Pollinator Flight Research Articles

Landscape configuration is an important predictor of sunflower yield in the Argentinean Pampas Region

Conventional agriculture is frequently associated with large-scale environmental degradation andlandscape homogenization. In contrast, ecological intensification incorporates natural habitat conservationand landscape complexity to improve important ecosystem services such as pollination and crop yields. Inan observational study of 105 fields in the Argentinean Pampas Region, we explored whether sunfloweryields were related to landscape composition (percentage of natural habitat) and configuration (field size andedge density), and covariates of agricultural management practices such as nitrogen fertilizer addition, seeddensity, sowing date and crop cultivar. Our mixed-effects models revealed that field size and edge densitiesbetween crop and natural habitat are important predictors of yield. For example, a doubling of edge densityfrom 40 m/ha to 80 m/ha predicted an 11.3% (269 kg/ha) yield increase, while a doubling in the field size from40 ha to 80 ha predicted a 6.1% (149 kg/ha) yield decrease. We suggest that pollination is an important driverof both effects as higher edge densities and smaller field sizes reduce wild pollinator flight distances to cropflowers and thus increases the chances for effective crop pollination. This study provides key information forsustainable management of sunflower agroecosystems.

Phenology and flowering overlap drive specialisation in plant-pollinator networks.

Variation in dietary specialisation stems from fundamental interactions between species and their environment. Consequently, understanding the drivers of this variation is key to understanding ecological and evolutionary processes. Dietary specialisation in wild bees has received attention due to their close mutualistic dependence on plants, and because both groups are threatened by biodiversity loss. Many principles governing pollinator specialisation have been identified, but they remain largely unvalidated. Organismal phenology has the potential to structure realised specialisation by determining concurrent resource availability and pollinator foraging activity. We evaluate this principle using mechanistic models of adaptive foraging in pollinators within plant-pollinator networks. While temporal resource overlap has little impact on specialisation in pollinators with extended flight periods, reduced overlap increases specialisation as pollinator flight periods decrease. These results are corroborated empirically using pollen load data taken from bees with shorter and longer flight periods across environments with high and low temporal resource overlap.

Changes in floral nectar are unlikely adaptive responses to pollinator flight sound.

Under noiseless experimental conditions, sugar concentration of secreted floral nectar may increase after flower exposure to nearby sounds of pollinator flight (Veits et al. 2019). However, we reject the argument that this represents adaptive plant behaviour, and consider that the appealing analogy between a flower and human ear is unjustified.

Field design can affect cross-pollination and crop yield in strawberry (Fragaria x ananassa D.)

The distance travelled by pollinators between successive flower visits can affect the quality of pollen transferred among plants. In cropping environments, especially monoculture systems, pollinators that travel between plants or rows may increase cross-pollination and consequently crop yield. However, the most commonly utilized crop pollinator, Apis mellifera L., tends to forage consecutively on nearest-neighbouring plants within rows. The level of cross-pollination can be further restricted in crops that are propagated by cloning. When a clonal variety is planted over large areas, the potential for outcrossed pollen deposition could be limited, regardless of pollinator flight distances. To investigate how pollinator movement and varietal diversity interact to affect crop pollination, we conducted an experiment with wild and honey bees in single- and multiple-variety strawberry fields. We hypothesized that the amount of cross-pollination provided by wild bees in multiple-variety strawberry fields would be greater than in single-variety fields, and greater than that provided by honey bees in either field type. We found that, indeed, flowers visited by wild bees produced larger strawberries than those visited by honey bees in multiple-variety plots, but only in the more self-incompatible of the two strawberry varieties tested. Strawberries resulting from honey bee pollination were of similar size regardless of the number of varieties planted in the field. Our results show that certain multiple-variety strawberry fields can benefit from the irregular foraging patterns of some solitary bee species, leading to increased cross-pollination and crop yield. Strawberry growers could take advantage of this effect by planting multiple varieties in close proximity and by supporting wild bee populations on farms.

Assessing Transportation Impacts to Alkali Bees (Hymenoptera: Halictidae) and Alfalfa Seed Production in Southeastern Washington State

The Washington State Department of Transportation (WSDOT) is proposing safety improvements to U.S. Highway 12 near the town of Touchet, Washington. The improvements include realignment to the north in order to accommodate a wider roadway. The proposed realignment route is within the Touchet-Lowden-Gardena alfalfa seed-growing district, an area critical to alfalfa seed production. The most effective and efficient pollinator for alfalfa is Nomia melanderi Cockerell, a native ground-dwelling bee that is raised in bee beds by area farmers. Relocation of the highway will bisect several bee beds and alfalfa fields. The alfalfa leafcutting bee, Megachile rotundata F., is also an important pollinator in the area. A study was conducted regarding potential impacts to these bees from the highway improvements. One of the objectives of the study was to determine pollinator flight heights over county roads. The “vehicular bee sweeper” was designed to capture insects at specific heights over the roadway and provided data regarding flight height. The majority of N. melanderi flew at heights below 2.1 meters when no other factors were considered, though most M. rotundata flew at or below 0.9 meters. Environmental conditions such as temperature and wind speed had an effect on flight behavior of both pollinators. Due to the low-flying nature of these solitary bees, vehicle strikes can be expected to cause mortality in bisected populations. WSDOT will be able to understand the impacts of the proposed highway to these important alfalfa pollinators and make recommendations to minimize the road’s effects.

Grid-Set-Match, an agent-based simulation model, predicts fruit set for the lowbush blueberry (Vaccinium angustifolium) agroecosystem

Fruit set, the proportion of flowers whose ovaries successfully bear fruit, is the product of dozens of processes, many of which are difficult to study and manipulate in situ. To establish which of these processes are most important in the lowbush blueberry (Vaccinium angustifolium Aiton; Ericaceae) agroecosystem, an agent-based simulation model, Grid-Set-Match, with temporal and spatial elements was constructed using the R software package. Pollination ecology data from this system were used to parameterize the model. Then, results from 1,000 iterations of the model were compared to field fruit set data from a survey of 162 lowbush blueberry fields from 1993 to 2015 as well as from a field study conducted from 2013 to 2015.Predicted fruit set for an average lowbush blueberry field was 0.366 according to Grid-Set-Match. Based on currently available field data, this estimate appears realistic, although it may be a slight underestimate in part because variability in pollinator densities between real fields is higher than the model accounted for. A multiple regression model indicated that, across a sample of clones created by Grid-Set-Match under default parameter settings, fruit set declined significantly as the average genetic load of a clone’s neighbors increased and as self-pollination rate increased, with the latter effect being ∼20% stronger than the former. As such, future research should be directed towards understanding and better managing factors that may influence rates of self- vs. cross-pollination in this system, such as pollen carryover, intra-hive pollen transfer, and pollinator flight distances between consecutively visited flowers.

Flower morphology, nectar traits and pollinators of Cerinthe major (Boraginaceae-Lithospermeae)

In April and May 2010, a natural population of Cerinthe major (Boraginaceae-Lithospermeae) was investigated with regard to: floral morphology, phenology, sexual receptivity during anthesis, the production of nectar and its sugar and amino acid content. The pollinator array of this species was also investigated. Cerinthe major has showy, pentamerous, hermaphroditic flowers with a deep yellow corolla tube arranged on numerous scorpioid inflorescences. Nectar and pollen are the main floral rewards for pollinators. The arrangement of stamens limits access to nectar and promotes pollen loading onto pollinator bodies as they force their way towards the source of nectar. By limiting the direct exposure of nectar to the environment, the corolla tube and the arrangement of anther filaments seemingly protect nectar from evaporation resulting from high temperatures and low relative humidity during flower anthesis. The green, annular nectary located at the base of the ovary lobes is composed of a very thin epidermis enclosing a dense mass of parenchyma. The epidermis lacks stomata, and the thin cuticle has an irregular surface. The parenchyma cells do not store starch during the pre-secretory stage, suggesting that immediate photosynthesis is the most likely source of nectar carbohydrates. Generally, anthesis lasts 4–5 days; the gynoecium becomes fully receptive on the second day and this is synchronous with anther dehiscence. Since nectar production begins during the bud stage, a substantial volume is available for flower visitors at anthesis. Nectar production decreases drastically in senescent flowers and, if not consumed, the nectar can be re-absorbed. Analysis of sugars revealed a sucrose-dominant nectar (sucrose=93.18±1.35%). Proline, GABA, taurine, leucine, citrulline and alanine were the main amino acids present and are probably implicated in pollinator flight performance.The bees Bombus hortorum, Anthophora sp. and Eucera sp. were constant and frequent visitors of C. major flowers. Moreover, the manner in which they interacted with the flower in order to obtain nectar and pollen loads was sufficient evidence for their role as pollinators. Their different foraging behaviours suggest that each species may promote differences in pollen flow both within and among individuals of the population.

An examination of synchrony between insect emergence and flowering in Rocky Mountain meadows

One possible effect of climate change is the generation of a mismatch in the seasonal timing of interacting organisms, owing to species-specific shifts in phenology. Despite concerns that plants and pollinators might be at risk of such decoupling, there have been few attempts to test this hypothesis using detailed phenological data on insect emergence and flowering at the same localities. In particular, there are few data sets on pollinator flight seasons that are independent of flowering phenology, because pollinators are typically collected at flowers. To address this problem, we established standardized nesting habitat (trap nests) for solitary bees and wasps at sites along an elevational gradient in the Rocky Mountains, and monitored emergence during three growing seasons. We also recorded air temperatures and flowering phenology at each site. Using a reciprocal transplant experiment with nesting bees, we confirmed that local environmental conditions are the primary determinants of emergence phenology. We were then able to develop phenology models to describe timing of pollinator emergence or flowering, across all sites and years, as a function of accumulated degree-days. Although phenology of both plants and insects is well described by thermal models, the best models for insects suggest generally higher threshold temperatures for development or diapause termination than those required for plants. In addition, degree-day requirements for most species, both plants and insects, were lower in locations with longer winters, indicating either a chilling or vernalization requirement that is more completely fulfilled at colder sites, or a critical photoperiod before which degree-day accumulation does not contribute to development. Overall, these results suggest that phenology of plants and trap-nesting bees and wasps is regulated in similar ways by temperature, but that plants are more likely than insects to advance phenology in response to springtime warming. We discuss the implications of these results for plants and pollinators, and suggest that phenological decoupling alone is unlikely to threaten population persistence for most species in our study area.

Effects of floral neighborhood on seed set and degree of outbreeding in a high-alpine cushion plant

Plants flowering together may influence each other's pollination and fecundity over a range of physical distances. Their effects on one another can be competitive, neutral, or facilitative. We manipulated the floral neighborhood of the high-alpine cushion plant Eritrichium nanum in the Swiss Alps and measured the effects of co-flowering neighbors on both the number of seeds produced and the degree of inbreeding and outbreeding in the offspring, as deduced from nuclear microsatellite markers. Seed set of E. nanum did not vary significantly with the presence or absence of two Saxifraga species growing as near neighbors, but it was higher in E. nanum cushions growing at low conspecific density than in those growing at high density. In addition, floral neighborhood had no detectable effect on the degree of selfing of E. nanum, but seeds from cushions growing at low conspecific density were more highly outbred than seeds from cushions at high density. Thus, there was no evidence of either competition or facilitation between E. nanum and Saxifraga spp. as mediated by pollinators at the spatial scale of our experimental manipulation. In contrast, the greater fecundity of E. nanum cushions at low density was consistent with reduced intraspecific competition for pollinators and might also represent a beneficial effect of highly outbred seeds as brought about by more long-distance pollinator flights under low-density conditions.

Seasonal Variation in the Nectar Sugar Concentration and Nectar Quantity in the Western Prairie Fringed Orchid, Platanthera praeclara (Orchidaceae)

Abstract The endangered western prairie fringed orchid, Platanthera praeclara, is found in remnant tall grass prairie in the central plains of North America. Platanthera praeclara is pollinated by several species of hawkmoths (Sphingidae) in Canada. There is minimal overlap between the flight period of hawkmoth pollinators and the flowering period of the Canadian orchid population, with orchids normally flowering at the end of the hawkmoth flight period. This study was designed to determine if orchids produce more nectar and higher concentrations of sugars in the nectar at the beginning of the flowering period coinciding with maximal pollinator flight times. As pollinators are nocturnally active, we also determined if orchids produce more nectar or nectar with increased concentrations of sugars during the night versus the daytime. Nectar sugar concentration and the amount of nectar per flower were highest at the beginning of the flowering period, and significantly decreased as the season progressed. Necta...

Reproductive biology of the andromonoecious Cucumis melo subsp. agrestis (Cucurbitaceae).

Cucumis melo subsp. agrestis (Cucurbitaceae) is cultivated in many African regions for its edible kernels used as a soup thickener. The plant, an annual, andromonoecious, trailing-vine species, is of high social, cultural and economic value for local communities. In order to improve the yield of this crop, the first step and our aim were to elucidate its breeding system. Eight experimental pollination treatments were performed during three growing seasons to assess spontaneous selfing, self-compatibility and effects of pollen source (hermaphroditic vs. male flowers). Pollination success was determined by pollen tube growth and reproductive success was assessed by fruit, seed and seedling numbers and characteristics. The pollinator guild was surveyed and the pollination distance determined both by direct observations and by indirect fluorescent dye dispersal. The species is probably pollinated by several Hymenoptera, principally by Hypotrigona para. Pollinator flight distances varied from 25 to 69 cm. No evidence for apomixis or spontaneous self-pollination in the absence of insect visitors was found. The self-fertility index (SFI = 0) indicated a total dependence on pollinators for reproductive success. The effects of hand pollination on fruit set, seed number and seedling fitness differed among years. Pollen tube growth and reproductive success did not differ between self- and cross-pollinations. Accordingly, a high self-compatibility index for the fruit set (SCI = 1.00) and the seed number (SCI = 0.98) and a low inbreeding depression at all developmental stages (cumulative delta = 0.126) suggest a high selfing ability. Finally, pollen origin had no effect on fruit and seed sets. This andromonoecious species has the potential for a mixed mating system with high dependence on insect-mediated pollination. The selfing rate through geitonogamy should be important.

Interspecific pollinator movements reduce pollen deposition and seed production inMimulus ringens(Phrymaceae)

Movement of pollinators between coflowering plant species may influence conspecific pollen deposition and seed set. Interspecific pollinator movements between native and showy invasive plants may be particularly detrimental to the pollination and reproductive success of native species. We explored the effects of invasive Lythrum salicaria on the reproductive success of Mimulus ringens, a wetland plant native to eastern North America. Pollinator flights between these species significantly reduced the amount of conspecific pollen deposited on Mimulus stigmas and the number of seeds in Mimulus fruits, suggesting that pollen loss is an important mechanism of competition for pollination. Although pollen loss is often attributed to pollen wastage on heterospecific floral structures, our novel findings suggest that grooming by bees as they forage on a competitor may also significantly reduce outcross pollen export and seed set in Mimulus ringens.

Long-distance pollen flow assessment through evaluation of pollinator foraging range suggests transgene escape distances

Foraging range, an important component of bee ecology, is of considerable interest for insect-pollinated plants because it determines the potential for outcrossing among individuals. However, long-distance pollen flow is difficult to assess, especially when the plant also relies on self-pollination. Pollen movement can be estimated indirectly through population genetic data, but complementary data on pollinator flight distances is necessary to validate such estimates. By using radio-tracking of cowpea pollinator return flights, we found that carpenter bees visiting cowpea flowers can forage up to 6 km from their nest. Foraging distances were found to be shorter than the maximum flight range, especially under adverse weather conditions or poor reward levels. From complete flight records in which bees visited wild and domesticated populations, we conclude that bees can mediate gene flow and, in some instances, allow transgene (genetically engineered material) escape over several kilometers. However, most between-flower flights occur within plant patches, while very few occur between plant patches.

The effects of floral mimics and models on each others' fitness

Plants that lack floral rewards may nevertheless attract pollinators by mimicking the flowers of rewarding plants. It has been suggested that both mimics and models should suffer reduced fitness when mimics are abundant relative to their models. By manipulating the relative densities of an orchid mimic Disa nivea and its rewarding model Zaluzianskya microsiphon in small experimental patches within a larger population we demonstrated that the mimic does indeed suffer reduced pollination success when locally common relative to its model. Behavioural experiments suggest that this phenomenon results from the tendency of the long-proboscid fly pollinator to avoid visits to neighbouring plants when encountering the mimic. No negative effect of the mimic on the pollination success of the model was detected. We propose that changes in pollinator flight behaviour, rather than pollinator conditioning, are likely to account for negative frequency-dependent reproductive success in deceptive orchids.

Effects of Animal Pollination on Pollen Dispersal, Selfing, and Effective Population Size of Tropical Trees: A Simulation Study

ABSTRACTAnimals, especially insects, are principal pollen vectors of tropical trees and have behavior patterns that affect gene dispersal. Here, we explore complex pollination systems using a new simulation model Eco‐Gene and considering, among other factors, flowering synchrony, spatial distribution of trees, degree of selfing, population densities, pollinator flight distances, pollen deposition, and pollinator response to floral display size. Sensitivity analyses using two contrasting tree data sets (Jacaranda copaia and Dipteryx odorata) determined the importance of each parameter on three response variables: the proportion of seeds from self‐pollination, effective population size, and pollen dispersal. Spatial considerations and attractiveness of floral displays were prominent features determining the population genetic result of pollinators, and some biological implications of the results are discussed.RESUMENAnimales, insectos en particular, son los vectores principals del polen de los arboles tropicales y como consecuencia su comportamiento afecta dispersión genética. Aquí se examina sistemas de la polinización en su totalidad, aplicando un nuevo programa de simulacro Eco‐Gene, que se toma en cuenta, entre otros factores, sincronicidad de floración, distribución de arboles, grado de auto‐fecundación, densidad poblacional, distancia de vuelo, polen deposición, respuesta comportamiental de polenizadores al tamaño del anuncio floral. Sensitivity análisis con datos contrastantes de dos arboles (Jacaranda copaia y Dipteryx odorata) evaluó la importancia de cada parametro y su resultado respeto a: la proporcion de semillas producidas por autofecundación, tamano poblacional efectivo, y distancia de dispersión del polen. Las cualidades espaciales de poblaciones, y la atractividad del anuncio floral determinaban fuertemente las consecuencias de polinizacion, y se considera implicaciones biológicas y genéticas de los resultados.

Long-distance pollinator flights and pollen dispersal between populations of Delphinium nuttallianum

Spatial processes in pollination biology are poorly understood, especially at levels above that of the local population. For example, little is known about how pollinators and pollen move among populations, although there is evidence that such movement can exceed what is predicted from intrapopulational movement. We explored pollination success in experimental isolates of the bumblebee- and hummingbird-pollinated wildflower Delphinium nuttallianum. We established a total of 15 arrays of potted plants isolated by 50-400m from ten natural "source" populations, as well as control arrays embedded within each source. Flowers on potted plants were emasculated, so any pollen received could be assumed to come from source populations. A total of 69h of observation suggested that pollinators were somewhat less abundant in isolates than in controls, but visited more plants and flowers once within an isolate. Consistent with this, 82.1% of all flowers in isolated arrays received pollen, versus 87.7% in controls. Mean receipt was more than 100 pollen grains per flower in most arrays, and seed set in isolates and controls respectively averaged 69.8% and 74.3% of ovules. Furthermore, pollen receipt in isolates declined relatively slowly with distance from the source. We conclude that pollinators of D. nuttallianum often will fly up to 400m among populations, and that substantial pollination ensues. Thus isolated populations of this species often belong to metapopulations in terms of pollen dispersal, with important consequences for genetic differentiation, and potential implications for the management of endangered plant species.

Ecological mechanisms of reproductive isolation between diploid and tetraploid Chamerion angustifolium

Summary 1 Theoretical models indicate that coexistence of diploid and polyploid individuals in sympatric populations is unlikely when mating is random among cytotypes and hybrids are inviable. However, coexistence may be facilitated by prezygotic isolating mechanisms that reduce intercytotype mating and increase assortative mating. 2 We examined the ecological factors regulating intercytotype mating in Chamerion (formerly Epilobium) angustifolium by measuring floral morphology, flowering synchrony and insect foraging preferences in a mixed population within a diploid–tetraploid contact zone. We also calculated the minimum rate of between‐cytotype mating from estimates of the frequency of triploid offspring. 3 Diploids had significantly shorter and narrower petals as well as shorter styles than tetraploids. Inflorescences were significantly taller in tetraploids than diploids, but the mean number of open flowers per inflorescence did not differ. Diploid and tetraploid flowering periods overlapped by 51%, with diploid stems flowering earlier. 4 In a plot of 20 diploid and 28 tetraploid stems that were flowering simultaneously, only 26% of all bee flights were between flowers on different stems. Of the total flights between inflorescences, only 15% were between different cytotypes. The combined effects of flowering asynchrony and insect foraging reduced the opportunities for intercytotype mating from 49% expected if mating is random to about 2% of the total number of pollinator flights. 5 A computer simulation indicated that the deficiency of pollinator flights between cytotypes was due largely to the spatial structure of cytotypes and limited pollinator flight distances within the observation plot. The frequency of triploid offspring produced during the period when both cytotypes were in flower was 6.6%, similar to the proportion of flights observed between flowers on different cytotypes (4%). 6 The results indicate that flowering phenology and insect behaviour (as influenced by clonal structure) have a significant effect on prezygotic mating isolation and triploid production, and may contribute to the maintenance of mixed cytotype populations in Chamerion angustifolium.

Pollen dispensers (inserts) increase fruit set and yield in almonds under some commercial conditions

SUMMARYMost commercial almond cultivars are self-incompatible and flowering occurs in early spring when weather conditions are often unfavourable for pollinator flight. Thus, inadequate cross-pollination frequently limits almond yield. We evaluated the effect of pollen dispensers (inserts), fixed onto honey bee hives, on almond fruit set and yield in orchards differing in planting design, i.e. varying in the arrangement and proximity of the main cultivar and pollinizers. Pollen dispensers did not increase fruit-set percentage and yield in the 1: 1: 1 planting design in which (a), pollinizer rows were planted on either side of the main cultivar rows; and (b), bloom overlap was good between the pollinizers (cv. Carmel and Monterey) and the main cultivar Nonpareil. In contrast, pollen dispensers increased fruit-set percentage and yield in the 1: 2: 1 (one pollinizer row: two Nonpareil rows: one pollinizer row) planting design in which the branches of the two Nonpareil rows facing each other were more distant from effective pollinizers, and bloom overlap between Nonpareil and one of its pollinizers (Mission) was suboptimal. The increase in fruit set and yield, attributable to the use of pollen dispensers occurred primarily on Nonpareil branches facing the adjacent Nonpareil row. The impact of pollen dispensers was significant at 50 m but not at 150 m from the hive. Although pollen dispensers have been used for more than 60 years, this is the first large-scale study with replication, conducted under commercial conditions that demonstrates their benefit when cross-pollination is limited.

Comparison of pollinator flight movements and gene dispersal patterns in Mimulus ringens

Pollinator movements and pollen-mediated gene dispersal were quantified in experimental populations of square-stemmed monkeyflower (Mimulus ringens), a wetland perennial herb with a mixed-mating system. Each population consisted of genets with unique multilocus combinations of homozygous genotypes, facilitating assignment of paternity to all sampled seeds. Replicate arrays were planted at each of three spacings spanning the range of densities typically observed in natural M. ringens populations. In all six arrays the distribution of gene dispersal distances differed significantly from the distribution of pollinator flight movements. The mean gene dispersal distance was 1.46 times as far as the mean pollinator flight distance. These differences were probably caused by pollen carryover as bumblebees visited up to 12 M. ringens plants on a single foraging trip. Although gene movements exceeded pollinator flight distances, estimates of neighbourhood size were consistently low, ranging from 1.66 to 5.53. Therefore, high levels of random local genetic differentiation are likely in this species.

The influence of population density on outcrossing rates in Mimulus ringens

The influence of population density on pollinator movements and outcrossing rates was studied in experimental arrays of Mimulus ringens (square-stemmed monkeyflower), a wetland perennial species with a mixed-mating system. Each population was composed of genets with unique multi-locus combinations of homozygous genotypes, facilitating determination of outcrossing rates through paternity exclusion. Replicate arrays were cloned from the same set of genets to minimize differences in floral and vegetative morphology among density treatments. Two arrays were planted at each of three spacings typical of the range of densities found in natural M. ringens populations. Both the proportion of pollinator flights between plants and the frequency of outcrossing were significantly greater at high density. These results suggest that ecological and demographic factors, such as population density, can significantly influence levels of inbreeding in species with mixed-mating systems.