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BR Staff Publications [b] (paper in not reviewed journal) --- cultivated landscapes --- endangered plants

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Pollinators are essential for a major part of flowering plants. By transporting pollen from one flower to the other, reproduction is made possible. Especially insects are important pollinators. We know that insect communities are declining at alarming rates. This decline could have a serious impact on plant reproduction in the future. It is important to understand the interactions between plants and pollinators to the best of our abilities so we can take adequate measures to protect pollinators from further decline. The pollination interaction is often characterised as a network with certain properties that reveal the general patterns structuring plant-pollinator interactions. Most networks are made at pollinator species level. However, there is ample evidence that individuals within the species differ in their foraging behaviour. Also differences between sexes are commonly observed. Networks that only consider insects at species level thus lose valuable information as a result of generalising individuals from the same species. The goal of our study was to evaluate whether there were differences in foraging between sexes and between individuals within the same insect species. We analysed the pollen present on individual insects and identified the plant species they collected pollen from with metabarcoding. Then we made three plant-pollinator networks that differed in pollinator levels, one at species level, one at sex level and one at individual level. We analysed the patterns and properties of these networks and compared them with each other. Our research revealed that individuals of the same insect species indeed differed in foraging behaviour. There were also significant differences in foraging between the sexes of the red-tailed bumblebee (Bombus lapidarius) and the hairy-legged mining bee (Dasypoda hirtipes). When comparing the three networks we also found significant differences in three network properties. The individual based networks were more specialised and more connected. Our results thus confirm that plant-pollinator networks at species level lose important information compared to networks at individual level. We think it is important that more pollination studies take individual pollinator behaviour into account, so we have a more accurate representation of plant pollinator interactions.

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The Sonian Forest is an old forest complex in the Region of Brussels and is one of the few Western European forests where the natural dominance of European beech (Fagus sylvatica L.) is preserved. Like many other tree species, F. sylvatica is reliant on fungal symbionts for growth and survival. Ectomycorrhizal (EcM) fungi colonize root tips and ameliorate the host’s nutrient and water acquisition in exchange for carbohydrates. These fungi can extend their mycelia and interlink host trees to establish an underground highway for nutrient exchange, which is labeled a common mycorrhizal network (CMN). For seedlings to not succumb from deficient photosynthates in the dark understory of beech-dominated forests while awaiting canopy opening, they can tap into a CMN allowing mature trees to shunt nutrients to the seedlings. Although natural regeneration was problematic for many decades in the Sonian Forest, it has recently rebounded. Therefore, our aim was to scrutinize the role of EcM fungi in the natural regeneration of F. sylvatica in the Sonian Forest. We collected soil cores and roots from seedlings, saplings, and pole wood from five locations within the forest, and applied next generation sequencing techniques to get an exhaustive overview of EcM fungal community compositions. EcM fungal communities were dominated by Russula, Cenococcum, Lactarius, Laccaria, Amanita, Inocybe, Xerocomellus, and Scleroderma lineages. We found a discrepancy in soil and root sampled EcM fungal communities. Our results suggest that Xerocomellus, Laccaria, Lactarius, Scleroderma, Melanogaster, and Tomentella EcM fungal lineages are frequently associated with regenerating beeches, while Russula, Inocybe, and Amanita are indicative for mature beeches. However, EcM fungal communities were spatially autocorrelated, which is presumably related to functionally redundant taxa and recent management in old growth set aside areas. Within the Zwaenepoel reserve, we found shifts in EcM fungal community composition as beeches age. Russula cf. puellaris, Clavulina cf. cristata, Cenococcum cf. geophilum, Lactarius cf. subdulcis, and Melanogaster cf. intermedius were indicative for regenerating beeches, whereas Cortinarius cf. lignicola, Amanita cf. rubescens, Russula cf. violeipes, Russula cf. velutipes, Meliniomyces, Elaphomyces cf. Leucosporus, and Genea cf. hispidula were related to older beeches. We found a decreasing diversity and increasing evenness of EcM fungal communities as beeches age, which suggests that either the host differentially allocates carbon to better performing EcM fungal taxa, or direct competition among EcM fungal taxa is structuring EcM fungal communities, or both. EcM fungal communities from the reserve were affected by soil moisture content, pH, and soil ammonium content. No distinction in soil EcM fungal communities was found between plots with frequent and without beech regeneration. Altogether, our findings suggest that favorable EcM fungal communities are not the key to successful regeneration. Rather, it is a combination of the accessibility to suitable EcM fungi with a favorable forest microclimate and small-scale increments in light availability that determines successful regeneration of beech.

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Plants display remarkable sexual diversity. Regardless of this variation, most flowering plants are hermaphrodites and contain flowers with both male and female sex organs. However, various sexual systems have evolved in which male and female organs have been separated between flowers and between individuals.In gynodioecious species, hermaphrodites co-exist with females, plants that lack pollen production (male-sterile individuals). Since females have lost their ability to produce pollen, they are dependent on hermaphrodites for fertilization. One necessary condition for the maintenance of this sexual polymorphism is the occurrence of a reproductive ‘female advantage’. The female advantage implies that females should produce more seeds or higher quality seedlings in comparison to hermaphrodites and the magnitude of the female advantage is dependent on the sex determination system. In the most common form of gynodioecy, nuclear-cytoplasmic gynodioecy, mutations that lead to male-sterility are located in the cytoplasm and the effect of these male-sterility mutations can be counteracted by nuclear alleles (male- fertility restorers). In species with nuclear-cytoplasmic gynodioecy, females require only a slight reproductive advantage over hermaphrodites to be maintained within a population (female advantage > 1). The female advantage is generally attributed to resource reallocation from pollen to seed production and avoidance of inbreeding depression since females are obligate outcrossers.In most gynodioecious species that have been studied over the years, females had a clear reproductive advantage over hermaphrodites, although the magnitude of the female advantage generally differed among populations. Variation in the magnitude of the female advantage is not surprising since seed production of females is strongly dependent on pollen availability. In populations or patches with a low number of hermaphrodites, females may experience low seed set due to pollen limitation, while in populations or patches with a high number of hermaphrodites, females may have a reproductive advantage. When females produce more seeds than hermaphrodites the frequency of females may locally increase, which in turn may contribute to variation in sex ratios among populations. Population female frequencies are highly variable and generally range from a low percentage to more than 50% females. Many gynodioecious species also have populations that consist purely of hermaphrodites. When the frequency of females within a population is low, floral sex ratios can still be highly variable, since sex expression can also vary within individuals. Hermaphrodites of many gynodioecious species are dichogamous, indicating that they separate the maturation of male and female organs in time. Differences in timing of male and female function of a flower, typically lead to a shift in floral sex ratio during a population’s flowering season.To gain insights into the various aspects that may affect seed production and genetic variation in gynodioecious plant species, I quantified seed production and offspring fitness across a wide range of populations that differed in population size and sex ratio to understand how these variables affected the female advantage and sex ratio evolution. I assessed genetic diversity in a number of spatially separated populations to understand how genetic variation is partitioned among populations and between sex morphs. Moreover, I studied temporal variation in female reproductive success within and among individuals across an entire flowering season to get a better understanding of the impact of within-population sex ratio variation on seed set. To address these research objectives, two gynodioecious species, Saxifraga granulata (meadow saxifrage) and Plantago coronopus (buck’s- horn plantain), were studied.In this thesis, I show that variation in sex expression within inflorescences, among individuals and among populations highly affected seed production of my study species. In populations of P . coronopus, seed production was highly dependent on population sex ratio, in populations with a low frequency of females both females and hermaphrodites produced more seeds than in populations with a high female frequency. Females produced fewer seeds than hermaphrodites on average, however, offspring fitness of females was higher than offspring fitness of hermaphrodites. Furthermore, genetic analyses showed that both females and hermaphrodites were highly genetically diverse, but adult hermaphrodites showed increased levels of homozygosity as well as severe inbreeding depression after selfing. In S. granulata, the occurrence of female individuals was low, but flowers of hermaphrodites differentially invested in male and female function; the first-opening central flower generally had a long female phase and produced significantly more seeds than early and late lateral flowers. Furthermore, early flowering plants produced more seeds than late flowering plants. Populations of S. granulata were highly genetically diverse, which was most likely related to its high ploidy level (octoploid) and the ability to reproduce clonally.Despite the differences between Saxifraga granulata and Plantago coronopus in terms of reproduction, floral biology, pollination mode, and ploidy level, I have shown that the large variation in sex expression within inflorescences, among individuals and among populations highly affected seed production. My results further showed that plant mating system and the extent of inbreeding depression affect the distribution of genetic variation among populations and sex morphs. Although not explicitly investigated, they also point to the importance of local spatial structure of gynodioecious populations for regulating the evolutionary maintenance of gynodioecy.

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Orchids have a mutualistic relationship in their roots with mycorrhizal fungi. Orchid mycorrhizal fungi (OMF) are endomycorrhizal fungi that form pelotons in the roots. These fungi support the growth of the orchid by delivering nutrients. Different fungal families and genera of the Basidiomycota and Ascomycota can be involved in the roots of orchid species throughout different populations and they occur in different distributions across the planet. Many environmental characteristics influence the diversity and abundance of OMF communities throughout different places. Bioclimatic variables are known to have an influence on arbuscular mycorrhiza and ectomycorrhiza, but only a few studies have investigated the influence of temperature and precipitation on orchid mycorrhizal fungi communities. In this study, the impact of bioclimatic variables and elevation on orchid mycorrhizal community composition was investigated for the terrestrial, partially mycoheterotrophic orchid Epipactis helleborine. This is a generalist orchid species that has a wide distribution throughout Europe and occurs in a wide variety of habitats with different environmental characteristics. Root samples were collected in 31 populations of E. helleborine in 9 different countries in Europe. High-throughput sequencing and meta-barcoding were used to detect and identify all fungi associating with E. helleborine. Dominant fungi were members of genera Tuber, Tomentella, Russula, Sebacina, Inocybe and Cortinarius, while members of Peziza, Psathyrella, Resinicium, Rhizoctonia and Wilcoxina were only sporadically observed. A non-parametric multivariate analysis of variance and beta diversity analysis were used to see if there were regional differences between populations and to see how dissimilar populations are. The dissimilarity matrix was then used in a Mantel test to see if dissimilarities in fungal communities were related to geographical distance. Nonmetric multidimensional scaling was used to summarize variation in community composition, while a redundancy analysis was used to investigate how bioclimatic variables were related to variation in community composition. The sampled populations showed large variation in mycorrhizal community composition with high dissimilarities between populations that were detected through beta diversity calculations (βsor = 0.955176). This high dissimilarity could be explained by high spatial turnover rates, which indicates that taxon replacement takes place and E. helleborine is a generalist species. Overall, there were no significant differences between different regions or countries, which indicates that there is no clear geographic pattern in mycorrhizal community composition. Nonetheless, orchid mycorrhizal fungi community composition was significantly related to the temperature of the hottest month, suggesting that some fungi are better adapted to the high temperatures of the Mediterranean climate than others. Overall, these results show that dissimilarities between populations are mainly the result of spatial turnover and there is no clear geographic pattern of orchid mycorrhizal fungi communities. Temperature of the hottest months appeared to be the most important factor determining mycorrhizal community composition in E. helleborine, suggesting that Mediterranean climates support different orchid mycorrhizal communities than more temperate areas.