magnoliids are currently a group of approximately 9000 extant flowering plants.  The magnoliids contain the well known order Magnoliales (with the Magnolia genus, of course), the familiar order Laurales – with its culinary members like Bay Laurel (Laurus nobilis), cinnamon (the Cinnamomum genus), and Persea americana (Avacado)-, the order Piperales (think Piper nigrum, otherwise known as Black Pepper), and the order Canellales. Fossil record of their distinctive pollen particles – with only one pore – indicate the Magnoliids were around 130 million years ago[5][7][8].

Chloranthaceae is another one of the early angiosperm orders from 120 million years ago with one living family today.  The flowers are without petals and sometimes even without sepals.  There are four extant genera with roughly 75 species between them[5][7].

The monocots contain approximately 60,000 distinct species alive today.  When people think about flowers in cultivation, especially in regards to floral design, they often think of monocots. Amaryllis, bromeliads, daffodils, irises, lilies,  orchids (orchids make up more than one third of all monocots), and tulips are all monocots, and so are corn, wheat, palm trees, rice, and sugar cane.  The earliest fossil monocots seem to appear roughly 120 million years ago in the early Cretaceous period[23].

125 million years ago, we meet Archaefructus liaoningensis, another one of the earliest known flowering plants. Three extinct species within the now lost Archaefrutus genus have been discovered although where this genus should be placed in our above tree is a bit of a mystery still. It has been proposed that Archaefructaceae should be a fourth basal angiosperm order, although this isn’t widely supported. Some suggest that Archaefructus  could actually be a member of the Nymphaeales, or perhaps a basal eudicot[28].

Eudicots are a well known modern collection of flowering plants that are dicots, meanings their seeds typically contain two embryonic leaves (separating them from monocots, that have one embryonic leaf). Now, the Eudicots, Magnoliids, Amborella, Nymphaeales, Austrobaileyales, Chloranthales, and Ceratophyllum are all dicots, but the eudicots are distinguished by having three parallel groves along their pollen grains that run along the polar axis of the pollen (plus, they’re seen to be far more genetically related to each other than to any of the other basal angiosperms). Eudicots may make up to 70% of all flowering plants, from Taraxacum (dandelions) to Acer (maple trees).

122.6–125.8 million years ago we meet Leefructus, a basal eudicot.

The diversity of angiosperm fossils we find from 130 to 120 million years ago tells us something important – flowering plants had probably been there for awhile, we just haven’t found older fossils yet.  There are many factors that affect whether fossilization can occur instead of say, compost. Leaves and flowers have to die in exactly the right spot, under exactly the right conditions for them to leave an imprint behind that will be able to last hundreds of millions of years. The variety of early angiosperms we see in the Cretaceous period makes us suspect a longer history of angiosperms than we have yet to uncover [1].

The Ceratophyllales are an interesting, and unassuming, early order of aquatic angiosperm, most commonly known as hornworts.  They were first found in the fossil record roughly 120 to 100 million years ago.  Today, there is only one genera of Ceratophyllales with perhaps 30 species that can be seen all over the world.  The fact that they actually are flowering plants, can take one by surprise, but flowers and fruit of the Ceratophyte Donlesia dakotensis have been found in sediment from the early Cretaceous period[22].

The Cretaceous period also saw the rise of pollinators. Perhaps unsurprisingly, pollinators and flowers evolved together, giving angiosperms the edge they needed over other plant life. Giving credit where credit is due, when in comes to floral design, is a bit of a tricky task. Do we credit the plants themselves for their variation in floral arrangement and inflorescence displays? Or do we credit the pollinators involved in exerting the selective pressure with creating that variation?

Plants that are wind pollinated have to expend much more energy than plants that are animal pollinated, because they have to produce more pollen (or spores) in a hope that it will end up at an appropriate receptacle.

Early insects discovered this pollen to be a good source of food and slowly over time became dependent on it, carrying pollen from flower to flower as they fed. Eventually, mutations arose that caused the creation of nectar, which lured pollinators all the more. Bright colors and shaped petals developed and were even more eye-catching for insects. Those without a protected ovule (ie. anyone with a ‘naked seed’) could be eaten by visiting pollinators, and were less likely to survive as a species. This is how the angiosperm became so successful.

Plants developed more specialized flowers as insects developed more specialized forms, as it was beneficial for both parties to be ‘monogamous’, so to speak. For the pollinator, having a food source that you and you alone can eat means less competition, and a greater chance of survival. For the plant, having a dedicated pollinator means less wasted pollen on casual passersby and if your pollinator is dependent on you, you’ll have a much better chance of being visited and pollinated [6].

65 million years ago, the Cretaceous–Paleogene extinction occurred, and roughly half of all animal species were wiped out.  Dinosaurs disappeared, leaving only a few bird ancestors behind, and mammals rapidly filled the void on land.  65 to 35  million years ago, we also find bees and butterflies in the fossil record, and we find flowers fit for a bouquet, as angiosperms replaced gymnosperms as the most plentiful and more diverse terrestrial plant life.

Here is a sampling of the Paleogene (65.5 ± 0.3 to 23.03 ± 0.05 million years ago) angiosperm fossil record:

The Earth’s climate changed significantly over the course of the Paleogene.  The world was less tropical than it had been during the Cretaceous period – deciduous plants and the newly evolved grasses became better competitors than the old tropical forest dwellers now that seasonal climate variation was more significant.   Separating continents, cooler temperatures, dryer weather, and new pollinators put pressure on plants to change.

An important example of pollination leading floral design is the yucca plant (example: Yucca whipplei) and its exclusive pollinator, the yucca moth (example: Tegeticula maculata).  Yuccas began to flourish roughly 40 million years ago with the Yucca moths appearing soon afterwards.  Today, Yucca moths generally only visit one species of yucca with a flower specifically aligned with their needs.  The moths arrive at sheltered flowers for a snack and to lay their eggs, while getting pollen on themselves in the process, before moving on to a new flower.  The flowers must be shaped in such a way to allow the eggs to stay safe, and allow the yucca moth to become covered in pollen during their visit. When the eggs hatch, the larvae feed on the Yucca seeds, but leave enough untouched so that the some seeds still mature.  Despite the somewhat parasitic actions of the Yucca moth, the relationship still ends up being beneficial for both parties[13].

Hummingbirds and the flowers they feed on are another classical example of coevolution. The first hummingbird fossils are 30 million years old[33-35], which is likely when bird pollination became an important force in floral design. Elongated nectar cavities, shades of red, and sucrose (instead of the typical fructose and glucose) concentrated nectar make certain flowers more appealing to  birds rather than to insects. As flowers diversified, beaks slowly adapted to find their lowest competition niche.  Bloom time of certain bird-pollinated flowers even lines up with specific hummingbird mating seasons. Hummingbirds aren’t the only bird pollinator though, and flowers have adapted to meet the needs of others. More than just colour and shape, recent research (on the cover of this June’s issue of the American Journal of Botany no less) suggests that certain flowers, Babiana ringens above, developed a special perch, to make visits from their prime pollinator easier.  By developing flowers lower to the ground, damage from mammalian herbivores is decreased, but birds may have a harder time stopping for nectar.  The modified, flowerless inflorescence axis that Babiana ringens  has developed compensates for the lower blooms, but creating a perfectly placed perch for their Malachite sunbird pollinator[3].  Brightly coloured, floral scented, eye-catchingly shaped flowers evolved for, and in some cases with, pollinators. A successful floral design for a sunbird is one that catches the eye and is easy to stop and have drink from – not exactly what one aims for with Ikebana arrangements.

In May of 1862, Charles Darwin published a book called “On the various contrivances by which British and foreign orchids are fertilised by insects, and on the good effects of intercrossing“, known more concisely as Darwin’s “Fertilisation of Orchids“[27].  In it, he discussed the evolutionary connection between plants and the insects that fertilized them while setting up a discussion of natural selection.   Many scientists, especially botanists, actually consider this to be Darwin’s most significant work, as it emphasized the importance of pollinators and cross-pollination for plants, which wasn’t fully appreciated at the time.

After detailed study of many distinctly moth pollinated orchids, Darwin came across Angraecum sesquipedale.  The shape of the spur (the elongated spike where nectar would be sucked from during pollen collection) told Darwin that A. sesquipedale would need to be pollinated by a moth with a 20 to 35 cm long proboscis. At the time of this assessment, no such moth was known to exist.  Everything Darwin had seen up until that point suggested that orchids and pollinators must have evolved together, to be a unique fit, so it wasn’t that A. sesquipedaledidn’t fit the pattern, it was that the pattern predicted the existence of a moth, with a 35 cm long proboscis, that had yet to be seen.

In 1903, the sphinx moth Xanthopan morgani  was discovered, absurdly long proboscis and all, and has been seen feeding from the orchids.

Orchids and moths are a must in any conversation on coevolution, although moths are not the only orchid pollinator.  Meliorchis caribea was a Miocene orchid, alive at least 20 to 15 million years ago. While Meliorchis is extinct, it appears to be a close relative of the modern orchid genus Ligeophila.  We know about Meliorchis caribea because scientists have found the above preserved bee, Proplebeia dominicana, seen on a 2007 cover of Nature, covered in orchid pollen[2].  Fossils like the above provide an exciting and rare window into the lives of extinct plants and animals.

An interesting study last month in the Proceedings of the Royal Society B [10] looked at flowering plants in Australia and their pollinators.  It’s not new knowledge that flower colour and shape are lures for bees[11][12], but how that relationship came about hasn’t always been well understood. Looking at the colour spectrum of 111 Australian native flowers and comparing that data to the visual abilities of a variety of important pollinators, the scientists noticed that flower colours were predominately those viewed best by bees, as opposed to butterflies or birds.  This is important because it’s believed that the visual system of hymenoptera (bees) predates angiosperms.  This means that bees and flower colouring didn’t evolve together, but that flowers independently evolved to be optimally viewed by bees.  North American flower colours align with the Australian results[10].

10 million years ago, the grasslands were well established and insects were diverse and numerous. Not long after, the first hominids (the great apes, like us) are found in the fossil record. Millions of years go by, and it’s not until 200,000 years ago that we find anatomically modern humans.

The earliest possible evidence for flowers being used for ceremonial or esthetic purposes comes not from humans, but from a related hominid, the Neanderthals. There is a burial site known as the Shanidar Cave, in the Kurdistan Region of Iraq, dating back 80,000 to 60,000 years ago. A site known as Shanidar 4, also called the “flower burial” contained an unusual amount of pollen, that some speculate is evidence of flowers being used as part of a ceremonial burial. Some speculate that non-hominid animals buried plant matter there for storage and that there was no ceremony intended, but at this point in time, we can’t know one way or the other.[24].

Angiosperms have been an important food source for animals as long as there have been angiosperms, but it has only been recently, relatively speaking, that they have been actively cultivated for these purposes. More than 12,500 years ago, humans were selecting grains, like rye, for larger seeds and better yields[36]. When the esthetic history of floral cultivation began is a little less clear.

The ancient Egyptians used images of flowers, with particular attention to the water lily, in all manners of artistry and story telling creations. Egyptian art shows evidence of formal gardens around important sites. Even a 3000 year old burial  in the Valley of the Kings had garlands of preserved flowers, strung together with gold, left behind as relics. While flowers had not been cultivated, at least by today’s standards, formal arrangements and bouquets were assembled from poppy, cornflower, water lily, and papyrus[30].

The earliest record of formal Chinese gardens appear during the Shang Dynasty(1600-1046 BCE). Gardens were created to not only house fruits and vegetables, but also birds and animals, some of which were hunted for sport by nobles.  It is possible that the cultivation of roses began in China as far back as 5000 years ago[31].

Possibly created by the Neo-Babylonian king, Nebuchadnezzar II, between 605 and 562 BCE, the Hanging Gardens of Babylon was a wonder of the ancient world. Interestingly, there is debate  over whether these gardens actually existed, as despite mention of them appearing in the writings of a great many ancient scholars, they were not written about by the Babylonians themselves, nor has any archeological evidence ever been unearthed to suggest their construction. Whether they were real gardens or poetic fantasy, at least the concept of a formal garden existed and flowers appeared symbolically and esthetically in art from the period.

Religion for the ancient Greeks was centred around colourful characters who personified natural phenomena. Above we see Eros, the god of love, as a creation of the famous Greek potter Kachrylion, holding a flower as a ‘gift of love’. While there were no private gardens in ancient Greece, gardens were planted around temples and floral imagery used heavily in art.

Flowers were an important design element in many early mosaics. Above, we see a portion of a design from the Villa del Ramalete, an ancient Roman site, located in what is now Navarre, Spain. The Roman empire, from 100 BCE – 500 CE was very interested in horticulture and botany, more so than the earlier Greeks.  There is evidence to suggest Romans cultivated roses[31], shaped topiary, and shared their best seeds.  The ruins of Pompeii even showed that gardens were not just for the wealthy or elite, but something that average Romans had in whatever space around their home was available.  Paintings from Pompeii  show that window box gardens and potted plants were used by would-be-gardeners whose space was in short supply[29] (some of us might be able to relate).

Here we see a close up of a mosaic from from the palace of Shapur I the Great, the king of the Second Persian Empire ( from 240 to  270 CE).  The Persians have a long history with gardens, especially formal gardens.  The great Pasargad Persian Garden was built in 500 BCE, although it has been suggested that Persian gardens existed as far back as 4000 BCE.  One of the most iconic styles of Persian gardens was the Charbagh, which originated during the first Persian Empire, at the time that the Pasargad Garden was built.   Overall geometric form was emphasized more than floral cultivation[32].

Images of flowers appear throughout modern human history – like our incredibly distant pollinating cousins, something about flowers draws our eye.

The modern floral trade took off in Europe in the 1500s after tulips arrived in Vienna from the Ottoman Empire in 1554.  This lead to the famous Tulip Mania during the Dutch Golden Age and the first economic ‘bubble’ to burst.  Despite the hardships to the Dutch floral trade in the 1600s, the Netherlands remains one of the most productive centres for the floral market to this day.

Instead of relying on pressure from pollinators, predators, and the weather, we now select for larger blooms and brighter colours artificially. Mutations that might not have survived in the wild, if they produce variegated foliage or double petals, are now cultivated in a multi-billion dollar industry. Nature is still doing her thing though, and new species can still come along without us.

For hobbyists looking to get into plant breeding, the University of Illinois has great resources to get you started.

References:

[1] Ge Sun, David L. Dilcher, Hongshan Wang & Zhiduan Chen “A eudicot from the Early Cretaceous of China”, Nature 471, 625–628 (31 March 2011) doi:10.1038/nature09811 (Paywall)

[2] Santiago R. Ramírez, Barbara Gravendeel, Rodrigo B. Singer, Charles R. Marshall, & Naomi E. Pierce. “Dating the origin of the Orchidaceae from a fossil orchid with its pollinator” Nature 448, 1042-1045 (30 August 2007) doi:10.1038/nature06039 (Paywall) (Press release)

[3] Caroli de Waal, Spencer C. H. Barrett, and Bruce Anderson, “The effect of mammalian herbivory on inflorescence architecture in ornithophilous Babiana (Iridaceae): Implications for the evolution of a bird perch” Am. J. Bot. June 2012. doi: 10.3732/ajb.1100295 (Paywall) (Press release)

[4] Else Marie Friis, Kaj Raunsgaard Pedersen, and Peter R. Crane, “Diversity in obscurity: fossil flowers and the early history of angiosperms” Philos Trans R Soc Lond B Biol Sci. 2010 February 12; 365(1539): 369–382. doi: 10.1098/rstb.2009.0227 (Open access)

[5] Gerhard Leubner, “The Seed Biology Place”, Gerhard Leubner Lab, Royal Holloway, University of London, 2000. Website

[6] J. Stein Carter, “Coevolution and Pollination”, Clermont College, Bio303 Course Notes, 1999,2005. Website

[7] John M. Miller, “Origin of Angiosperms” & “Research”, University of California, Berkeley, November 2011. Website & Research

[8] Crepet WL, Nixon KC. “Two new fossil flowers of magnoliid affinity from the Late Cretaceous of New Jersey.” Am J Bot. 1998 Sep;85(9):1273-88. (Open access)

[9] Jules Janick, “History of Horticulture”, Purdue University, HORT 303, 2002. Website

[10] Adrian G. Dyer1, Skye Boyd-Gerny, Stephen McLoughlin, Marcello G. P. Rosa, Vera Simonov, and Bob B. M. Wong. “Parallel evolution of angiosperm colour signals: common evolutionary pressures linked to hymenopteran vision”. The Proceedings of the Royal Society B. June 6, 2012, doi: 10.1098/rspb.2012.0827. (Paywall) (News article)

[11] Lars Chittka and Randolf Menzel. “The evolutionary adaptation of flower colours and the insect pollinators’ colour vision”. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology. Volume 171, Number 2 (1992), 171-181, DOI: 10.1007/BF00188925. (Paywall)

[12] Yosuke Yoshioka, Kazuharu Ohashi, Akihiro Konuma, Hiroyoshi Iwata, Ryo Ohsawa and Seishi Ninomiya. “Ability of Bumblebees to Discriminate Differences in the Shape of Artificial Flowers of Primula sieboldii(Primulaceae) “. Ann Bot (2007) 99 (6): 1175-1182. doi: 10.1093/aob/mcm059. (Open Access)

[13] Olle Pellmyr and James Leebens-Mack. “Forty million years of mutualism: Evidence for Eocene origin of the yucca-yucca moth association” PNAS August 3, 1999 vol. 96 no. 16 9178-9183. doi: 10.1073/pnas.96.16.9178 . (Open Access)

[15] Taylor, D.W.; Li, H.; Dahl, J.; Fago, F.J.; Zinniker, D.; Moldowan, J.M. “Biogeochemical evidence for the presence of the angiosperm molecular fossil oleanane in Paleozoic and Mesozoic non-angiospermous fossils.” Paleobiology 32(2), 179-190. doi: 10.1666/0094-8373(2006)  (Paywall) (earlier press release from April 2001 American Chemical Society Biogeochemistry of Terrestrial Organic Matter”symposium)

[16] J. Michael Moldowan, Jeremy Dahl, Bradley J. Huizinga, Frederick J. Fago, Leo J. Hickey, Torren M. Peakman, David Winship Taylor. “The Molecular Fossil Record of Oleanane and Its Relation to Angiosperms”.  Science 5 August 1994:  Vol. 265 no. 5173 pp. 768-771  DOI: 10.1126/science.265.5173.768. (Paywall)

[17] Daniel L. Nickrent,”Elements of Plant Systematics”, Plant Biology 304, Southern Illinois University Carbondale. February 2012. Website

[18] Peter R. Crane, “The Fossil History of the Gnetales”, International Journal of Plant Sciences, Vol. 157, No. 6, Supplement: Biology and Evolution of the Gnetales (Nov., 1996), pp. S50-S57. (Paywall)

[19] Catarina Rydin and Else M Friis, “A new Early Cretaceous relative of Gnetales: Siphonospermum simplex gen. et sp. nov. from the Yixian Formation of Northeast China”. BMC Evolutionary Biology 2010, 10:183 doi:10.1186/1471-2148-10-183. (Open Access)

[20] Michael W. Frohlich, “MADS about Gnetales”, Proceedings of the National Academy of Sciences, PNAS August 3, 1999 vol. 96 no. 16 8811-8813. doi: 10.1073/pnas.96.16.8811. (Open Access)

[21] David Grimaldi, “The Co-Radiations of Pollinating Insects and Angiosperms in the Cretaceous”, Annals of the Missouri Botanical Garden , Vol. 86, No. 2 (Spring, 1999), pp. 373-406. (Paywall)

[22] David L. Dilcher and Hongshan Wang, “An Early Cretaceous fruit with affinities to Ceratophyllaceae”. American Journal of Botany 96(12): 2256–2269. 2009. doi: 10.3732/ajb.0900049. (Open Access)

[23] Else Marie Friis, Kaj Raunsgaard Pedersen, and Peter R. Crane, “Araceae from the Early Cretaceous of Portugal: Evidence on the emergence of monocotyledons”, PNAS November 23, 2004 vol. 101 no. 47 16565-16570, doi: 10.1073/pnas.0407174101. (Open Access)

[24] Owen Edwards, “The Skeletons of Shanidar Cave”, Smithsonian magazine, March 2010. (Open Access, journalism).

[25] Yin-Long Qiu, Jungho Lee, Fabiana Bernasconi-Quadroni, Douglas E. Soltis, Pamela S. Soltis, Michael Zanis, Elizabeth A. Zimmer, Zhiduan Chen, Vincent Savolainen & Mark W. Chase, “The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes” Nature 402, 404-407 (25 November 1999) | doi:10.1038/46536. (Open Access)

[26] THE ANGIOSPERM PHYLOGENY GROUP, “An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III”, Botanical Journal of the Linnean Society, Volume 161, Issue 2, pages 105–121, October 2009. DOI: 10.1111/j.1095-8339.2009.00996.x (Open Access)

[27] Charles Darwin, “On the various contrivances by which British and foreign orchids are fertilised by insects, and on the good effects of intercrossing“. London, John Murray, Albermarle Street, 1862. (Wikipedia)

[28] Else Marie Friis, James A. Doyle, Peter K. Endress, and Qin Leng, “”Archaefructus – angiosperm precursor or specialized early angiosperm?”, Trends in Plant Science, Volume 8, Issue 8, 369-373, 1 August 2003, doi:10.1016/S1360-1385(03)00161-4. (Paywall) (News)

[29] Tanya Kane, “Garden Paintings of Pompeii: Context and
Meaning”, Master’s Thesis, McMaster University, 5-1-1998. (Open Access)

[30] Robert McDuffie, “Outline of notes from class on Ancient gardens”, Virginia Tech, Hort3524. (Open Access pdf)

[31] “The History of Roses”, University of Illinois Extension Services. Website

[32] D. Fairchild Ruggles, Islamic Gardens and Landscapes, University of Pennsylvania Press, 2008, p.39.

[33] “Plant Evolution Timeline”, University of Cambridge, Centre for Applied Research in Educational Technology. (Downloadable tool)

[34] “History of life through time”, University of California Museum of Paleontology. Website

[35] “Plant and Animal Evolution” The University of Waikato, School of Science and Engineering. Animal Evolution Website Plant Evolution Website

[36] Ehud Weiss, Mordechai E. Kislev, Anat Hartmann, “Autonomous Cultivation Before Domestication”, Science 16 June 2006: Vol. 312 no. 5780 pp. 1608-1610 DOI: 10.1126/science.1127235 (Paywall)

Because of the length of this post, I would not be surprised at all to find errors in the above, especially if I grabbed an out of date reference. If you see any mistakes, or out of date material, please let me know. Hopefully I didn’t violate any copyright laws in the images used above (the Nature covers may not acceptable use), so if I’ve used an image without appropriate permission, please let me know so I can remove it. Apologies to those who started reading expecting an actual history of flower arrangement (I’ll try to write one at some point).

Update on December 6th, 2012: Since writing this an interesting new paper has come out that those ending up here might enjoy: Clément Coiffard, Bernard Gomez, Véronique Daviero-Gomez, and David L. Dilcher, Rise to dominance of angiosperm pioneers in European Cretaceous environments, PNAS 2012, doi: 10.1073/pnas.1218633110. (Paywall).  A press release on the paper is available here: “Research yields understanding of Darwin’s ‘abominable mystery’” from Indiana University.