Reproduction alternation in trees: testing the resource depletion hypothesis using experimental fruit removal in Quercus ilex.

The keystones of resource budget models to explain mast seeding are that fruit production depletes tree stored resources, which become subsequently limiting to flower production the following year. These two hypotheses have, however, rarely been tested in forest trees. Using a fruit removal experiment, we tested whether preventing fruit development would increase nutrient and carbohydrates storage and modify allocation to reproduction and vegetative growth the following year. We removed all the fruits from nine adult Quercus ilex L. trees shortly after fruit set and compared, with nine control trees, the concentrations of nitrogen (N), phosphorus (P), zinc (Zn), potassium (K) and starch in leaves, twigs and trunk before, during and after the development of female flowers and fruits. The following year, we measured the production of vegetative and reproductive organs as well as their location on the new spring shoots. Fruit removal prevented the depletion of N and Zn in leaves during fruit growth. It also modified the seasonal dynamics in Zn, K and starch in twigs, but had no effect on reserves stored in the trunk. Fruit removal increased the production of female flowers and leaves the following year, and decreased the production of male flowers. Our results show that resource depletion operates differently for male and female flowering, because the timing of organ formation and the positioning of flowers in shoot architecture differ between male and female flowers. Our results suggest that N and Zn availability constrain flower production in Q. ilex, but also that other regulatory pathways might be involved. They strongly encourage further experiments manipulating fruit development over multiple years to describe the causal relationships between variations in resource storage and/or uptake, and male and female flower production in masting species.

Holm oak fecundity does not acclimate to a drier world.

Climate change might impact tree fecundity by altering the relative influences of meteorological and physiological drivers, and by modifying resource investment in reproduction. Using a 13-yr monitoring of Quercus ilex reproduction in a rainfall exclusion experiment, we analysed the interactive effects of long-term increased aridity and other environmental drivers on the inter-annual variation of fecundity (male flower biomass, number of initiated and mature fruits). Summer-autumn water stress was the main driver of fruit abortion during fruit growth. Rainfall exclusion treatment strongly reduced the number of initiated and mature fruits, even in masting years, and did not increase fruit tolerance to severe drought. Conversely, the relative contribution of the meteorological and physiological drivers, and the inter-annual variability of fruit production were not modified by rainfall exclusion. Rather than inducing an acclimation of tree fecundity to water limitation, increased aridity impacted it negatively through both lower fruit initiation due to changes in resource allocation, and more severe water and resource limitations during fruit growth. Long-term increased aridity affected tree reproduction beyond what is expected from the current response to inter-annual drought variations, suggesting that natural regeneration of holm oak forest could be jeopardised in the future.

Resource manipulation through experimental defoliation has legacy effects on allocation to reproductive and vegetative organs in Quercus ilex.

BACKGROUND AND AIMS: In plants, high costs of reproduction during some years can induce trade-offs in resource allocation with other functions such as growth, survival and resistance against herbivores or extreme abiotic conditions, but also with subsequent reproduction. Such trade-offs might also occur following resource shortage at particular moments of the reproductive cycle. Because plants are modular organisms, strategies for resource allocation to reproduction can also vary among hierarchical levels. Using a defoliation experiment, our aim was to test how allocation to reproduction was impacted by resource limitation. METHODS: We applied three levels of defoliation (control, moderate and intense) to branches of eight Quercus ilex trees shortly after fruit initiation and measured the effects of resource limitation induced by leaf removal on fruit development (survival, growth and germination potential) and on the production of vegetative and reproductive organs the year following defoliation. KEY RESULTS: We found that defoliation had little impact on fruit development. Fruit survival was not affected by the intense defoliation treatment, but was reduced by moderate defoliation, and this result could not be explained by an upregulation of photosynthesis. Mature fruit mass was not affected by defoliation, nor was seed germination success. However, in the following spring defoliated branches produced fewer shoots and compensated for leaf loss by overproducing leaves at the expense of flowers. Therefore, resource shortage decreased resource allocation to reproduction the following season but did not affect sex ratio. CONCLUSIONS: Our results support the idea of a regulation of resource allocation to reproduction beyond the shoot scale. Defoliation had larger legacy effects than immediate effects.

Divergent selection on flowering phenology but not on floral morphology between two closely related orchids.

Closely related species often differ in traits that influence reproductive success, suggesting that divergent selection on such traits contribute to the maintenance of species boundaries. Gymnadenia conopsea ss. and Gymnadenia densiflora are two closely related, perennial orchid species that differ in (a) floral traits important for pollination, including flowering phenology, floral display, and spur length, and (b) dominant pollinators. If plant-pollinator interactions contribute to the maintenance of trait differences between these two taxa, we expect current divergent selection on flowering phenology and floral morphology between the two species. We quantified phenotypic selection via female fitness in one year on flowering start, three floral display traits (plant height, number of flowers, and corolla size) and spur length, in six populations of G. conopsea s.s. and in four populations of G. densiflora. There was indication of divergent selection on flowering start in the expected direction, with selection for earlier flowering in two populations of the early-flowering G. conopsea s.s. and for later flowering in one population of the late-flowering G. densiflora. No divergent selection on floral morphology was detected, and there was no significant stabilizing selection on any trait in the two species. The results suggest ongoing adaptive differentiation of flowering phenology, strengthening this premating reproductive barrier between the two species. Synthesis: This study is among the first to test whether divergent selection on floral traits contribute to the maintenance of species differences between closely related plants. Phenological isolation confers a substantial potential for reproductive isolation, and divergent selection on flowering time can thus greatly influence reproductive isolation and adaptive differentiation.

Floral trait differentiation in Anacamptis coriophora: Phenotypic selection on scents, but not on colour.

Current divergent selection may promote floral trait differentiation among conspecific populations in flowering plants. However, whether this applies to complex traits such as colour or scents has been little studied, even though these traits often vary within species. In this study, we compared floral colour and odour as well as selective pressures imposed upon these traits among seven populations belonging to three subspecies of the widespread, generalist orchid Anacamptis coriophora. Colour was characterized using calibrated photographs, and scents were sampled using dynamic headspace extraction and analysed using gas chromatography-mass spectrometry. We then quantified phenotypic selection exerted on these traits by regressing fruit set values on floral trait values. We showed that the three studied subspecies were characterized by different floral colour and odour, with one of the two predominant floral volatiles emitted by each subspecies being taxon-specific. Plant size was positively correlated with fruit set in most populations, whereas we found no apparent link between floral colour and female reproductive success. We detected positive selection on several taxon-specific compounds in A. coriophora subsp. fragrans, whereas no selection was found on floral volatiles of A. coriophora subsp. coriophora and A. coriophora subsp. martrinii. This study is one of the first to document variation in phenotypic selection exerted on floral scents among conspecific populations. Our results suggest that selection could contribute to ongoing chemical divergence among A. coriophora subspecies.

Flower phenology as a disruptor of the fruiting dynamics in temperate oak species.

Many perennial plants display masting, that is, fruiting with strong interannual variations, irregular and synchronized between trees within the population. Here, we tested the hypothesis that the early flower phenology in temperate oak species promotes stochasticity into their fruiting dynamics, which could play a major role in tree reproductive success. From a large field monitoring network, we compared the pollen phenology between temperate and Mediterranean oak species. Then, focusing on temperate oak species, we explored the influence of the weather around the time of budburst and flowering on seed production, and simulated with a mechanistic model the consequences that an evolutionary shifting of flower phenology would have on fruiting dynamics. Temperate oak species release pollen earlier in the season than do Mediterranean oak species. Such early flowering in temperate oak species results in pollen often being released during unfavorable weather conditions and frequently results in reproductive failure. If pollen release were delayed as a result of natural selection, fruiting dynamics would exhibit much reduced stochastic variation. We propose that early flower phenology might be adaptive by making mast-seeding years rare and unpredictable, which would greatly help in controlling the dynamics of seed consumers.