Leo J. Hickey

Early cretaceous fossil evidence for angiosperm evolution

Morphological, stratigraphic, and sedimentological analyses of Early Cretaceous pollen and leaf sequences, especially from the Potomac Group of the eastern United States, support the concept of a Cretaceous adaptive radiation of the angiosperms and suggest pathways of their initial ecological and systematic diversification. The oldest acceptable records of angiosperms are rare monosulcate pollen grains with columellar exine structure from probable Barremian strata of England, equatorial Africa, and the Potomac Group, and small, simple, pinnately veined leaves with several orders of reticulate venation from the Neocomian of Siberia and the basal Potomac Group. The relatively low diversity and generalized character of these fossils and the subsequent coherent pattern of morphological diversification are consistent with a monophyletic origin of the angiosperms not long before the Barremian. PatuxentArundel floras (Barremian-early Albian?) of the Potomac Group include some pollen and leaves with monocotyledonous features as well as dicotyledonous forms. Patuxent angiosperm pollen is strictly monosulcate and has exine sculpture indicative of insect pollination. Rare Patuxent-Arundel angiosperm leaves are generally small, have disorganized venation, and are largely restricted to sandy stream margin lithofacies; the largest are comparable to and may include ancestors of woody Magnoliidae adapted to understory conditions. Patapsco floras (middle to late Albian?) contain rapidly diversifying tricolpate pollen and several new complexes of locally abundant angiosperm leaves. Ovate-cordate and peltate leaves in clayey pond lithofacies may includeancestors of aquatic Nymphaeales and Nelumbonales. Pinnatifid and later pinnately compound leaves with increasingly regular venation which are abundant just above rapid changes in sedimentation are interpreted as early successional “weed trees” transitional to but more primitive than the modern subclass Rosidae. Apparently related palmately lobed, palinactinodromous leaves which develop rigidly percurrent tertiary venation and become abundant in uppermost Potomac stream margin deposits (latest Albian-early Cenomanian?) are interpreted as riparian trees ancestral to the order Hamamelidales. Comparisons of dated pollen floras of other regions indicate that one major subgroup of angiosperms, tricolpate-producing dicots (i.e., excluding Magnoliidae of Takhtajan) originated in the Aptian of Africa-South America at a time of increasing aridity and migrated poleward into Laurasia and Australasia. However, the earlier (Barremian) monosulcate phase of the angiosperm record is represented equally in Africa-South America and Laurasia before marked climatic differentiation between the two areas. These trends are considered consistent with the hypothesis that the angiosperms originated as small-leafed shrubs of seasonally arid environments, and underwent secondary expansion of leaf area and radiated into consecutively later successional stages and aquatic habitats after entering mesic regions as riparian “weeds,” as opposed to the concept that they arose as trees of mesic forest environments.

The molecular fossil record of oleanane and its relation to angiosperms.

Oleanane has been reported in Upper Cretaceous and Tertiary source rocks and their related oils and has been suggested as a marker for flowering plants. Correspondence of oleanane concentrations relative to the ubiquitous microbial marker 17α-hopane with angiosperm diversification (Neocomian to Miocene) suggests that oleanane concentrations in migrated petroleum can be used to identify the maximum age of unknown or unavailable source rock. Rare occurrences of pre-Cretaceous oleanane suggest either that a separate lineage leads to the angiosperms well before the Early Cretaceous or that other plant groups have the rarely expressed ability to synthesize oleanane precursors.

Phylogenetic evidence for the herbaceous origin of angiosperms

The ancestral angiosperm is commonly interpreted as an arborescent to shrubby magnolialean with large, multiparted, complex flowers. We examined this hypothesis using a phylogenetic analysis of new and reevaluated characters polarizabled with outgroup comparison. Our cladistic analysis of basal angiosperms placed the nonmagnolialeanChloranthaceae andPiperaceae at the bottom of the tree. We further inferred the probable ancestral states of characters not polarizable with outgroup comparison by examining their distribution among taxa at the base of our cladogram. The sum of ancestral character states suggests that the protoangiosperm was a diminutive, rhizomatous to scrambling perennial herb, with small, simple flowers.

Plant and mammal diversity in the Paleocene to early Eocene of the Bighorn Basin

Abstract Abundant plant and vertebrate fossils have been recovered from fluvial sediments deposited in the Bighorn Basin, Wyoming, during the first 13 m.y. of the Tertiary. Here we outline and discuss changes in the composition and diversity of floras and faunas during this period, which includes the recovery of terrestrial ecosystems from the K/T boundary extinctions, and later, during the Paleocene-Eocene transition, the greatest global warming of the Cenozoic. Floral diversity has been studied at three levels of spatial resolution: sub-local (at individual collecting sites), local (along a single bed or stratigraphic horizon), and basin-wide (regional). Sub-local diversity shows a moderate increase from the early to late Paleocene, followed by a decrease across the Paleocene/Eocene boundary, then an increase into the later early Eocene. Local heterogeneity was lower in Paleocene backswamp floras, although distinct groups of species dominated in different local fluvial settings such as backswamps and alluvial ridges. Heterogeneity of backswamp forests increased by about 65% from the early to late Wasatchian (early Eocene). The number of plant species inferred from the Bighorn Basin dataset rose gradually from the Puercan to an early Clarkforkian peak of about 40 species, declined sharply to about 25 species by the Clarkforkian/Wasatchian boundary, then rose through the Wasatchian to about 50 species. A regional analysis of mammalian genera shows high turnover and a rapidly increasing number of genera within a million years of the K/T boundary (10–50 genera), a slight decline to 40 genera by the early Clarkforkian, then an increase from 40 to 75 genera by the late Wasatchian. Our analyses found no major extinctions in mammals during the Paleocene and early Eocene in the Bighorn Basin, but a one-third decrease in the number of plant species at about the Paleocene/Eocene boundary. Rates of taxonomic turnover were much higher for mammals than plants. The diversity trends for plants and mammals show little congruence, implying that the two groups responded in a very different manner to post K/T extinction opportunities. There is also little congruence between plant diversity levels and change in mean annual temperature (MAT) as inferred from foliar physiognomy.

An Aptian Plant with Attached Leaves and Flowers: Implications for Angiosperm Origin

Recent phylogenetic studies and fossil finds support a new view of the ancestral angiosperm. A diminutive fossil angiosperm from the Aptian of Australia has attached leaves, with intermediate pinnate-palmate, low-rank venation, and lateral axes bearing pistillate organs subtended by bracts and bracteoles that are the oldest direct evidence of flowers. A variety of data suggests a similar morphology for the ancestral angiosperm. This hypothesis explains similarities between rhizomatous to herbaceous Magnoliidae and basal monocots, scarcity of early agniosperm wood, and lack of recognition of earlier remains.

Carbon isotope evidence implying high O2/CO2 ratios in the Permo-Carboniferous atmosphere

Abstract Theoretical models predict a marked increase in atmospheric O2 to ∼35% during the Permo-Carboniferous (∼300 Ma) occurring against a low (∼0.03%) CO2 level. An upper O2 value of 35%, however, remains disputed because ignition data indicate that excessive global forest fires would have ensued. This uncertainty limits interpretation of the role played by atmospheric oxygen in Late Paleozoic biotic evolution. Here, we describe new results from laboratory experiments with vascular land plants that establish that a rise in O2 to 35% increases isotopic fractionation (Δ13C) during growth relative to control plants grown at 21% O2. Despite some effect of the background atmospheric CO2 level on the magnitude of the increase, we hypothesize that a substantial Permo-Carboniferous rise in O2 could have imprinted a detectable geochemical signature in the plant fossil record. Over 50 carbon isotope measurements on intact carbon from four fossil plant clades with differing physiological ecologies and ranging in age from Devonian to Cretaceous reveal a substantial Δ13C anomaly (5‰) occurring between 300 and 250 Ma. The timing and direction of the Δ13C excursion is consistent with the effects of a high O2 atmosphere on plants, as predicted from photosynthetic theory and observed in our experiments. Preliminary calibration of the fossil Δ13C record against experimental data yields a predicted O2/CO2 mixing ratio of the ancient atmosphere consistent with that calculated from long-term models of the global carbon and oxygen cycles. We conclude that further work on the effects of O2 in the combustion of plant materials and the spread of wildfire is necessary before existing data can be used to reliably set the upper limit for paleo-O2 levels.

Ecological conservatism in the “living fossil” Ginkgo

Abstract The living species Ginkgo biloba is phylogenetically isolated, has a relictual distribution, and is morphologically very similar to Mesozoic and Cenozoic congenerics. To investigate what adaptations may have allowed this lineage to persist with little or no morphological change for over 100 Myr, we analyzed both sedimentological and floral data from 51 latest Cretaceous to middle Miocene Ginkgo-bearing fossil plant sites in North America and northern Europe. The resulting data indicate that throughout the late Cretaceous and Cenozoic Ginkgo was largely confined to disturbed streamside and levee environments, where it occurred with a consistent set of other plants. These inferred habitats are surprising because the life-history traits of Ginkgo (e.g., slow growth rate, late reproductive maturity, extended reproductive cycle, large and complex seeds, large and slowly developing embryos) are counter to those considered advantageous in modern disturbed habitats. Many flowering plant lineages first appeared or became common in disturbed riparian habitats, and are inferred to have had reproductive and growth traits (e.g., rapid reproduction, small easily dispersed seeds, rapid growth) suited to such habitats. Paleoecological inferences based on both morphology and sedimentary environments thus support the idea that Ginkgo was displaced in riparian habitats by angiosperms with better adaptations to frequent disturbance.

Evidence for and Implications of an Herbaceous Origin for Angiosperms

For over a century, botanists have speculated on the ancestral morphology of the angiosperms and on the adaptive characteristics that led to their success. Most discussions have centered on the ancestral form of the flower and associated organs. At present, there are two major alternative views regarding the morphology of the first angiosperm. The first of these, which we term the Magnolialean hypothesis, is concordant with the Anthostrobilus or Euanthial floral hypothesis (Fig. 8.1) of Arber and Parkin (1907) and pictures early angiosperms as having been woody shrubs or small trees with large, complex, multiparted flowers. Living species regarded as similar to the archetype are members of the winteroids and Magnoliales (Fig. 11.1 and 11.2). The second view parallels the Pseudanthial hypothesis (Fig. 8.1) of Wettstein (1907a). In this formulation, the ancestral angiosperm is perceived as a rhizomatous herb with small, simple flowers as in living herbaceous magnoliids such as Chloranthaceae and Piperaceae.

Burning of forest materials under late Paleozoic high atmospheric oxygen levels

Theoretical models suggest that atmospheric oxygen reached concentrations as high as 35% O2 during the past 550 m.y. Previous burning experiments using strips of paper have challenged this idea, concluding that ancient wildfires would have decimated plant life if O2 significantly exceeded its present level of 21%. New thermochemistry and flame-spread experiments using natural fuels contradict these results and indicate that sustained burning of forest fuels at moisture contents common to living plants does not occur between 21% and 35% O2. Therefore, the fires under atmospheres with high oxygen concentrations would not have prevented the persistence of plant communities. Times of high O2 also agree with observations of concurrent fire-resistant plant morphology, large insects, and high concentrations of fossil charcoal.

Leaf economic traits from fossils support a weedy habit for early angiosperms

Many key aspects of early angiosperms are poorly known, including their ecophysiology and associated habitats. Evidence for fast-growing, weedy angiosperms comes from the Early Cretaceous Potomac Group, where angiosperm fossils, some of them putative herbs, are found in riparian depositional settings. However, inferences of growth rate from sedimentology and growth habit are somewhat indirect; also, the geographic extent of a weedy habit in early angiosperms is poorly constrained. Using a power law between petiole width and leaf mass, we estimated the leaf mass per area (LMA) of species from three Albian (110-105 Ma) fossil floras from North America (Winthrop Formation, Patapsco Formation of the Potomac Group, and the Aspen Shale). All LMAs for angiosperm species are low (<125 g/m(2); mean = 76 g/m(2)) but are high for gymnosperm species (>240 g/m(2); mean = 291 g/m(2)). On the basis of extant relationships between LMA and other leaf economic traits such as photosynthetic rate and leaf lifespan, we conclude that these Early Cretaceous landscapes were populated with weedy angiosperms with short-lived leaves (<12 mo). The unrivalled capacity for fast growth observed today in many angiosperms was in place by no later than the Albian and likely played an important role in their subsequent ecological success.