David L. Dilcher

Approaches to the identification of angiosperm leaf remains

During the past 125 years the history of early angiosperms, interpreted through the fossil leaf record has been largely an exercise in paleofloristic studies, ignoring evolution. Imprecise identifications of ancient leaves “matched” to extant genera and families have been used as the basis for reconstructions of paleocommunities and paleoclimates. However, as the result of careful morphological studies of leaf form, venation and cuticular features new insights into the evolution of angiosperms are now available. In this paper considerations are given to the usefulness and shortcomings of leaf form, venation and cuticular analysis as diagnostic tools of plant identification. Many techniques for the study of the morphology of modern and fossil leaves are included in this paper as well as tables outlining features of leaf venation and the epidermis. Careful morphological studies of leaf form (such as the venation and epidermal characters emphasized in this paper) will provide better understanding of the relationships of living angiosperms and transform the fossil leaf record into useful data that can be used to study the evolution of the angiosperms.KurzfassungDie Geschichte der frühen Angiospermen, wie sie sich in der Überlieferung durch Blattabdrücke darstellt, wurde in den letzten 125 Jahren hauptsächlich paläofloristisch betrachtet und die Evolution vernachlässigt. Ungenaue Bestimmungen von fossilen Blättern, die die Fossilien mit lebenden Gattungen und Familien in Verbindung brachten, wurden benutzt, um sowohl fossile Pflanzengesellschaften als auch klimatische Bedingungen zu rekonstruieren. Sorgfältige Untersuchungen jüngeren Datums von Blattform, Aderungsverlauf und Kutikula haben ein neues Verständnis der AngiospermenEvolution möglich gemacht. In dieser Veröffentlichung werden die Möglichkeiten und Grenzen der Analyse von Blattform, Aderung und Kutikula als Hilfsmittel zur Bestimmung dargestellt. Es werden zahlreiche Methoden Zur Untersuchung der Morphologie rezenter und fossiler Blätter diskutiert und wesentliche Eigenschaften von Aderung und Epidermis in Form von Tabellen zusammengestellt. Sorgfältige morphologische Untersuchungen von Angiospermenblättern, wie sie in dieser Arbeit diskutiert sind, werden zu einem besseren Verständnis der Verwandtschaft rezenter Angiospermen untereinander führen und Daten von fossilen Blättern liefern, die direkt zur Entzifferung der Angiospermen-Evolution beitragen werden.ResumenDurante los pasados 125 años, la historia de los angiospermos primitivos, interpretada por las huellas de hojas fosilizadas, ha sido mayormente un ejercicio en los estudios paleoflorísticos, ignorando la evolución. Identificaciones imprecisas de hojas primitivas, comparadas con géneros y familias existentes, han sido usadas como la base para reconstrucciones de paleocomunidades y paleoclimas. Sin embargo, como el resultado de diligentes estudios morfológicos de formas de hojas, disposiciones de las nervosidades, y características cuticulares, han surgido nuevos informes sobre la evolución de angiospermos. En este trabajo, se dan consideraciones a las utilidades y las insuficiencias de forma de hojas, disposiciones de las nervosidades, y análisis cuticulares como instrumentos diagnósticos pára investigaciones vegetales. Se incluyen en este trabajo muchas técnicas para el estudio de la morfología hojas existentes y fosilizadas así como tablas bosquejando los rasgos de la disposición de las nervosidades y epidérmis de hojas. Los diligentes estudios morfológicos de formas de hojas (como la disposición de las nervosidades y características epidérmicas acentuadas en este trabajo) nos darán un mejor conocimiento de las relaciones entre angiospermos vivos y transformarán las huellas de hojas fosilizadas en datos utiles que se pueden usar para estudiar la evolución de los angiospermos.РЕФЕРАТВ теченив последних 125 лет история ранних покрытосеменных, истолкованная на основе отпечатков ископаемых листьев, составляла в значительной степени пренебрегающее эволюцией упражнение в области палеофлористики. Неточно определенные древние листья, “подогнанные” под сохранившиеся роды и семейства, служили основой для восстановления палеосообществ и палеоклиматов. Однако в результате тщательных морфологических исследований формы листа, жилкования и кутикулярных признаков создались новые понятия об эволюции покрытосеменных. В настоящем докладе разбираются полезность и недостатки формы листа, жилкования и особенностей кутикулы в качестве диагностических признаков при распознавании растений. В докладе упоминается множество различных технических приемов, используемых при исследовании морфологии современных и ископаемых листьев, а также и схемы, дающие в общих чертах особенности листового жилко вания и эпидермы. Тщательные морфологические исследования формы листа (типа выделенных в настоящем докладе жилкования и признаков эпидермы) обеспечат более глубокое понимание соотношений современных покрытосеменных и превратят сведения об ископаемых листьях в полезные данные, которые можно будет использовать при исследовании эволюции покрытосеменных.

The impact of Miocene atmospheric carbon dioxide fluctuations on climate and the evolution of terrestrial ecosystems.

The Miocene is characterized by a series of key climatic events that led to the founding of the late Cenozoic icehouse mode and the dawn of modern biota. The processes that caused these developments, and particularly the role of atmospheric CO2 as a forcing factor, are poorly understood. Here we present a CO2 record based on stomatal frequency data from multiple tree species. Our data show striking CO2 fluctuations of ≈600–300 parts per million by volume (ppmv). Periods of low CO2 are contemporaneous with major glaciations, whereas elevated CO2 of 500 ppmv coincides with the climatic optimum in the Miocene. Our data point to a long-term coupling between atmospheric CO2 and climate. Major changes in Miocene terrestrial ecosystems, such as the expansion of grasslands and radiations among terrestrial herbivores such as horses, can be linked to these marked fluctuations in CO2.

Paleoatmospheric Signatures in Neogene Fossil Leaves

An increase in the atmospheric carbon dioxide (CO2) concentration results in a decrease in the number of leaf stomata. This relation is known both from historical observations of vegetation over the past 200 years and from experimental manipulations of microenvironments. Evidence from stomatal frequencies of fossil Quercus petraea leaves indicates that this relation can be applied as a bioindicator for changes in paleoatmospheric CO2 concentrations during the last 10 million years. The data suggest that late Neogene CO2 concentrations fluctuated between about 280 and 370 parts per million by volume.

Oak leaves as biosensors of late Neogene and early Pleistocene paleoatmospheric CO2 concentrations

Abstract Complementary to the interpretation of δ 13 C values of biogenic carbonate and sedimentary organic carbon in marine sediments, paleoatmospheric CO 2 levels can be estimated by considering the inverse relationship between atmospheric CO 2 concentration and stomatal parameters (frequency, size) on leaves of land plants. In woody plants, the significance of this (species-specific) physiological response to changing CO 2 regimes is now repeatedly confirmed, both experimentally and from historical sequences of leaves collected since the onset of industrialization. A corollary of this relationship is that analysis of stomatal parameters on fossil leaves has the potential of determining changes in paleoatmospheric CO 2 levels at different time scales. Well-preserved cuticle remains of oak leaves from late Miocene, Pliocene and early Pleistocene sediments of the Lower Rhine Embayment (Germany, The Netherlands) give promise of extending the record of stomatal frequency response to the last 10 Ma. During intervals with warm-temperate to subtropical climatic conditions, oak leaves are characterized by a high stomatal resistance (or low conductance) to CO 2 diffusion and low stomatal frequencies; during cooler intervals we observe an opposite picture. Comparison with historical relations between CO 2 concentration and stomatal properties suggests that paleoatmospheric CO 2 concentrations were not significantly higher than during the last 200 years and fluctuated several times between 280 and 370 ppmv in covariation with contrasting regional climatic conditions. On a global scale, intervals with reduced CO 2 levels match glacial pulses characterized by the occurrence of ice-rafted detritus in high-latitude oceanic sediments.

Life in the end-Permian dead zone.

The fossil record of land plants is an obvious source of information on the dynamics of mass extinctions in the geological past. In conjunction with the end-Permian ecological crisis, ≈250 million years ago, palynological data from East Greenland reveal some unanticipated patterns. We document the significant time lag between terrestrial ecosystem collapse and selective extinction among characteristic Late Permian plants. Furthermore, ecological crisis resulted in an initial increase in plant diversity, instead of a decrease. Paradoxically, these floral patterns correspond to a “dead zone” in the end-Permian faunal record, characterized by a paucity of marine invertebrate megafossils. The time-delayed, end-Permian plant extinctions resemble modeled “extinction debt” responses of multispecies metapopulations to progressive habitat destruction.

Correlations of climate and plant ecology to leaf size and shape: potential proxies for the fossil record

The sizes and shapes (physiognomy) of fossil leaves are widely applied as proxies for paleoclimatic and paleoecological variables. However, significant improvements to leaf-margin analysis, used for nearly a century to reconstruct mean annual temperature (MAT), have been elusive; also, relationships between physiognomy and many leaf ecological variables have not been quantified. Using the recently developed technique of digital leaf physiognomy, correlations of leaf physiognomy to MAT, leaf mass per area, and nitrogen content are quantified for a set of test sites from North and Central America. Many physiognomic variables correlate significantly with MAT, indicating a coordinated, convergent evolutionary response of fewer teeth, smaller tooth area, and lower degree of blade dissection in warmer environments. In addition, tooth area correlates negatively with leaf mass per area and positively with nitrogen content. Multiple linear regressions based on a subset of variables produce more accurate MAT estimates than leaf-margin analysis (standard errors of ±2 vs. ±3°C); improvements are greatest at sites with shallow water tables that are analogous to many fossil sites. The multivariate regressions remain robust even when based on one leaf per species, and the model most applicable to fossils shows no more signal degradation from leaf fragmentation than leaf-margin analysis.

A Probable Pollination Mode Before Angiosperms: Eurasian, Long-Proboscid Scorpionflies

Long-Lost Pollinators The rise of angiosperms in the Early Cretaceous (∼140 million years ago) was accompanied by coevolution of a variety of insects, including flies, bees, and wasps required for pollination. Ren et al. (p. 840; see the Perspective by Ollerton and Coulthard) show that three families of scorpionflies had already evolved specialized mouth parts for feeding on the nectar of gymnosperms, as early as the Middle Jurassic (∼170 million years ago). The diversity and specialization of these insects and related plant structures suggests that they were also involved in pollination. These families died out later in the Cretaceous as angiosperms began to dominate. Prior to the coevolution of angiosperms and pollinating insects, scorpionflies may have been pollinating gymnosperms. The head and mouthpart structures of 11 species of Eurasian scorpionflies represent three extinct and closely related families during a 62-million-year interval from the late Middle Jurassic to the late Early Cretaceous. These taxa had elongate, siphonate (tubular) proboscides and fed on ovular secretions of extinct gymnosperms. Five potential ovulate host-plant taxa co-occur with these insects: a seed fern, conifer, ginkgoopsid, pentoxylalean, and gnetalean. The presence of scorpionfly taxa suggests that siphonate proboscides fed on gymnosperm pollination drops and likely engaged in pollination mutualisms with gymnosperms during the mid-Mesozoic, long before the similar and independent coevolution of nectar-feeding flies, moths, and beetles on angiosperms. All three scorpionfly families became extinct during the later Early Cretaceous, coincident with global gymnosperm-to-angiosperm turnover.

Early angiosperm reproduction: An introductory report

Abstract The phylogeny of angiosperms presented by various authors is based principally upon our knowledge of modern plants. The fossil history of flowering plants has had little influence upon current concepts of primitive features of the flower. Several reproductive characters of non-angiospermous plants demonstrate the diversity of flower-like characters common to some extinct major groups of plants. Various Lower and Middle Cretaceous angiosperm reproductive structures illustrate the nature of the early receptacles, carpels and perianth parts. Pteridosperms (seed ferns), which bore separate clusters of ovules and microsporangia are considered a likely ancestral source of the angiosperms. Probable radiations of both diclinous (unisexual), mainly wind-pollinated, and monoclinous (bisexual), mainly insect-pollinated, lines are suggested for the ancestral flowering plants. The primitive flower types are thought to be quite simple with subsequent elaboration and other modifications of the flower, resulting from the adaptive ecological strategies of reproductive mechanisms through time. Insects have played a major role in floral evolution but not to the exclusion of ancient wind-pollinated forms. There have been major and minor shifts of the reproductive ecology in various groups of angiosperms so that the diverse flowers and fruits seen today are the product of reticulate patterns of evolution.

Global CO2 rise leads to reduced maximum stomatal conductance in Florida vegetation

A principle response of C3 plants to increasing concentrations of atmospheric CO2 (CO2) is to reduce transpirational water loss by decreasing stomatal conductance (gs) and simultaneously increase assimilation rates. Via this adaptation, vegetation has the ability to alter hydrology and climate. Therefore, it is important to determine the adaptation of vegetation to the expected anthropogenic rise in CO2. Short-term stomatal opening–closing responses of vegetation to increasing CO2 are described by free-air carbon enrichments growth experiments, and evolutionary adaptations are known from the geological record. However, to date the effects of decadal to centennial CO2 perturbations on stomatal conductance are still largely unknown. Here we reconstruct a 34% (±12%) reduction in maximum stomatal conductance (gsmax) per 100 ppm CO2 increase as a result of the adaptation in stomatal density (D) and pore size at maximal stomatal opening (amax) of nine common species from Florida over the past 150 y. The species-specific gsmax values are determined by different evolutionary development, whereby the angiosperms sampled generally have numerous small stomata and high gsmax, and the conifers and fern have few large stomata and lower gsmax. Although angiosperms and conifers use different D and amax adaptation strategies, our data show a coherent response in gsmax to CO2 rise of the past century. Understanding these adaptations of C3 plants to rising CO2 after decadal to centennial environmental changes is essential for quantification of plant physiological forcing at timescales relevant for global warming, and they are likely to continue until the limits of their phenotypic plasticity are reached.

Early steps of angiosperm–pollinator coevolution

The hypothesis that early flowering plants were insect-pollinated could be tested by an examination of the pollination biology of basal angiosperms and the pollination modes of fossil angiosperms. We provide data to show that early fossil angiosperms were insect-pollinated. Eighty-six percent of 29 extant basal angiosperm families have species that are zoophilous (of which 34% are specialized) and 17% of the families have species that are wind-pollinated, whereas basal eudicot families and basal monocot families more commonly have wind and specialized pollination modes (up to 78%). Character reconstruction based on recent molecular trees of angiosperms suggests that the most parsimonious result is that zoophily is the ancestral state. Combining pollen ornamentation, size, and aperture characteristics and the abundance of single-species pollen clumps of Cenomanian angiosperm-dispersed pollen species from the Dakota Formation demonstrates a dominance of zoophilous pollination (76% versus 24% wind pollination). The zoophilous pollen species have adaptations for pollination by generalist insects (39%), specialized pollen-collecting insects (27%), and other specialized pollinators (10%). These data quantify the presences of more specialized pollination modes during the mid-Cretaceous angiosperm diversification.