Pollen Limitation Index Research Articles

Neutral influence of animal pollination in the common bean (Phaseolus vulgaris L., Fabaceae) production and seed germination

The influence of animal pollination on the common bean (Phaseolus vulgaris L., Fabaceae) production is quite variable, but there is a tendency towards the predominance of strong self-fertility. Few studies tested for the influence of pollination on quality aspects of production and seed germination. In view of the global economic importance of the common bean, and the pollinator crisis that the planet is experiencing, the objective of this study was to investigate the influence of animal pollination in the amount and quality of fruits, seeds, and seed germination of the common bean, using four plantations of the ‘mulatinho’ variety in a region under semiarid climate of NE Brazil as a model. Our hypotheses are: 1) Flowers are visited mainly by bees; 2) The production of fruits, seeds and seed germination are favored by pollinators. Data were collected during the 2017 and 2018 plantings, when data on floral visitors were collected. Controlled crosses (spontaneous self-, cross- and natural pollinations) were performed and the number and morphometry of fruits, number, morphometry, and germination of seeds were compared between the experiments. Reproductive efficiency (RE) and pollen limitation index (PLI) were calculated. Number of formed fruits, measurements, weight, and germination resulting from spontaneous self-pollination showed higher values than those formed by natural and cross-pollination. In 2017, the RE was high (1.44) and the ILP was 0.14, indicating no pollen limitation. In 2018, RE was also high (1.8), but the ILP was 0.3, indicating pollen limitation. Overall, the frequency of visits on focal individuals was low. Conversely to what was expected, butterflies and moths were the most frequent floral visitors, although the flowers were also visited by bees, ants, flies beetles and spiders. None were considered pollinators because they did not touch the reproductive structures of the flower. The bee Xylocopa sp. was the only species capable of pollinating the flowers, as its size allows it to expose the reproductive parts present inside the keel when it lands on the flower to collect the floral resource. However, its frequency was very low, and it did not visit the focal plants. Apparently, low temperatures and high rainfall negatively interfered with pollination and, consequently, with the production. The common bean can be considered a relevant crop in the face of the current global pollinator crisis, as it does not depend on pollinators to produce food, the flowers are used by several pollinator groups and, additionally, it contributes to soil nitrogenating, reducing input costs for farmers.

Variability in mating strategies in a widespread cactus in the Chihuahuan Desert

Opuntia is the most diverse and widespread genus in the Cactaceae; several species have broad distribution ranges and have successfully adapted to distinct habitats. One explanation for their success is the diversity of their reproductive systems. Opuntia macrocentra is one of the most common widespread species in North American deserts. A previous work on a northern population documented that this species has a mixed‐mating system and receives a low frequency of pollinators. In a southern population of O. macrocentra, we described its floral visitors, anthesis schedules and flower morphometry. Through controlled pollination experiments (selfing, outcrossing, supplementary pollen and natural pollination), we assessed the breeding and mating systems and measured pollen limitation. Eight different bee species visited the flowers. Based on their conduct, Diadasia rinconis and Lasioglossum sp. were the main pollinators. Flowers were homogamous and herkogamous. Floral traits and pollination experiments showed that O. macrocentra is xenogamous and self‐incompatible. Fruit set of the natural pollination, outcrossing and supplementary pollen treatments were not statistically different. Seed set was higher in natural pollination and the pollen limitation index for seed set was negative. Based on these results, we conclude that O. macrocentra is not pollen limited in the studied population. These results contrast with those of the previously studied population; therefore, we caution about making generalizations about the reproductive system based solely on studies in one population. The diversity of mating systems displayed by O. macrocentra may explain its broad distribution and adaptation to different environmental factors, one of which may be pollinator availability. Our results highlight the need to describe the reproductive ecology of populations instead of species, because reproductive systems and ecological factors such as plant–animal interactions may differ across their distribution range.

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

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.

Pollination efficiency and pollen limitation in bistaminate vs tetrastaminate Lamiaceae

AbstractThe evolution of bilabiate flowers in Lamiaceae has several times led to a reduction in stamen number. It is generally assumed that stamen reduction goes along with decreasing pollen production. One should, therefore, expect that bistaminate flowers have either a more efficient pollen transfer mechanism or a higher selfíng rate than tetrastaminate species to adapt to the stamen reduction. We tested this hypothesis in a community of Lamiaceae including three bistaminate and three tetrastaminate species. The results of selfing experiments, extra‐pollination, counting pollen number, and stigmatic pollen load analysis were used to calculate the autonomous selfing index, the pollen limitation index, and the pollination efficiency index. The results indicate a significantly lower pollen number in bistaminate flowers than in tetrastaminate flowers of similar anther size. Bistaminate species shared a higher selfing rate which was related to their structural adaptation to delayed selfing. In Ziziphora clinopodioides, the delayed selfing was accompanied by low pollination efficiency, and plants suffered from pollen limitation at the location studied. However, in Salvia sclarea and Salvia hypoleuca, which benefited from a relatively high pollination efficiency, no pollen limitation was observed. Our results reveal a close association between adaptive mechanisms such as increasing precision of pollen transfer and evolution of delayed selfing with stamen reduction in bistaminate Lamiaceae.

Are Reproductive Traits Related to Pollen Limitation in Plants? A Case Study from a Central European Meadow.

The deficiency of pollen grains for ovule fertilization can be the main factor limiting plant reproduction and fitness. Because of the ongoing global changes, such as biodiversity loss and landscape fragmentation, a better knowledge of the prevalence and predictability of pollen limitation is challenging within current ecological research. In our study we used pollen supplementation to evaluate pollen limitation (at the level of seed number and weight) in 22 plant species growing in a wet semi-natural meadow. We investigated the correlation between the pollen limitation index (PL) and floral traits associated with plant reproduction or pollinator foraging behavior. We recorded significant pollen limitation for approximately 41% of species (9 out of 22 surveyed). Seven species had a significant positive response in seed production and two species increased in seed weight after pollen supplementation. Considering traits, PL significantly decreased with the number of pollinator functional groups. The relationship of PL with other examined traits was not supported by our results. The causes of pollen limitation may vary among species with regard to (1) different reproductive strategies and life history, and/or (2) temporary changes in influence of biotic and abiotic factors at a site.

Breeding-system comparison between alien invasive Solanum rostratum and its non-invasive congener S. americanum

Solanum rostratum is a severely invasive alien plant species in China. Using four S. rostratum populations and non-invasive congener S. americanum, we conducted a common garden experiment to compare their breeding systems. No significant difference in average seed set between the two species under open pollination and supplementary pollination conditions. However, under the bagged self-pollination condition, S. rostratum had significantly lower average seed set (29.5%) than S. americanum (47.0%). No fertile seeds were detected in the emasculation treatments for both species, suggesting no autonomous apomixis in them. S. rostratum had a lower average autofertility index (0.38) than S. americanum (0.64). S. rostratum had higher average pollen limitation index (0.29) and average pollinator's contribution index (0.49) than S. americanum (0.08 and 0.31, respectively). S. rostratum was found in 12 provinces of China and in 3835 locations globally, which were lower than S. americanum with 18 Chinese provinces and 10897 locations globally. The invasive alien S. rostratum had lower self-compatibility than the non-invasive alien S. americanum. Thus, the invasiveness of those two species was not significantly correlated with their self-compatibility, but positively correlated with their distribution range.

Comparative pollen limitation and pollinator activity of Caragana korshinskii Kom in natural and fragmented habitats

In many flowering plants, fragmented habitats may affect pollen limitation, pollinator behavior, and plant-pollinator interactions. Pollen limitation may decrease plant reproduction due to low levels of pollen transfer and inadequate pollen receipt. However, how fragmented habitats affect the pollen limitation and pollinator activity of Caragana korshinskii Kom. still needs further study. We designed a pollen supplementation treatment to understand how pollen limitation affects seed set. We calculated the visiting patterns and frequency of pollinators in different habitat types (natural and fragmented) to determine the effect of fragmented habitats on pollinator activity and on the pollination success of a desert-grassland shrub. Our results demonstrated that pollen supplementation was found to significantly increase seed set per flower, which is pollen-limited in the studied species. Moreover, the pollen limitation index in fragmented habitats was increased compared to that of natural habitats. Apis mellifera was found to be the dominant pollinator, with more pollinators and a higher visitation frequency of A. mellifera found in natural habitats compared to fragmented habitats. Our results showed that pollen limitation intensity was significantly correlated with the pollinator visitation frequency in the both habitats. Outcrossing was dominant in the breeding system, and insect pollination played a critical role in outcrossing. We found that fragmented habitats could affect pollinator activity, which might reduce pollen dispersal among flowers and the probability of outcrossing in the studied habitats.

Pollen limitation and its effect on seed germination

AbstractIn nature, fruit and seed production in many plants have been shown to be pollen limited. Pollen limitation is demonstrated when open-pollinated plants that are hand-supplemented (Ps) with outcross pollen produce more fruits and/or seeds than open-pollinated controls that are not hand-pollinated (Po). There are three categories of results in such studies: Ps> Po, Ps= Poand Ps< Po, in which case pollen limitation indices are positive, zero and negative, respectively. In an index widely used to calculate pollen limitation, 1 – (Po/Ps), the bounds for Ps≥ Poare 0 to + 1, whereas the bounds for Ps< Poare 0 to –∞. The first aim of this review was to show how the pollen limitation index can be modified so that the bounds of Ps< Poare 0 and –1, whereupon the index gives equal weight to the best performer (Psor Po) and worst performer (Psor Po). In addition to seed quantity, pollen supplementation can affect seed quality, including germinability. Thus, our second aim was to summarize the results of studies that have also tested the effect of pollen limitation on seed germination. In short, the 30 case studies in 15 families, 16 genera and 18 species that we identified show that seed germination percentage increased, was not affected or decreased by pollen supplementation in 12, 11 and seven cases, respectively. The effect of pollen limitation on seed germination, which can be quite large, has not been considered in developing population growth models to determine the effect of pollen limitation on λ.

The Floral Biology, Breeding System and Pollination Efficiency of Schima superba Gardn. et Champ. (Theaceae)

Schima superba Gardn. et Champ. is a perennial, evergreen tree valued for its eco-protection and commercial values in China. In this study, we investigate the breeding system, reproductive ecology and pollination biology of S. superba in a seed orchard. The flowers are hermaphrodite and protogynous. The viability of the pollen is inactivated rapidly, and the stigma maintains a high receptivity within the flower lifespan. Flowers typically offer pollen and nectar to visitors. The flowers possess a typical insect pollination syndrome, and three visitors (Apis cerana cerana Fabricius, Protaetia brevitarsis Lewis, and Popillia mutans Newman) are observed on flowers during the study period. The visitation frequency per minute and capability of pollen removal and deposition of A. cerana are significantly higher than P. brevitarsis and P. mutans, although the pollinator efficiency is lower than those shown by the two beetles. Fruit set (28.27%) and seed set (6.57%) percentages resulting from open-pollination are significantly lower than those resulting from cross-pollination (fruit/seed set, 43.73%/11.66%), and the pollen limitation index (L) was 0.34, suggesting that seed production is pollen-limited in the seed orchard. The pollen/ovule ratio (P/O) and outcrossing index (OCI) values are 6686.67 and 4, respectively. The self-incompatibility index (ISI) was estimated to be 0.95. Results from hand-pollination, pollen tube growth experiments and the ISI value show that S. superba is late-acting self-incompatible. The synthetic results indicate that A. cerana is the most efficient pollinator of S. superba, and seed production is frequently limited by pollinators, fruit abortion, and pollen quality.

Pollen Limitation in a Rare Cactus with Synchronous Mass Flowering

Abstract: Plant fitness is reduced by pollen limitation when the amount and quality of pollen deposited on stigmas is restricted. Pollen limitation has direct implications in mating system and floral evolution, and negatively affects population dynamics. We assessed pollen limitation in the cactus Ariocarpus kotschoubeyanus from the western Chihuahuan Desert. We performed a supplementary pollen treatment then compared outcomes with naturally pollinated flowers using generalized linear models (GLM) and a pollen limitation index (L). Floral aperture was compared between days of anthesis using a single ANOVA, whereas nectar production was contrasted between covered/uncovered flowers and days of anthesis using a factorial ANOVA. Results of both GLM and L show that seed set proportion decreases 0.22 as a result of pollen limitation in natural pollinated flowers contrasted with pollen-supplemented flowers. Most flowers opened two days, and floral aperture between the first and second day varied slightly. Nectar...

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

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.

Pollen limitation affects reproductive outcome in the bird-pollinated mangrove Bruguiera gymnorrhiza (Lam.) in a highly urbanized environment

Urban mangrove systems are increasingly common in SE Asia but little is known about the potential changes in pollinator ecology in highly urbanized and fragmented landscapes. We detected pollen limitation across four Bruguiera gymnorrhiza populations in Singapore with a pollen limitation index (compromised seed production due to insufficient pollen receipt) ranging from 0.633 to 0.878. Trees in larger patches had higher pollinator visitation rates than in smaller patches, and lower pollinator visitation rates resulted in reduced fruit sets. These results suggest a cascading link between habitat patch size, pollinator visitation rate, and reproductive outcomes in B. gymnorrhiza. Mating system analysis indicated that B. gymnorrhiza may have an internal mechanism acting against inbreeding depression, leading to reduced fruit set under circumstances of reduced pollinator visitation. Our results underscore the importance of pollinator service in mangroves and highlight the need for an in-depth understanding of changing plant–pollinator relationships in urban mangroves systems.

Dependence on sunbird pollination for fruit set in three West African montane mistletoe species

Abstract:Theory predicts that not all plant species will be equally affected by disruption to their pollinator mutualisms because traits such as breeding system and mutualism strength can affect their response. We investigated these traits in three species of Afromontane mistletoe Globimetula braunii, Agelanthus brunneus and A. djurensis in Ngel Nyaki Forest Reserve, Nigeria, to test whether the traits were reliable indicators of relative reproductive success and could be used to predict relative vulnerability to pollinator loss. For each mistletoe species, insect and bird visitors were identified during a 160–240-min observation period of 4–10 plants and their roles in flower opening and fruit set were investigated using exclusion experiments applied to 250–500 flowers. We found that all three mistletoes are self-compatible but not capable of autonomous self-fertilization. The pollinator assemblage comprised four species of sunbird (Cyanomitris spp., Cinnyris spp.) and a small social wasp (Vespinae). None of the mistletoes requires birds for flower opening: G. braunii flowers self-opened in the absence of pollinators, whereas insects opened both Agelanthus spp. Irrespective of flower opening, each mistletoe species requires sunbirds for effective pollination and fruit set. Only G. braunii demonstrated pollen limitation (pollen limitation index = 0.504) which may be an early indication of mutualism breakdown. We suggest that mistletoes be considered as indicators of habitat condition and functioning within Afromontane forest ecosystems.

Insects facilitate wind pollination in pollen-limited Crateva adansonii (Capparaceae)

Low fruit-set in obligately outbreeding plant species is attributed to a variety of reasons that can be ascertained from reproductive studies. In the present work, the causes of poor natural fruit-set in Crateva adansonii DC. were investigated. Floral biology, the role of wind and insects in pollination and the breeding system of the species were studied in two natural populations for three consecutive seasons (2006–08). The flowers exhibited traits conducive to a mixture of wind and insect pollination (ambophily). Although a variety of insects visited the flowers, they were ineffective in pollinating. Nevertheless, active foraging by the honeybees (Apis dorsata, A. mellifera and A. cerana indica) facilitated enhanced pollen dispersal in the air and resulted in indirect pollination by wind. Airborne pollen grains pollinated the plants only up to 10 m. Fruit-set from open pollination was comparable to wind-pollinated flowers. Supplemental pollination treatments established the occurrence of strong self-incompatibility (SI) (index of SI = 0.14). Spontaneous autogamy was prevented by pronounced herkogamy. Low natural fecundity in C. adansonii is due to pollination failure, pollen limitation (pollen limitation index = 0.98) and the sparse distribution of the conspecifics; partial SI may partly ensure reproductive assurance through geitonogamy. In the absence of a pollinator wind appears to act as a secondary mode of pollination.

Is the pollen‐limited mistletoe Peraxilla tetrapetala (Loranthaceae) also seed limited?

Abstract Seed production in the endemic New Zealand mistletoe Peraxilla tetrapetala (Loranthaceae) has been shown to be consistently pollen limited, but to date there has been no test of whether the species is also seed limited. If it is not seed limited, then pollen limitation may have no effect on population size. We tested for seed limitation by sowing seeds onto host trees at high and low densities at two sites, and following survival for up to 69 months. Our rationale was that unless there is strong density‐dependent seedling mortality sufficient to negate increases in seed supply, the species would be seed limited. We simultaneously measured pollen limitation at both sites using pollen augmentation. Peraxilla tetrapetala was strongly pollen limited at both sites over 7 years at Ohau (mean Pollen Limitation Index 0.62), and 12 years at Craigieburn (mean PLI 0.44), before and during the seed‐limitation study. There was no significant overall negative effect of density on survival in sown P. tetrapetala seeds over 42–69 months. There was a significant positive effect: seeds were more likely to adhere to branches when sown at high densities. This initial advantage to high‐density seeds was gradually eroded by slightly (but non‐significantly) lower survival rates of adhered seeds at high density. By the end of the study there was no significant difference in overall survival in high and low density plantings. This means that P. tetrapetala was apparently both pollen limited and seed limited at both our sites. Hence, reduced densities of native bird pollinators caused by introduced mammalian carnivores are likely to reduce the density of adult mistletoes in the next generation. However, the generality of this result may be affected by the fact that mistletoes do not have a dense ‘seedling shadow’ under the parent mistletoe.