Nocturnal Pollinators Research Articles

The relative contribution of diurnal and nocturnal pollinators to plant female fitness in a specialized nursery pollination system.

Plants involved in specialized pollinator interactions, such as nursery pollination, may experience trade-offs in their female fitness, as the larvae of their pollinators may also consume seeds produced by the flowers they pollinate. These interactions could potentially shift between mutualism and parasitism, depending on the presence and abundance of both the nursery pollinator and of other pollinators. We investigated the fitness trade-off in a Mediterranean plant (Silene latifolia), which has a specialist nocturnal nursery pollinator moth (Hadena bicruris) and is also visited by several diurnal pollinators. We estimated the pollination rates and fecundity of S. latifolia in both natural and experimental populations in the Mediterranean. We estimated natural pollination rates in different flowering times and with presence/absence of the H. bicruis moth. Then by exposing plants to each pollinator group either during the day or at night, we quantified the contribution of other diurnal pollinators and the specialized nocturnal nursery pollinator to plant female fitness. We found no difference in plant fruit set mediated by diurnal versus nocturnal pollinators, indicating that non-specialist pollinators contribute to plant female fitness. However, in both natural and experimental populations, H. bicruris was the most efficient pollinator in terms of seeds produced per fruit. These results suggest that the female fitness costs generated by nursery pollination can be overcome through higher fertilization rates relative to predation rates, even in the presence of co-pollinators. Quantifying such interactions is important for our understanding of the selective pressures that promote highly specialized mutualisms, such as nursery pollination, in the Mediterranean region, a centre of diversification of the carnation family.

Low overnight temperatures delay ‘Hass’ avocado (<i>Persea americana</i>) female flower opening, leading to nocturnal flowering

Avocado (Persea americana) has synchronously protogynous flowers: flowers open first in female phase before closing and opening the next day in male phase. Cultivars are grouped based on whether the flowers typically first open in female phase in the morning (type A), or in the afternoon (type B). However, it is known that environmental factors can alter the timing of flower opening, with cold temperatures being shown to affect the timing of flowering. The aim of this study was to investigate how low spring temperatures in New Zealand affect the flowering cycle of commercial avocado cultivars, focusing primarily on the receptive female phase of ‘Hass’, a type A cultivar. Time-lapse photography was used to assess flower opening times of ‘Hass’ over three years. Decreasing minimum overnight temperatures were associated with a delay in the timing of ‘Hass’ female flower phases and resulted in nocturnal flowering of both male and female phase flowers. We recorded insects visiting female flowers at night, and some nocturnal flower visitors collected were carrying avocado pollen. Our study suggests that nocturnal pollination needs to be considered for avocados grown in temperate regions. Furthermore, as the timing of the female phase of ‘Hass’ varied significantly with overnight temperature, the activity patterns of potential pollinators need to be considered to ensure adequate pollinator activity across the range of times in which ‘Hass’ flowers are receptive.

Noctuid moths as potential hybridization agents for Platanthera orchids

Zoophilous flowering plants communicate with pollinators to ensure pollen transfer. Pin-pointing which species are effective pollinators is not only essential to better understand plant-pollinator networks, but equally so to better understand the potential of hybridization in plant systems, such as in orchids. As a case study, we studied two sympatric populations of the congeneric orchids Platanthera bifolia and P. chlorantha in order to assess their nocturnal pollinators by checking which moth species carried pollinaria, and of which orchid species. Moths carrying Platanthera pollinaria were photographed and identified. The carried pollinaria were identified and counted, and their attachment position on the moth’s head was scored. Based on these observations we show that three species of noctuid moths visited the Platanthera inflorescences. Although Noctua pronuba visited P. chlorantha, only Cucullia umbratica and Autographa gamma turned out to be potential pollinators for both orchid species. As such, we here demonstrate that the latter two noctuids have high potential to facilitate hybridization among these two orchid species, especially so in sympatric populations.

Pollination context alters female advantage in gynodioecious Silene vulgaris.

Gynodioecy, the co-occurrence of females and hermaphrodites, is arguably the most common angiosperm gender polymorphism in many florae. Females' ability to invade and persist among hermaphrodites depends, in part, on pollinators providing adequate pollination to females. We directly measured diurnal and nocturnal pollinators' contributions to female and hermaphrodite seed production in artificial populations of gynodioecious Silene vulgaris by experimentally restricting pollinator access. We found that female relative seed production in this system depended strongly on pollination context: females produced more than twice as many seeds as hermaphrodites in the context of abundant, nectar-collecting moths. Conversely, females showed no seed production advantage in the context of pollen-collecting syrphid flies and bees due to acutely hermaphrodite-biased visitation. We infer that variation in pollinator type, behaviour and abundance may be important for achieving the female relative fitness thresholds necessary for the maintenance of gynodioecy. Generally, our study illustrates how pollinator-mediated mechanisms may influence the evolution of breeding systems and associated suites of floral traits. Segments of a pollinator community may facilitate gynodioecy by selecting for plant characteristics that increase the attractiveness of both sexes to pollinators, such as nectar rewards. Conversely, discriminating visitors in search of pollen may restrict gynodioecy in associated plant lineages by reducing male steriles' fitness below threshold levels.

Nocturnal pollinators go dark under street lamps

Plants illuminated by artificial lights see a drop in the number of insects that move pollen at night.

Artificial light at night as a new threat to pollination.

Pollinators are declining worldwide and this has raised concerns for a parallel decline in the essential pollination service they provide to both crops and wild plants. Anthropogenic drivers linked to this decline include habitat changes, intensive agriculture, pesticides, invasive alien species, spread of pathogens and climate change. Recently, the rapid global increase in artificial light at night has been proposed to be a new threat to terrestrial ecosystems; the consequences of this increase for ecosystem function are mostly unknown. Here we show that artificial light at night disrupts nocturnal pollination networks and has negative consequences for plant reproductive success. In artificially illuminated plant-pollinator communities, nocturnal visits to plants were reduced by 62% compared to dark areas. Notably, this resulted in an overall 13% reduction in fruit set of a focal plant even though the plant also received numerous visits by diurnal pollinators. Furthermore, by merging diurnal and nocturnal pollination sub-networks, we show that the structure of these combined networks tends to facilitate the spread of the negative consequences of disrupted nocturnal pollination to daytime pollinator communities. Our findings demonstrate that artificial light at night is a threat to pollination and that the negative effects of artificial light at night on nocturnal pollination are predicted to propagate to the diurnal community, thereby aggravating the decline of the diurnal community. We provide perspectives on the functioning of plant-pollinator communities, showing that nocturnal pollinators are not redundant to diurnal communities and increasing our understanding of the human-induced decline in pollinators and their ecosystem service.

Pollen Transport in the Dark: Hawkmoths Prefer Non Crop Plants to Crop Plants in an Agricultural Landscape

In many previous studies hawkmoths have been found to be involved in nocturnal pollination of many plants. But their role in crop pollination is still unexplored. This study tried to evaluate their potential to carry pollens of crop. Hawkmoths were collected by light traps and slides were made from the pollen attached to their body. The hawkmoths and the pollens were identified. A pollen transport network was created using the data. The species level indices of each plant species in the network were estimated. Only a small fraction of pollens were made by the crops among the total types of pollens carried by the hawkmoths. Rest of the pollens belonged to that of the non crops. The species level indices suggest the crop pollens to be relatively less important in the network as reflected in the lower values of species degree and species strength. The higher species level specialisation values of crop pollens suggested they are restricted to be carried by few hawkmoth species only. It is clearly revealed that hawkmoths carry mostly non crop pollens, not crop pollens.

Related allopolyploids display distinct floral pigment profiles and transgressive pigments.

Both polyploidy and shifts in floral color have marked angiosperm evolution. Here, we investigate the biochemical basis of the novel and diverse floral phenotypes seen in allopolyploids in Nicotiana (Solanaceae) and examine the extent to which the merging of distinct genomes alters flavonoid pigment production. We analyzed flavonol and anthocyanin pigments from Nicotiana allopolyploids of different ages (N. tabacum, 0.2 million years old; several species from Nicotiana section Repandae, 4.5 million years old; and five lines of first-generation synthetic N. tabacum) as well as their diploid progenitors. Allopolyploid floral pigment profiles tend not to overlap with their progenitors or related allopolyploids, and allopolyploids produce transgressive pigments that are not present in either progenitor. Differences in floral color among N. tabacum accessions seems mainly to be due to variation in cyanidin concentration, but changes in flavonol concentrations among accessions are also present. Competition for substrates within the flavonoid biosynthetic pathway to make either flavonols or anthocyanins may drive the differences seen among related allopolyploids. Some of the pigment differences observed in allopolyploids may be associated with making flowers more visible to nocturnal pollinators.

Patterns and Processes in Nocturnal and Crepuscular Pollination Services.

Night, dawn, and dusk have abiotic features that differ from the day. Illumination, wind speeds, turbulence, and temperatures are lower while humidity may be higher at night. Nocturnal pollination occurred in 30% of angiosperm families across 68% of orders, 97% of families with C3, two-thirds of families with crassulacean acid metabolism (CAM), and 71% dicot families with C4 photosynthesis. Despite its widespread occurence, nocturnal pollination occurs in more families with xerophytic adaptations than helophytes or mesophytes, suggesting that nocturnal flowering is primarily an adaptation to water stress since flowering is a water-intensive process. We propose the arid or water stress hypothesis for nocturnal flowering suggesting that plants facing water stress in a habitat (e.g., deserts) or a habitat stratum (e.g., upper canopy for epiphytes) gain a selective advantage by nocturnal flowering by reducing water loss through evapotranspiration, leading to larger flowers that provide more nectar or other resources, to support pollinators with higher rewards. Contrary to the wide taxonomic occurrence of nocturnal flowering, few animal taxa serve as nocturnal pollinators. We discuss the sensory and physiological abilities that enable pollinator movement, navigation, and detection of flowers within the nocturnal temporal niche and present a unified framework for investigation of nocturnal flowering and pollination.

Pollination of Campomanesia phaea (Myrtaceae) by night-active bees: a new nocturnal pollination system mediated by floral scent.

Bees are the most important diurnal pollinators of angiosperms. In several groups of bees a nocturnal/crepuscular habit developed, yet little is known about their role in pollination and whether some plants are adapted specifically to these bees. We used a multidisciplinary approach to investigate the reproductive biology and to understand the role of nocturnal/crepuscular bees in pollination of Campomanesia phaea (Myrtaceae), popularly named cambuci. We studied the floral biology and breeding system of C.phaea. We collected the floral visitors and tested the pollinators' effectiveness. We also determined the floral scents released at night and during daytime, and studied behavioural responses of crepuscular/nocturnal bees towards these scents. The flowers of cambuci were self-incompatible and had pollen as the only resource for flower visitors. Anthesis lasted around 14h, beginning at 04:30h at night. The flowers released 14 volatile compounds, mainly aliphatic and aromatic compounds. We collected 52 species of floral visitors, mainly bees. Nocturnal and crepuscular bees (four species) were among the most frequent species and the only effective pollinators. In field bioassays performed at night, nocturnal/crepuscular bees were attracted by a synthetic scent blend consisting of the six most abundant compounds. This study describes the first scent-mediated pollination system between a plant and its nocturnal bee pollinators. Further, C.phaea has several floral traits that do not allow classification into other nocturnal pollination syndromes (e.g. pollinator attraction already before sunrise, with pollen as the only reward), instead it is a plant specifically adapted to nocturnal bees.

Land-use change has no detectable effect on reproduction of a disturbance-adapted, hawkmoth-pollinated plant species.

Land-use change is cited as a primary driver of global biodiversity loss, with myriad consequences for species, populations, and ecosystems. However, few studies have examined its impact on species interactions, particularly pollination. Furthermore, when the effects of land-use change on pollination have been studied, the focus has largely been on species pollinated by diurnal pollinators, namely, bees and butterflies. Here, we focus on Oenothera harringtonii, a night-flowering, disturbance-adapted species that has experienced a range-wide gradient of land-use change. We tested the hypothesis that the negative impacts of land-use change are mitigated by long-distance pollination. Our study included both temporal (4 yr) and spatial (19 populations range-wide, and 1, 2, and 5 km from the population center) data, providing a comprehensive understanding of the role of land-use change on pollination biology and reproduction. We first confirmed that O. harringtonii is self-incompatible and reliant on pollinators for reproduction. We then showed that hawkmoths (primarily Hyles lineata) are highly reliable and effective pollinators in both space and time. Unlike other studies, we did not detect an effect of population size, increased isolation, or a reduction in suitable habitat in areas with evidence of land-use change on pollination (visitation, pollen removal and deposition). Furthermore, the proportion of suitable habitat and other fragmentation metrics examined were not associated with population size or density in this plant species. We conclude that nocturnal pollination of Oenothera harringtonii via hawkmoths is robust to the negative impacts of land-use change.

Comparative analyses of flower scent inSileneaereveal a contrasting phylogenetic signal between night and day emissions

AbstractFlower scents are complex blends of volatile compounds often shaped by selection pressures exerted by mutualistic and antagonistic interaction partners, but also by phylogenetic constraints. So far, little is known about the relative effect of selection and phylogenetic signal on scent patterns, and no study to date analyzed the phylogenetic signal in multivariate semiquantitative scent patterns. We analyzed the phylogenetic signal in qualitative and semi‐quantitative patterns of flower scents in 47 Sileneae (Caryophyllaceae) species using phylogenetic principal component analysis (pPCA) and several indices of univariate and multivariate phylogenetic signal. As previous results showed that Sileneae species are visited by diurnal and nocturnal pollinators and flower scents also vary along the day, we compared the phylogenetic signal between night and day. MultivariatepPCAanalyses identified compounds that correlate with the phylogeny at both night and day; however, multivariate Bloomberg′s K detected phylogenetic signal in the dataset of night scents, but not of day scents. In multivariate qualitative datasets, phylogenetic signal was neither found for day nor for night scents. In univariate analyses, phylogenetic signal was detected for some compounds both for day and night scents. Overall, we found that the phylogenetic signal is stronger in night compared to day scents, which might be owed to the different guilds of pollinators at day and night. At day, the phylogenetic resemblance of Sileneae scents might be masked by or disappear due to divergent selective pressures exerted by a diverse guild of pollinators on the different species. In contrast, we hypothesize that the nocturnal moth pollinators exert similar selective pressures; thus, the phylogenetic similarity of scent profiles might be conserved. Future studies of scent phylogenetic signal must consider not only the usage of qualitative measures but also semiquantitative analyses.

Settling moths as potential pollinators of Uncaria rhynchophylla (Rubiaceae)

Nocturnal pollinators such as moths have received less attention than diurnal insects. To elucidate whether nocturnal moths are important pollinators, we observed both the diurnal and nocturnal visitors to the flowers of Uncaria rhynchophylla (Rubiaceae) in a warm-temperate forest in central Japan. The diurnal visitors included various taxonomic groups (e.g., bees, hoverflies and butterflies). The nocturnal visitors were exclusively moths (Geometridae, Erebidae, Noctuidae and Crambidae). Pollen grains of U. rhynchophylla were attached to both diurnal and nocturnal visitors. Although diurnal flower visitors carried pollen grains of other plant species, nocturnal moths did not carry heterospecific pollen grains. These results suggest that nocturnal moths, as well as diurnal insects, are important pollinators of U. rhynchophylla.

Circadian rhythm of a Silene species favours nocturnal pollination and constrains diurnal visitation.

Background and Aims Traits related to flower advertisement and reward sometimes vary in a circadian way, reflecting phenotypic specialization. However, specialized flowers are not necessarily restricted to specialized pollinators. This is the case of most Silene species, typically associated with diurnal or nocturnal syndromes of pollination but usually showing complex suites of pollinators. Methods A Silene species with mixed floral features between diurnal and nocturnal syndromes was used to test how petal opening, nectar production, scent emission and pollination success correlate in a circadian rhythm, and whether this is influenced by environmental conditions. The effect of diurnal and nocturnal visitation rates on plant reproductive success is also explored in three populations, including the effect of the pollinating seed predator Hadena sancta. Key Results The result showed that repeated petal opening at dusk was correlated with nectar secretion and higher scent production during the night. However, depending on environmental conditions, petals remain opened for a while in the morning, when nectar and pollen still were available. Pollen deposition was similarly effective at night and in the morning, but less effective in the afternoon. These results were consistent with field studies. Conclusions The circadian rhythm regulating floral attractiveness and reward in S. colorata is predominantly adapted to nocturnal flower visitors. However, favourable environmental conditions lengthen the optimal daily period of flower attraction and pollination towards morning. This allows the complementarity of day and night pollination. Diurnal pollination may help to compensate the plant reproductive success when nocturnal pollinators are scarce and when the net outcome of H. sancta shifts from mutualism to parasitism. These results suggest a functional mechanism explaining why the supposed nocturnal syndrome of many Silene species does not successfully predict their pollinator guilds.

Geometrid moth assemblages reflect high conservation value of naturally regenerated secondary forests in temperate China

The widespread destruction of mature forests in China has led to massive ecological degradation, counteracted in recent decades by substantial efforts to promote forest plantations and protect secondary forest ecosystems. The value of the resulting forests for biodiversity conservation is widely unknown, particularly in relation to highly diverse invertebrate taxa that fulfil important ecosystem services. We aimed to address this knowledge gap, establishing the conservation value of secondary forests on Dongling Mountain, North China based on the diversity of geometrid moths – a species-rich family of nocturnal pollinators that also influences plant assemblages through caterpillar herbivory. Results showed that secondary forests harboured geometrid moth assemblages similar in species richness and phylogenetic diversity, but with a species composition distinctly different to assemblages in one of China’s last remaining mature temperate forests in the Changbaishan Nature Reserve. Species overlap between these sites was about 30%, and species did not form separate phylogenetic clusters according to site. Species assemblages at Dongling Mountain were strongly differentiated according to forest type; a pattern not found at Changbaishan. Our results indicate that protected naturally regenerated secondary forests in northern China provide suitable habitats for species-rich and genetically diverse geometrid moth assemblages, highlighting the potential importance of these forests for conservation and ecosystem function provision across the wider landscape.

Floral longevity, nectar production, pollen release, and stigma receptivity in Haskap (<i>Lonicera caerulea</i>)

Haskap (Lonicera caerulea L.) is a temperate fruiting shrub grown commercially in northern regions of Europe, Asia, and North America. Haskap is self-incompatible and requires insect pollinators in order to set fruit; however, very little is currently known about its floral biology or pollinator specializations, particularly in North American cultivars. Here, we examine floral longevity, nectar dynamics, the timing of anther dehiscence, and stigma receptivity in flowers of greenhouse-grown ‘Tundra’, a Haskap cultivar developed and grown in Saskatchewan, Canada. Anthesis lasted 83.3 ± 25.9 hours (mean ± SD) in un-pollinated flowers; pollination caused early senescence within 34.3 ± 15.2 hours after pollination. Nectar was present from the onset of anthesis, and nectar volume peaked at 9-16 hours after opening. Nectar volume was maintained throughout anthesis and was not resorbed prior to abscission of the corolla from the ovary, and nectar removed during anthesis was replenished to the original volume. The stigma showed a reaction to hydrogen peroxide while still in the bud stage, suggesting it is receptive even before the flower opens. Early stigma receptivity, nectar production, and anther dehiscence maximize opportunities to be successfully pollinated, along with high floral longevity and pollination-triggered senescence. These results suggest that Haskap flowers utilize a generalist, rather than a specialized, pollination strategy. Observations that some flowers open in the evening or were already open in the morning suggest that nocturnal pollinators such as moths may be important, in addition to known diurnal pollinators.

MYB-FL controls gain and loss of floral UV absorbance, a key trait affecting pollinator preference and reproductive isolation.

Adaptations to new pollinators involve multiple floral traits, each requiring coordinated changes in multiple genes. Despite this genetic complexity, shifts in pollination syndromes have happened frequently during angiosperm evolution. Here we study the genetic basis of floral UV absorbance, a key trait for attracting nocturnal pollinators. In Petunia, mutations in a single gene, MYB-FL, explain two transitions in UV absorbance. A gain of UV absorbance in the transition from bee to moth pollination was determined by a cis-regulatory mutation, whereas a frameshift mutation caused subsequent loss of UV absorbance during the transition from moth to hummingbird pollination. The functional differences in MYB-FL provide insight into the process of speciation and clarify phylogenetic relationships between nascent species.

Diel Variation in Flower Scent Reveals Poor Consistency of Diurnal and Nocturnal Pollination Syndromes in Sileneae.

The composition of flower scent and the timing of emission are crucial for chemical communication between plants and their pollinators; hence, they are key traits for the characterization of pollination syndromes. In many plants, however, plants are assigned to a syndrome based on inexpensive to measure flower traits, such as color, time of flower opening, and shape. We compared day and night scents from 31 Sileneae species and tested for quantitative and semi-quantitative differences in scent among species classified a priori as diurnal or nocturnal. As most Sileneae species are not only visited by either diurnal or nocturnal animals as predicted by their syndrome, we hypothesized that, even if flower scent were preferentially emitted during the day or at night, most species also would emit some scents during the opposing periods of the day. This phenomenon would contribute to the generalized assemblage of flower visitors usually observed in Sileneae species. We found that diel variations of scent often were not congruent with the syndrome definition, but could partially be explained by taxonomy and sampling times. Most species emitted compounds with attractive potential to insects during both the night and day. Our results highlight the current opinion that syndromes are not watertight compartments evolved to exclude some flower visitors. Thus, important information may be lost when scents are collected either during day- or night-time, depending on the a priori classification of the species as diurnal or nocturnal.

Odd for an Ericad: Nocturnal Pollination of Lyonia lucida (Ericaceae)

Abstract Studies of pollination biology are largely diurnally biased, especially in plant species whose flowers conform to diurnal pollination syndromes. Though these syndromes can be useful in generating hypotheses regarding a species’ primary pollinators, they may also lead to incorrect assumptions. This study explores the relative contributions of diurnal and nocturnal pollination to fruit set in Lyonia lucida, an ericaceous shrub of the southeastern United States whose floral form suggests pollination by bumble bees. Floral visitation to L. lucida and pollen loads of visitors were quantified in a population of the species in Central Florida (U.S.A.), and the relative contributions of diurnal and nocturnal pollination tested. Mating system characteristics of L. lucida were also examined. Results show L. lucida flowers are visited mainly by nocturnal moths, who are capable of carrying large pollen loads, and nocturnal pollination is the primary driver of fruit set. In addition L. lucida at the study sit...

Spatial variation in pollinator-mediated selection on phenology, floral display and spur length in the orchid Gymnadenia conopsea.

Spatial variation in plant-pollinator interactions may cause variation in pollinator-mediated selection on floral traits, but to establish this link conclusively experimental studies are needed. We quantified pollinator-mediated selection on flowering phenology and morphology in four populations of the fragrant orchid Gymnadenia conopsea, and compared selection mediated by diurnal and nocturnal pollinators in two of the populations. Variation in pollinator-mediated selection explained most of the among-population variation in the strength of directional and correlational selection. Pollinators mediated correlational selection on pairs of display traits, and on one display trait and spur length, a trait affecting pollination efficiency. Only nocturnal pollinators selected for longer spurs, and mediated stronger selection on the number of flowers compared with diurnal pollinators in one population. The two types of pollinators caused correlational selection on different pairs of traits and selected for different combinations of spur length and number of flowers. The results demonstrate that spatial variation in interactions with pollinators may result in differences in directional and correlational selection on floral traits in a plant with a semi-generalized pollination system, and suggest that differences in the relative importance of diurnal and nocturnal pollinators can cause variation in selection.