Generalized Pollination System Research Articles

Pollination by multiple species of nectar foraging Hymenoptera in Prasophyllum innubum, a critically endangered orchid of the Australian Alps

Context Australia has numerous threatened species of terrestrial orchid, with a particularly high incidence of rarity in the genus Prasophyllum R.Br. Although there has been research on mycorrhizal associations and propagation, little is known about the reproductive ecology of threatened Prasophyllum. Understanding which animals are responsible for pollination and the impact of herbivores on reproduction may inform conservation actions. Aims For the nationally Critically Endangered Prasophyllum innubum, we aimed to determine the pollinator species, test for self-pollination, quantify levels of reproductive success and herbivory, and identify herbivores. Methods Pollinator observations were undertaken at wild populations of P. innubum, whereas an experiment testing for self-pollination was undertaken in shadehouse conditions. We quantified reproductive success and herbivory at two populations and attempted to identify herbivores using game cameras. Key results Pollination occurred via three species of bee and a sphecid wasp, all of which attempted feeding on floral nectar. Fruit set averaged 72–84% at wild sites, whereas only 6% of flowers set fruit via self-pollination when insects were excluded. Just 4% of inflorescences were completely consumed by herbivores, and no herbivory was captured on camera. Conclusions P. innubum has a generalist rewarding pollination system that confers high levels of reproductive success, with herbivory having little impact on reproduction. Implications Pollinator availability is unlikely to restrict conservation translocation site selection of P. innubum because of a generalist pollination system. If herbivores are a threat for this species, it is likely to be through alteration of habitat rather than direct grazing.

Generalist southern African temperate forest canopy tree species have distinct pollinator communities partially predicted by floral traits

AbstractForest canopies provide important resources for insect communities via flowers. Yet, pollination systems of tall forest trees are poorly studied, resulting from the difficulties in observing pollinator activity at the canopy level and great temporal variation in flower production. In temperate forest canopies of the southern hemisphere, small, whitish and generalist flowers seem to dominate. Here, we observed insect flower visitors, at the canopy level, to four southern Afrotemperate forest tree species bearing small, white to green flowers in a large, indigenous forest. Additionally, we quantified flower traits and collected pollen from representative insect visitors. A total of 105 insect species, from 48 families and 7 orders, were observed visiting flowers. In terms of total flower visits, the generalist Cape honey bee (Apis mellifera capensis) made up ca. 57% of all flower visits. A third of the total observation time covered crepuscular to nocturnal flower visits; yet only 12.68% of total visits took place during this time. Interestingly, despite both trees and insects being largely generalist in their interactions with one another (supported by the presence of conspecific and heterospecific pollen on most flower visitors), some insect species showed strong preferences for specific species of tree, driving dissimilar, interspecific assemblages of flower visitors. The pollinator community disparity may be explained through the unique and dissimilar floral traits for each tree species, both in flower size and in petal reflectance. We conclude that within generalist pollination systems, distinct and non‐random mutualisms can develop between different species of plants and a diverse suite of pollinators, and that floral traits could partially predict such interactions.

Heterospecific pollen avoidance strategy prevails in the generalized plant-pollinator network on Yongxing Island.

Heterospecific pollen (HP) deposition varies widely among species in communities, which has been explicated by two adaptation strategies: HP avoidance and HP tolerance. Studies of the plant-pollinator network have uncovered that oceanic island communities are highly generalized and strongly connected. It remains unclear, however, which strategy prevails in such communities. We examined stigma pollen deposition on 29 plant species, and assessed patterns of HP load size and diversity in the Yongxing Island community. We assessed the effects of phenotypic specialization and species-level network structural properties of plant species on pollen deposition among species. The hypothesis of three accrual patterns of HP within species was tested by illustrating the relationship between conspecific pollen (CP) and HP receipt. Extensive variation occurred among species in HP receipt, while 75.9% of species received less than 10% HP and one species received more than 40% HP throughout the community. Flower size strongly drives the variation of HP receipt, while network structural properties had no effect on the pollen receipt. Nineteen species showed no relationship between the number of HP and CP loads, and they received smaller HP load sizes and lower HP proportions. Most plant species evolved HP avoidance strategy, and HP receipt was an occasional event for most plant species in the generalized community. HP and CP receipts are independent of each other in plant species with the HP avoidance mechanism. Our results highlight that plants in the generalized pollination system may preferentially select to minimize the HP load on stigmas.

Night and day: Contributions of diurnal and nocturnal visitors to pollen dispersal, paternity diversity, and fruit set in an early-blooming shrub, Daphne jezoensis.

Under uncertain pollinator visit conditions, plants often exhibit long flowering periods and generalized pollination systems. Flowering of the gynodioecious shrub Daphne jezoensis occurs in early spring in cool temperate forests. Pollination by nocturnal moths is expected, given the species' tubular-shaped flowers with sweet fragrance and nectar. However, the effectiveness of nocturnal moths under cool conditions is unknown. We evaluated the relative importance of diurnal and nocturnal visitors as pollinators in early spring. We investigated flowering duration, flower visitors, and floral scents in a natural population. We experimentally exposed flowers to visitors only during daytime or nighttime using bagging treatments and evaluated the contributions of diurnal and nocturnal insects to fruit set, pollen dispersal distance, and paternity diversity using 16 microsatellite markers. Female flowers lasted ~3 wk, which was ~8 d longer than the flowering period of hermaphrodites. Various insects, including Coleoptera, Diptera, Hymenoptera, and Lepidoptera, visited the flowers during both daytime and nighttime. Flowers emitted volatiles, such as lilac aldehyde isomers and β-ocimene, which are known to attract moths. Fruit-set rate in the night-open treatment was similar to or higher than that in the day-open treatment. However, pollen dispersal distance in the night-open treatment was shorter than that in the day-open treatment. Paternity diversity was similar in day-open and night-open treatments. Early-blooming plants ensure pollen receipt and dispersal by having a long flowering period and using both diurnal and nocturnal flower visitors, suggesting the importance of a generalized pollination system under uncertain pollinator visit conditions.

Pollination biology of Sicyos angulatus: An invasive plant primarily pollinated by the native insects and introduced honeybee Apis mellifera

AbstractBurcucumber (Sicyos angulatus), first introduced in 1952 from North America to Japan, has recently become a seriously invasive alien species that has spread nationwide. The pollination mode is likely to play a crucial role in seed production and invasion. Burcucumbers have been characterized as self‐compatible flowers with distinct anthers and stigmas, indicating pollen vector‐mediated pollination. In this study, we aimed to describe the floral biology of burcucumbers and clarify their relationships with pollinators. We found that: (1) primarily native insects (at least 70 species) repeatedly visited burcucumbers, both during the day and night; (2) in terms of visitation frequency and pollen‐carrying load, honeybees, vespid wasps, and hoverflies were the most important diurnal pollinators, followed by sphingid and noctuid moths as nocturnal ones; and (3) the production of highly concentrated nectar as floral reward coupled with floral scents, predominantly aliphatic compounds such as heptanal and hexanol, may mediate the visitation of floral visitors. Our observations confirmed that burcucumber visitation is dominated by native pollinators, indicating the integration of burcucumbers into native pollinator webs. Our findings highlight the significance of a generalized pollination system in alien plants to overcome reproductive failure within a new region.

Putative Signals of Generalist Plant Species Adaptation to Local Pollinator Communities and Abiotic Factors.

The reproductive success of flowering plants with generalized pollination systems is influenced by interactions with a diverse pollinator community and abiotic factors. However, knowledge about the adaptative potential of plants to complex ecological networks and the underlying genetic mechanisms is still limited. Based on a pool-sequencing approach of 21 natural populations of Brassica incana in Southern Italy, we combined a genome-environmental association analysis with a genome scan for signals of population genomic differentiation to discover genetic variants associated with the ecological variation. We identified genomic regions putatively involved in the adaptation of B. incana to the identity of local pollinator functional categories and pollinator community composition. Interestingly, we observed several shared candidate genes associated with long-tongue bees, soil texture, and temperature variation. We established a genomic map of potential generalist flowering plant local adaptation to complex biotic interactions, and the importance of considering multiple environmental factors to describe the adaptive landscape of plant populations.

Secondary pollinators contribute to reproductive success of a pink-flowered sand verbena population.

Secondary pollinators contribute to reproductive success of a pink-flowered sand verbena population.

Are floral traits and their phenotypic variability related to plants with generalized or specialized pollination systems? A community perspective

Flower traits under selection by specialized pollinators may experience a decrease in their phenotypic variation. Another viewpoint suggests that flower traits of plants under selection by generalized pollinators could display comparable variability to that of plant species with a specialized pollination system. We evaluated the following alternatives: (a) species with specialized pollination system (zygomorphic flowers, long corolla tube and higher amount of nectar, and visited by only one group of pollinators) will present higher natural fruit set and less floral phenotypic variation in comparison with species with generalized pollination system (actinomorphic flowers with short corolla tube and comparatively lower amount of nectar, and visited by a wide spectrum of taxonomically diverse pollinator species); (b) alternatively, if species with generalized pollination system show similar reproductive success to that of with specialized pollination system, comparable phenotypic variation in flower traits will be expected between them. Natural fruit set, corolla tube length, amount of nectar per flower, nectar sugar composition, and variability of these floral traits were measured in 43 biotically-pollinated species growing in a Chaco Serrano community from central Argentina. Plants were classified as specialists or generalists based on focal observations made to record their pollinators. Correlations and General Linear Models were used to compare fruit set and flower traits between plant species with generalized and specialized pollination system. Plants with specialized pollination system display flowers with higher amounts of nectar than plants with generalized pollination system. Nevertheless, species with generalized and specialized pollination system showed similar fruit set and floral phenotypic variation (except for the percentage of sucrose). The trends observed in species with generalized or specialized pollination systems from the Chaco forests suggest that pollinators could be an effective evolutionary force in selecting primary and secondary floral traits for both types of plant species.

Heterostyly, incompatibility system and pollinators in Varronia spinescens Borhidi (L.) (Cordiaceae)

Heterostyly, the reciprocal position of sexual organs between different morphs within a population, is assumed to promote cross-pollination in hermaphroditic plants. Heterostyly is usually linked to an incompatibility system where only the crosses between the different morphs produce fruit. Although heterostyly has been frequently studied in plant species with specialized pollination systems, few studies have investigated this in species with a broad spectrum of floral visitors. Here, we describe the heterostyly of Varronia spinescens and conducted hand-pollination experiments in the field to determine the incompatibility system. We also analysed perianth morphology, morph-ratio, adaptive inaccuracy in reciprocity and pollinator visitation rate in relation to floral morph and number of open flowers. Our results indicate that V. spinescens is a distylous species with a high degree of reciprocity between the sexual organs, presenting a non isoplethic morph ratio with a bias towards the long style (L-) morph. The incompatibility system is heteromorphic and the studied population received visits by a very high number of visitor and pollinator species. Varronia spinescens is thus the heterostylous species of the genus with the second-highest number of registered pollinators. Our results suggest that in a generalist pollination system with little floral morphological restriction to pollinators, the maintenance of sexual polymorphism is likely associated with a high reciprocity between morphs.

Highlighted articles for March 2022.

Highlighted articles for March 2022.

Reproductive biology of the invasive Gleditsia triacanthos L. (Fabaceae)

Biotic invasions constitute a threat for natural communities, affecting ecological and evolutionary integrity of natural ecosystems. Gleditsia triacanthos is an invasive species in many regions of the world. In Argentina, its populations are expanding over native vegetation of different ecoregions. The aim of this work is to study the reproductive biology of the invasive honey locust, characterizing the reproductive individuals, the assemblage of pollinators, the pollination process, the compatibility system, and the reproductive success. Considering that G. triacanthos could be characterized as a novel invader in Argentina and plant-pollinator interactions could be important to facilitate plant invasions, we expect to find (a) an assembly of generalist floral visitors that promote pollination; (b) that fruits and seeds could be produced through self- (autogamy) or cross-pollination (mediated by pollinators); (c) that pollinators can increase reproductive success of exposed flowers compared to those experimentally isolated from pollinators. The studied populations (Córdoba Province, central Argentina) can be characterized as polygamous andro-dioecious, with a higher proportion of male individuals. Although honeybees were the most frequent pollinator, all floral visitors could be potential pollinators and the honey locust can be characterized as pollinator-generalist. G. triacanthos produces fruits and seeds by spontaneous self-pollination, but a higher reproductive success was observed after hand cross- or natural pollinations. Producing both self- and cross-pollinated seeds could be advantageous for this species during different stages of the invasion process. The generalist pollination system presented by G. triacanthos, the high production of pollen by male individuals compared to the individuals with perfect flowers, and the higher fruit and seed set by cross- or natural pollinated flowers are all traits favouring the invasion process. These reproductive traits could be considered when designing management strategies to control the expansion of this invasive species.

First report on generalized pollination systems in Melastomataceae for the Andean páramos

AbstractMelastomataceae is a megadiverse family with records of transitions from specialized to generalized pollination systems for several species. These transitions are associated with the colonization of new, unpredictable and/or impoverished pollinator habitats or habitats where specialized pollinators are scarce (e.g., in highland environments). The bee species diversity is low in highlands. Therefore, autonomous breeding systems such as apomixis and self‐pollination emerge in these environments. In this paper, we studied the floral traits associated with the generalization of pollination systems and registered the floral visitors of two species in the Colombian Andes: Miconia cataractae and M. elaeoides. We investigated the breeding system of M. elaeoides. Both species presented small flowers, short anthers of medium pore size, and nectar‐producing stomata on the base of the anthers. Miconia cataractae produced an average of 1.62 μl nectar/flower, a sugar concentration of 6.78%, whereas M. elaeoides produced 0.09 μl nectar/flower, a sugar concentration of 6.13%. We recorded a wide diversity of pollinators for both species, mainly insects from the orders Hymenoptera and Diptera. Miconia elaeoides presented a mixed breeding system and was also capable of setting fruits by apomixis. We conclude that flower and anther morphology, combined with nectar production, thus represent convergent traits resulting in a generalist pollination system shared by M. cataractae and M. elaeoides. Here, we presented the first generalist pollination system recorded for Miconia (and the Melastomataceae) in the Andes, the first report for a species from the small‐pored section Amblyarrhena, and the first report for a species from the large‐pored section Cremanium in Colombia.

Two dioecious Simarouba species with a specialized pollination system and low reproductive efficacy in Central Brazil

Abstract Several possible correlations between dioecy and eco-morphological features have been suggested to infer the conditions that would favor this sexual system. Dioecy has been associated either with specialized or generalized pollination systems. The genus Simarouba has six dioecious species that seem to have generalized pollinators. In this study, we examined the reproductive biology aspects of two Simarouba species to evaluate which of their eco-morphological attributes may favor dioecy. Our data suggest that S. amara and S. versicolor have small, inconspicuous, and abundant flowers of nocturnal anthesis and are only pollinated by nocturnal moths. They have a stable sexual system with flower, inflorescence, and flowering phenology dimorphism that is part of their pollination system strategies. Male plants of both species produce more flowers per individual than do female plants. A larger floral display may have an essential role in increasing male reproductive success. However, both species showed low reproductive efficacy, especially S. versicolor. The low reproductive efficacy may be due to the lack of pollinators or to the inefficacy of the pollinators available locally.

Nocturnal ant integrates generalist pollination system in the Caatinga dry forest.

Nocturnal ant integrates generalist pollination system in the Caatinga dry forest.

Phenotypic plasticity guides Moricandia arvensis divergence and convergence across the Brassicaceae floral morphospace.

Many flowers exhibit phenotypic plasticity. By inducing the production of several phenotypes, plasticity may favour the rapid exploration of different regions of the floral morphospace. We investigated how plasticity drives Moricandia arvensis, a species displaying within-individual floral polyphenism, across the floral morphospace of the entire Brassicaceae family. We compiled the multidimensional floral phenotype, the phylogenetic relationships, and the pollination niche of over 3000 species to construct a family-wide floral morphospace. We assessed the disparity between the two M. arvensis floral morphs (as the distance between the phenotypic spaces occupied by each morph) and compared it with the family-wide disparity. We measured floral divergence by comparing disparity with the most common ancestor, and estimated the convergence of each floral morph with other species belonging to the same pollination niches. Moricandia arvensis exhibits a plasticity-mediated floral disparity greater than that found between species, genera and tribes. The novel phenotype of M. arvensis moves outside the region occupied by its ancestors and relatives, crosses into a new region where it encounters a different pollination niche, and converges with distant Brassicaceae lineages. Our study suggests that phenotypic plasticity favours floral divergence and rapid appearance of convergent flowers, a process which facilitates the evolution of generalist pollination systems.

Phylogenetic conservation and shifts of pollination niche in generalist epiphytic cacti

Plant-pollinator interactions are influenced, among other factors, by evolutionary history of the organisms. Thus, closely related species are expected to interact with similar pollinator assemblages. The aim of this study was to examine the evolution of pollination niches in neotropical epiphytic cacti. We recorded floral visitors and determined the pollination niche of 11 species of Rhipsalis and one species of Hatiora by using bipartite modularity, a metric of complex networks that is effective to identify pollination niches. Afterwards we explored how these niches evolved along the phylogeny of Rhipsalis. We recorded a total of 56 insect species belonging to nine functional groups pollinating those species of Rhipsalis. The most frequent floral visitors were bees. Pollination systems in Rhipsalis broadly combined a high phenotypic floral generalization with moderate richness of pollinator species and some functional pollinator group specialization. Four pollination niches were identified, mainly characterized by variations in the frequency of the functional groups of pollinators. The closer the species of Rhipsalis were, the more they interacted with the same functional groups of pollinators, as indicated by a positive phylogenetic signal for pollinating niches. The most likely ancestral pollination niche was associated with short-tongued bees. From the niche defined by small bees at least three shifts occurred towards the niches defined by extra-small bees, short-tongued medium bees, and flies. Considering the perspective of the evolution of each pollinator group, short-tongued bees were conserved along the branches of Rhipsalis phylogeny, with niche broadening or shifts associated with other groups such as flies, large bees, wasps, beetles and butterflies. Distinct generalist pollination niches have evolved in the genus. Shifts in pollination niches were related to differences in floral morphology. Moreover, the distribution of pollination niches only partially corresponded to the infrageneric classification of Rhipsalis. Our results support that generalist pollination systems encompass different pollinating niches, which may be consistently distributed across clades in angiosperm lineages.

Flowering segregation and pollinator distinctiveness contribute to coexistence in an extremely generalist plant group

Background Flowering time determines potential plant mates, and it is related to gene flow within and among plant populations arising from different selective forces and interspecific interactions between plants with similar pollination niches. However, these effects on flowering phenology of plants with generalist pollination systems have received little attention and hence our knowledge of the contribution of generalised pollination systems on the evolution of adaptative traits, such as the flowering time contains lacunae. Aims To verify the effective contribution of interspecific plant interactions in a generalised pollination system to the structuring of flowering phenology. Methods We recorded the reproductive phenophases of four Baccharis species in a subtropical grassland. We evaluated their flowering patterns by a niche overlap index and compared it with a null model. We used ecological network metrics from insect visitors recorded to determine the pollinator network structure. Results A staggered flowering pattern and distinctiveness of insect pollinators with non-signal of modularity and a variation in the Baccharis-pollinators network structure throughout the year were observed. The distinctiveness on pollinators with a strong bee-dependence added to temporal divergence on flowering among the species leads to no negative effects on fruit set. Conclusion The temporal segregation on flowering peaks and low pollinator similarity appear to underlie to coexistence of Baccharis species studied in southern Brazil.

Comparative Pollination Ecology of Five EuropeanEuphorbiaSpecies

Premise of research. Flowers of the genus Euphorbia are arranged in a unique type of inflorescence called cyathia, packed into more or less dense synflorescences. These synflorescences can be showy or inconspicuous, suggesting different pollination strategies.Methodology. We described and compared the morphology, color, scent, and insect guilds visiting the synflorescences of five European Euphorbia species, two with inconspicuous synflorescences and three with showy ones.Pivotal results. All five species present their reproductive structures openly, with easily accessible nectaries. In the inconspicuous E. peplus and E. dulcis, there was little color contrast between the reproductive parts and the vegetative parts. Both species attracted low numbers of insects (Diptera and Hymenoptera), and these insects carried little (E. peplus) or no (E. dulcis) pollen. We did not detect any floral scent for E. peplus. In the showy E. amygdaloides, E. virgata, and E. verrucosa, the color of the reproductive parts and of the relatively large nectaries was standing out clearly against vegetative organs. These species attracted up to 14 times more insects (Diptera, Hymenoptera, Coleoptera) than the inconspicuous species, and these insects carried larger amounts of pollen on their bodies. In E. verrucosa, nearly half of the pollinators were sawflies from the genus Tenthredo feeding and mating on the synflorescences. All Euphorbia species except E. peplus were also visited by ants. However, the role of ants as pollinators remains to be tested. Finally, E. peplus and E. dulcis can reproduce without insect pollination, whereas among the showy species, E. virgata did not produce seeds when pollinators were excluded.Conclusions. We found that all study species had similar generalist pollination systems, with the showy species attracting significantly more insects and the inconspicuous species being largely independent of insect visits for reproduction. Our study tentatively indicates that the degree of entomophily seems positively correlated with showiness and size of attractive and rewarding organs.

Nocturnal and diurnal pollination in Copaifera coriacea, a dominant species in sand dunes of the Middle São Francisco River Basin, Northeastern Brazil

Background and aims – Copaifera coriacea, a species in the resin-producing clade Detarioideae (Leguminosae), is an endemic and abundant species found in sand dunes in Brazilian Caatinga domain vegetation – a Quaternary paleodesert. We investigated floral traits and aspects of pollination biology, focusing on the pollination system of C. coriacea. Material and methods – Anthesis duration, stigma receptivity, pollen viability, nectar concentration, and the presence of osmophores and pigments reflecting UV light were assessed. Floral visitors were classified as potential pollinators, occasional pollinators or thieves, based on the time and foraging behaviour and resource collected. Pollination effectiveness were assessed for potential pollinators by the detection of pollen tubes on the stigma or stylar canal by epifluorescence microscopy.Key results – The species has white and small flowers, with anthesis beginning in the dark (ca 00:30) and the flowers are completely opened approximately 3 h later, when a sweet odour is perceptible. The onset of stigma receptivity and pollen grain viability occurs only after the completion of flower opening, and a concentrated nectar is available during the day. The presence of pollen tubes confirmed the efficiency of the main insects in the transfer of pollen. Conclusion – Our result demonstrates that C. coriacea has a generalist pollination system mediated mainly by two distinct guilds of insect pollinators: moths (nocturnal, searching for nectar) and bees (diurnal, pollen collectors). This finding can provide more information about diversification in the genus Copaifera.

Insects or Wind? New findings on the pollination system of Euterpe edulis (Arecaceae)

The palm Euterpe edulis is an important palm species for the extraction of palm heart, a highly profitable consumable product. Due to its importance, much research has been conducted around the ecology of this palm species. Nevertheless, information available on its reproductive ecology is quality-deficient and fragmented, resulting in misleading views of the pollination and reproductive ecology of E. edulis. Here we conduct the first thorough study assessing the relative dependence on animal pollination of E. edulis in Argentina, and conduct parallel detailed observations on floral visitors. Also, we integrate our results with those available for the species in the literature. Here we found that E. edulis has an ambophilic pollination system. However, in our study system, there was a predominance of wind pollination over insect pollination and the species can also set seeds in the absence of pollen. Also, our study shows in great detail the large diversity of insects visiting E. edulis, indicating the generalist pollination system of the species, where Hymenoptera and Diptera stand out in richness and frequency of visits. The palm represents a key resource for a wide diversity of insect visitors, but the palm does not rely on their efficiency to act as pollinators. The varied levels of reproductive dependence on animal versus wind pollination of E. edulis may be shaped by climatic and landscape conditions. Such alternative versatile strategies allow the species to guarantee the reproductive success under different ecological contexts.