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  • 1.
    Johansson, Veronika A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Recruitment ecology and fungal interactions in mycoheterotrophic Ericaceae2014Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    There are generally two contrasting alternatives to what limits recruitment in plants, namely the availability of seeds (seed limitation) or the quality or quantity of suitable sites (microsite limitation). Dust seeds, the smallest existing seeds, lack or have minimal nutrient reserves. During germination and initial development they consequently parasitize on mycorrhizal fungi. This is called mycoheterotrophy, and can vary in degree of fungal dependency in adult plants from full, partial or initial mycoheterotrophy.

    The aim of this thesis was to investigate the recruitment ecology of mycoheterotrophic Ericaceae (tribe Pyroleae) species with dust seeds, and to determine what limits their recruitment. The investigated species were: Chimaphila umbellata, Moneses uniflora, Orthilia secunda, Pyrola chlorantha, P. minor and P. rotundifolia. This aim was achieved by combining field experiments (seed sowing) with isotope analysis and fungal host pyrosequencing.

    Results provide evidence that the species in Pyroleae are heterogeneous, not only with regard to their degree of mycoheterotrophy, but also concerning germination and early seedling development. A combination of microsite and seed limitation is thus likely to be of importance for all studied species, but the relative importance of these limitations varies among species. Despite having adaptations for wind dispersal the majority of the seeds were deposited in close vicinity of the seed source. But with high seed production at least some seeds should be able to disperse long-distance. Seedlings of all studied species were found to associate with a wide range of ectomycorrhizal fungi, at least during their initial developmental stages. There seems to be a tendency for host narrowing in some Pyroleae species, but not as strict as the host specialization seen in fully mycoheterotrophic Monotropa hypopitys, supporting the hypothesis of geographical and developmental host shifts.

  • 2.
    Johansson, Veronika A.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Bahram, M.
    Tedersoo, L.
    Koljalg, U.
    Eriksson, Ove
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Specificity of fungal associations of Pyroleae and Monotropa hypopitys during germination and seedling development2017In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 26, no 9, p. 2591-2604Article in journal (Refereed)
    Abstract [en]

    Mycoheterotrophic plants obtain organic carbon from associated mycorrhizal fungi, fully or partially. Angiosperms with this form of nutrition possess exceptionally small 'dust seeds' which after germination develop 'seedlings' that remain subterranean for several years, fully dependent on fungi for supply of carbon. Mycoheterotrophs which as adults have photosynthesis thus develop from full to partial mycoheterotrophy, or autotrophy, during ontogeny. Mycoheterotrophic plants may represent a gradient of variation in a parasitism-mutualism continuum, both among and within species. Previous studies on plant-fungal associations in mycoheterotrophs have focused on either germination or the adult life stages of the plant. Much less is known about the fungal associations during development of the subterranean seedlings. We investigated germination and seedling development and the diversity of fungi associated with germinating seeds and subterranean seedlings (juveniles) in five Monotropoideae (Ericaceae) species, the full mycoheterotroph Monotropa hypopitys and the putatively partial mycoheterotrophs Pyrola chlorantha, P. rotundifolia, Moneses uniflora and Chimaphila umbellata. Seedlings retrieved from seed sowing experiments in the field were used to examine diversity of fungal associates, using pyrosequencing analysis of ITS2 region for fungal identification. The investigated species varied with regard to germination, seedling development and diversity of associated fungi during juvenile ontogeny. Results suggest that fungal host specificity increases during juvenile ontogeny, most pronounced in the fully mycoheterotrophic species, but a narrowing of fungal associates was found also in two partially mycoheterotrophic species. We suggest that variation in specificity of associated fungi during seedling ontogeny in mycoheterotrophs represents ongoing evolution along a parasitism-mutualism continuum.

  • 3.
    Johansson, Veronika A.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Bahram, Mohammad
    Tedersoo, Leho
    Kõljalg, Urmas
    Eriksson, Ove
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Diversity of ectomycorrhizal fungi associated with Pyroleae and  Monotropa hypopitys during germination and seedling developmentManuscript (preprint) (Other academic)
  • 4.
    Johansson, Veronika A.
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Cousins, Sara A. O.
    Stockholm University, Faculty of Science, Department of Physical Geography and Quaternary Geology.
    Eriksson, Ove
    Stockholm University, Faculty of Science, Department of Botany.
    Remnant Populations and Plant Functional Traits in Abandoned Semi-Natural Grasslands2011In: Folia Geobotanica, ISSN 1211-9520, E-ISSN 1874-9348, Vol. 46, no 2-3, p. 165-179Article in journal (Refereed)
    Abstract [en]

    Although semi-natural grasslands in Europe are declining there is often a time delay in the local extinction of grassland species due to development of remnant populations, i.e., populations with an extended persistence despite a negative growth rate. The objectives of this study were to examine the occurrence of remnant populations after abandonment of semi-natural grasslands and to examine functional traits of plants associated with the development of remnant populations. We surveyed six managed semi-natural grasslands and 20 former semi-natural grasslands where management ceased 60-100 years ago, and assessed species response to abandonment, assuming a space-for-time substitution. The response of species was related to nine traits representing life cycle, clonality, leaf traits, seed dispersal and seed mass. Of the 67 species for which data allowed analysis, 44 species declined after grassland abandonment but still occurred at the sites, probably as remnant populations. Five traits were associated with the response to abandonment. The declining but still occurring species were characterized by high plant height, a perennial life form, possession of a perennial bud bank, high clonal ability, and lack of dispersal attributes promoting long-distance dispersal. Traits allowing plants to maintain populations by utilizing only a part of their life cycle, such as clonal propagation, are most important for the capacity to develop remnant populations and delay local extinction. A considerable fraction of the species inhabiting semi-natural grasslands maintain what is most likely remnant populations after more than 60 years of spontaneous succession from managed semi-natural grasslands to forest.

  • 5.
    Johansson, Veronika A.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Eriksson, Ove
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Recruitment limitation, germination of dust seeds, and early development of underground seedlings in six Pyroleae species2013In: Botany, ISSN 1916-2790, E-ISSN 1916-2804, Vol. 91, no 1, p. 17-24Article in journal (Refereed)
    Abstract [en]

    We investigated recruitment of six mixotrophic Pyroleae species in relation to soil and adult presence. Pyroleae have dust seeds containing minimal nutrient reserves, and subterranean seedlings are mycoheterotrophic needing fungal hosts for germination and development. Germination and seedling development were studied by retrieving seed bags that had been placed within plots with adults present and at unoccupied control plots. There are two main alternatives to what limits recruitment of plants, seed limitation or microsite limitation. Results suggested that a combination of microsite and seed limitation was important for all investigated species. Microsite availability was the main limiting factor for Chimaphila umbellata (L.) W. P. C. Barton, Orthilia secunda (L.) House, and Pyrola chlorantha Sw., whereas seed availability was the main limiting factor for Pyrola minor L. For Moneses uniflora L. A. Gray and Pyrola rotundifolia L., it was not clear whether microsite or seed limitation dominated. Growth of seedlings responded positively to adult presence (O. secunda and P. minor), whereas others were negatively affected (M. uniflora and P. chlorantha). Increased levels of soil nutrients (N and P) had a negative effect on seedling growth in C. umbellata and P. chlorantha. These results provide the first evidence of the importance of microsite and seed limitation for germination and development of seedlings of Pyroleae species.

  • 6.
    Johansson, Veronika A.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Mikusinska, Anna
    Ekblad, Alf
    Eriksson, Ove
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Partial mycoheterotrophy in Pyroleae: nitrogen and carbon stable isotope signatures during development from seedling to adult2015In: Oecologia, ISSN 0029-8549, E-ISSN 1432-1939, Vol. 177, no 1, p. 203-211Article in journal (Refereed)
    Abstract [en]

    Mycoheterotrophic plants (MHP) are divided into non-photosynthesizing full MHP and green-leaved partial or initial MHP. We investigated 13C and 15N isotope enrichment in five putatively partial MHP species in the tribe Pyroleae (Ericaceae): Chimaphila umbellata, Moneses uniflora, Orthilia secunda, Pyrola chlorantha and Pyrola minor, sampled from forest sites on Öland, Sweden. For M. uniflora and P. chlorantha, we investigated isotope signatures of subterranean seedlings (which are mycoheterotrophic), to examine how the use of seedlings instead of full MHP species (Hypopitys monotropa) as reference species affects the assessment of partial mycoheterotrophy. Our main findings were as follows: (1) All investigated Pyroleae species were enriched in 15N compared to autotrophic reference plants. (2) significant fungal-derived C among the Pyroleae species was found for O. secunda and P. chlorantha. For the remaining species of C. umbellata, M. uniflora and P. minor, isotope signatures suggested adult autotrophy. (3) C and N gains, calculated using seedlings as a full MHP reference, yielded qualitatively similar results as when using H. monotropa as a reference. However, the estimated differences in C and N gains became larger when using seedlings as an MHP reference. (4) A previously unknown interspecific variation in isotope signature occurs during early ontogeny, from seed production to developing seedlings. Our findings suggest that there is a variation among Pyroleae species concerning partial mycoheterotrophy in adults. Adult autotrophy may be most common in Pyroleae species, and these species may not be as dependent on fungal-derived nutrients as some green orchids.

  • 7.
    Johansson, Veronika A.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Mueller, Gregor
    Eriksson, Ove
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Dust seed production and dispersal in Swedish Pyroleae species2014In: Nordic Journal of Botany, ISSN 0107-055X, E-ISSN 1756-1051, Vol. 32, no 2, p. 209-214Article in journal (Refereed)
    Abstract [en]

    Dust seeds are the smallest seeds in angiosperms weighing just about a few micrograms. These seeds are characteristic of most orchids, and several studies have been performed on seed features, fecundity and dispersal of orchid dust seeds. In this study we examine seed features, seed production and seed dispersal in another plant group with dust seeds, the Pyroleae (Monotropoideae, Ericaceae), focusing on six species: Pyrola chlorantha, P. minor, P. rotundifolia, Chimaphila umbellata, Moneses uniflora and Orthilia secunda. Seed production per capsule among these species was in the range between ca 1000 and 7800, and seed production per capsule bearing shoot was in the range between ca 7000 and 60 000. Combining our results with published information on pollen-ovule ratios suggests that these Pyroleae species have a generally efficient pollination system. The most fecund species was P. minor, the only species among the investigated that is probably largely self-pollinating. The investigated Pyroleae species have a seed production comparable to the less fecund orchid species. We studied seed dispersal in the field in one of the species, P. chlorantha. Despite the extremely small and potentially buoyant seeds, the vast majority of seeds are deposited close to the seed source, within a few meters. Further studies on the recruitment ecology of the investigated Pyroleae species are currently under way.

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