Winged Fruits Research Articles

First fruit record of Pterocarya (Juglandaceae) from the upper Eocene of the central Qinghai-Tibetan Plateau, China

The Juglandaceae family experienced significant diversification during the early Tertiary, as evidenced by fossil records showing a broad expansion of both extant and extinct taxa. The genus Pterocarya is characterized by its distinctive fruit with butterfly-shaped wings and a small nutlet. Macrofossil records suggest that this genus was distributed widely in the Northern Hemisphere. However, the fossil record of Pterocarya in China is limited. In this study, we describe a well-preserved Pterocarya fossil winged fruit from the middle-upper member of the Niubao Formation (the upper Eocene) of the central Qinghai-Tibetan Plateau, China. The winged fruit is identified as Pterocarya liae sp. nov. based on detailed morphological comparison, representing the earliest known record of Pterocarya winged fruit in Asia. The new finding extends the paleobiogeographic distribution of Pterocarya during the Eocene and provides new insights into the early stage of the diversification of this genus.

Persistent inner tepals and wings protect developing seeds of Rheum nanum from insect herbivory in Central Asian cold deserts.

Although the postdispersal functions of diaspore (fruit and its appendages) have been reported, little is known about their protective/defensive functions. In this context, diaspores with appendages (persistent inner tepals and/or fruit wings) that experienced predispersal herbivory by insects in natural populations of Rheum nanum were investigated, and the seed abortion percentage, seed and embryo masses, and germination of seeds from diaspores with different categories of insect herbivory were measured and compared. Predispersal insect herbivory of R. nanum diaspores was prevalent in the four investigated populations, but the percentage of diaspores with appendages (persistent inner tepals and and/or fruit wings) damaged by insects was significantly higher than that of diaspores with the pericarp damaged by insects. Seeds from diaspores with gnawed appendages experienced significantly less damage than those with gnawed pericarps. Importantly, we conclude that fruit appendages of R. nanum help to mechanically protect developing seeds from predispersal insect herbivory.

Folding angle and wing flexibility influence the flight performance of origami winged fruits

Folding angle and wing flexibility influence the flight performance of origami winged fruits

Fruit wings accelerate germination in Anacyclus clavatus.

The lateral membranous expansions of fruits, commonly referred to as wings, have long been theorized to serve only dispersal functions. Alternatively, because winged fruits typically have earlier seed germination than unwinged fruits, we hypothesized that wings could increase the contact surface with water, ultimately triggering earlier germination. We investigated this alternative hypothesis by exploring the potential role of fruit wings on germination in the heterocarpic species Anacyclus clavatus (Desf.) Pers. (Asteraceae), which produces both winged and unwinged fruits. First, we measured the speed and degree of water absorption in winged and unwinged fruits. Second, we investigated the effects of wings on germination performance, by either reducing wing size or by preventing water absorption by sealing wings with wax. Next, we tested the influence of water availability on the germination performance of winged and unwinged fruits by reducing the water potential. Winged fruits absorbed more water at a faster rate than unwinged fruits. The sealing of wings delayed germination, whereas germination time was not significantly altered by wing cutting. The restriction of water availability by decreasing water potential significantly delayed seed germination of unwinged fruits, whereas winged fruits remained unaffected. Altogether, our results support the effect of wings on germination and cast doubt on the unique role of wings in dispersal. Whether or not wings contribute to dispersal, we propose that they also improve seed germination and seedling establishment by facilitating water absorption after the release from their mother plants.

Protection against insect predation during fruit development: the role of fleshy fruit wings of three species of Zygophyllum in the cold desert of Central Asia.

Fruit wings serve various ecological functions, including facilitating wind dispersal, providing physical protection to seeds, and regulating seed germination. While many studies have reported the role of fruit wings in plants, little is known about their protective function during fruit development. In this study, winged fruits damaged by insects in natural populations of three Zygophyllum species (Z. potaninii, Z. lehmannianum and Z. macropterum) were investigated. We measured and compared the percentage of damaged winged fruits, seed set, seed mass, seed germination, and seedling growth of different insect herbivory categories. The results revealed that the percentage of winged fruits with damaged wings only (low predation) was significantly higher than that of with damaged both fruit wings and fruit bodies (high predation). Furthermore, winged fruits with low predation had significant higher seed set, seed mass, seed germination, and dry mass and relative growth rate (RGR) in the seedlings which grown from the seeds, than that from winged fruits with high predation. These results demonstrate that the presence of the fruit wings may provide protection for the seeds to alleviate harm from insect predation before dispersal. These findings provide new insights into the function of fruit wings and the reproductive strategies of desert plants.

First fossil evidence of samaras of Ailanthus Desf. (Simaroubaceae) from India and its implications

Even though it is now widespread in Asia and was widely distributed in the Northern Hemisphere during the Cenozoic, fruits of the genus Ailanthus Desf. (Simaroubaceae) have not previously been documented from the Cenozoic of India. Here, we report the first Indian occurrence of fossil winged fruits corresponding to the modern genus Ailanthus having samaroid mericarps with a centrally placed seed from the latest Neogene sediments of Chotanagpur Plateau, eastern India. We determine their taxonomic position based on a detailed morphological comparison with similar modern and fossil specimens and discuss their palaeoclimatic significance. The fossil fruits are elongated, elliptic samaroid mericarps with a centrally placed seed and a marginal ventral vein starting from the seed extend to the base of the fruit. The fruits are 24–39 mm long and 11–16 mm wide. Based on the available morphological characters including locations of the stylar scar, main ventral vein, and the size of the samara, we assign these specimens to the fossil species Ailanthus confucii Unger. This species has a rich fossil record from the Cenozoic sediments of Europe, North America, and eastern Asia. However, this is the first report of A. confucii in India, which is significant for this species’s biogeographic and evolutionary history. Based on morphological comparisons, A. confucii shows affinity to modern A. altissima. Here, we also review the biogeographic history of Ailanthus and suggest its possible migratory routes.

Inclusions of flowers of Podopterus (Polygonaceae) in the Miocene amber of Simojovel de Allende, Chiapas, Mexico

Background and Aims: The Miocene amber from Chiapas, Mexico, shows high diversity of biological inclusions such as plants, fungi, arthropods, and vertebrates, being one of the most important amber-bearing areas worldwide. The aim of this work is to describe a new record based on four bisexual flowers belonging to the fossil species Podopterus mijangosae, that has been described recently based on its winged fruits only.Methods: The morphological and anatomical characteristics of the four fossil flowers were observed using a binocular stereoscopic microscope. The taxonomic affinity was decided by consulting specialized literature, as well as the review of herbarium material of the genera Podopterus, Fallopia, and Neomillspaughia of Polygonaceae.Key results: The four fossil specimens are bisexual, small, and have actinomorphic flowers, with differentiated perianth, three petals and three sepals per series, stamens are free and with thread-like filaments, anthers are dithecal and basifixed, the ovary is superior, syncarpous, 3-angular, with three free styles, and capitate stigmas. Conclusions: This new report of flowers of Podopterus adds more evidence that the family Polygonaceae was an important component of the tropical forest of Simojovel de Allende, Chiapas, Mexico, during the Miocene.

First reliable Miocene fossil winged fruits record of Engelhardia in Asia through anatomical investigation

Fossil genera with similar features to the winged fruits of the living Engelhardia Lesch. ex Blume (e.g., Palaeocarya G. Saporta) have been widely reported in Cenozoic fossil floras of the Northern Hemisphere. However, fossil winged fruits of Engelhardia with detailed anatomical structures have only been found in the upper Eocene of North America. This study reports the first Engelhardia fossil winged fruits with detailed anatomical structures in East Asia from the Miocene Erzitang Formation of Guangxi, South China. The anatomical and morphological features of the new fossils, including the unique structure of secondary septa, clearly distinguish them from other fossil genera and show unambiguously their attribution to the genus Engelhardia. This discovery suggests that Engelhardia had reached its modern distribution during the Miocene and the climate of the Guiping Basin in Guangxi during the Miocene was similar to that of present-day tropical and subtropical regions in Asia.

Winged Fruits of Friisifructus aligeri gen. et sp. nov. from the Late Cretaceous of Western North America

Premise of research. Fossil flowers and fruits with unresolved affinities among extant angiosperms may potentially represent extinct families or orders. The characterization and systematic assessments of such fossils will undoubtedly further our understanding of extinct angiosperm diversity, which is crucial for reconstructing the evolution of angiosperms in deep time. Here, we report two three-dimensionally preserved winged fruits from Campanian (∼82–80 Ma) deposits on Sucia Island, Washington State, that represent a new genus. We explore potential phylogenetic relationships of this genus relative to higher taxa across the angiosperm phylogeny.Methodology. The fossils were studied using microcomputed tomography (μCT) scanning and light microscopy. A three-dimensional reconstruction of one winged fruit was created from the μCT scans. The phyloscan method was used to assess the systematic positions of the winged fruits. Using the reconstruction, the fossil fruits were compared to extant angiosperms and extinct winged fruits to assess potential affinities.Pivotal results. The μCT scans and reconstruction of the winged fruit reveal a pentamerous perianth, five pairs of fin-wings, two whorls of persistent stamens, five semicircular nectary pads, an inferior unilocular ovary, and a style with three stylar branches. Phyloscan analyses recover the winged fruits within the rosid clade, but they cannot be assigned to any extant family or order within the group because of differing floral and fruit morphologies.Conclusions. The winged fruits are assigned to Friisifructus aligeri gen. et sp. nov. This new genus and species add to the diversity of winged fruits from the Cretaceous, which are relatively uncommon. Moreover, the unique morphology of Friisifructus indicates that this genus may belong to an extinct family of rosids.

The load-bearing mechanism of plant wings: A multiscale structural and mechanical analysis of the T. tipu samara.

Spinning winged fruits ("helicopter" samaras) generate significant lift forces at relatively low velocities, which enable the wind to disperse them across long distances. The biological material of the samara sustains the aerodynamic loadings and maintains the physical shape of the samara in the air via a yet unknown load-bearing mechanism. Here, positing that this mechanism fundamentally originates from the macro-to-microscale structural and mechanical characteristics of the samara, we use sub-micron computer tomography, electron microscopy, and multi-scale mechanical experiments to map the structural and mechanical characteristics of the tipu tree (Tipuana tipu) samara down to the micrometer length scale. Then, using theoretical models, we characterize the multiscale structural-mechanical principles of the samara and use these principles to disclose the underlying load-bearing mechanism. We found that the structural motifs of the tipu tree samara are closely analogous to various other types and forms of winged fruits, suggesting that this load-bearing mechanism is widespread in plant wings. The structural-mechanical principles governing the samara bear unconventional design concepts, which pave the way toward the development and engineering of small-scale wing elements for miniature aviation platforms with specialized mechanical capabilities. STATEMENT OF SIGNIFICANCE: The biomaterial of plant wings grants them mechanical resistance to flight forces during wind dispersal. "Helicopter seeds" demonstrate an intricate load-bearing mechanism that spans three structure-functional scales of their biomaterial. This mechanism appears widespread in plant wings and may promote novel micro-engineering design guidelines for futuristic flight materials and small-scale aviation platforms.

Wind variability limits the potential influence of propagule morphology and descent rate on dispersal in the winged fruits of Carpinus (Betulaceae)

The dispersal of propagules is an important aspect of land plant life history that has the potential to impact diverse evolutionary and ecological processes. Identifying the relationship between form and function of extant propagules provides the opportunity to infer past dispersal processes using morphological information from fossils, especially for abiotic dispersal of winged propagules. Many studies under laboratory conditions have identified wing loading (propagule mass divided by wing area) as the character most important for descent rates of winged propagules, but its influence on dispersal distances in natural environments over entire dispersal seasons remains unclear. To clarify this relationship, morphological measurements and experimental drops were performed on dispersed propagules from two species of Carpinus collected along highly resolved transects radiating from individual source trees. A significant relationship was found between wing loading and descent rate in still air, but the relationship between wing loading and actual dispersal distance in the field was random in all directions. Results indicate that variable wind conditions over a dispersal season can erase any signal of form and descent rate on dispersal patterns. Consequently, this randomization should impact evolutionary patterns by hampering selective potential for details of form that might further slow descent rates once enough of a wing evolves for propagules to exhibit a consistent specialized aerodynamic behavior.

Deuterogyny and the Association of Two Vagrant Eriophyoid Mites (Acariformes, Eriophyoidea) with the Host-plant Generative Organs of Two Broad-leaved Trees in North-West Russia.

Phytoparasitic mites of the superfamily Eriophyoidea Nalepa live and feed on mature leaf surfaces, between leaf bud scales, and (though less commonly) on flowers or fruits. In this study, we focused on the seasonal associations of two eriophyoid species, Shevtchenkella serrata (Nalepa 1892) with the Norway maple tree (Acer platanoides L.), and Brevulacus reticulatus Manson 1984 with the common oak (Quercus robur L.). These species have complex life cycles with two morphologically different, seasonal female forms, the protogyne and deutogyne. In B. reticulatus, both forms retain all the major generic characteristics but in S. serrata only the protogynes conform to the diagnosis of Shevtchenkella, whereas the deutogynes have the typical traits of Anthocoptes. We confirmed the conspecificity of the protogynes and deutogynes of both eriophyoid species by sequencing a barcode fragment of the Cox1 gene from which we obtained four pairwise identical sequences: ON920305/ON920306 (S. serrata) and ON920307/ON920308 (B. reticulatus). In addition, taxonomical studies on Shevtchenkella and Brevulacus resulted in new synonymies and combinations: (1) Oxypleurites obtusus Roivainen 1947 is considered a deutogyne of S. serrata and treated as a junior synonym of S. serrata; (2) two rhyncaphytoptine species from North America are transferred from the genus Rhyncaphytoptus to Brevulacus: B. albus (Keifer 1959) comb. nov. and B. atlanticus (Keifer 1959) comb. nov.; and (3) one species, B. salicinus Soika et al. 2017, is excluded from Brevulacus and transferred to Rhyncaphytoptus: Rhyncaphytoptus salicinus (Soika et al. 2017) comb. nov. Apart from distinct morphological deuterogyny in S. serrata and B. reticulatus, we observed the persistent association of S. serrata with the generative organs of the maple tree, A. platanoides, leading to transmission to the next host generation via the seed-containing winged fruits (samaras) and subsequent colonization of seedlings. In B. reticulatus, similar synchronization with host-plant dispersal was not detected; however, in mid-summer, temporary colonization of immature acorns and feeding was observed. Additional studies conducted in various ecosystems and including different ecological groups of plants, especially anemochorous plants, are needed to estimate the frequency of the association of eriophyoids with plant generative organs, seeds and seedlings to better understand what role in mite ecology such associations may play.

Loxopteroides weeksae gen. et sp. nov. (Anacardiaceae) samaras and associated foliage from the Eocene of western North America

An extinct kind of winged fruit found at several Eocene sites in California and Oregon, western USA, occurs in association with pinnately compound anacardiaceous leaves that have been called Rhus mixta. The samaras were previously treated along with isolated leaves from the Chalk Bluffs flora of California in an extinct sapindaceous genus, Thouiniopsis myricaefolia (Lesquereux) MacGinitie. However, the samaras are nonschizocarpic and hence readily distinguished from the mericarps of extant Sapindaceae such as Acer, Thouinia and Thouinidium. We reassign the fruits to Anacardiaceae and note similarity to the extant Neotropical genus Loxopterygium which differs, however, in the shape of the endocarp and placement of the style. Fruits of Loxopteroides weeksae gen. et sp. nov. co-occur with leaves of Rhus mixta at multiple localities in California and Oregon.

Extinct Anacardiaceous Samaras and Sumac-Like Leaves from the Eocene of Western North America

An extinct kind of asymmetric samara occurs in the Eocene of Colorado, Utah, and Wyoming. The distinctive winged fruits were attributed to Anacardiaceae by Roland Brown in the 1920s and 1930s and were placed in the fossil genus Anacardites. However, that generic name, based on leaves from the Oligocene of France described a century earlier by Saporta, is inappropriate for these fruits. The samaras, which were not previously described in detail, are pedicellate, with a scar of hypogynous perianth and disk, and are nonschizocarpic, with an elliptical single-seeded endocarp and a lateral wing supplied with arching subparallel venation. We recognize these fruits as an extinct genus, Barkleya gen. nov. Although morphologically unique, the fruits share some characters in common with samaroid fruits of subfamily Anacardioideae, including Amphipterygium, Faguetia, Loxopterygium, Orthopterygium, and Schinopsis. We also provide an emended diagnosis for Rhus nigricans foliage and speculate, on the basis of co-occurrence and shared familial relationships, that the fruits of Barkleya schinoloxus (RW Brown) comb. nov. were produced by the same plant, which was a common element of the early to middle Eocene Green River flora.

On the capacity for rapid adaptation and plastic responses to herbivory and intraspecific competition in insular populations of Plectritis congesta.

A capacity for rapid adaptation should enhance the persistence of populations subject to temporal and spatial heterogeneity in natural selection, but examples from nature remain scarce. Plectritis congesta (Caprifoliaceae) is a winter annual that exhibits local adaptation to browsing by ungulates and hypothesized to show context‐dependent trade‐offs in traits affecting success in competition versus resistance or tolerance to browsing. We grew P. congesta from 44 insular populations historically exposed or naïve to ungulates in common gardens to (1) quantify genetic, plastic and competitive effects on phenotype; (2) estimate a capacity for rapid adaptation (evolvability); and (3) test whether traits favoured by selection with ungulates present were selected against in their absence. Plants from browsed populations bolted and flowered later, had smaller inflorescences, were less fecund and half as tall as plants from naïve populations on average, replicating patterns in nature. Estimated evolvabilities (3–36%) and narrow‐sense heritabilities (h2; 0.13–0.32) imply that differences in trait values as large as reported here can arise in 2–18 generations in an average population. Phenotypic plasticity was substantial, varied by browsing history and fruit phenotype and increased with competition. Fecundity increased with plasticity in flowering height given competition (0.47 ± 0.02 florets/cm, β ± se), but 23–77% faster in naïve plants bearing winged fruits (0.53 ± 0.04) than exposed‐wingless plants (0.43 ± 0.03) or exposed‐winged and naïve‐wingless plants (0.30 ± 0.03, each case). Our results support the hypothesis that context‐dependent variation in natural selection in P. congesta populations has conferred a substantial capacity for adaptation in response to selection in traits affecting success in competition versus resistance or tolerance to browsing in the absence versus presence of ungulates, respectively. Theory suggests that conserving adaptive capacity in P. congesta will require land managers to maintain spatial heterogeneity in natural selection, prevent local extinctions and maintain gene flow.

Extending beyond Gondwana: Cretaceous Cunoniaceae from western North America.

Cunoniaceae are important elements of rainforests across the Southern Hemisphere. Many of these flowering plants are considered Paleo-Antarctic Rainforest Lineages that had a Gondwanan distribution since the Paleocene. Fossils of several modern genera within the family, such as Ceratopetalum, have indicated biogeographical connections between South America and Australia in the Cenozoic. Here, we report a dramatic geographical range extension for Ceratopetalum, and Cunoniaceae as a whole, based on two exceptionally preserved fossil winged fruits from Campanian (c. 82-80 Ma old) deposits on Sucia Island, Washington, USA. The fossils were studied using physical sectioning, light microscopy, micro-computed tomography scanning and multiple phylogenetic analyses. The fossil fruits share diagnostic characters with Ceratopetalum such as the presence of four to five persistent calyx lobes, a prominent nectary disk, persistent stamens, a semi-inferior ovary and two persistent styles. Based on morphological comparisons with fruits of extant species and support from phylogenetic analyses, the fossils are assigned to a new species Ceratopetalum suciensis. These fossils are the first unequivocal evidence of crown Cunoniaceae from the Cretaceous of North America, indicating a more complicated biogeographical history for this important Gondwanan family.

Diversity and Cytogenomic Characterization of Wild Carrots in the Macaronesian Islands.

The Macaronesian islands constitute an enormous reservoir of genetic variation of wild carrots (subtribe Daucinae; Apiaceae), including 10 endemic species, but an accurate understanding of the diversification processes within these islands is still lacking. We conducted a review of the morphology, ecology, and conservation status of the Daucinae species and, on the basis of a comprehensive dataset, we estimated the genome size variation for 16 taxa (around 320 samples) occurring in different habitats across the Macaronesian islands in comparison to mainland specimens. Results showed that taxa with larger genomes (e.g., Daucus crinitus: 2.544 pg) were generally found in mainland regions, while the insular endemic taxa from Azores and Cabo Verde have smaller genomes. Melanoselinum decipiens and Monizia edulis, both endemic to Madeira Island, showed intermediate values. Positive correlations were found between mean genome size and some morphological traits (e.g., spiny or winged fruits) and also with habit (herbaceous or woody). Despite the great morphological variation found within the Cabo Verde endemic species, the 2C-values obtained were quite homogeneous between these taxa and the subspecies of Daucus carota, supporting the close relationship among these taxa. Overall, this study improved the global knowledge of DNA content for Macaronesian endemics and shed light into the mechanisms underpinning diversity patterns of wild carrots in the western Mediterranean region.

Begonia shenzhenensis, a new species of Begoniaceae from Guangdong, China.

Begonia shenzhenensis D.K.Tian & X.Yun Wang, sp. nov., a new species in Begonia sect. Platycentrum of Begoniaceae from Shenzhen of Guangdong province, China, is described and illustrated. Morphologically, it is primarily similar to B. coelocentroides in the same section but differs by its denser hairs on leaf, petiole, and pedicel, abtuse anther apex, hairy ovary, and narrower adaxial fruit wing. Based on only one small population found to date, its conservation status is assigned to Critical Endangered according to the IUCN Red List Categories and Criteria.

Fossil fruits of Illigera (Hernandiaceae) from the Eocene of central Tibetan Plateau

AbstractIlligera (Hernandiaceae) is a liana genus distributed mainly in the tropical Asia and Africa. Previous fossil records suggested that Illigera was restricted in western North America during the Eocene. Recent paleobotanical investigation has unveiled a Paleogene flora that is totally different from today's vegetation in central Tibet. This provides novel insights into the paleoenvironmental change during the evolution of the Tibetan Plateau (TP). Here, we investigated 10 fruit impressions of Illigera from the early middle Eocene Niubao Formation in the Bangor Basin, central TP. The fossil winged fruits are characterized by their eroded fruit wings, well preserved fusiform locular areas with a median ridge bisecting the fruit, and short veins fanning radially outward. These features allow us to assign these fossils to Illigera eocenica, a species originally discovered in the Eocene of western North America. This is the second fossil occurrence of Illigera worldwide, and the first in Asia. Our finding suggests a warm and humid climate in the central TP during the early middle Eocene, and a close floristic link between Asia and North America during the Paleogene. We also propose a Northern Hemisphere origin and a Paleogene dispersal event from Northern Hemisphere to Africa for Illigera.

Lepidium khalkhalicum (Brassicaceae), a new wild relative of the garden cress (L. sativum) from northwestern Iran

Lepidium khalkhalicum, a new species from northwestern Iran, is described. It appears to be a local endemic restricted to open slopes of marl hills in the Khalkhal region (Ardabil province). The novel species is easily distinguished from similar species by a set of both vegetative and generative characters such as less developed indumentum, undivided leaves, much longer style, more divaricate, non‐thickened pedicels exceeding silicles, poorly developed fruit wing, etc. A detailed description accompanied by color photographs, distribution and habitat data, and a proposed conservation status of the new species are provided. The particular interest of the discovery in view of its close relationship to the garden cress, L. sativum, is stressed.