Cenozoic seeds of Vitaceae reveal a deep history of extinction and dispersal in the Neotropics.

The remarkably diverse plant communities of the Neotropics are the result of diversification driven by multiple biotic (for example, speciation, extinction and dispersal) and abiotic (for example, climatic and tectonic) processes. However, in the absence of a well-preserved, thoroughly sampled and critically assessed fossil record, the associated processes of dispersal and extinction are poorly understood. We report an exceptional case study documenting patterns of extinction in the grape family (Vitaceae Juss.) on the basis of fossil seeds discovered in four Neotropical palaeofloras dated between 60 and 19 Ma. These include a new species that provides the earliest evidence of Vitaceae in the Western Hemisphere. Eight additional species reveal the former presence of major clades of the family that are currently absent from the Neotropics and elucidate previously unknown dispersal events. Our results indicate that regional extinction and dispersal have substantially impacted the evolutionary history of Vitaceae in the Neotropics. They also suggest that while the Neotropics have been dynamic centres of diversification through the Cenozoic, extant Neotropical botanical diversity has also been shaped by extensive extinction over the past 66 million years.

A Pliocene-Pleistocene continental biota from Venezuela.

The Pliocene-Pleistocene transition in the Neotropics is poorly understood despite the major climatic changes that occurred at the onset of the Quaternary. The San Gregorio Formation, the younger unit of the Urumaco Sequence, preserves a fauna that documents this critical transition. We report stingrays, freshwater bony fishes, amphibians, crocodiles, lizards, snakes, aquatic and terrestrial turtles, and mammals. A total of 49 taxa are reported from the Vergel Member (late Pliocene) and nine taxa from the Cocuiza Member (Early Pleistocene), with 28 and 18 taxa reported for the first time in the Urumaco sequence and Venezuela, respectively. Our findings include the first fossil record of the freshwater fishes Megaleporinus, Schizodon, Amblydoras, Scorpiodoras, and the pipesnake Anilius scytale, all from Pliocene strata. The late Pliocene and Early Pleistocene ages proposed here for the Vergel and Cocuiza members, respectively, are supported by their stratigraphic position, palynology, nannoplankton, and 86Sr/88Sr dating. Mammals from the Vergel Member are associated with the first major pulse of the Great American Biotic Interchange. In contrast to the dry conditions prevailing today, the San Gregorio Formation documents mixed open grassland/forest areas surrounding permanent freshwater systems, following the isolation of the northern South American basin from western Amazonia. These findings support the hypothesis that range contraction of many taxa to their current distribution in northern South America occurred rapidly during at least the last 1.5 million years.

Extinction at the end-Cretaceous and the origin of modern Neotropical rainforests.

The end-Cretaceous event was catastrophic for terrestrial communities worldwide, yet its long-lasting effect on tropical forests remains largely unknown. We quantified plant extinction and ecological change in tropical forests resulting from the end-Cretaceous event using fossil pollen (>50,000 occurrences) and leaves (>6000 specimens) from localities in Colombia. Late Cretaceous (Maastrichtian) rainforests were characterized by an open canopy and diverse plant-insect interactions. Plant diversity declined by 45% at the Cretaceous-Paleogene boundary and did not recover for ~6 million years. Paleocene forests resembled modern Neotropical rainforests, with a closed canopy and multistratal structure dominated by angiosperms. The end-Cretaceous event triggered a long interval of low plant diversity in the Neotropics and the evolutionary assembly of today's most diverse terrestrial ecosystem.

Phloem networks in leaves.

The survival of all vascular plants depends on phloem and xylem, which comprise a hydraulically coupled tissue system that transports photosynthates, water, and a variety of other molecules and ions. Although xylem hydraulics has been extensively studied, until recently, comparatively little is known quantitatively about the phloem hydraulic network and how it is functionally coupled to the xylem network, particularly in photosynthetic leaves. Here, we summarize recent advances in quantifying phloem hydraulics in fully expanded mature leaves with different vascular architectures and show that (1) the size of phloem conducting cells across phylogenetically different taxa scales isometrically with respect to xylem conducting cell size, (2) cell transport areas and lengths increase along phloem transport pathways in a manner that can be used to model Münch's pressure-flow hypothesis, and (3) report observations that invalidate da Vinci's and Murray's hydraulic models as plausible constructs for understanding photosynthate transport in the leaf lamina.

Eocene lantern fruits from Gondwanan Patagonia and the early origins of Solanaceae.

The nightshade family Solanaceae holds exceptional economic and cultural importance. The early diversification of Solanaceae is thought to have occurred in South America during its separation from Gondwana, but the family's sparse fossil record provides few insights. We report 52.2-million-year-old lantern fruits from terminal-Gondwanan Patagonia, featuring highly inflated, five-lobed calyces, as a newly identified species of the derived, diverse New World genus Physalis (e.g., groundcherries and tomatillos). The fossils are considerably older than corresponding molecular divergence dates and demonstrate an ancient history for the inflated calyx syndrome. The derived position of these early Eocene fossils shows that Solanaceae were well diversified long before final Gondwanan breakup.

The scaling of the hydraulic architecture in poplar leaves.

Although much is known about the hydraulics of xylem, the hydraulic interconnectivity and dimensional scaling of phloem with respect to xylem in leaves has not been adequately studied to test alternative hydraulic architectural rules such as da Vinci's rule or Murray's rule, or physiological models such as Münch's Pressure Flow hypothesis. Using confocal and electron microscopy as well as mathematical analyses, we examined the hydraulic architecture of the mature leaves of the model species Populus tremula × alba across all seven hierarchical orders of the vascular branching. We show that: phloem and xylem conductive areas increase from minor to major veins; the sum of the conductive areas for each vein order increases exponentially from major to minor veins; the volume of individual sieve tube and vessel members increases from minor to major veins; and phloem conductive area scales isometrically with respect to xylem area across all vein orders. The application of first principles to our data shows that conductive areas scale according to da Vinci's rule and not according to Murray's rule, and that the phloem network in poplar leaves can generate the pressure gradient envisioned in Münch's hypothesis.

The hydraulic architecture of Ginkgo leaves.

PREMISE OF THE STUDY: The hydraulics of xylem has been widely studied in numerous species and organ types. However, comparatively little is known about how phloem and xylem are hydraulically coupled or about many of the basic structural properties of phloem (such as conducting cell numbers and conductive areas), which nevertheless have direct bearing on understanding phloem loading and unloading. METHODS: Using a combination of light, epifluorescence, confocal, and transmission electron microscopy, we quantified the hydraulic architecture of Ginkgo biloba leaf laminae and examined the scaling relationships between phloem and xylem in five fully mature leaves. KEY RESULTS: The conductive areas and lengths of sieve cells and tracheids increase basipetally toward the petiole in a manner that is consistent with Münch's pressure flow hypothesis for phloem transport. This trend holds true for individual veins, the sum of conductive areas across all veins at any distance from the petiole, and for individual sieve cells and tracheids. Further, the conductive areas of phloem and xylem are isometrically correlated across the entire vasculature of the leaf lamina. The data for conducting cell areas do not conform with the predictions of the hydraulic models of da Vinci and Murray. CONCLUSIONS: The scaling of Ginkgo lamina hydraulics complies with that observed in leaves of other gymnosperms and most angiosperms and is inconsistent with theoretical models that assume that the volume of transported incompressible fluids is conserved.

Spatiotemporal distribution of essential elements through Populus leaf ontogeny.

We examined the spatiotemporal distribution and accumulation of calcium (Ca), potassium (K), and zinc (Zn) during the growth and maturation of grey poplar (Populus tremula × alba) leaves covering plastochrons 01 through 10. This period spans the sugar sink-to-source transition and requires coordinated changes of multiple core metabolic processes that likely involve alterations in essential and non-essential element distributions as tissues mature and effect a reversal in phloem flow direction. Whole-leaf elemental maps were obtained from dried specimens using micro X-ray fluorescence spectroscopy. Additional cross-sections of fresh leaves were scanned to check for tissue specificity in element accumulation. The anatomical distribution of Zn and K remains relatively consistent throughout leaf development; Ca accumulation varied across leaf developmental stages. The basipetal allocation of Ca to the leaf mesophyll matched spatially and temporally the sequence of phloem maturation, positive carbon balance, and sugar export from leaves. The accumulation of Ca likely reflects the maturation of xylem in minor veins and the enhancement of the transpiration stream. Our results independently confirm that xylem and phloem maturation are spatially and temporally coordinated with the onset of sugar export in leaves.

A Late Cretaceous Piper (Piperaceae) from Colombia and diversification patterns for the genus.

PREMISE OF THE STUDY: Documented fossil floras in the neotropics are sparse, yet their records provide evidence on the spatial and temporal occurrence of taxa, allowing for testing of biogeographical and diversification scenarios on individual lineages. A new fossil Piper from the Late Cretaceous of Colombia is described here, and its importance for assessing diversification patterns in the genus is addressed. METHODS: Leaf architecture of 32 fossil leaf compressions from the Guaduas Formation was compared with that of 294 extant angiosperm species. The phylogenetic position of the fossil named Piper margaritae sp. nov. was established based on leaf traits and a molecular scaffold of Piper. The age of the fossil was independently used as a calibration point for divergence time estimations. KEY RESULTS: Natural affinities of P. margaritae to the Schilleria clade of Piper indicate that the genus occurred in tropical America by the Late Cretaceous. Estimates of age divergence and lineage accumulation reveal that most of the extant diversity of the genus accrued during the last ∼30 Myr. CONCLUSIONS: The recent radiation of Piper is coeval with both the Andean uplift and the emergence of Central America, which have been proposed as important drivers of diversity. This pattern could exemplify a recurrent theme among many neotropical plant lineages.

Insect leaf-chewing damage tracks herbivore richness in modern and ancient forests.

The fossil record demonstrates that past climate changes and extinctions significantly affected the diversity of insect leaf-feeding damage, implying that the richness of damage types reflects that of the unsampled damage makers, and that the two are correlated through time. However, this relationship has not been quantified for living leaf-chewing insects, whose richness and mouthpart convergence have obscured their value for understanding past and present herbivore diversity. We hypothesized that the correlation of leaf-chewing damage types (DTs) and damage maker richness is directly observable in living forests. Using canopy access cranes at two lowland tropical rainforest sites in Panamá to survey 24 host-plant species, we found significant correlations between the numbers of leaf chewing insect species collected and the numbers of DTs observed to be made by the same species in feeding experiments, strongly supporting our hypothesis. Damage type richness was largely driven by insect species that make multiple DTs. Also, the rank-order abundances of DTs recorded at the Panamá sites and across a set of latest Cretaceous to middle Eocene fossil floras were highly correlated, indicating remarkable consistency of feeding-mode distributions through time. Most fossil and modern host-plant pairs displayed high similarity indices for their leaf-chewing DTs, but informative differences and trends in fossil damage composition became apparent when endophytic damage was included. Our results greatly expand the potential of insect-mediated leaf damage for interpreting insect herbivore richness and compositional heterogeneity from fossil floras and, equally promisingly, in living forests.

First record of Todea (Osmundaceae) in South America, from the early Eocene paleorainforests of Laguna del Hunco (Patagonia, Argentina).

PREMISE OF THE STUDY: The early Eocene Laguna del Hunco caldera-lake paleoflora (ca. 52 Ma) from Chubut Province, Argentina, is notably diverse and includes many conifer and angiosperm lineages that are extinct in South America but extant in Australasian rainforests. No ferns have been previously described from Laguna del Hunco. We describe and interpret a new species of fossil Osmundaceae based on fertile and sterile pinnae. • METHODS: The fossil specimens were compared with other extant and fossil Osmundaceae based on living and herbarium material and published descriptions. A morphological matrix based on 29 characters was constructed for 17 living species in Osmundaceae, four species assigned to the fossil genus Todites, and the new fossil species. Phylogenetic analyses were conducted under parsimony using morphology and total evidence matrices. • KEY RESULTS: Both the new fossil and the Todites species were consistently resolved within the leptopteroid clade of Osmundaceae, and the new species resolved in a clade with the two living Todea species, which are now restricted to Australia, New Guinea, New Zealand, and southern Africa. • CONCLUSIONS: Todea amissa sp. nov. is the first record of Todea, living or fossil, in South America and only the second fossil record worldwide. The distribution of extant Todea on Gondwanan continents other than South America is broadly shared with other taxa from Laguna del Hunco, further indicating that a large component of this flora represents a Gondwanic biome that is no longer found on the South American continent.

Phytogeographic implications of fossil endocarps of Menispermaceae from the Paleocene of Colombia.

PREMISE OF THE STUDY: Fossil leaves of Menispermaceae were previously described from the Paleocene of Colombia. Because of strong homoplasy of leaf characters, the fossils could not be placed more specifically within recognized clades, and additional data were needed to specify intrafamilial and paleogeographic relationships during the Paleocene. METHODS: Fossil endocarps of Menispermaceae were collected from the Cerrejón Formation, the recently discovered Bogotá flora, and Wyoming (∼60 Ma). We surveyed the endocarp morphology of almost all extant genera, conducted character optimization, a molecular scaffold analysis, and critically reviewed the related fossil genera. KEY RESULTS: Parallel syndromes of fruit characters have appeared in unrelated clades of the family according to current phylogenetic reconstructions. However, mapping selected endocarp characters across those clades that contain horseshoe-shaped endocarps facilitates identification and phylogenetic assessment of the fossils. Three fossil species are recognized. One of them belongs to the extant genus Stephania, which today grows only in Africa and Australasia. Palaeoluna gen. nov. is placed within the pantropical clade composed of extant Stephania, Cissampelos, and Cyclea; this morphogenus is also recognized from the Paleocene of Wyoming. Menispina gen. nov. shows similarity with several unrelated clades. CONCLUSIONS: The new fossils from Colombia reveal a complex paleobiogeographic history of the recognized clades within Menispermaceae, suggesting a more active exchange among neotropical, paleotropical, North American, and European paleoforests than previously recognized. In addition, the new fossils indicate that neotropical forests were an important biome for the radiation and dispersal of derived lineages in Menispermaceae after the Cretaceous-Paleogene boundary.

Paleocene Malvaceae from northern South America and their biogeographical implications.

PREMISE OF THE STUDY: The clade Bombacoideae + Malvoideae ('Malvatheca group' sensu Baum et al.) in Malvaceae comprises a mostly tropical lineage with derived taxa that now thrive in higher latitudes. The sparse fossil record, especially for Malvoideae, obscures interpretations of past distributions. We describe fossil leaves of Malvoideae from the middle-late Paleocene Cerrejón Formation in Colombia, which contains evidence for the earliest known neotropical rainforest. METHODS: Fifty-six leaf compressions belonging to Malvaceae were collected from the Cerrejón Formation in northern Colombia. Leaf architectural characters were scored and optimized for 81 genera of Malvaceae. Synapomorphic characters and unique character combinations support natural affinities for the fossil leaves. Fossil pollen from the same formation was also assessed. KEY RESULTS: Despite convergence of overall leaf architecture among many Malvaceae, Malvaciphyllum macondicus sp. nov. can be assigned to the clade Eumalvoideae because of distal and proximal bifurcations of the costal secondary and agrophic veins, a synapomorphy for this clade. CONCLUSIONS: The leaf compressions, the oldest fossils for Eumalvoideae, indicate a minimum divergence time of 58-60 Ma, older than existing estimates from molecular analyses of living species. The abundance of eumalvoid leaves and of bombacoid pollen in the midlate Paleocene of Colombia suggests that the Malvatheca group (Malvoideae + Bombacoideae) was already a common element in neotropical forests and does not support an Australasian origin for Eumalvoideae.