Pollinator-dependent Plants Research Articles

Beyond pollen:ovule ratios: Evolutionary consequences of pollinator dependence and pollination efficiency for pollen and ovule production in angiosperms.

The relative per-flower production of ovules and pollen varies broadly with angiosperm mating systems, with outcrossing types commonly producing more pollen grains per ovule than selfing types. The evolutionary causes of this variation are contentious, especially the relevance of pollination risk. Resolution of this debate may have been hampered by its focus on pollen:ovule (P:O) ratios rather than on the evolution of pollen and ovule numbers per se. Using published mean ovule and pollen counts, we analyzed associations with the proportion of removed pollen that reaches stigmas (pollen-transfer efficiency) and differences between pollinator-dependent and autogamous forms within and among species. Analyses involved Bayesian methods that simultaneously considered variation in pollen and ovule numbers and accounted for phylogenetic relatedness. We also assessed the utility of P:O ratios as mating-system proxies and their association with female outcrossing rates. Median pollen number declined consistently with pollen-transfer efficiency among species, whereas median ovule number did not. Similarly, in both intraspecific and interspecific analyses, pollinator-dependent plants produced more pollen than autogamous plants, whereas ovule production did not differ statistically. Distributions of P:O ratios overlapped extensively for self-incompatible and self-compatible species and for different mating-system classes, and P:O ratios correlated weakly with outcrossing rate. Our findings demonstrate that pollinator dependence and pollination efficiency commonly influence the evolution of pollen number per flower but have more limited effects on ovule number. P:O ratios provide ambiguous, possibly misleading, information about mating systems, especially when compared among clades.

Increasing density enhances pollination and fecundity in the rewarding orchid Gymnadenia conopsea

Conspecific density is an important factor in determining the fecundity of pollinator-dependent plants. However, the outcome of increased conspecific density can range from reduced per capita pollination rates and fecundity (competition) to increased per capita pollination rates and fecundity (facilitation). I tested whether local conspecific density influenced pollination and fecundity in the rewarding orchid, Gymnadenia conopsea. I measured the distance to each of the nearest five plants in sixty patches of varying density in a large population in the Italian Apennine mountains. I examined whether pollen removal, pollen deposition, fruit, and seed set varied according to mean distance from conspecifics and plant height. After controlling for plant position in the population, the proportion of pollen removal, pollen deposition, and fruit set decreased with increasing distance from conspecifics, while pollen removal and deposition, but not fruit set, increased with increasing plant height. The proportion of viable seeds per fruit did not vary according to conspecific distance. Decreases in pollen removal, pollen deposition, and fruit set occurred within an average of 1 m distance from conspecific plants, indicating that local aggregation is an important determinant of both pollination success and fecundity. These results suggest that despite being a geographically widespread orchid, G. conopsea may suffer reduced fecundity when it occurs in small, isolated populations. Such field investigations can potentially lead to better predictions for successful re-establishment of populations of orchids under conservation-aided restoration efforts.

Plasticity in floral longevity and sex-phase duration of Lobelia siphilitica in response to simulated pollinator declines.

Pollinator declines can reduce the quantity and quality of pollination services, resulting in less pollen deposited on flowers and lower seed production by plants. In response to these reductions, plant species that cannot autonomously self-pollinate and thus are dependent on pollinators to set seed could plastically adjust their floral traits. Such plasticity could increase the opportunity for outcross pollination directly, as well as indirectly by affecting inflorescence traits. To test whether plants can respond to pollinator declines by plastically adjusting their floral traits, we simulated declines by experimentally reducing pollinator access to Lobelia siphilitica plants and measuring two traits of early- and late-season flowers: (1) floral longevity; and (2) sex-phase duration. To test whether plasticity in these floral traits affected inflorescence traits, we measured daily display size and phenotypic gender. We found that experimentally reducing pollination did not affect female-phase duration, but did extend the male-phase duration of early-season flowers by 13% and the longevity of late-season flowers by 12.8%. However, plants with an extended male phase did not have a more male-biased phenotypic gender, and plants with an extended floral longevity did not have a larger daily display. Our results suggest that plants can respond to pollinator declines by plastically adjusting both the longevity and sex-phase duration of their flowers. If this plasticity increases the opportunity for outcross pollination, then it could be one mechanism by which pollinator-dependent plant species maintain seed production as pollinators decline.

Pollinators enhance crop yield and shorten the growing season by modulating plant functional characteristics: A comparison of 23 canola varieties

Insect pollination of flowers should change the within-season allocation of resources in plants. But the nature of this life-history response, particularly regarding allocation to roots, photosynthetic structures, and flowers, is empirically unresolved. This study uses a greenhouse experiment to investigate the effect of insect pollination on the reproductive output of 23 varieties of a globally important crop—canola (Brassica napus). Overall, insect pollination modified the functional characteristics (flower timing & effort, plant size & shape, seed packaging, root biomass) of canola, increasing seed production and quality, and pollinator dependence. Reproductive output and pollinator dependence were defined by strong trait trade-offs, which ranged from more pollinator-dependent plants favouring early reproductive effort, to less pollinator-dependent plants favouring a prolonged phenology with smaller plant size and lower seed quality. Seed production decreased with pollinator dependence in the absence of pollinators. The agricultural preference for hybrid varieties will increase seed production compared to open-pollinated varieties, but, even so, pollinators typically enhance seed production of both types. Our study elucidates how insect pollination alters the character and function of a globally important crop, supporting optimization of yield via intensification of insect pollination, and highlights the beneficial effects of insect pollination early in the season.

Pollinator or pedigree: which factors determine the evolution of pollen nutrients?

A prime example of plant-animal interactions is the interaction between plants and pollinators, which typically receive nectar and/or pollen as reward for their pollination service. While nectar provides mostly carbohydrates, pollen represents the main source of protein and lipids for many pollinators. However, the main function of pollen is to carry nutrients for pollen tube growth and thus fertilization. It is unclear whether pollinator attraction exerts a sufficiently strong selective pressure to alter the nutritional profile of pollen, e.g., through increasing its crude protein content or protein-to-lipid ratio, which both strongly affect bee foraging. Pollen nutritional quality may also be merely determined by phylogenetic relatedness, with pollen of closely related plants showing similar nutritional profiles due to shared biosynthetic pathways or floral morphologies. Here, we present a meta-analysis of studies on pollen nutrients to test whether differences in pollen nutrient contents and ratios correlated with plant insect pollinator dependence and/or phylogenetic relatedness. We hypothesized that if pollen nutritional content was affected by pollinator attraction, it should be different (e.g., higher) in highly pollinator-dependent plants, independent of phylogenetic relatedness. We found that crude protein and the protein-to-lipid ratio in pollen strongly correlated with phylogeny. Moreover, pollen protein content was higher in plants depending mostly or exclusively on insect pollination. Pollen nutritional quality thus correlated with both phylogenetic relatedness and pollinator dependency, indicating that, besides producing pollen with sufficient nutrients for reproduction, the nutrient profile of zoophilous plants may have been shaped by their pollinators' nutritional needs.

A review of European studies on pollination networks and pollen limitation, and a case study designed to fill in a gap.

Anthropogenic environmental change disrupts interactions between plants and their animal pollinators. To assess the importance of different drivers, baseline information is needed on interaction networks and plant reproductive success around the world. We conducted a systematic literature review to determine the state of our knowledge on plant–pollinator interactions and the ecosystem services they provide for European ecosystems. We focussed on studies that published information on plant–pollinator networks, as a community-level assessment of plant–pollinator interactions and pollen limitation, which assesses the degree to which plant reproduction is limited by pollinator services. We found that the majority of our knowledge comes from Western Europe, and thus there is a need for baseline assessments in the traditional landscapes of Eastern Europe. To address this data gap, we quantified plant–pollinator interactions and conducted breeding system and pollen supplementation experiments in a traditionally managed mountain meadow in the Western Romanian Carpathians. We found the Romanian meadow to be highly diverse, with a healthy plant–pollinator network. Despite the presence of many pollinator-dependent plant species, there was no evidence of pollen limitation. Our study is the first to provide baseline information for a healthy meadow at the community level on both plant–pollinator interactions and their relationship with ecosystem function (e.g. plant reproduction) in an Eastern European country. Alongside the baseline data, we also provide recommendations for future research, and the methodological information needed for the continued monitoring and management of Eastern European meadows.

High niche diversity in Mesozoic pollinating lacewings

Niche diversity of pollinating insects plays a vital role in maintaining extant terrestrial ecosystems. A key dimension of pollination niches refers to the insect proboscis length that commonly matches the floral tube length. Here we describe new kalligrammatid lacewings (an iconic Mesozoic pollinating insect lineage) from late Cretaceous Burmese amber and Mesozoic sediments in China. Kalligrammatids display complex configurations of elongate mouthpart elements consisting of well-developed maxillae, labium and their palps. The mouthpart lengths vary among species, from 0.6 to 18.0 mm, suggesting corresponding variability in the floral tube lengths of Mesozoic plants. With the diversification of pollinating habits, the kalligrammatids presented highly divergent traits related to chemical communication and defence mechanisms. Together with other Mesozoic long-proboscid insects, these fossils not only reveal the high niche diversity of Mesozoic pollinating insects but also highlight the diversity of Mesozoic pollinator-dependent plants prior to the rise of angiosperms.

Scale-dependent effects of conspecific flower availability on pollination quantity and quality in an invasive shrub.

Pollen limitation can strongly influence reproduction of pollinator-dependent plants. Flower abundance can affect pollination 'quantity' and 'quality' due to its influence on pollen availability and foraging patterns of pollinators, ultimately impacting on seed production. We complemented individual-based measurements with landscape-level metrics to assess the influence of conspecific flower availability at different spatial scales on the quantity and quality components of pollination, and their impact on seed production in the invasive shrub Cytisus scoparius. In 2013-2014, we sampled 40 C. scoparius populations in Nahuel Huapi National Park, Patagonia (Argentina). In each population, we estimated the proportion of tripped flowers, fruit- and seed-set in five randomly selected individuals. The proportion of tripped flowers and the proportion of them setting fruit were used as proxies of pollination quantity and quality, respectively. Conspecific flower availability at distinct spatial scales (5-1000m) was estimated as the area covered by flowering C. scoparius from color aerial photographs. Flower availability influenced seed output due to contrasting scale-dependent effects on pollination quantity and quality. Increasing flower availability at the landscape-scale reduced pollination quantity, whereas at the neighborhood-scale it increased pollination quality. The overall positive effect of flower availability on seed output at the neighborhood scale was slightly higher than the overall negative effect at the landscape scale. Moreover, pollination quality had a higher positive effect on seed output than pollination quantity. Our results demonstrate that pollination quality may severely limit plant reproduction. Pollination quality limitation can act independently of pollination quantity limitation because these factors operateat different spatial scales.

The factors affecting the evolution of the anthocyanin biosynthesis pathway genes in monocot and dicot plant species

BackgroundThe available data demonstrate that even in universal metabolic pathways, some species-specific regulatory features of structural genes are present. For instance, in the anthocyanin biosynthesis pathway (ABP), genes may be regulated by ABP-specific regulatory factors, and their expression levels may be strongly associated with anthocyanin pigmentation, or they may be expressed independently of pigmentation. A dataset of orthologous ABP genes (Chs, Chi, F3h, F3’h, Dfr, Ans) from monocot and dicot plant species that have distinct gene regulation patterns and different types of pollination was constructed to test whether these factors affect the evolution of the genes.ResultsUsing a maximum likelihood approach, we demonstrated that although the whole set of the ABP genes is under purifying selection, with greater selection acting on the upstream genes than on the downstream genes, genes from distinct groups of plant species experienced different strengths of selective pressure. The selective pressure on the genes was higher in dicots than in monocots (F3h and further downstream genes) and in pollinator-dependent plants than in pollinator-independent species (Chi and further downstream genes), suggesting an important role of pollination type in the evolution of the anthocyanin biosynthesis gene network. Contrasting effects of the regulation patterns on evolution were detected for the F3h and Dfr genes, with greater selective pressure on the F3h gene in plant species where the gene expression was not strongly associated with pigmentation and greater selective pressure on Dfr in plant species where the gene expression was associated with pigmentation.ConclusionsWe demonstrated the effects of pollination type and patterns of regulation on the evolution of the ABP genes, but the evolution of some of the genes could not be explained in the framework of these factors, such as the weaker selective pressure acting on Chs in species that attract pollinators or the stronger selective pressure on F3h in plant species where the gene expression was not associated with pigmentation. The observations suggest that additional factors could affect the evolution of these genes. One such factor could be an effect of gene duplication with further division of functions among gene copies and relaxed selective pressure acting on them. Additional tests with an appropriate dataset combining data on duplicated gene sequences and their functions in the flavonoid biosynthesis pathway are required to test this hypothesis.

Using Pollinator Seed Mixes in Landscape Restoration Boosts Bee Visitation and Reproduction in the Rare Local Endemic Santa Susana Tarweed,Deinandra minthornii

ABSTRACT: Restoration practices that enhance pollinator habitat can improve conservation outcomes, including support of pollinator-dependent plant species. Yet, limited background research has assessed the benefits of incorporating greater native forb diversity into larger-scale restoration operations to justify the often increased costs of pollinator seed mixes. This study examined changes in pollination services received by Santa Susana tarweed, Deinandra minthornii, a California-listed Rare (CR) endemic of the Santa Susana Mountains that were associated with a native forb seed mix used in a large-scale remediation program at the Santa Susana Field Lab (SSFL) in Los Angeles, California. A four-year study of pollinator community dynamics and services was conducted from 2011 to 2014 examining aggregations of D. minthornii near to and farther from restoration activities. We hypothesized that D. minthornii located closer to the areas seeded with the forb mixes would be visited by more pollinators and receiv...

Pollination services enhanced with urbanization despite increasing pollinator parasitism.

Animal-mediated pollination is required for the reproduction of the majority of angiosperms, and pollinators are therefore essential for ecosystem functioning and the economy. Two major threats to insect pollinators are anthropogenic land-use change and the spread of pathogens, whose effects may interact to impact pollination. Here, we investigated the relative effects on the ecosystem service of pollination of (i) land-use change brought on by agriculture and urbanization as well as (ii) the prevalence of pollinator parasites, using experimental insect pollinator-dependent plant species in natural pollinator communities. We found that pollinator habitat (i.e. availability of nesting resources for ground-nesting bees and local flower richness) was strongly related to flower visitation rates at the local scale and indirectly influenced plant pollination success. At the landscape scale, pollination was positively related to urbanization, both directly and indirectly via elevated visitation rates. Bumblebees were the most abundant pollinator group visiting experimental flowers. Prevalence of trypanosomatids, such as the common bumblebee parasite Crithidia bombi, was higher in urban compared with agricultural areas, a relationship which was mediated through higher Bombus abundance. Yet, we did not find any top-down, negative effects of bumblebee parasitism on pollination. We conclude that urban areas can be places of high transmission of both pollen and pathogens.

Effects of nectar robbing on male and female reproductive success of a pollinator-dependent plant.

Nectar robbers affect host fitness in different ways and by different magnitudes, both directly and indirectly, and potentially constitute an important part of pollination interactions. The aim of this study was to assess the effect of nectar robbing on several variables that characterize the reproductive success of Lonicera etrusca, a pollinator-dependent plant with long, tubular flowers that produce abundant nectar. Using fluorescent powder dye as a proxy for pollen, the distance of pollen dispersal was compared for robbed and non-robbed flowers. Artificial nectar robbing treatments were applied to test its effects on four additional measures of reproductive success, namely the quantity of pollen exported, fruit set, seed/ovule ratio and seed weight. Nectar robbing was not found to have any significant negative consequences on female and male components of reproductive success as determined through the five variables that were measured. Although L. etrusca exhibits high levels of nectar robbing and nectar robbers are common floral visitors, no evidence was found of detrimental changes in the components of reproductive success. A combination of morphological and ecological mechanisms is proposed to explain how plants may compensate for the energetic loss caused by the nectar robbers.

Parallel responses of bees to Pleistocene climate change in three isolated archipelagos of the southwestern Pacific.

The impacts of glacial cycles on the geographical distribution and size of populations have been explored for numerous terrestrial and marine taxa. However, most studies have focused on high latitudes, with only a few focused on the response of biota to the last glacial maximum (LGM) in equatorial regions. Here, we examine how population sizes of key bee fauna in the southwest Pacific archipelagos of Fiji, Vanuatu and Samoa have fluctuated over the Quaternary. We show that all three island faunas suffered massive population declines, roughly corresponding in time to the LGM, followed by rapid expansion post-LGM. Our data therefore suggest that Pleistocene climate change has had major impacts across a very broad tropical region. While other studies indicate widespread Holarctic effects of the LGM, our data suggest a much wider range of latitudes, extending to the tropics, where these climate change repercussions were important. As key pollinators, the inferred changes in these bee faunas may have been critical in the development of the diverse Pacific island flora. The magnitude of these responses indicates future climate change scenarios may have alarming consequences for Pacific island systems involving pollinator-dependent plant communities and agricultural crops.

Insect visitation rates to wild flowers increase in the presence of arid agriculture in South Sinai, Egypt

In temperate and tropical environments agricultural intensification has primarily negative consequences for pollinator conservation. However, in arid environments agriculture is often highly dependent on irrigation and farms can offer higher availability of floral resources than the external environment.This study compares floral visitation rates to wild plants inside and outside 40 agricultural gardens in South Sinai, Egypt. The mean number of flower visitors per plant during a 30 min focal watch was significantly higher inside the gardens than outside, and this was true of orders Diptera, Hymenoptera and Lepidoptera.In total, 23 insect families were recorded inside the garden and 17 outside. The average family richness per plant was significantly higher inside the gardens, with higher rates of family accumulation across focal plants. Pollinating insects (hoverflies, solitary bees and honeybees) all had higher visitation rates inside the gardens.Seed set was assessed for two common pollinator-dependent plants, Stachys aegyptiaca and Alkanna orientalis. Neither species showed a significant difference in the seed set achieved inside and outside of the gardens, but S. aegyptiaca produced a higher number of seeds per plant inside the gardens because plants tended to be larger.In contrast to many other studies, the presence of agriculture appears to increase the abundance and diversity of flower visitors in this under-studied system, with no negative effect on the seed set of two common wild species.

Male interference with pollination efficiency in a hermaphroditic orchid.

Hermaphroditism can lead to both intra- and intersexual conflict between male and female gender functions. However, the effect that such gender conflicts have on pollination efficiency has seldom been investigated. By artificially reducing the number of available male gametes on an individual, we quantified whether male interference with pollination efficiency occurs in the self-compatible, moth-pollinated orchid Satyrium longicauda. We partially emasculated S.longicauda inflorescences and compared pollination success and fecundity in these plants to intact controls. Pollen in both groups of plants was colour-labelled so that its dispersal by pollinators could be tracked directly in the field. Intact flowers on partially emasculated inflorescences exported more pollen and received more cross-pollen and less self-pollen than those on intact inflorescences. Proportion of fruit set per plant was similar between the two treatments; however, fruits on partially emasculated plants had proportionally more viable seeds than those on intact controls. These results provide empirical evidence that male interference with pollination efficiency can occur in a hermaphroditic plant and that such interference can compromise fecundity. The most likely mechanism for such male interference is competition for placement on the proboscis of hawkmoth pollinators. Consequently, male competition for siring success may influence the evolution of sexual systems in hermaphroditic pollinator-dependent plants.

English

Pollinator-dependent production of food nutrients in China has not been evaluated previously. Using Food and Agriculture Organization (FAO) crop production data and United States Department of Agriculture (USDA) food composition data, we examined the nutritional values of 41 common fruits and vegetables to assess the contribution of animal pollination to human nutrition. Most of these crops rely on insect pollinators to set fruit or seed to some degree. Pollinator-dependent plants yielded more than 80% of the protein, fat, zinc, selenium, calcium, phosphorus, potassium, copper, vitamin B1 and vitamin B5, over 90% of the dietary fiber, vitamin B6 and vitamin C, almost the entire quantity of alpha-carotene and beta-tocopherol, and the full amount of beta-cryptoxanthin and lycopene. On average, pollinator-dependent crops accounted for approximately 80% of the food nutrients produced by the plants surveyed in this study, and 20% of all nutrient output was directly derived from insect pollination. Careful management of insect pollinator populations is therefore of vital importance to providing a nutritionally adequate diet for the people of China.   Key words: China, Food and Agriculture Organization (FAO), food nutrients, fruits, insect pollinators, vegetables.

Habitat conversion, extinction thresholds, and pollination services in agroecosystems

Parallel declines of wild pollinators and pollinator-dependent plants have raised alarms over the loss of pollination services in agroecosystems. A spatially explicit approach is needed to develop specific recommendations regarding the design of agricultural landscapes to sustain wild pollinator communities and the services they provide. I modeled pollination services in agroecosystems using a pair of models: a stochastic individual-based simulation model of wild pollinators, pollinator-dependent plants, and crop pollination; and a set of coupled difference equations designed to capture the nonspatial component of the simulation model. Five spatially explicit models of habitat conversion to crops were simulated, and results for pollination services were compared. Mean-field behavior of the simulation model was in good agreement with analysis of the difference equations. A major feature of the models was the presence of a cusp leading to loss of stability and extinction of pollinators and pollinator-dependent plants beyond a critical amount of habitat loss. The addition of pollen obtained from crop visitation caused a breakdown of the cusp preventing extinction of pollinators, but not of wild pollinator-dependent plants. Spatially restricted foraging and dispersal also altered model outcomes relative to mean-field predictions, in some cases causing extinction under parameter settings that would otherwise lead to persistence. Different patterns of habitat conversion to crops resulted in different levels of pollination services. Most interesting was the finding that optimal pollination services occurred when the size of remnant habitat patches was equal to half the mean foraging and dispersal distance of pollinators and the spacing between remnant patches was equal to the mean foraging and dispersal distance. Conservation of wild pollinators and pollinator-dependent plants in agroecosystems requires careful attention to thresholds in habitat conversion and spatial pattern and scale of remnant habitats. Maximization of pollination services was generally incompatible with conservation of wild pollinator-dependent plants. My prediction is that pollination services will be maximized by providing islands of nesting habitat where interisland distance matches mean foraging distances of wild pollinators.

Interaction of pollinators and herbivores on plant fitness suggests a pathway for correlated evolution of mutualism- and antagonism-related traits.

Different kinds of plant-animal interactions are ordinarily studied in isolation, yet considering the combined fitness effects of mutualistic and antagonistic interactions is essential to understanding plant character evolution. Functional, structural, or phylogenetic associations between attractive and defensive traits may be nonadaptive or result from correlational selection on sets of herbivory- and pollination-linked traits. Nonadditivity of fitness effects of mutualists and antagonists, a requisite for correlational selection, was experimentally tested in the field. We created experimental populations of the insect-pollinated perennial herb, Helleborus foetidus, at 16 different locations distributed among three regions in the Iberian Peninsula. Plants experienced one of four possible selective regimes generated by independently weakening the effects of pollinators and herbivores (flower and fruit predators) according to a two-way fully factorial design. Effects were assessed in terms of number of next-generation offspring recruited per mother plant under natural field conditions. Differences among H. foetidus plants in the strength of their interactions with pollinators and herbivores translated into differential fitness, as measured in terms of recruited offspring, and subsequent changes in plant population densities. A strong, geographically consistent nonadditivity in the fitness consequences of pollinators and herbivores was found also. Plants possessing the particular combination of "traits" simultaneously enhancing pollination and escape from herbivores enjoyed a disproportionate fitness advantage over plants possessing any of the other three possible "trait" combinations. Results suggest a simple, possibly widespread ecological pathway favoring the adaptive correlated evolution of mutualism- and antagonism-related plant traits in pollinator-dependent plants suffering intense flower and fruit herbivory.