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  • 1.
    Bolinder, Kristina
    Stockholms universitet, Naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och botanik.
    Pollen and pollination in Ephedra (Gnetales)2017Doktorsavhandling, sammanläggning (Övrigt vetenskapligt)
    Abstract [en]

    Ephedra (Gnetales) is a gymnosperm genus with a long evolutionary history; the first dispersed pollen grains with affinity to the group are known already from the Permian. This thesis focuses on the evolutionary history of the group and different aspects of its pollination mechanisms. Despite the limited number of extant species of the genus (50-60), and a low morphological and genetic divergence among species, there is variation in pollination syndrome in the genus. The prevailing state in Ephedra, and most gymnosperms, is wind pollination. It is therefore surprising that one species, E. foeminea, is insect-pollinated. Together with co-workers I documented the pollination syndromes of E. foeminea and a sympatric species, E. distachya, based on long term field experiments in north-eastern Greece and aerodynamic investigations and calculations. Placing the results into an evolutionary framework reveals that the insect-pollinated species E. foeminea is sister to the remaining (mostly wind-pollinated) genus, and indicates that insect pollination is the ancestral state in the Gnetales. During the course of evolution of the group there has been a shift to wind pollination, which may have played a crucial role for the diversification of the crown group in the Paleogene. Pollination biology is often correlated with the morphology of the pollen such that pollen grains of anemophilous plants are small with a smooth surface, whereas pollen grains of entomophilous plants are larger with an ornamented surface and a covering of pollenkitt. The pollen morphology of Ephedra can be broadly divided into two types: an ancestral type with an unbranched pseudosulcus between each pair of plicae, and a derived type with a branched pseudosulcus between each pair of plicae. Further, the pollen morphology and ultrastructure of the pollen wall in Ephedra are to some degree correlated with the pollination syndrome and capability of long distance dispersal. Pollen of E. foeminea has a denser ultrastructure, as a result a higher settling velocity and is therefore capable of flying shorter distances than does pollen of the anemophilous E. distachya, and other investigated anemophilous species that show a more spacious ultrastructure of the pollen grain. These results can be useful in the reconstruction of the pollination mechanism of extinct taxa of the Ephedra-lineage in the future.

  • 2.
    Bolinder, Kristina
    Stockholms universitet, Naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och botanik.
    Pollination in Ephedra (Gnetales)2014Licentiatavhandling, sammanläggning (Övrigt vetenskapligt)
    Abstract [en]

    Pollination, i.e., the transport of male gametophytes to female gametophytes, can occur with biotic or abiotic vectors and is necessary for fertilization and completion of the lifecycle in all seed plants. Insect pollination and the co-evolution between angiosperms and insects have during the last century been discussed as one possible solution to Darwin’s abominable mystery and an important explanation for the relatively abrupt turn-over from a vegetation dominated by gymnosperms to a vegetation dominated by angiosperms in the Cretaceous. Insect pollination is, however, a much older phenomenon that can be traced back to the Devonian, but is it an ancestral trait that has been lost in many seed plant groups, or has it originated multiple times in parallel? These questions have to be addressed in a phylogenetic framework comprising extant and extinct seed plant groups. The Gnetales are constantly in focus in studies of seed plant phylogeny, probably because they have repeatedly been suggested, and refuted, to be the closest living relatives of angiosperms. The order consists of three genera, Gnetum, Welwitschia and Ephedra, of which the former two have long been known to be insect pollinated. Pollination biology in Ephedra has, however, been poorly studied and understood. In this thesis pollination mechanisms in Ephedra (Gnetales) are investigated by field experiments and observations (Paper I) and aerodynamic simulations and studies of pollen morphology (Paper II). The results show that there are multiple pollination mechanisms within this otherwise morphologically and ecologically uniform genus. Further, in contrast to what has often been assumed, insect pollination is shown to be ancestral in the Gnetales and not a derived feature that has evolved within the group. Using this new information on pollination biology in the Gnetales and data from the literature, I explore evolution of pollen morphology and pollination mode in seed plants.

  • 3.
    Bolinder, Kristina
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och botanik.
    Humphreys, Aelys M.
    Stockholms universitet, Naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och botanik. Royal Botanic Gardens, UK.
    Ehrlén, Johan
    Stockholms universitet, Naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och botanik.
    Alexandersson, Ronny
    Ickert-Bond, Stefanie M.
    Rydin, Catarina
    Stockholms universitet, Naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och botanik.
    From near extinction to diversification by means of ashift in pollination mechanism in the gymnosperm relict Ephedra (Ephedraceae, Gnetales)2016Ingår i: Botanical journal of the Linnean Society, ISSN 0024-4074, E-ISSN 1095-8339, Vol. 180, nr 4, s. 461-477Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Pollination in gymnosperms is usually accomplished by means of wind, but some groups are insect-pollinated. We show that wind and insect pollination occur in the morphologically uniform genus Ephedra (Gnetales). Based on field experiments over several years, we demonstrate distinct differences between two Ephedra species that grow in sympatry in Greece in pollen dispersal and clump formation, insect visitations and embryo formation when insects are denied access to cones. Ephedra distachya, nested in the core clade of Ephedra, is anemophilous, which is probably the prevailing state in Ephedra. Ephedra foeminea, sister to the remaining species of the genus, is entomophilous and pollinated by a range of diurnal and nocturnal insects. The generalist entomophilous system of E.foeminea, with distinct but infrequent insect visitations, is in many respects similar to that reported for Gnetum and Welwitschia and appears ancestral in Gnetales. The Ephedra lineage is well documented already from the Early Cretaceous, but the diversity declined dramatically during the Late Cretaceous, possibly to near extinction around the Cretaceous-Palaeogene boundary. The clade imbalance between insect- and wind-pollinated lineages is larger than expected by chance and the shift in pollination mode may explain why Ephedra escaped extinction and began to diversify again.

  • 4.
    Bolinder, Kristina
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och botanik.
    Niklas, Karl J.
    Rydin, Catarina
    Stockholms universitet, Naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och botanik.
    AERODYNAMICS AND POLLEN ULTRASTRUCTURE IN EPHEDRA2015Ingår i: American Journal of Botany, ISSN 0002-9122, E-ISSN 1537-2197, Vol. 102, nr 3, s. 457-470Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Premise of the study: Pollen dispersal is affected by the terminal settling velocity (U-t) of the grains, which is determined by their size, bulk density, and by atmospheric conditions. The likelihood that wind-dispersed pollen is captured by ovulate organs is influenced by the aerodynamic environment created around and by ovulate organs. We investigated pollen ultrastructure and U-t of Ephedra foeminea (purported to be entomophilous), and simulated the capture efficiency of its ovules. Results were compared with those from previously studied anemophilous Ephedra species. Methods: U-t was determined using stroboscopic photography of pollen in free fall. The acceleration field around an average ovule was calculated, and inflight behavior of pollen grains was predicted using computer simulations. Pollen morphology and ultrastructure were investigated using SEM and STEM. Key results: Pollen wall ultrastructure was correlated with U-t in Ephedra. The relative proportion and amount of granules in the infratectum determine pollen bulk densities, and (together with overall size) determine U-t and thus dispersal capability. Computer simulations failed to reveal any functional traits favoring anemophilous pollen capture in E. foeminea. Conclusion: The fast U-t and dense ultrastructure of E. foeminea pollen are consistent with functional traits that distinguish entomophilous species from anemophilous species. In anemophilous Ephedra species, ovulate organs create an aerodynamic microenvironment that directs airborne pollen to the pollination drops. In E. foeminea, no such microenvironment is created. Ephedroid palynomorphs from the Cretaceous share the ultrastructural characteristics of E. foeminea, and at least some may, therefore, have been produced by insect-pollinated plants.

  • 5.
    Bolinder, Kristina
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och botanik.
    Norbäck Ivarsson, Lena
    Humphreys, Aelys M.
    Stockholms universitet, Naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och botanik. Imperial College London, UK.
    Ickert-Bond, Stefanie M.
    Han, Fang
    Hoorn, Carina
    Rydin, Catarina
    Stockholms universitet, Naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och botanik.
    Pollen morphology of Ephedra (Gnetales) and its evolutionary implications2016Ingår i: Grana, ISSN 0017-3134, E-ISSN 1651-2049, Vol. 55, nr 1, s. 24-51Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    The Ephedra lineage can be traced at least to the Early Cretaceous. Its characteristically polyplicate pollen is well-represented in the fossil record and is frequently used as an indicator of paleoclimate. However, despite previous efforts, knowledge about variation and evolution of ephedroid pollen traits is poor. Here, we document pollen morphology of nearly all extant species of Ephedra, using a combination of scanning electron microscopy (SEM) and light microscopy (LM), and reconstruct ancestral states of key pollen traits. Our results indicate that the ancestral Ephedra pollen type has numerous plicae interspaced by unbranched pseudosulci, while the derived pollen type has branched pseudosulci and (generally) fewer plicae. The derived type is inferred to have evolved independently twice, once along the North American stem branch and once along the Asian stem branch. Pollen of the ancestral type is common in Mesozoic fossil records, especially from the Early Cretaceous, but it is less commonly reported from the Cenozoic. The earliest documentation of the derived pollen type is from the latest Cretaceous, after which it increases strongly in abundance during the Paleogene. The results of the present study have implications for the age of crown group Ephedra as well as for understanding evolution of pollination syndromes in the genus.

  • 6. Han, Fang
    et al.
    Rydin, Catarina
    Stockholms universitet, Naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och botanik.
    Bolinder, Kristina
    Stockholms universitet, Naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och botanik.
    Dupont-Nivet, Guillaume
    Abels, Hemmo A.
    Koutsodendris, Andreas
    Zhang, Kexin
    Hoorn, Carina
    Steppe development on the Northern Tibetan Plateau inferred from Paleogene ephedroid pollen2016Ingår i: Grana, ISSN 0017-3134, E-ISSN 1651-2049, Vol. 55, nr 1, s. 71-100Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Steppe vegetation represents a key marker of past Asian aridification and is associated with monsoonal intensification. Little is, however, known about the origin of this pre-Oligocene vegetation, its specific composition and how it changed over time and responded to climatic variations. Here, we describe the morphological characters of Ephedraceae pollen in Eocene strata of the Xining Basin and compare the pollen composition with the palynological composition of Late Cretaceous and Paleocene deposits of the Xining Basin and the Quaternary deposits of the Qaidam Basin. We find that the Late Cretaceous steppe was dominated by Gnetaceaepollenites; in the transition from the Cretaceous to the Paleocene, Gnetaceaepollenites became extinct and Ephedripites subgenus Ephedripites dominated the flora with rare occurrences of Ephedripites subgen. Distachyapites; the middle to late Eocene presents a strong increase of Ephedripites subgen. Distachyapites; and the Quaternary/Recent is marked by a significantly lower diversity of Ephedraceae (and Nitrariaceae) compared to the Eocene. In the modern landscape of China, only a fraction of the Paleogene species diversity of Ephedraceae remains and we propose that these alterations in Ephedreaceae composition occurred in response to the climatic changes at least since the Eocene. In particular, the strong Eocene monsoons that enhanced the continental aridification may have played an important role in the evolution of Ephedripites subgen. Distachyapites triggering an evolutionary shift to wind-pollination in this group. Conceivably, the Ephedraceae/Nitrariaceae dominated steppe ended during the Eocene/Oligocene climatic cooling and aridification, which favoured other plant taxa.

  • 7.
    Rydin, Catarina
    et al.
    Stockholms universitet, Naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och botanik.
    Bolinder, Kristina
    Stockholms universitet, Naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och botanik.
    Moonlight pollination in the gymnosperm Ephedra (Gnetales)2015Ingår i: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 11, nr 4, artikel-id 20140993Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Most gymnosperms are wind-pollinated, but some are insect-pollinated, and in Ephedra (Gnetales), both wind pollination and insect pollination occur. Little is, however, known about mechanisms and evolution of pollination syndromes in gymnosperms. Based on four seasons of field studies, we show an unexpected correlation between pollination and the phases of the moon in one of our studied species, Ephedra foeminea. It is pollinated by dipterans and lepidopterans, most of them nocturnal, and its pollination coincides with the full moon of July. This may be adaptive in two ways. Many nocturnal insects navigate using the moon. Further, the spectacular reflection of the full-moonlight in the pollination drops is the only apparent means of nocturnal attraction of insects in these plants. In the sympatric but wind-pollinated Ephedra distachya, pollination is not correlated to the full moon but occurs at approximately the same dates every year. The lunar correlation has probably been lost in most species of Ephedra subsequent an evolutionary shift to wind pollination in the clade. When the services of insects are no longer needed for successful pollination, the adaptive value of correlating pollination with the full moon is lost, and conceivably also the trait.

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