The interplay between ovule number, pollination and resources as determinants of seed set in a modular plant

BackgroundA classical dichotomous perspective proposes that either pollination or plant resources limit seed production. However, ovule number could also be limiting when pollination results in complete ovule fertilization and there are more plant resources available than needed to develop seeds. Moreover, this dichotomous view assumes that all flowers of a plant have equal access to a shared pool of resources, although these are frequently compartmentalized within plant modules, for example, inflorescences. How ovule number, pollination and resources affect seed production in physiologically-compartmentalized rather than physiologically-integrated plants has yet to be explored. We used raspberry (Rubus idaeus) to address this question.MethodsWe first assessed if ovule number affected the fraction of ovules that develop into seed (i.e., seed set) and whether this effect related to the extent of physiological integration among flowers within plants. This was achieved by statistically testing predictions on the sign and level of plant organization (i.e., among flowers within inflorescences, among inflorescences within ramets, and among ramets) of the relation between ovule number and seed set given different degrees of physiological integration. We then explored whether the relation between ovule number and seed set was affected by plant age (used here as a surrogate of resource availability) and pollination intensity (open-pollination vs. exclusion).ResultsWithin inflorescences, flowers with more ovules set a larger fraction of seeds. On the other hand, seed set at the inflorescence level was negatively related to the average number of ovules per flower. Seed set increased with ovule number and open-pollination, and decreased with ramet age. However, ovule number explained more variation in seed set than ramet age and pollination treatment. Ramet age affected the strength of the relation of seed set to ovule number, which was stronger in old than young ramets. Pollination did not alter the strength of this relation to any significant extent.DiscussionResults reveal the importance of ovule number as an overriding factor affecting seed set. Within inflorescences, resources appear to be differentially allocated to developing fruits from flowers with many ovules. This is consistent with the fact that in the raspberry a large proportion of the carbon invested in fruit development is fixed by the inflorescence subtending leaf. Differential resource allocation to flowers with many ovules is not affected by pollinator exclusion, being stronger in resource-exhausted ramets. This suggests that the effects of pollen limitation and resource allocation are compartmentalized at the inflorescence level. Consequently, modular plants can be viewed as reproductive mosaics where either ovule number, pollination or resources limit the number of seeds set by different flowers, so that improvements in any of them could increase plant seed production.

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What determines the number of seed produced in a flowering event? A case study of Calyptrogyne ghiesbreghtiana (Arecaceae)

Australian Journal of Botany ◽

10.1071/bt99012 ◽

2000 ◽

Vol 48 (5) ◽

pp. 659 ◽

Cited By ~ 9

Author(s):

Saul A. Cunningham

Keyword(s):

Resource Allocation ◽

Seed Production ◽

Natural Variation ◽

Seed Set ◽

Plant Seed ◽

Flower Production ◽

Number Of Seeds ◽

Female Flowers

Calyptrogyne ghiesbreghtiana Linden ex. H. Wendl. is an understorey palm that occurs at La Selva Biological Station, Costa Rica. In this paper I combine analysis of natural variation and results of experimental manipulations to ask (1) what limits seed production? and (2) what processes cause variation in seed production by C. ghiesbreghtiana? The number of seed produced per inflorescence ofC. ghiesbreghtiana was limited substantially by the loss of female flowers to floral herbivores. Much variation in the number of seed produced perinflorescence of C. ghiesbreghtiana was due to losses of developing fruits to predators. Together these phenomena illustrate the influential role of natural enemies in the reproductive success of this plant. Seed-set efficiency (number of seeds/number of female flowers) was highly variable in this species, and such high levels of variation appear to be common in other species. For species with highly variable seed-set efficiency, the role of resource allocation to flower production in determining differences in seed production among individual plants is likely to be relatively small.

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Inter-annual variation in seed production has increased over time (1900–2014)

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2017.1666 ◽

2017 ◽

Vol 284 (1868) ◽

pp. 20171666 ◽

Cited By ~ 30

Author(s):

Ian S. Pearse ◽

Jalene M. LaMontagne ◽

Walter D. Koenig

Keyword(s):

Seed Production ◽

Seed Set ◽

Global Climate ◽

Mast Seeding ◽

Plant Seed ◽

Subtle Change ◽

Animal Populations ◽

Wide Range ◽

Seed Crops ◽

Over Time

Mast seeding, or masting, is the highly variable and spatially synchronous production of seeds by a population of plants. The production of variable seed crops is typically correlated with weather, so it is of considerable interest whether global climate change has altered the variability of masting or the size of masting events. We compiled 1086 datasets of plant seed production spanning 1900–2014 and from around the world, and then analysed whether the coefficient of variation (CV) in seed set, a measure of masting, increased over time. Over this 115-year period, seed set became more variable for plants as a whole and for the particularly well-studied taxa of conifers and oaks. The increase in CV corresponded with a decrease in the long-term mean of seed set of plant species. Seed set CV increased to a greater degree in plant taxa with a tendency towards masting. Seed set is becoming more variable among years, especially for plant taxa whose masting events are known to affect animal populations. Such subtle change in reproduction can have wide-ranging effects on ecosystems because seed crops provide critical resources for a wide range of taxa and have cascading effects throughout food webs.

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Pollination services provided by various size classes of flower visitors to Eucalyptus globulus ssp. globulus (Myrtaceae)

Australian Journal of Botany ◽

10.1071/bt03002 ◽

2004 ◽

Vol 52 (3) ◽

pp. 353 ◽

Cited By ~ 21

Author(s):

A. B. Hingston ◽

B. M. Potts ◽

P. B. McQuillan

Keyword(s):

Seed Production ◽

Eucalyptus Globulus ◽

Seed Set ◽

Pollen Limitation ◽

Pollination Services ◽

Flower Visitors ◽

Large Numbers ◽

Introduced Honeybee ◽

Commercially Important ◽

Almost All

Flowers of the commercially important tree Eucalyptus globulus Labill. ssp. globulus were visited by a wide variety of insects and birds within its natural distribution. Flowers were visited so frequently that most available nectar was consumed, but seed production within 5 m of the ground was consistently far less than the maximum possible, indicating the presence of large numbers of inefficient pollinators and few efficient pollinators. Pollen limitation was more severe on fully self-incompatible trees than on partially self-compatible trees, demonstrating that pollinator inefficiency resulted from infrequent outcrossing rather than inability to deposit pollen on stigmas. The flower visitors that were responsible for almost all nectar consumption from flowers within 5 m of the ground were insects that were able to permeate cages with 5-mm apertures but not cages with 1-mm apertures, the most abundant of which was the introduced honeybee Apis mellifera L. These insects contributed less than 20% of the maximum possible seed set, indicating that they were inefficient pollinators. Birds and smaller insects made lesser contributions to seed production, but consumed little nectar within 5 m of the ground. However, anthophilous birds appeared to mostly forage higher in the trees and probably consumed more nectar from, and provided more pollination services to, flowers higher in the trees.

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Spatiotemporal Variations in Seed Set and Pollen Limitation in Populations of the Rare Generalist Species Polemonium caeruleum in Poland

Frontiers in Plant Science ◽

10.3389/fpls.2021.755830 ◽

2022 ◽

Vol 12 ◽

Author(s):

Justyna Ryniewicz ◽

Katarzyna Roguz ◽

Paweł Mirski ◽

Emilia Brzosko ◽

Mateusz Skłodowski ◽

...

Keyword(s):

Reproductive Success ◽

Population Size ◽

Seed Production ◽

Seed Set ◽

Pollen Limitation ◽

Monthly Precipitation ◽

Small Populations ◽

Flower Visitors ◽

Visitation Frequency ◽

Average Monthly Precipitation

A vast majority of angiosperms are pollinated by animals, and a decline in the number and diversity of insects often affects plant reproduction through pollen limitation. This phenomenon may be particularly severe in rare plant species, whose populations are shrinking. Here, we examined the variability in factors shaping reproductive success and pollen limitation in red-listed Polemonium caeruleum L. During a 5-year study in several populations of P. caeruleum (7–15, depending on year), we assessed the degree of pollen limitation based on differences in seed set between open-pollinated (control) and hand-pollinated flowers. We analysed the effects of flower visitors, population size, and meteorological data on plant reproductive success and pollen limitation. Our study showed that pollen limitation rarely affected P. caeruleum populations, and was present mainly in small populations. Pollen limitation index was negatively affected by the size of population, visitation frequency of all insects, and when considering the visitation frequency of individual groups, also by honeybee visits. Seed production in control treatment was positively influenced by the population size, average monthly precipitation in June and visits of hoverflies, while visits of honeybees, average monthly temperature in September, and average monthly precipitation in August influenced seed production negatively. As generalist plant P. caeruleum can be pollinated by diverse insect groups, however, in small populations their main visitors, the honeybees and bumblebees, may be less attracted, eventually leading to the disappearance of these populations. In pollination of P. caeruleum managed honeybees may play a dual role: while they are the most frequent and efficient flower visitors, their presence decreases seed set in open-pollinated flowers, which is most probably related to efficient pollen collection by these insects.

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Reproductive biology and breeding system in Casuarina equisetifolia (Casuarinaceae) – implication for genetic improvement

Australian Journal of Botany ◽

10.1071/bt15184 ◽

2016 ◽

Vol 64 (2) ◽

pp. 120 ◽

Cited By ~ 4

Author(s):

Y. Zhang ◽

C.L. Zhong ◽

Q. Han ◽

Q.B. Jiang ◽

Y. Chen ◽

...

Keyword(s):

Reproductive Biology ◽

Breeding System ◽

Genetic Improvement ◽

Fruit Set ◽

Seed Set ◽

Pollen Limitation ◽

Casuarina Equisetifolia ◽

Open Pollination ◽

Floral Longevity ◽

Improvement Programs

Understanding the reproductive biology of plant species is essential for successful domestication and genetic improvement programs. Casuarina equisetifolia L. is an important plantation species in China and India but information on reproductive biology is limited. To address this issue, grafted ramets of C. equisetifolia were used to study floral biology, breeding system and progeny performance. The female floral longevity of C. equisetifolia reached 28.4 days under non-pollination conditions, which was significantly longer than that of supplementary pollination (5.5 days) and open pollination (12.2 days), implying successful pollination would accelerate senescence of female flowers. Higher fruit set (88.8%) and seed set (35.7%) under supplementary pollination were obtained, compared with 75.9% and 21.7%, respectively, under open pollination, although there were no fruit set and seed set under non-pollination conditions. Pollen limitation was evident based on pollen limitation index (0.39) in seedling plantations of C. equisetifolia. Selfed seedlings had low height and diameter growth in both nursery and field trials and markedly lower survival in field trial, indicating inbreeding depression. Microsatellite-based estimates of selfing rate of open pollinated, monoecious individuals was 42%, suggesting that monoecious C. equisetifolia individuals are self-compatible, and that the breeding system should be classified as facultative xenogamy.

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Occurrence and Prevention of Delayed Autonomous Selfing in Salvia umbratica (Lamiaceae)

Frontiers in Plant Science ◽

10.3389/fpls.2021.635310 ◽

2021 ◽

Vol 12 ◽

Author(s):

Han-Wen Xiao ◽

Yan-Bo Huang ◽

Yu-Hang Chang ◽

Yun Chen ◽

Richard J. Abbott ◽

...

Keyword(s):

Fruit Set ◽

Seed Set ◽

Pollen Limitation ◽

Pollen Grains ◽

Flower Longevity ◽

Plant Resources ◽

Floral Longevity ◽

Hand Pollination ◽

Pollen Vector ◽

Highly Correlated

Delayed autonomous selfing (DAS) provides reproductive assurance under conditions of pollinator and/or pollen-limitation. Few plant species have been investigated to determine if DAS is terminated when a flower is sufficiently pollinated by a pollen vector, thereby saving plant resources for other purposes. We examined this possibility in bumblebee-pollinated Salvia umbratica. We first showed that DAS resulting in high fruit set (100%) and seed set (>80%) per flower occurred in the absence of insect pollinators by means of style recurvature and was completed in 94% of flowers 72 h after they opened. In contrast, in flowers pollinated immediately after opening, DAS was prevented by corollas dropping away before styles recurve toward the upper thecae. We next showed that hand-pollination of flowers immediately after they opened resulted in high fruit set (100%) and seed set (>80%) when 5–10 pollen grains or more were deposited on their stigmas, whereas fruit set and seed set were reduced to 45.00 and 22.50%, respectively, when pollen loads were reduced to 1–3 pollen grains. Finally, we showed that on average single pollinator visits deposited 26 pollen grains on stigmas of flowers that had just opened, which is more than enough to ensure high fruit and seed set. Our results indicate that flower longevity is highly correlated with the pollinator environment and female fitness of S. umbratica, with extended flower longevity allowing DAS to occur being advantageous when pollinators are absent, while reduced floral longevity and prevention of DAS being favored when flowers are pollinated by pollinators. Thus, flower longevity in S. umbratica varies so as to optimize reproductive output and resource efforts, and is dependent on the availability and effectiveness of pollinators to pollinate flowers.

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The influence of floral morph ratios and low plant density on mating and fertility in a tristylous colonizing species

Botany ◽

10.1139/cjb-2018-0032 ◽

2018 ◽

Vol 96 (8) ◽

pp. 533-545 ◽

Cited By ~ 1

Author(s):

Christopher M. Balogh ◽

Spencer C.H. Barrett

Keyword(s):

Field Experiment ◽

Seed Set ◽

Plant Density ◽

Pollen Limitation ◽

Lythrum Salicaria ◽

Long Distance ◽

Experimental Conditions ◽

Wide Range ◽

Morph Ratios ◽

Floral Morph

Sexual reproduction in heterostylous populations may be vulnerable to demographic conditions because of the small number of mating types in populations. Here, we investigate mating and fertility under natural and experimental conditions in tristylous Lythrum salicaria L., an invasive species that exhibits a wide range of floral morph ratios and demographic contexts. We grew 147 open-pollinated seed families from six populations with different morph structures to estimate intermorph mating (d). In a field experiment, we used progeny ratios from 47 spatially isolated individuals to estimate d, and measured the intensity of pollen limitation experienced by the morphs. The M- and S-morphs experienced high rates of d, regardless of population size or morph ratio. Estimates for the L-morph revealed low levels of intramorph mating in three dimorphic and two trimorphic populations, but near complete intramorph mating in a monomorphic population. Despite high levels of intermorph mating in the field experiment, the morphs experienced significant pollen limitation of fruit and seed set, but this did not differ in intensity among the morphs. Our field experiment demonstrates that although plant isolation was associated with pollen limitation of seed set, “long-distance” bee-mediated pollen flow served to maintain intermorph mating. Tristyly in L. salicaria is remarkably robust to the demographic variation associated with colonization.

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Predator Effects on Plant-Pollinator Interactions, Plant Reproduction, Mating Systems, and Evolution

Annual Review of Ecology Evolution and Systematics ◽

10.1146/annurev-ecolsys-012120-094926 ◽

2020 ◽

Vol 51 (1) ◽

pp. 319-340

Author(s):

Amanda D. Benoit ◽

Susan Kalisz

Keyword(s):

Mating Systems ◽

Seed Set ◽

Pollen Limitation ◽

Plant Traits ◽

Plant Reproduction ◽

Trophic Levels ◽

Interaction Networks ◽

Pollinator Abundance ◽

Plant Pollinator ◽

Predator Effects

Plants are the foundation of the food web and therefore interact directly and indirectly with myriad organisms at higher trophic levels. They directly provide nourishment to mutualistic and antagonistic primary consumers (e.g., pollinators and herbivores), which in turn are consumed by predators. These interactions produce cascading indirect effects on plants (either trait-mediated or density-mediated). We review how predators affect plant-pollinator interactions and thus how predators indirectly affect plant reproduction, fitness, mating systems, and trait evolution. Predators can influence pollinator abundance and foraging behavior. In many cases, predators cause pollinators to visit plants less frequently and for shorter durations. This decline in visitation can lead to pollen limitation and decreased seed set. However, alternative outcomes can result due to differences in predator, pollinator, and plant functional traits as well as due to altered interaction networks with plant enemies. Furthermore, predators may indirectly affect the evolution of plant traits and mating systems.

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