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Mesozoic Angiosperm Paleobiodiversity
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E S S A Y C O N T E N T S |
[ Mesozoic Angiosperm Paleobiodiversity ]
JOHN M. MILLER, PH.D.
Molecular substitution and phylogenetic studies suggest that differentiation of flowering plants into a stem and crown group is feasible. Further, I reject the assertion by some workers that angiosperms first appeared in the Cretaceous Period (Feild and Arens 2007).
Stem and crown group flowering plants are discussed from a paleobotanical perspective in this third of three essays on the origin of angiosperms. I also briefly review the literature on the basic biology and molecular evolution of extant basal angiosperms as defined by the Angiosperm Phylogeny Group (2003) to include enigmatic monocotyledonous Hydatellaceae (Friis and Crane 2007).
Douglas E. Soltis et al. (2005) provide a detailed discussion of basal flowering plants. The 2005 book is updated in a recent review (D. E. Soltis et al. 2008).
Finally, the fossil history of Arthur Cronquist's subclasses of flowering plants (1981) is discussed in the context of the Angiosperm Phylogeny Group's (APG II) proposed classification of basal angiosperms, magnoliids, monocots, and eudicots including rosids and asterids (2003).
Alexandr Rasnitsyn and Donald Quicke (2002) edit the most complete book on fossil insects available at this time.
The picture of the rock slab to the left is of an indeterminate fossil flower (IU15713-3429) from the Lower Cretaceous Dakota Formation of North America (photographed by the author in 1981 at Indiana University with the permission of Professor David L. Dilcher).
Retallack and Dilcher (1981) reported that IU15713-3429, detached stamens and petals, and detached Acerites multiformis leaves were found in the same Rose Creek locality bedding plane with brackish water Brachidontes bivalves.
Comprehensive accounts of the past literature on Mesozoic angiosperms are published by Dilcher (1979), Crane et al. (1986), Crane and Herendeen (1996), Crepet et al. (2004), and Friis et al. (2006).
Fossilized pollen casings known as palynomorphs are known from middle Triassic sediments recovered from deep well bore-holes drilled off the island of Spitzbergen (Hochuli and Feist-Burkhardt 2004). These palynomorphs may represent the first Mesozoic records of stem group angiosperms, but whole plant fossils are lacking.
Triassic angiosperm-like fossils of detached or crumpled pieces of whole plants are known (Cornet 1986, 1989, 1993). However, interpretation of poorly-preserved reproductive structures of the Triassic seed plant Sanmiguelia lewisii is controversial and the subject of much debate.
Fossils of several other enigmatic flowering plants have been recovered from Mesozoic rocks but reproductive details and the morphology of whole plants are unclear due to problems with poor preservation and uncertain stratigraphic control (Muller 1981, G. Sun and Dilcher 1997, G. Sun et al. 1998, G. Sun et al. 2001, Friis et al. 2006, X. Wang et al. 2007).
The next chapter discusses the fossil history of stem group angiosperms. Please note that the numbering of tables in this chapter follows table 3 in the previous essay on the Paleobotany of Angiosperm Origins.
Fossil History of Stem Group Flowering Plants:
The Cretaceous Yixian Formation of Asia yields potentially interesting fossilized inflorescences, flowers, seed, and pollen of stem group angiosperms including Asiatifolium, Jixia, Shenkuoa, and Xingxueina (G. Sun et al. 2001). Hyrcantha decussata (Sinocarpus decussatus, Leng and Friis 2006) is the most recently studied angiosperm-like fossil recovered from these sediments (Dilcher et al. 2007).
The drawing to the right is Lesqueria elocata (family uncertain, Magnoliales, Magnoliidae) from page 399 of Crane and Dilcher (1984), Lesqueria: an early angiosperm fruiting axis from the mid-Cretaceous, Annals of the Missouri Botanical Garden 71(2): 384-402, reproduced by permission from Peter Crane, David Dilcher, and the Missouri Botanical Garden.
"Figure 47. Reconstruction of the Lesqueria elocata fruiting axis."
Archaefructus liaoningensis (Magnoliophyta, Magnoliopsida, Archaemagnoliidae), has been described (G. Sun and Dilcher 1997) and discussed within the context of a Jurassic aquatic origin of flowering plants (G. Sun et al. 1998). Radioisotope decay data suggest that the Yixian Formation is much younger than originally believed by Ge Sun and colleagues (see Friis et al. 2006).
Phylogenetic placement of Archaefructus as a stem group flowering plant is problematic (Friis et al. 2003). Several workers suggest that the angiosperm fossils from the Cretaceous Yixian Formation are better placed with the crown group of angiosperms.
Fossilized flowers are also known from exposed Cretaceous sediments of Antarctica (Eklund 2003), Asia (G. Sun et al. 1998, Poinar and Chambers 2005), North America (Crane and Herendeen 1996), South America (Endressinia brasiliana, Mohr and Bernardes-de-Oliveira 2004), and elsewhere (Friis et al. 2006).
Another interesting but incomplete Cretaceous North American angiosperm fossil is Archaeanthus linnenbergerii (Dilcher and Crane 1985). The morphology of pollen-bearing organs and stem anatomy of Archaeanthus is unknown, therefore critical comparison with Afropollis pollen and fossil wood of Cretaceous Winteraceae from Antarctica (Poole and Francis 2000) is impossible.
Several angiosperm-like extinct groups of seed plants including bennettitaleans, corystosperms, and pentoxylalians coexisted in the Cretaceous Period with certain modern flowering plant groups. The Corystospermales represented by the Paleogene Tasmanian fossil Komlopteris cenozoicus, is the only group of seed ferns that survived the K-T asteroid impact (McLoughlin et al. 2008).
Are Jurassic corystosperms ancestors of the stem group of flowering plants as proposed by Frohlich (2002)?
Rapid diversification of flowering plants during the Albian of the early Cretaceous Period is demonstrable based on paleontologic evidence gathered to date (Friis et al. 2006), and phylogenetic analyses (D. E. Soltis et al. 2008).
Was the "Big Bang" of angiosperm evolution during the Aptian Age (Gallic Epoch) attributable to the effects of the end-Barremian Age (Neocomian Epoch) biogeochemical perturbation (BaCCE) on coevolving angiosperm hosts and insect antagonists?
Heimhofer et al. (2005) suggest that the BaCCE might have accelerated the diversification of early magnoliid flowering plants and possibly monocots. Phylogenetic analysis supports the idea that an explosive radiation of the Malpighiales sensu APG II occurred during the Aptian Age of the Gallic Epoch, a few million years after the BaCCE (Davis et al. 2005, Figure 1).
More paleobotanical work is needed to elucidate the angiosperm stem group, which is possibly derived from older Mesozoic and Paleozoic seed plant stock.
Angiosperm Classification Systems:
It is important to review the phylogenetic position and naming of modern flowering plant groups within a general evolutionary framework for purposes of later comparison and discussion.
The kodachrome to the left is Adonis amurensis (Ranunculaceae, Ranunculales, Magnoliidae) photographed by the author.
Classification levels of order and genus are used in the tabulations below because the number of genera in extant floras is the most commonly used biogeographically significant measure of biodiversity. Some of the many classic references on "dicotyledonous" and monocotyledonous angiosperm classification include Engler (1964), Thorne (1968), Cronquist (1981), Dahlgren and Clifford (1982), Dahlgren et al. (1985), Takhtajan (1997), and Angiosperm Phylogeny Group (2003), among others.
The Angiosperm Phylogeny Group (2003) updated classification is best suited as a framework to discuss early flowering plant evolution. The graphic below is redrawn from the Angiosperm Phylogeny Group (2003) Figure 1. The APGII phylogenetic tree shows relationships of some families and orders of angiosperms supported by jackknife and bootstrap frequencies over 50% (not all flowering plant families and orders are included because data are missing or do not exceed the 50% confidence value), based on 18S rDNA, rbcL, and atpB molecular sequences (Angiosperm Phylogeny Group 2003).
The color of typescript allows cross-reference to Cronquist's subclasses of flowering plants (Cronquist 1981). Monocots are in various shades of green or orange (Alismatidae are denoted by blue-green type, Arecidae with yellow type, Zingiberidae are shown in gold letters, Commelinidae have green letters, and Liliidae are depicted in lime-green type). Cronquist's Magnoliidae are shown with indigo brown type. Hamamelidae are depicted with magenta letters. Dilleniidae appear on the dendrogram labels in royal blue. The Caryophyllidae are depicted in purple type. Rosidae are colored red and Asteridae appear in black type.
Table 4 summarizes the stratigraphic distribution and microfossil, megafossil, and mesofossil history of the subclasses of flowering plants. I did not include numerous reports and descriptions of Mesozoic leaf morphotype genera (e.g. Dilcher and Basson 1990, Upchurch and Dilcher 1990, among others) to avoid guesswork on their taxonomic placement without benefit of reproductive structures.
"Angiosperm phylogeny is riddled with examples of convergent morphologies.... Any classification based on a single organ has a greater potential for error than one based on a variety of organs.... Although one solution to this problem would be to restrict the systematic analysis of angiosperm megafossils to taxa known from both reproductive and vegetative organs, this approach would greatly restrict information about the flora as a whole, given the dominance of isolated vegetative organs in the megafossil record."
The above statement is from page 3 of Upchurch and Dilcher (1990), Cenomanian Angiosperm Leaf Megafossils, Dakota Formation, Rose Creek Locality, Jefferson County, Southeastern Nebraska, U.S. Geological Survey Bulletin 1915.
Integers in Table 4 represent the total number of taxonomic orders and genera (in parentheses) for each of Cronquist's subclasses of flowering plants. Separate columns are devoted to extant and extinct taxa. The number of extant genera (in parentheses) in the table below was compiled from Cronquist's family descriptions (1981). Certain fossil species reported in the scientific literature are not assignable to any extant angiosperm subclass. The Archaemagnoliidae is lumped with the Magnoliidae.
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Table 4. Mesozoic Fossil History of Subclasses, Orders, and Genera of Flowering Plants. |
Taxonomic Subclass |
Extant Orders (Genera) |
Mesozoic Orders (Genera) |
Malm - Jurassic |
Neocomian - Cretaceous |
Gallic - Cretaceous |
Senonian - Cretaceous |
Not Assignable to a Known Subclass |
Not Applicable |
?(7) |
0 |
?(1) |
?(4) |
?(4) |
Alismatidae |
4(60) |
2(4) |
0 |
1(2) |
1(2) |
? |
Arecidae |
4(330) |
3(11) |
0 |
1(1) |
1(1) |
3(5) |
Asteridae |
11(3584) |
?(2) |
0 |
0 |
0 |
2(2) |
Caryophyllidae |
3(397) |
0(0) |
0 |
0 |
0 |
1(1) |
Commelinidae |
7(703) |
0(0) |
0 |
0 |
0 |
? |
Dilleniidae |
13(1452) |
5(11) |
0 |
0 |
3(4) |
5(7) |
Hamamelidae |
11(148) |
3(18) |
0 |
0 |
3(13) |
4(23) |
Liliidae |
2(1463) |
1(1) |
0 |
0 |
1(1) |
1(1) |
Magnoliidae/Archaemagnoliidae |
8(482) |
6(42) |
0 |
3(4) |
6(25) |
1(3) |
Rosidae |
18(3185) |
10(23) |
0 |
0 |
5(11) |
9(19) |
Zingiberidae |
2(134) |
1(2) |
0 |
0 |
0 |
1(1) |
TABLE IS UPDATED PERIODICALLY
There is a significant increase in the number of orders and genera of fossil flowering plants by the Aptian Age of the Gallic Epoch of the Cretaceous Period, based on data in Table 4. When the compression floras of leaves are added, a late Cretaceous explosive radiation of angiosperms is clear (Friis et al. 2006).
Fossil History of Crown Group Flowering Plants:
This chapter reviews the scientific literature on the basic biology of extant basal angiosperms, and summarizes the fossil record of crown group eudicots, rosids, asterids, and monocots.
The hot links (underlined words, below) lead the reader to the section where the fossil history of each Cronquist subclass of flowering plants (Cronquist 1981) is discussed from a paleontological perspective. Cronquist's flowering plant subclasses (with cross-referenced groupings used by APGII in parentheses) are:
Alismatidae (monocots)
Arecidae (monocots)
Asteridae (asterid I and II eudicots)
Caryophyllidae (eudicots)
Commelinidae (monocots and a basal angiosperm)
Dilleniidae (eudicots, ericanae, asterid III and IV eudicots)
Hamamelidae (eudicots and rosid I eudicots)
Liliidae (monocots)
Magnoliidae (basal angiosperms and magnoliids)
Rosidae (rosid I and II eudicots)
Zingiberidae (monocots)
The image to the right is a flower of Protea compacta (Proteaceae, Proteales, Rosidae) photographed by the author.
In 1981, Friis and Skarby reported a remarkable find of abundant indeterminate and tiny angiosperm eudicot flowers from the Late Santonian-Early Campanian Age (Senonian Epoch, Late Cretaceous Period). Crane et al. (1986), Eklund (2003), Friis (1985), Friis and Skarby (1981), Knobloch and Mai (1986), Kvacek and Eklund (2003), Schönenberger and Friis (2001), and Friis et al. (2006) are key pieces of the scientific literature on early angiosperm floras and fossils.
Studies of Cretaceous permineralized woods (Page 1967) paint a different picture of Maastrichtian forests once thought to be dominated by gymnosperms. A recent study of wood permineralizations sampled from large, fallen in situ logs from southwestern North American Maastrichtian (Senonian) deposits of the Aguja and Javelina Formation suggests that "dicotyledonous" trees were more abundant than conifers. Petrified stumps of Javelinoxylon multiporosum (Malvales, Dilleniidae) were more than a meter in diameter with extrapolated tree axes up to 40 meters tall (Wheeler and Lehman 2000).
Existence of dilleniid trees assignable to the Malvales (a derived crown group of eudicots) as important floristic element of late Cretaceous stratified tropical forests of southwestern North America detract from the idea that early flowering plants were paleoherbs of upland habitats.
Basal angiosperms. Certain ANITA-grade basal flowering plants first appear in the fossil record of the Cretaceous Period (Friis et al. 2000, Friis et al. 2001, Krassilov and Golovneva 2004, Takahashi et al. 2007). The fossil history of basal angiosperms is reviewed by Friis et al. (2006).
D. E. Soltis et al. (2005) in a remarkable book, support the assignment of ANITA-grade angiosperms to a basal position in several calibrated, bootstrap-supported, molecular-based phylogenies of extant flowering plants. The acronym ANITA is composed of first letters from the taxa Amborella, Nymphaeales, Illiciaceae, Trimeniaceae, and Austrobaileyaceae.
Basal flowering plants sensu Cronquist (1981) belong to Amborellaceae and Trimeniaceae (Laurales), Austrobaileyaceae (Magnoliales), Hydatellales (monocots), Illiciales, and Nymphaeales. Certain other Magnoliales once regarded by Cronquist (1981) as primitive angiosperms (e.g. Degeneriaceae, Magnoliaceae, and Winteraceae) are in a more derived position on phylogenetic trees based on molecular data (Wikström et al. 2001, Leebens-Mack et al. 2005, Qiu et al. 2006, D. E. Soltis et al. 2007) than ANITA-grade taxa.
Tremendous progress has been made in the last decade on understanding the anatomy, basic biology, developmental genetics, ecology, molecular evolution, morphology, natural history, and phylogenetic systematics of ANITA grade basal angiosperms (J. A. Doyle and Endress 2000, Endress and Igersheim 2000, Floyd and Friedman 2000, Mathews and Donoghue 2000, Qiu et al. 2000, P. S. Soltis et al. 2000, Thien et al. 2000, Endress 2001, Furness and Rudall 2001, Friedman 2001, Yamada et al. 2001, Borsch et al. 2003, Feild et al. 2003, Ronse De Craene et al. 2003, Schneider et al. 2003, Zanis et al. 2003, Aoki et al. 2004, Endress 2004, Carpenter 2005, Kim et al. 2005, Leebens-Mack et al. 2005, Podoplelova and Ryzhakov 2005, Qiu et al. 2005, Carpenter 2006, P. S. Soltis et al. 2006, Endress and J. A. Doyle 2007, Feild and Arens 2007, Moore et al. 2007, D. E. Soltis et al. 2007, and Rudall et al. 2008).
Hydatellaceae regarded by Cronquist (1981) as advanced commelinid monocots now occupy a basal position together with extant ANITA-grade dicots (Rudall et al. 2007, Saarela et al. 2007, Friedman 2008, Rudall et al. 2008).
Key research papers that focus on Amborellaceae include Tobe et al. (2000), Endress and Igersheim (2000), Hesse (2001), Yamada et al. (2001), Posluszny and Tomlinson (2003), Thien et al. (2003), and Buzgo et al. (2004), among others. Nymphaeales have been studied by numerous students of ANITA-grade angiosperms including Yamada et al. (2003), Yoo et al. (2005), Grob et al. (2006), Borsch et al. (2007), Löhne et al. (2007), M. L. Taylor et al. (2008), Zhou and Fu (2008), and Nixon (2008).
Hao et al. (2000), Carlquist and Schneider (2002), Friedman et al. (2003), Williams and Friedman (2004), Denk and Oh (2005), Lyew et al. (2007), and Morris et al. (2007), have published results of detailed studies of the Illiciales. Work on the pollination biology of Trimeniaceae appears in research published by Bernhardt et al. (2003). Finally, Yamada et al. (2003), Williams and Kennard (2006), and Tobe et al. (2007) report key findings on developmental morphology and genetics of certain Austrobaileyales.
Crepet et al. (2004) subjected nucleic acid sequence data from selected taxa or groups representing the major basal lineages of flowering plants to cladistic analysis, and mapped minimum ages in millions of years (M.Y.A.) to main branch points where each clade diverged. The graphic below is redrawn from Figure 16 of Crepet et al. (2004). Results of the phylogenetic analysis by Crepet et al. (2004) are condensed, displaying certain taxa of interest, but leaving out the majority of basal angiosperm families and genera. Friis et al. (2000) also describe the phylogenetic relationships of basal flowering plants.
I colored the taxon and/or group names on the dendrogram so that cross-referencing with the higher order classification of Cronquist (1981) is facilitated. Magnoliidae are shown with indigo brown type. Hamamelidae are depicted with magenta letters. Monocots are labeled in green, and the Rosidae are colored red. The remainder of the eudicots make-up most of Cronquist's Dilleniidae, Rosidae, and Asteridae (these subclasses comprise the majority of extant flowering plant species).
The Crepet et al. (2004) minimum age dates on the above dendrogram fall within the Neocomian Epoch of the Early Cretaceous Period that ended about 121 M.Y.A. and Gallic Epoch (ending at 89 M.Y.A.). The remainder of the Late Cretaceous Period is the Senonian Epoch culminating with the K-T Event 65 M.Y.A. (Tables 4-15).
However, molecular clock methods used in calibrating the point of divergence of angiosperms from gymnosperms between 220 and 300 million years ago, and paleobotanical evidence (Cornet 1986, 1989), do not support application of the adjectives "ancestral, "early," or "primitive" to Amborellaceae by certain workers.
The frequency of flowering plant reproductive fossils of core eudicots, magnoliids, ANITA-clade orders and families, and monocots increases dramatically by the Albian Age of the Cretaceous Period (Friis et al. 2006).
I now review the Mesozoic fossil history of flowering plants following Cronquist's (1981) classification with notes from APGII.
Magnoliidae. In total, subclass Magnoliidae consist of 8 orders, 39 families, and about 12,000 extant species spread among some 482 genera (Cronquist 1981). A molecular phylogeny of the group has been proposed (Azuma 2001) and additional studies on plastid genes have been published (Qiu et al. 1993).
Complex insect pollinator-plant interactions evidently were in place in Nymphaeaceae during Cretaceous time (Gandolfo et al. 2004). Yet, only a few genera are known from the early Cretaceous Yixian Formation of Asia (and elsewhere in the world among other strata), consisting of fossilized, detached plant parts and flowers, and the fossil remains of other plants classifiable in a couple orders and families (Friis et al. 1997, G. Sun and Dilcher 1997, G. Sun et al. 2001).
The evolutionary history of magnoliid angiosperms is reviewed by Friis et al. (1986), Loconte and Stevenson (1991), Friis et al. (1997), Kimoto and Tobe (2001), and Oginuma and Tobe (2006). The Piperales, including Chloranthaceae, occupy an evolutionary position between true magnoliids and hamamelids (Crane 1989).
Fossilized stamens, pollen, and small flowers assignable to Chloranthaceae (Eklund et al. 2004, Friis et al. 2006) have been found in sediments Barremian in Age (late Neocomian Epoch, Early Cretaceous). Extinct Piperalians, including Chloranthaceae are represented in the fossil record as pollen classifiable to certain Asteropollenites, Clavatipollenites hughesii, and Stephanocolpites (Crane 1989).
Stamens and flowers discovered in several younger rock formations of the Late Cretaceous Period add another layer of evolutionary complexity to magnoliids and basal eudicots, including the Hamamelidae and Trochodendraceae (Crane 1989).
I cast the available data on the fossil history of magnoliids and certain basal flowering plants into Table 5. Please note that the number in each cell represents the number of species (or genera, as the case may be).
A branch bearing a flower and flower buds of Degeneria vitiensis (Degeneriaceae) is shown to the left (photographed by Paddy Ryan, Ph.D.). Degeneriaceae are related to Winteraceae and Magnoliaceae (A. C. Smith 1981, Cronquist 1981).
Unclassified angiosperms. Several fossil genera cannot be classified in any of the known subclasses of flowering plants. The paleontologic record (tabulated below in bold type) of these enigmatic flowering plant fossil flowers and fruits is summarized together with magnoliids in Table 5.
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Table 5. Mesozoic Stratigraphic Distribution of Archaemagnoliidae, Magnoliidae, and Unclassified Angiosperms. |
Order |
Scientific Name and Publication |
Fossilized Remains |
Malm - Jurassic |
Neocomian - Cretaceous |
Gallic - Cretaceous |
Senonian - Cretaceous |
Nymphaeales |
Nelumbonaceae under study (Gandolfo and Cuneo 2005) |
leaves and detached fruits |
0 |
0 |
0 |
1 |
Nymphaeales? |
taxonomy under study (Friis et al. 2001) |
staminate inflorescences and pollen |
0 |
? |
? |
0 |
Laurales |
undescribed (Eklund and Kvacek 1998, Eklund 2000) |
four unnamed flowers |
0 |
0 |
0 |
4? |
Assignment to Subclass in Doubt |
Afrasita lejalnicoliae (Krassilov et al. 2004) |
infructescences |
0 |
0 |
1 |
0 |
Piperales |
Anacostia (Friis et al. 1997) |
pollen and fruits |
0 |
1 |
1 |
0 |
Assignment to Subclass in Doubt |
Appomattoxia ancistrophora (Friis et al. 1995) |
fruits |
0 |
0 |
1 |
0 |
Nymphaeales |
Aquatifolia fluitans (Hongshan Wang and Dilcher 2006) |
leaves |
0 |
0 |
1 |
0 |
Assignment in Doubt |
Araripia florifera (Mohr and Eklund 2003) |
flowers |
0 |
0 |
1 |
0 |
Magnoliales |
Archaeanthus linnenbergerii (Dilcher and Crane 1985) |
fruit cluster (flowers, bud scales, and leaves described as form genera) |
0 |
0 |
1 |
0 |
Assignment in Doubt |
Archaefructus (Sun et al. 1998, 2001) |
flowers and leafy fruiting axes |
0 |
2 |
0 |
0 |
Piperales |
Asteropollis (Friis et al. 2000, Eklund et al. 2004) |
palynomorphs inside stamens, staminate inflorescences and pistillate flowers |
0 |
1 |
0 |
0 |
Assignment to Subclass in Doubt |
Baasoxylon parenchymatosum (Wheeler and Lehman 2000) |
wood |
0 |
0 |
0 |
1 |
Assignment to Subclass in Doubt |
Beipiaoa (Sun et al. 2001) |
fruits |
0 |
3 |
0 |
0 |
Nymphaeales |
Brasenites kansense (Hongshan Wang and Dilcher 2006) |
leaves |
0 |
0 |
1 |
0 |
Ranunculales |
Callicrypta chlamydea (Krassilov and Golovneva 2004) |
flowers |
0 |
0 |
1 |
0 |
Assignment to Subclass in Doubt |
Caloda delevoryana (Dilcher and Kovach 1986) |
inflorescence and fruit |
0 |
0 |
1 |
0 |
Ranunculales? |
Caspiocarpus paniculiger (Krassilov 1997) |
flowers |
0 |
0 |
1 |
0 |
Piperales |
Chloranthistemon (Crane et al. 1989, Eklund et al. 1997) |
inflorescences and flowers |
0 |
0 |
0 |
>2 |
Piperales |
Clavatipollenites (Friis et al. 2000, Eklund et al. 2004) |
palynomorphs inside stamens, staminate inflorescences and pistillate flowers |
0 |
1 |
0 |
0 |
Piperales |
Couperites mauldinensis (Pedersen et al. 1991) |
fruits |
0 |
0 |
1 |
0 |
Magnoliales? Laurales? |
Cronquistiflora sayrevillensis (Crepet and Nixon 1998) |
flowers and fruits |
0 |
0 |
1 |
0 |
Magnoliales? Laurales? |
Detrusandra mystagoga (Crepet and Nixon 1998) |
flowers and fruits |
0 |
0 |
1 |
0 |
Magnoliales |
Endressinia brasiliana (Mohr and Bernardes-de-Oliveira 2004) |
flowers |
0 |
0 |
1 |
0 |
Ranunculales |
Freyantha sibirica (Krassilov and Golovneva 2001) |
staminate inflorescence and flowers |
0 |
0 |
1 |
0 |
Laurales? Magnoliales? |
Hidakanthus (Nishida et al. 1996) |
carpels |
0 |
0 |
0 |
1 |
Assignment in Doubt |
Hyrcantha decussata (Friis et al. 2006, Leng and Friis 2006, Dilcher et al. 2007) |
flowers and leaves associated with flowers, infructescences |
0 |
0 |
1 |
0 |
Ranunculales |
Hyrcantha karatscheensis (Krassilov et al. 1983) |
inflorescence |
0 |
0 |
1 |
0 |
Illiciales |
Illiciospermum (Frumin and Friis 1999) |
seeds |
0 |
0 |
1 |
0 |
Laurales |
Jerseyanthus calycanthoides (Crepet et al. 2005) |
flowers, stamens, staminodes, and pollen |
0 |
0 |
1 |
0 |
Laurales? Magnoliales? |
Keraocarpon (Ohana et al. 1999) |
fruits |
0 |
0 |
0 |
2 |
Magnoliales |
Lactoripollenites africanus (Zavada and Benson 1987) |
palynomorphs |
0 |
0 |
0 |
1 |
Laurales |
Lauranthus (Takahashi et al. 2001) |
flower |
0 |
0 |
0 |
1? |
Assignment in Doubt |
Lesqueria elocata (Crane and Dilcher 1984) |
fruiting axis |
0 |
0 |
1 |
0 |
Magnoliales |
Liriodendroidea (Knobloch and Mai 1986, Frumin and Friis 1996, 1999) |
pollen and wood |
0 |
0 |
4 |
4 |
Magnoliales? |
Litocarpon beardii (Delevoryas and Mickle 1995) |
fruit with follicles |
0 |
0 |
0 |
1 |
Laurales |
Mauldinia (Drinnan et al. 1990, Eklund and Kvacek 1998, Frumin et al. 2004, Friis et al. 2006) |
flowers and inflorescences |
0 |
0 |
1 |
>2 |
Assignment to Subclass in Doubt |
Metcalfeoxylon kirtlandense (Wheeler and Lehman 2000) |
wood |
0 |
0 |
0 |
1 |
Nymphaeales |
Microvictoria (Gandolfo et al. 2004) |
flowers |
0 |
0 |
1 |
0 |
Assignment in Doubt |
Myricanthium (Kvacek and Eklund 2003) |
flowers |
0 |
0 |
2 |
0 |
Laurales |
Neusenia (Eklund 2000) |
flowers |
0 |
0 |
0 |
1? |
Assignment to Subclass in Doubt |
Noferinia fusicarpa (Lupia et al. 2002) |
flowers |
0 |
0 |
0 |
1 |
Assignment to Subclass in Doubt |
Pageoxylon cretaceum (Wheeler and Lehman 2000) |
wood |
0 |
0 |
0 |
1? |
Assignment in Doubt |
Palaeoanthella huangii (Poinar and Chambers 2005) |
flower |
0 |
0 |
1 |
0 |
Assignment in Doubt |
Paraphyllanthoxylon anazasii (Wheeler et al. 1995) |
wood |
0 |
0 |
0 |
1 |
Laurales |
Perseanthus (Herendeen et al. 1994) |
flower |
0 |
0 |
1 |
0 |
Laurales? |
Pragocladus lauroides (Kvacek and Eklund 2003) |
inflorescences |
0 |
0 |
1 |
0 |
Assignment in Doubt |
Prisca reynoldsii (Retallack and Dilcher 1981, Drinnan et al. 1990) |
flowers? inflorescences? |
0 |
0 |
1 |
0 |
Assignment in Doubt |
Protomonimia kasai-nakajhongii (Nishida and Nishida 1988) |
carpels and fruits |
0 |
0 |
1 |
0 |
Nymphaeales |
Scutifolium jordanicum (D. W. Taylor et al. 2008) |
leaves and axes |
0 |
0 |
1 |
0 |
Assignment to Subclass in Doubt |
Silvianthemum suecicum (Friis 1990) |
inflorescence and fruit |
0 |
0 |
0 |
1 |
Nymphaeales |
Symphaenale futabensis (Takahashi et al. 2007) |
seeds |
0 |
0 |
0 |
1 |
Ranunculales |
Teixeiraea lusitanica (von Balthazar et al. 2005) |
male flower, flower buds, and pollen |
0 |
0 |
1 |
0 |
Laurales? |
Virginianthus calycanthoides (Friis et al. 1994) |
flower |
0 |
0 |
1 |
0 |
Magnoliales |
Winteroxylon (Poole and Francis 2000) |
wood |
0 |
0 |
0 |
2 |
Assignment in Doubt |
Xingxueiana heilongjiangensis (Sun and Dilcher 1997) |
inflorescence |
0 |
1 |
0 |
0 |
TABLE IS UPDATED PERIODICALLY
Eudicots. Phylogenetic relationships of basal and derived eudicots are reviewed by Judd and Olmstead (2004), Magallón (2004), and Worberg et al. (2007). Work on the evolutionary-developmental biology of eudicots has been published by Endress and Mathews (2006), among others. Several workers suggest that the term "dicot" should be abandoned. I concur.
The dendrogram drawn below is meant to complement the phylogenetic reconstruction that precedes Table 5. The base of the condensed phylogenetic tree below connects with the "remainder of eudicots" branch on the other diagram. The figure is redrawn from Figure 17 of Crepet et al. (2004).
Key phylogenetic and evolutionary studies of eudicots are published by Hoot et al. (1999), Fishbein et al. (2001), D. E. Soltis et al. (2003), Kim et al. (2004), R.-Q. Li (2004), C. L. Anderson et al. (2005), and De Bodt et al. (2006), among others.
Cronquist's (1981) Magnoliidae are shown with indigo brown type. Hamamelidae are depicted with magenta letters. Dilleniidae appear on the dendrogram labels in royal blue. The Caryophyllidae are depicted in purple type. Rosidae are colored red. The original phylogenetic tree was condensed from original cladistic analysis such that many important and diverse families of flowering plants belonging to Cronquist's Caryophyllidae, Dilleniidae, Rosidae, and Asteridae were left out (Crepet et al. 2004).
The Crepet et al. (2004) minimum age dates on the above dendrogram fall within the Gallic Epoch (ending at 89 M.Y.A.) and the Senonian Epoch that culminates with the K-T Event 65 M.Y.A.
Hamamelidae. Witch hazels, sweet gums, wax myrtles, beeches, alders, oaks, and beefwoods belong to the Hamamelidae, consisting of 11 orders, 24 families, and 148 genera, and approximately 3,400 species (Cronquist 1981). The group may be more ancient than the fossil record suggests (Table 6).
The fossil history and phylogenetic systematics of the Hamamelidae is discussed by Manchester (1987), Donoghue and J. A. Doyle (1989), Crepet et al. (1992), Chen et al. 1999, Zhou et al. (2001).
During the Cretaceous Period the hamamelids and relatives might have been important floristic elements in many localities as judged from the common occurrence of Normapollis palynomorphs. Albian compression floras contain a high frequency of platanoid leaves and definitive leaf-forms which are classifiable to Trochodendrales (Upchurch and Wolfe 1987). According to Friis et al. (2006), normapolles pollen have been found in situ in several fossilized flowers of primitive beeches and oaks, among other hamamelids now extinct.
Phylogenetic relationships within extant genera classified in the birch family (Betulaceae) ascertained from studies of rbcL, ITS, and morphology are congruent with paleobotanical and paleoecological data (Chen et al. 1999).
To the right is a picture of a mature stand of Alnus rhombifolia (Betulaceae, Fagales, Hamamelidae) at a spring and meadow ("cienega") which supplies hydrology to the East Fork of Santa Paula Creek of the Topa Topa Mountains of western North America (photographed by the author).
I cast the available data on the fossil history of the Subclass Hamamelidae into Table 6. Please note that the number in each cell represents the number of species (or genera, as the case may be). Platanoid and baileyan permineralized wood types including Icacinoxylon and Plataninium (Wheeler and Lehman 2000) are excluded from this table because of uncertainty on where to classify these "dicotyledonous" fossils.
|
|
Table 6. Mesozoic Stratigraphic Distribution of the Hamamelidae.
|
Order |
Scientific Name and Publication |
Fossilized Remains |
Malm - Jurassic |
Neocomian - Cretaceous |
Gallic - Cretaceous |
Senonian - Cretaceous |
Hamamelidales |
unclassified platanoid leaves and fertile structures (Upchurch and Wolfe 1987, Mindell et al. 2006) |
leaves, flowers, and inflorescences |
0 |
0 |
>2 |
>2 |
Trochodendrales |
unclassified leaves (Upchurch and Wolfe 1987) |
leaves |
0 |
0 |
>2 |
>2 |
Assignment in Doubt |
Allonia decandra (Magallon-Puebla et al. 1996) |
flower |
0 |
0 |
0 |
1 |
Betulales |
Alnipollenites (Miki 1977) |
palynomorphs |
0 |
0 |
0 |
1 |
Hamamelidales |
Androdecidua endressii (Magallón et al. 2001) |
floral fragments with stamens |
0 |
0 |
0 |
1 |
Fagales |
Antiquacupula (Herendeen et al. 1995, Sims et al. 1998) |
flowers and inflorescences |
0 |
0 |
0 |
1 |
Fagales |
Antiquocarya (Friis 1983) |
fruits |
0 |
0 |
0 |
1 |
Hamamelidales |
Aquia brookensis (Crane et al. 1993) |
staminate inflorescences |
0 |
0 |
1 |
0 |
Fagales |
Archamamelis bivalvis (Endress and Friis 1991) |
flower |
0 |
0 |
0 |
1 |
Fagales |
Bedellia (Sims et al. 1999) |
flowers and fruits |
0 |
0 |
0 |
1 |
Betulales |
Betulaceoipollenites (Miki 1977, X.-J. Sun et al. 1979) |
palynomorphs |
0 |
0 |
0 |
1 |
Betulales |
Betulaepollenites (Miki 1977) |
palynomorphs |
0 |
0 |
0 |
1 |
Juglandales |
Budvaecarpus (Knobloch and Mai 1986) |
flower |
0 |
0 |
1 |
0 |
Juglandales |
Caryanthus (Friis 1983) |
flowers and fruits |
0 |
0 |
0 |
3 |
Fagales |
Dahlgrenianthus (Friis et al. 2006) |
flowers |
0 |
0 |
0 |
3 |
Hamamelidales |
Dewalquea pulchella (Nichols and Jacobson 1982) |
leaves |
0 |
0 |
1 |
0 |
Fagales |
Endressianthus (Friis et al. 2003) |
staminate inflorescences |
0 |
0 |
0 |
1 |
Hamamelidales |
Hamatia (Pederson et al. 1994) |
flower and inflorescence |
0 |
0 |
1 |
0 |
Trochodendrales |
Joffrea (Crane 1989) |
leaves and winged fruits |
0 |
0 |
0 |
>2 |
Juglandales |
Manningia (Friis 1983, Knobloch and Mai 1986, Friis and Crane 1989) |
flowers and fruits |
0 |
0 |
0 |
1 |
Hamamelidales |
Microaltingia apocarpela (Zhou et al. 2001) |
pistillate inflorescences and infructescences |
0 |
0 |
1 |
0 |
Trochodendrales |
Nordenskioldia (Crane 1989) |
leaves, inflorescences, fruits, and fruitlets, shoots |
0 |
0 |
0 |
1 |
Assignment in Doubt |
Normanthus (Schonenberger et al. 2001, Friis et al. 2003) |
inflorescence |
0 |
0 |
1 |
0 |
Betulales |
Paraalnipollenites (X.-J. Sun et al. 1979) |
palynomorphs |
0 |
0 |
0 |
1 |
Hamamelidales |
Platananthus (Friis et al. 1988) |
inflorescence |
0 |
0 |
1 |
0 |
Hamamelidales |
Platanocarpus brookensis (Crane et al. 1993) |
pistillate inflorescences and infructescences |
0 |
0 |
1 |
0 |
Hamamelidales |
Platanocarpus marylandensis (Friis et al. 1988) |
flowers and fruits |
0 |
0 |
1 |
0 |
Fagales |
Protofagacea allonensis (Herendeen et al. 1995, Sims et al. 1998) |
flowers and inflorescences |
0 |
0 |
0 |
1 |
Hamamelidales |
Quadriplatanus georgianus (Magallon-Puebla et al. 1997) |
staminate and pistillate flowers |
0 |
0 |
0 |
1 |
Hamamelidales |
Sapindopsis (Hickey and J. A. Doyle 1977) |
leaves |
0 |
0 |
>2 |
>2 |
TABLE IS UPDATED PERIODICALLY
Hamamelids were evidently common | | |
