Miocene Dipteronia (Sapindaceae) samaras from South Korea and their biogeographical implications.

Dipteronia, now endemic to East Asia, was widely distributed in North America during the Paleogene; however, its fossil records in Asia are scarce and none are of the Neogene. Here, we report the first Neogene Dipteronia samaras from South Korea. The more complete fossil records suggest that Dipteronia possibly originated in either Asia or North America and that its two known lineages have different geographical histories. The Dipteronia sinensis lineage was established in Asia and North America in the Paleocene and reached its maximum range in the Eocene, followed by stepwise range contraction and extirpation in North America, South Korea, and southwestern China, finally becoming endemic to central China. In contrast, the Dipteronia dyeriana lineage might have been restricted to southwestern China, where it originated, indicating historical confinement. The current restricted distribution of Dipteronia possibly resulted from its evolutionary deceleration in a constantly changing environment.

Leaf fossils of Sabalites (Arecaceae) from the Oligocene of northern Vietnam and their paleoclimatic implications.

Recent paleobotanical investigations in Vietnam provide a good opportunity to improve our understanding of the biodiversity and paleoclimatic conditions in the geological past of Southeast Asia. Palms (Arecaceae) are a diverse family of typical thermophilous plants with a relatively low tolerance for freezing. In this study, we describe well-preserved fossil palm leaves from the Oligocene Dong Ho Formation of Hoanh Bo Basin, northern Vietnam. Characters of the fossil leaves, such as a fan-shaped costapalmate lamina, an unarmed petiole, a costa slightly enlarged at the base that then tapers distally into the blade, and well-preserved amphistomatic leaves with cuticles, suggest that they represent a new fossil species, which we herein designate Sabalites colaniae A. Song, T. Su, T. V. Do et Z.K. Zhou sp. nov. Together with other paleontological and palaeoclimatic evidence, we conclude that a warm climate prevailed in northern Vietnam and nearby areas during the Oligocene.

Orographic evolution of northern Tibet shaped vegetation and plant diversity in eastern Asia.

The growth of the Tibetan Plateau throughout the past 66 million years has profoundly affected the Asian climate, but how this unparalleled orogenesis might have driven vegetation and plant diversity changes in eastern Asia is poorly understood. We approach this question by integrating modeling results and fossil data. We show that growth of north and northeastern Tibet affects vegetation and, crucially, plant diversity in eastern Asia by altering the monsoon system. This northern Tibetan orographic change induces a precipitation increase, especially in the dry (winter) season, resulting in a transition from deciduous broadleaf vegetation to evergreen broadleaf vegetation and plant diversity increases across southeastern Asia. Further quantifying the complexity of Tibetan orographic change is critical for understanding the finer details of Asian vegetation and plant diversity evolution.

Fossil fruits of Firmiana and Tilia from the middle Miocene of South Korea and the efficacy of the Bering land bridge for the migration of mesothermal plants.

Determining whether the high-latitude Bering land bridge (BLB) was ecologically suitable for the migration of mesothermal plants is significant for Holarctic phytogeographic inferences. Paleobotanical studies provide a critical source of data on the latitudinal positions of different plant lineages at different times, permitting assessment of the efficacy of the BLB for migration. Here we report exceptionally preserved fossils of Firmiana and Tilia endochrysea from the middle Miocene of South Korea. This represents a new reliable record of Firmiana and the first discovery of the T. endochrysea lineage in the fossil record of Asia. The occurrence of these fossils in South Korea indicates that the two lineages had a distribution that extended much farther north during the middle Miocene, but they were still geographically remote from the BLB. In light of the broader fossil record of Asia, our study shows that, in the middle Miocene, some mesothermal plants apparently inhabited the territory adjacent to the BLB and thus they were possibly capable of utilizing the BLB as a migratory corridor. Some other mesothermal plants, such as Firmiana and the T. endochrysea lineages, however, are restricted to more southern regions relative to the BLB based on current fossil evidence. These lineages may have been ecologically unable to traverse the BLB, which raises questions about the efficacy of the BLB as a universal exchange route for mesothermal plants between Asia and North America during the middle Miocene.

A Middle Eocene lowland humid subtropical "Shangri-La" ecosystem in central Tibet.

Tibet's ancient topography and its role in climatic and biotic evolution remain speculative due to a paucity of quantitative surface-height measurements through time and space, and sparse fossil records. However, newly discovered fossils from a present elevation of ∼4,850 m in central Tibet improve substantially our knowledge of the ancient Tibetan environment. The 70 plant fossil taxa so far recovered include the first occurrences of several modern Asian lineages and represent a Middle Eocene (∼47 Mya) humid subtropical ecosystem. The fossils not only record the diverse composition of the ancient Tibetan biota, but also allow us to constrain the Middle Eocene land surface height in central Tibet to ∼1,500 ± 900 m, and quantify the prevailing thermal and hydrological regime. This "Shangri-La"-like ecosystem experienced monsoon seasonality with a mean annual temperature of ∼19 °C, and frosts were rare. It contained few Gondwanan taxa, yet was compositionally similar to contemporaneous floras in both North America and Europe. Our discovery quantifies a key part of Tibetan Paleogene topography and climate, and highlights the importance of Tibet in regard to the origin of modern Asian plant species and the evolution of global biodiversity.

Three new fossil records of Equisetum (Equisetaceae) from the Neogene of south-western China and northern Vietnam.

Three fossil species of Equisetum (Equisetaceae) were reported from the Neogene of south-western China and northern Vietnam, based on well-preserved rhizomes with tubers. Equisetum cf. pratense Ehrhart from the middle Miocene of Zhenyuan County, Yunnan Province, China is characterised by a bunch of three ovate tubers with longitudinal ridges on the surface. Equisetum yenbaiense A.T. Aung, T. Su, T.V. Do & Z.K. Zhou, sp. nov. from the late Miocene of Yenbai Province, Vietnam is characterised by four bunches of elongate tubers arranged in a whorl on a node. Equisetum yongpingense A.T. Aung, T. Su & Z.K. Zhou, sp. nov. from the late Pliocene of Yunnan is characterised by fibrous roots on most nodes and two to four bunches of large cylindrical tubers arranged in a whorl on a node. Floristic assemblages suggest that these species might have grown near a riverside or lakeshore. These new fossil records improve our understanding of species richness of Equisetum and their distribution range during the Neogene in Asia.

Asclepiadospermum gen. nov., the earliest fossil record of Asclepiadoideae (Apocynaceae) from the early Eocene of central Qinghai-Tibetan Plateau, and its biogeographic implications.

PREMISE: Apocynaceae is common in the fossil record, especially as seed remains from the Neogene of Europe and North America, but rare in Asia. Intrafamilial assignment is difficult due to the lack of diagnostic characters, and new fossil and modern data are needed to understand the paleobiogeography of this group. METHODS: We studied three Apocynaceae seed impressions from the Lower Eocene Niubao Formation, Jianglang village, Bangor County, central Qinghai-Tibetan Plateau. Morphological data from living and fossil species were phylogenetically mapped to enable systematic assignment. RESULTS: We describe a new genus, Asclepiadospermum gen. nov., and two new species, A. marginatum sp. nov. and A. ellipticum sp. nov. These species are characterized by an elliptical seed, a margin surrounding the central part of the seed, and polygonal, irregular, and small epidermal cells, and differ mainly in terms of the size of the margin and the shape of the apex. All these characters indicate that this new genus belongs to the subfamily Asclepiadoideae (Apocynaceae). CONCLUSIONS: These fossils represent the earliest fossil seed records of Asclepiadoideae. Asclepiadospermum indicates a humid tropical to subtropical flora during the early Eocene in central Tibet. Moreover, our discoveries indicate a close floristic connection between Eurasia and Africa during the early Eocene, which expands our knowledge of the floristic linkage between Tibet and other regions at that time.

Stomatal frequency of Quercus glauca from three material sources shows the same inverse response to atmospheric pCO2.

BACKGROUND AND AIMS: The inverse correlation between atmospheric CO2 partial pressure (pCO2) and stomatal frequency in many plants has been widely used to estimate palaeo-CO2 levels. However, apparent discrepancies exist among the obtained estimates. This study attempts to find a potential proxy for palaeo-CO2 concentrations by analysing the stomatal frequency of Quercus glauca (section Cyclobalanopsis, Fagaceae), a dominant species in East Asian sub-tropical forests with abundant fossil relatives. METHODS: Stomatal frequencies of Q. glauca from three material sources were analysed: seedlings grown in four climatic chambers with elevated CO2 ranging from 400 to 1300 ppm; extant samples collected from 14 field sites at altitudes ranging from 142 to 1555 m; and 18 herbarium specimens collected between 1930 and 2011. Stomatal frequency-pCO2 correlations were determined using samples from these three sources. KEY RESULTS: An inverse correlation between stomatal frequency and pCO2 was found for Q. glauca through cross-validation of the three material sources. The combined calibration curves integrating data of extant altitudinal samples and historical herbarium specimens improved the reliability and accuracy of the curves. However, materials in the climatic chambers exhibited a weak response and relatively high stomatal frequency possibly due to insufficient treatment time. CONCLUSIONS: A new inverse stomatal frequency-pCO2 correlation for Q. glauca was determined using samples from three sources. These three material types show the same response, indicating that Q. glauca is sensitive to atmospheric pCO2 and is an ideal proxy for palaeo-CO2 levels. Quercus glauca is a nearest living relative (NLR) of section Cyclobalanopsis fossils, which are widely distributed in the strata of East Asia ranging from the Eocene to Pliocene, thereby providing excellent materials to reconstruct the atmospheric CO2 concentration history of the Cenozoic. Quercus glauca will add to the variety of proxies that can be widely used in addition to Ginkgo and Metasequoia.

Uplift, climate and biotic changes at the Eocene-Oligocene transition in south-eastern Tibet.

The uplift history of south-eastern Tibet is crucial to understanding processes driving the tectonic evolution of the Tibetan Plateau and surrounding areas. Underpinning existing palaeoaltimetric studies has been regional mapping based in large part on biostratigraphy that assumes a Neogene modernization of the highly diverse, but threatened, Asian biota. Here, with new radiometric dating and newly collected plant-fossil archives, we quantify the surface height of part of the south-eastern margin of Tibet in the latest Eocene (∼34 Ma) to be ∼3 km and rising, possibly attaining its present elevation (3.9 km) in the early Oligocene. We also find that the Eocene-Oligocene transition in south-eastern Tibet witnessed leaf-size diminution and a floral composition change from sub-tropical/warm temperate to cool temperate, likely reflective of both uplift and secular climate change, and that, by the latest Eocene, floral modernization on Tibet had already taken place, implying modernization was deeply rooted in the Palaeogene.

A primitive honey bee from the Middle Miocene deposits of southeastern Yunnan, China (Hymenoptera, Apidae).

While fossils of honey bees (Apini: Apis Linnaeus) are comparatively abundant in European Oligocene and Miocene deposits, the available material from Asia is scant and represented by only a handful of localities. It is therefore significant to report a new deposit with a fossil honey bee from southern China. Apis (Synapis) dalica Engel & Wappler, sp. n., is described and figured from Middle Miocene sediments of Maguan County, southeastern Yunnan Province, China. This is the first fossil bee from the Cenozoic of southern China, and is distinguished from its close congeners present at the slightly older locality of Shanwang, Shandong in northeastern China. The species can be distinguished on the basis of wing venation differences from other Miocene Apis.

Warm-cold colonization: response of oaks to uplift of the Himalaya-Hengduan Mountains.

Clarifying the relationship between distribution patterns of organisms and geological events is critical to understanding the impact of environmental changes on organismal evolution. Quercus sect. Heterobalanus is now distributed across the Himalaya-Hengduan Mountains (HHM) and warm lowland in East China, yet how the distribution patterns of this group changed in response to the HHM uplift remains largely unknown. This study examines the effect of tectonic events in the HHM region on the oaks, providing a biological perspective on the geological history of this region. Fifty-six populations of Quercus sect. Heterobalanus were genotyped using four chloroplast DNA regions and nine nuclear simple sequence repeat loci to assess population structure and diversity, supplemented by molecular dating and ancestral area reconstructions. The underlying demographic dynamics were compared using ecological niche models of the species distributions during the last glacial maximum and the present. These analyses illustrate that Quercus sect. Heterobalanus diversified as the HHM uplifted and climatic cooling during the mid-Miocene, colonizing the cold habitats from warm broadleaf mixed forests. Lineages in cold highlands and warm lowlands have diverged as a consequence of local adaptation to diverging climates since the late Miocene. Our results suggest that continuous uplift of the HHM in the late Miocene to early Pliocene accompanied by simultaneous cooling triggered the differentiation of oaks. The biogeography of Quercus sect. Heterobalanus illuminates the geological events responsible for the modern-day HHM.

Pre-dispersal strategies by Quercus schottkyana to mitigate the effects of weevil infestation of acorns.

We investigated how pre-dispersal strategies may mitigate the effects of weevil infestation of acorns in a population of Quercus schottkyana, a dominant oak in Asian evergreen broad-leaved forests, and assess if weevil infestation contributes to low seedling recruitment. We counted the number of acorns produced, daily from the end of August to mid-late November for 9 years from 2006-2014. We also recorded the rate of acorn infestation by weevils and acorn germination rates of weekly collections. Annual acorn production was variable, but particularly low in 2011 and 2013. There was no trade-off between acorn production and acorn dry mass. However, acorns produced later in the season were significantly heavier. For most years: (i) the rate of weevil infestation was negatively density dependent (a greater proportion of acorns died with increased acorn density), (ii) the percentage germination of acorns was positively density dependent (proportionately more acorns germinated with increased density), and (iii) as the season progressed, the percentage of infested acorns declined while germination rates increased. Finally, (iv) maximum acorn production, percentage infestation and percentage germination were asynchronous. Although pre-dispersal mortality is important it is unlikely to be the primary factor leading to low recruitment of oak seedlings.

The oldest Mahonia (Berberidaceae) fossil from East Asia and its biogeographic implications.

Interpretation of the biogeography of the genus Mahonia (Berberidaceae) is limited by the lack of fossil records in East Asia. Compressed fossil foliage, described here as Mahonia mioasiatica sp. nov., were collected from the Upper Miocene Xiaolongtan Formation in Wenshan, Yunnan, southwest China. These specimens represent the oldest reliable fossil record of Mahonia in East Asia. This new fossil species shows a general similarity to Group Orientales and is most similar to the extant eastern Asian Mahonia conferta. Considering other fossil evidence of Mahonia, we propose a migration route of this genus to Asia over the North Atlantic Land Bridge rather than the Bering Land Bridge. Our results also suggest that North America, Europe and East Asia have been successive centers of diversity for the genus, as a consequence of diversification in Group Orientales potentially related to historical climate change.

New fossil seeds of Eurya (Theaceae) from East Asia and their paleobiogeographic implications.

Eurya has an excellent fossil record in Europe, but it has only a few fossil occurrences in East Asia though this vast area houses the highest modern diversity of the genus. In this study, three-dimensionally preserved fossil seeds of Eurya stigmosa (Ludwig) Mai from the late Pliocene of northwestern Yunnan, southwestern China are described. The seeds are compressed and flattened, slightly campylotropous, and nearly circular to slightly angular in shape. The surface of the seeds is sculptured by a distinctive foveolate pattern, consisting of funnel-shaped and finely pitted cells. Each seed valve contains a reniform or horseshoe-shaped embryo cavity, a characteristic condyle structure and an internal raphe. These fossil seeds represent one of the few fossil records of Eurya in East Asia. This new finding therefore largely extends the distributional ranges of Eurya during Neogene. Fossil records summarized here show that Eurya persisted in Europe until the early Pleistocene, but disappeared thereafter. The genus might have first appeared in East Asia no later than the late Oligocene, and dispersed widely in regions such as Japan, Nepal, and southwestern China.

Late Pliocene diversity and distribution of Drynaria (Polypodiaceae) in western Yunnan explained by forest vegetation and humid climates.

The palaeodiversity of flowering plants in Yunnan has been extensively interpreted from both a molecular and fossil perspective. However, for cryptogamic plants such as ferns, the palaeodiversity remains poorly known. In this study, we describe a new ferny fossil taxon, Drynaria lanpingensis sp. nov. Huang, Su et Zhou (Polypodiaceae), from the late Pliocene of northwestern Yunnan based on fragmentary frond and pinna with in situ spores. The frond is pinnatifid and the pinnae are entirely margined. The sori are arranged in one row on each side of the primary vein. The spores have a semicircular to bean-shaped equatorial view and a tuberculate surface. Taken together with previously described fossils, there are now representatives of three known fossil taxa of Drynaria from the late Pliocene of western Yunnan. These finds suggest that Drynaria diversity was considerable in the region at that time. As Drynaria is a shade-tolerant plant, growing preferably in wet conditions in the understory of forests, its extensive existence may indicate forest vegetation and humid climates in western Yunnan during the late Pliocene. This is in line with results from floristic investigations and palaeoclimatic reconstructions based on fossil floras.

First occurrence of Cedrelospermum (Ulmaceae) in Asia and its biogeographic implications.

Cedrelospermum (Ulmaceae) is an extinct genus with extensive fossil records in Europe and North America. However, no fossil of the genus has been reported from Asia. Here we describe Cedrelospermum asiaticum L.B. Jia, Y.J. Huang et Z.K. Zhou sp. nov. based on compressed fruits from the late Miocene of Yunnan, southwestern China. The fossil fruits are characterized by an ovate fruit body adjoined by double wings, with the veins on the primary wing converging toward a stigmatic area. According to the historical geographic distribution of the genus, we hypothesize that Cedrelospermum originated in North America where both single-winged and double-winged fruits were reported. The single-winged form subsequently spread into Europe via the North Atlantic land bridge and the double-winged form dispersed into Asia via the Bering land bridge. From the Eocene to Oligocene, a southward retreat of the genus distribution probably took place, which coincided with the global surface cooling initiated during the Eocene-Oligocene transition. The extinction of Cedrelospermum from Asia may be related to the intensification of the East Asian monsoon.

A new positive relationship between pCO2 and stomatal frequency in Quercus guyavifolia (Fagaceae): a potential proxy for palaeo-CO2 levels.

BACKGROUND AND AIMS: The inverse relationship between atmospheric CO2 partial pressure (pCO2) and stomatal frequency in many species of plants has been widely used to estimate palaeoatmospheric CO2 (palaeo-CO2) levels; however, the results obtained have been quite variable. This study attempts to find a potential new proxy for palaeo-CO2 levels by analysing stomatal frequency in Quercus guyavifolia (Q. guajavifolia, Fagaceae), an extant dominant species of sclerophyllous forests in the Himalayas with abundant fossil relatives. METHODS: Stomatal frequency was analysed for extant samples of Q. guyavifolia collected from17 field sites at altitudes ranging between 2493 and 4497 m. Herbarium specimens collected between 1926 and 2011 were also examined. Correlations of pCO2-stomatal frequency were determined using samples from both sources, and these were then applied to Q. preguyavaefolia fossils in order to estimate palaeo-CO2 concentrations for two late-Pliocene floras in south-western China. KEY RESULTS: In contrast to the negative correlations detected for most other species that have been studied, a positive correlation between pCO2 and stomatal frequency was determined in Q. guyavifolia sampled from both extant field collections and historical herbarium specimens. Palaeo-CO2 concentrations were estimated to be approx. 180-240 ppm in the late Pliocene, which is consistent with most other previous estimates. CONCLUSIONS: A new positive relationship between pCO2 and stomatal frequency in Q. guyavifolia is presented, which can be applied to the fossils closely related to this species that are widely distributed in the late-Cenozoic strata in order to estimate palaeo-CO2 concentrations. The results show that it is valid to use a positive relationship to estimate palaeo-CO2 concentrations, and the study adds to the variety of stomatal density/index relationships that available for estimating pCO2. The physiological mechanisms underlying this positive response are unclear, however, and require further research.

Sequoia maguanensis, a new Miocene relative of the coast redwood, Sequoia sempervirens, from China: implications for paleogeography and paleoclimate.

UNLABELLED: • PREMISE OF THE STUDY: The paleogeographical origin of the relict North American Sequoia sempervirens is controversial. Fossil records indicate a Neogene origin for its foliage characteristics. Although several fossils from the Miocene sediments in eastern Asia have been considered to have close affinities with the modern S. sempervirens, they lack the typical features of a leafy twig bearing linear as well as scale leaves, and the fertile shoots terminating by a cone. The taxonomic status of these fossils has remained unclear.• METHODS: New better-preserved fossils from the upper Miocene of China indicate a new species of Sequoia. This finding not only confirms the former presence of this genus in eastern Asia, but it also confirms the affinity of this Asian form to the modern relict S. sempervirens.• KEY RESULTS: The principal foliage characteristics of S. sempervirens had already originated by the late Miocene. The eastern Asian records probably imply a Beringian biogeographic track of the ancestor of S. sempervirens in the early Neogene, at a time when the land bridge was not too cool for this thermophilic conifer to spread between Asia and North America.• CONCLUSIONS: The climatic context of the new fossil Sequoia in Southeast Yunnan, based on other floristic elements of the fossil assemblage in which it is found, is presumed to be warm and humid. Following the uplift of the Qinghai-Tibet Plateau, this warm, humid climate was replaced by the present monsoonal climate with dry winter and spring. This change may have led to the disappearance of this hygrophilous conifer from eastern Asia.

New Biogeographic insight into Bauhinia s.l. (Leguminosae): integration from fossil records and molecular analyses.

BACKGROUND: Given that most species that have ever existed on earth are extinct, it stands to reason that the evolutionary history can be better understood with fossil taxa. Bauhinia is a typical genus of pantropical intercontinental disjunction among the Asian, African, and American continents. Geographic distribution patterns are better recognized when fossil records and molecular sequences are combined in the analyses. Here, we describe a new macrofossil species of Bauhinia from the Upper Miocene Xiaolongtan Formation in Wenshan County, Southeast Yunnan, China, and elucidate the biogeographic significance through the analyses of molecules and fossils. RESULTS: Morphometric analysis demonstrates that the leaf shapes of B. acuminata, B. championii, B. chalcophylla, B. purpurea, and B. podopetala closely resemble the leaf shapes of the new finding fossil. Phylogenetic relationships among the Bauhinia species were reconstructed using maximum parsimony and Bayesian inference, which inferred that species in Bauhinia species are well-resolved into three main groups. Divergence times were estimated by the Bayesian Markov chain Monte Carlo (MCMC) method under a relaxed clock, and inferred that the stem diversification time of Bauhinia was ca. 62.7 Ma. The Asian lineage first diverged at ca. 59.8 Ma, followed by divergence of the Africa lineage starting during the late Eocene, whereas that of the neotropical lineage starting during the middle Miocene. CONCLUSIONS: Hypotheses relying on vicariance or continental history to explain pantropical disjunct distributions are dismissed because they require mostly Palaeogene and older tectonic events. We suggest that Bauhinia originated in the middle Paleocene in Laurasia, probably in Asia, implying a possible Tethys Seaway origin or an "Out of Tropical Asia", and dispersal of legumes. Its present pantropical disjunction resulted from disruption of the boreotropical flora by climatic cooling after the Paleocene-Eocene Thermal Maximum (PETM). North Atlantic land bridges (NALB) seem the most plausible route for migration of Bauhinia from Asia to America; and additional aspects of the Bauhinia species distribution are explained by migration and long distance dispersal (LDD) from Eurasia to the African and American continents.

Miocene leaves of Elaeagnus (Elaeagnaceae) from the Qinghai-Tibet Plateau, its modern center of diversity and endemism.

UNLABELLED: • PREMISE OF THE STUDY: The Qinghai-Tibet Plateau is a major center of plant diversity and endemism, but little is known about how this developed due to the region's very scarce paleobotanical record. The silverberry genus Elaeagnus (Elaeagnaceae) reaches its greatest diversity (54 species) and endemism (36 species) in this area. Fossil Elaeagnaceae could provide significant evidence for the phylogeny and biogeography of the family and contribute primary data regarding the evolution of the unique Qinghai-Tibet Plateau flora in its dramatic setting of tectonic and climatic change.• METHODS: We describe four fossil leaves with diagnostic features of Elaeagnus from the late Miocene of eastern Tibet, modern altitude of 3910 m a.s.l.. We also review prior fossil records of Elaeagnaceae.• KEY RESULTS: The well-preserved, densely packed, stellate scales on fossil leaf surfaces are diagnostic of Elaeagnaceae. We assign these fossil leaves to Elaeagnus tibetensis T. Su et Z.K. Zhou sp. nov., comprising the first confirmed fossil Elaeagnus leaves worldwide.• CONCLUSIONS: Elaeagnus was present in eastern Tibet by the late Miocene. Together with previous fossil records, the new species supports a Holarctic history of the family. The diversification of Elaeagnus in the Qinghai-Tibet Plateau and adjacent areas might have been driven by continuous uplift at least since the late Miocene, causing formation of complex topography and climate with high rainfall seasonality. The characteristic scales on leaf surfaces are likely to be an important functional adaptation to seasonal droughts during early spring.