Nectar cardenolides and floral volatiles mediate a specialized wasp pollination system.

Specialization in plant pollination systems can arise from traits that function as filters of flower visitors. This may involve chemical traits such as floral volatiles that selectively attract favoured visitors and non-volatile nectar constituents that selectively deter disfavoured visitors through taste or longer-term toxic effects or both. We explored the functions of floral chemical traits in the African milkweed Gomphocarpus physocarpus, which is pollinated almost exclusively by vespid wasps, despite having nectar that is highly accessible to other insects such as honeybees. We demonstrated that the nectar of wasp-pollinated G. physocarpus contains cardenolides that had greater toxic effects on Apis mellifera honeybees than on Vespula germanica wasps, and also reduced feeding rates by honeybees. Behavioural experiments using natural compositions of nectar compounds showed that these interactions are mediated by non-volatile nectar chemistry. We also identified volatile compounds with acetic acid as a main component in the floral scent of G. physocarpus that elicited electrophysiological responses in wasp antennae. Mixtures of these compounds were behaviourally effective for attraction of V. germanica wasps. The results show the importance of both volatile and non-volatile chemical traits as filters that lead to specialization in plant pollination systems.

The economy of pollen dispersal in flowering plants.

Mating success of flowering plants depends strongly on the efficiencies of pollen removal from flowers and its subsequent dispersal to conspecific stigmas. We characterized the economy of pollen dispersal in flowering plants by analysing pollen fates and their correlates for 228 species. The mean percentage of pollen removed from flowers (removal efficiency) varied almost twofold according to the type of pollen-dispersal unit, from less than 45% for orchids and milkweeds with solid pollinia, to greater than 80% for species with granular monads or sectile (segmented) pollinia. The mean percentage of removed pollen reaching stigmas (pollen transfer efficiency, PTE) varied from 2.4% for species with separate monads to 27.0% for orchids with solid pollinia. These values tended to be higher in plants with single pollinator species and in those with non-grooming pollinators. Nectar production increased removal efficiency, but did not influence PTE. Among types of pollen-dispersal units, the net percentage of produced pollen that was dispersed to stigmas varied negatively with removal efficiency and positively with PTE, indicating the relative importance of the latter for overall pollen economy. These findings confirm the key importance of floral traits, particularly pollen packaging, for pollen dispersal outcomes and highlight the under-appreciated pollination efficiency of non-grooming pollinators.

'Bleeding' flowers of Ceropegia gerrardii (Apocynaceae-Asclepiadoideae) mimic wounded insects to attract kleptoparasitic fly pollinators.

Kleptomyiophily, where flowers imitate wounded insects to attract 'kleptoparasitic' flies as pollinators, is one of the most specialized types of floral mimicry and often involves physical trapping devices. However, the diversity of pollinators and functional floral traits involved in this form of mimicry remain poorly understood. We report a novel example of kleptomyiophily in the nontrapping flowers of Ceropegia gerrardii and explore the floral traits responsible for attracting pollinators. The pollinators, reproductive biology and floral traits (including epidermal surfaces, spectral reflectance and the composition of nectariferous petal secretions and scent) were investigated. Attractive volatiles were identified using electrophysiological and behavioural experiments. Ceropegia gerrardii was predominantly pollinated by kleptoparasitic Desmometopa spp. (Milichiidae) flies. The flower corollas extrude a protein- and sugar-containing secretion, similar to the haemolymph of wounded insects, on which the flies feed. Floral scent was chemically similar to that of injured honey bees. Four out of 24 electrophysiologically active compounds, all released by injured honey bees, were identified as key players in pollinator attraction. Our results suggest that C. gerrardii flowers chemically mimic wounded honey bees to attract kleptoparasitic flies and reward them with a secretion similar to the haemolymph on which they would normally feed.

The enantiostylous floral polymorphism of Barberetta aurea (Haemodoraceae) facilitates wing pollination by syrphid flies.

BACKGROUND AND AIMS: Sexual polymorphisms of flowers have traditionally been interpreted as devices that promote cross-pollination, but they may also represent adaptations for exploiting particular pollination niches in local environments. The cross-pollination function of enantiostyly, characterized by flowers having either left- or right-deflected styles, has been uncertain in some lineages, such as the Haemodoraceae, because the positioning of stamens and styles is not always completely reciprocal among morphs. METHODS: We examined the floral biology of populations of the poorly known species Barberetta aurea (Haemodoraceae) across its native range in South Africa to establish the general features of its enanatiostylous reproductive system and the agents and mechanism of pollen transfer. RESULTS: We confirmed that B. aurea has a system of dimorphic enantiostyly. Style morph ratios varied among populations sampled, but with an overall tendency to being equal. Crossing experiments demonstrated that B. aurea is fully self-compatible, that intra- and inter-morph crosses are equally fertile and that it is wholly dependent on pollinator visits for seed production. Pollination is mainly by syrphid flies that transfer the sticky pollen via their wings, which contact the anthers and stigma precisely as they hover during approach and feeding. The majority of syrphid fly visitors feed on a film of highly concentrated nectar situated at the base of ultraviolet-absorbent 'nectar guides'. Because one of the three stamens is deflected in the same direction as the style, we predicted a high likelihood of intra-morph pollination, and this was corroborated by patterns of transfer of coloured dye particles in cage experiments involving syrphid flies. CONCLUSIONS: Barbaretta aurea exhibits dimorphic enantiostyly and, in contrast to most enantiostylous species, which are pollinated by bees, its flowers are specialized for pollination by syrphid flies. The lack of complete reciprocity of the enantiostylous arrangement of sexual organs facilitates both inter- and intra-morph pollen transfer on the wings of these flies.

The lady's 'slippery' orchid: functions of the floral trap and aphid mimicry in a hoverfly-pollinated Phragmipedium species in Brazil.

BACKGROUND AND AIMS: Trap flowers are fascinating cases of adaptation, often linked to oviposition-site mimicry systems. Some trap flowers do not imprison pollinators for a pre-determined period, but rather force them to move through a specific path, manipulating their movements in a way that culminates in pollen transfer, often as they leave through a secondary opening. METHODS: We investigated the previously unknown pollination system of the lady's slipper orchid Phragmipedium vittatum and assessed the function of micro-morphological traits of its trap flowers. KEY RESULTS: Our observations revealed that P. vittatum is pollinated by females of two hoverfly species (Syrphidae). Eggs laid by flies on or near raised black spots on the flowers indicate that the orchid mimics aphids which serve as food for their aphidophagous larvae. Dark, elevated aphid-like spots appear to attract the attention of hoverflies to a slipping zone. This region has downward projecting papillate cells and mucilage secretion that promote slipperiness, causing potential pollinators to fall into the labellum. They then follow a specific upward route towards inner aphid-like spots by holding onto upward oriented hairs that aid their grip. As hoverflies are funnelled by the lateral constriction of the labellum, they pass the stigma, depositing pollen they may be carrying. Later, they squeeze under one of the articulated anthers which places pollen smears onto their upper thorax. Then, they depart through one of the narrow lateral holes by holding onto hairs projecting from the petals. CONCLUSIONS: This study confirms the system of aphid mimicry in Phragmipedium and highlights the sophisticated micro-morphological traits used by trap flowers in pollinator attraction, trapping, guidance and release, thus promoting precise pollen transfer.

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

PREMISE: 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. METHODS: 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. RESULTS: 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. CONCLUSIONS: 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.

Why honeybees are poor pollinators of a mass-flowering plant: Experimental support for the low pollen quality hypothesis.

PREMISE: Honeybees dominate the flower-visitor assemblages of many plant species, yet their efficiency in terms of the quality of pollen delivered to stigmas is largely unknown. We investigated why honeybees are poor pollinators of Aloe ferox, a self-incompatible succulent treelet with large numbers of flowers. Honeybees are very frequent visitors to flowers of this species, yet contribute very little to seed production. METHODS: We assessed pollen loads on honeybees, studied their visitation behavior, selectively excluded birds from plants to determine direct effects of bees on pollen deposition, seed set, and ovule abortion, and used a novel "split-pollinator" method to test whether honeybees deposit mainly low-quality self pollen. For the latter, we captured honeybees, and with their existing pollen loads, used them to either pollinate virgin flowers on the plant on which they were caught or to pollinate virgin flowers on different plants. RESULTS: Honeybees cumulatively deposit as much pollen on stigmas as do birds, but our experiments showed that the pollen deposited by honeybees is mostly low-quality self pollen that leads to substantial ovule discounting and depressed seed set. CONCLUSIONS: Lack of movement among A. ferox plants during individual honeybee foraging bouts is the most likely explanation for their deposition of low-quality self pollen on stigmas. The "split-pollinator" method is a simple and cost-effective technique to test the quality of pollination.

Biomechanics of nectar feeding explain flower orientation in plants pollinated by long-proboscid flies.

The function of flower orientation is much debated, with adaptation to pollinator mouthparts being a particularly compelling explanation, but also one that has lacked empirical support from broad-scale comparative studies. The two families of long-proboscid fly pollinators show similar hovering behaviour while feeding on nectar but differ in the biomechanics of their proboscides which can be up to 80 mm in length: Tabanidae have a fixed forward-pointing proboscis while Nemestrinidae can swivel their proboscis downwards. We predicted that this difference has implications for the evolution of flower orientation. We established the flower angles of 156 South African plant species specialised for pollination by long-proboscid flies. Using a phylogenetically corrected analysis, we found that flowers pollinated by Tabanidae tend to be horizontally orientated, while those pollinated by Nemestrinidae tend to be more variable in orientation and more often vertically orientated. These results confirm the importance of pollinator biomechanics for the evolution of floral traits and highlight a potential mechanism of reproductive isolation between sympatric plant species pollinated by different long-proboscid fly families.

Mechanisms of Male-Male Interference during Dispersal of Orchid Pollen.

AbstractSiring success of flowering plants depends on the fates of male gametophytes, which compete for access to stigmas, stylar resources, and ovules. Although rarely considered, pollen may often compete during dispersal, affecting the processes required for export to stigmas: pollen pickup, transport, and deposition. We quantified dispersal interference by tracking bee-mediated dispersal of stained Anacamptis morio (Orchidaceae) pollen from individual donor flowers and inferred the affected dispersal mechanisms on the basis of the fit of a process-based model. During individual trials, all recipient flowers were either emasculated, precluding interference with donor pollen, or intact, adding potentially interfering pollen to the pollinator. The presence of competing pollinaria on bees reduced pickup of additional pollinaria, doubled the overall proportion of lost donor pollen, and reduced total pollen export by 27%. Interference specifically increased loss of donor pollen between successive flower visits and variation in deposition among trials, and it likely also reduced pollen contact with stigmas and pollen deposition when contact occurred. Thus, by altering pollen removal, transport, and deposition, male-male interference during pollen dispersal can significantly-and perhaps commonly-limit plant-siring success.

Optimising backscatter from multiple beam interference.

Optical sensing applications are usually reliant on the intensity of the measured signal. For remote sensing applications where a target is probed with a laser beam, the sensitivity will be limited by the amount of backscattered light returned from the target to the detector. We demonstrate a method of increasing the signal returned to the detector by illuminating the target with a number of independently controlled beams, where both the position and phase are optimised. We show an improvement in the backscattered signal that is proportional to the number of beams used. The method is demonstrated within a laser microphone, measuring audio signal due to vibrations in surfaces, showing a significant improvement in the signal-to-noise of the measurement.

Florivory can facilitate rain-assisted autogamy in a deceptive tropical orchid.

Florivores and rainfall generally have negative impacts on plant fecundity. However, in some cases, they can mediate fruit set. Some plants face severe pollen-limited fecundity and any additional fruit set, even if from self-pollination, can be advantageous. This is the case in some tropical deceptive orchids, such as the threatened Cyrtopodium hatschbachii. Here we test the hypothesis that florivory of the anther cap would facilitate rain-assisted autogamy in this species. In the field, we followed flowers in which the anther cap was removed by the orthopteran Stenopola sp. and found cases where pollinia self-deposited after rainfall and in one case this resulted in swelling of the column typical of fruit development. This event comprised 33% of all fruit set in the population in 2019. We then experimentally varied anther cap removal and rainfall in a factorial design and found increased fruit set in the group with cap removal (simulated florivory) followed by rain. The water absorption by pollinia makes them heavier, causing the stipe to bend. The droplet of water on the stigma then shrinks and pulls the pollinia back onto the stigma, causing self-pollination. Seeds from self-pollination have considerable viability and may allow population persistence, given that bee-mediated cross-pollination is uncertain and even absent in some years. Our study provides a unique example of how two unrelated factors (i.e., florivory and rain) that are detrimental alone may together promote fruit set.

Does acoustic priming 'sweeten the pot' of floral nectar?

A recent claim that evening primrose flowers adaptively secrete nectar in response to vibrations from hovering bees lacks supporting evidence. The authors fail to demonstrate that bees can access the concealed nectar and that their visits enhance plant fitness. Reanalysis of the authors' data raises additional concerns about their conclusions.

Dung mimicry: the function of volatile emissions and corolla patterning in fly-pollinated Wurmbea flowers.

It has been suggested that flowers of some angiosperms mimic vertebrate faeces (dung) in order to exploit insect pollinators that utilize faeces as a source of food and/or oviposition sites. We investigated a potential case of mimicry in Wurmbea elatior (Colchicaceae), a lily that exhibits a faecal odour and pattern of dark spots on the corolla. We found that W. elatior is pollinated by a broad assemblage of coprophagous flies and is dependent on pollinator visits for seed production. The flowers emit volatiles that are characteristic of vertebrate faeces, and three of these compounds - skatole, indole, and an unidentified compound - elicited electrophysiological antennal responses from flies. Artificial flowers laced with indole and skatole or skatole alone attracted the same assemblage of flies as was recorded on flowers of W. elatior. Spotted artificial flowers attracted twice as many flies as did those lacking spots. Experimental addition of indole and skatole to flowers of Wurmbea kraussii, a congener with unscented flowers pollinated by hoverflies, induced a shift to an insect visitor assemblage dominated by coprophagous flies. This study clarifies the roles of volatile emissions (particularly skatole) and visual signals in floral dung mimicry.

Single-pixel imaging 12 years on: a review.

Modern cameras typically use an array of millions of detector pixels to capture images. By contrast, single-pixel cameras use a sequence of mask patterns to filter the scene along with the corresponding measurements of the transmitted intensity which is recorded using a single-pixel detector. This review considers the development of single-pixel cameras from the seminal work of Duarte et al. up to the present state of the art. We cover the variety of hardware configurations, design of mask patterns and the associated reconstruction algorithms, many of which relate to the field of compressed sensing and, more recently, machine learning. Overall, single-pixel cameras lend themselves to imaging at non-visible wavelengths and with precise timing or depth resolution. We discuss the suitability of single-pixel cameras for different application areas, including infrared imaging and 3D situation awareness for autonomous vehicles.

Flower orientation in Gloriosa superba (Colchicaceae) promotes cross-pollination via butterfly wings.

BACKGROUND AND AIMS: Complex modifications of angiosperm flowers often function for precise pollen placement on pollinators and to promote cross-pollination. We explore the functional significance of the unusually elaborate morphology of Gloriosa superba flowers, which are divided into one hermaphrodite meranthium and five male meranthia (functional pollination units of a single flower). METHODS: We used controlled pollination experiments, floral measurements, pollen load analyses and visitor observations in four populations of G. superba in South Africa to determine the breeding system, mechanism of pollination and role of flower in the promotion of cross-pollination. KEY RESULTS: We established that G. superba is self-compatible, but reliant on pollinators for seed production. Butterflies, in particular the pierid Eronia cleodora, were the primary pollinators (>90 % of visitors). Butterflies brush against the anthers and stigma during nectar feeding and pollen is carried on their ventral wing surfaces. Butterfly scales were positively correlated with the number of pollen grains on stigmas. We demonstrate that the styles were orientated towards clearings in the vegetation and we confirm that the highest proportion of initial visits was to hermaphrodite meranthia pointing towards clearings. CONCLUSIONS: The flower morphology of G. superba results in effective pollen transfer on the wings of butterfly visitors. The style-bearing hermaphrodite meranthium of the flowers orientates towards open spaces in the vegetation, thus increasing the probability that butterflies land first on the hermaphrodite meranthium. This novel aspect of flower orientation is interpreted as a mechanism that promotes cross-pollination.

Diel scent and nectar rhythms of an African orchid in relation to bimodal activity patterns of hawkmoth pollinators.

BACKGROUND AND AIMS: The temporal dimensions of floral adaptation to pollinators are not yet well understood, partly because we lack accurate information on the diel rhythms of flower visitation for many pollinators. We investigated whether diel patterns of pollinator visitation to flowers of the African woodland orchid Bonatea polypodantha are synchronized with rhythms of floral anthesis, scent emission and nectar availability. METHODS: Direct observations and motion-activated cameras were used to identify pollinators of B. polypodantha and to document their activity periods. The timing of pollinaria removal from flowers, emission of scent and availability of nectar was also measured. RESULTS: We found that B. polypodantha is pollinated exclusively by short-tongued hawkmoths. Pollinaria of the orchid are affixed between the labial palps of the moths and brush over the protruding stigmatic arms. The flowers also receive visits by long-tongued hawkmoths, but these act as nectar thieves. Tracking of pollinaria removal from flowers confirmed that pollination occurs only at night. Camera footage revealed a striking crepuscular pattern of foraging by short-tongued hawkmoths with peaks of activity during the twilight periods at dusk and at dawn. In contrast, long-tongued hawkmoths were found to visit flowers throughout the night. Flowers of B. polypodantha exhibit unimodal peaks of anthesis, scent emission (dominated by nitrogenous aromatics) and nectar availability before or around dusk. CONCLUSIONS: Flowers of B. polypodantha are pollinated exclusively by short-tongued hawkmoths, which show crepuscular foraging activity at dusk and dawn. Floral phenophases of the orchid are closely synchronized with the peak of pollinator activity at dusk.

Scent chemistry is key in the evolutionary transition between insect and mammal pollination in African pineapple lilies.

Volatile emissions may play a key role in structuring pollination systems of plants with morphologically unspecialised flowers. Here we test for pollination by small mammals in Eucomis regia and investigate whether its floral scent differs markedly from fly- and wasp-pollinated congeners and attracts mammals. We measured floral traits of E. regia and made comparisons with insect-pollinated congeners. We observed floral visitors and examined fur and faeces of live-trapped mammals for pollen. We determined the contributions of different floral visitors to seed set with selective exclusion and established the breeding system with controlled pollination experiments. Using bioassays, we examined whether mammals are attracted by the floral scent and are effective agents of pollen transfer. Eucomis regia differs from closely related insect-pollinated species mainly in floral scent, with morphology, colour and nectar properties being similar. We found that mice and elephant-shrews pollinate E. regia, which is self-incompatible and reliant on vertebrates for seed production. Mammals are strongly attracted to the overall floral scent, which contains unusual sulphur compounds, including methional (which imparts the distinctive potato-like scent and which was shown to be attractive to small mammals). The results highlight the important role of scent chemistry in shifts between insect and mammal pollination systems.

A light-in-flight single-pixel camera for use in the visible and short-wave infrared.

Single-pixel cameras reconstruct images from a stream of spatial projection measurements recorded with a single-element detector, which itself has no spatial resolution. This enables the creation of imaging systems that can take advantage of the ultra-fast response times of single-element detectors. Here we present a single-pixel camera with a temporal resolution of 200 ps in the visible and short-wave infrared wavelengths, used here to study the transit time of distinct spatial modes transmitted through few-mode and orbital angular momentum mode conserving optical fiber. Our technique represents a way to study the spatial and temporal characteristics of light propagation in multimode optical fibers, which may find use in optical fiber design and communications.

The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study.

Background and Aims: Large clades of angiosperms are often characterized by diverse interactions with pollinators, but how these pollination systems are structured phylogenetically and biogeographically is still uncertain for most families. Apocynaceae is a clade of >5300 species with a worldwide distribution. A database representing >10 % of species in the family was used to explore the diversity of pollinators and evolutionary shifts in pollination systems across major clades and regions. Methods: The database was compiled from published and unpublished reports. Plants were categorized into broad pollination systems and then subdivided to include bimodal systems. These were mapped against the five major divisions of the family, and against the smaller clades. Finally, pollination systems were mapped onto a phylogenetic reconstruction that included those species for which sequence data are available, and transition rates between pollination systems were calculated. Key Results: Most Apocynaceae are insect pollinated with few records of bird pollination. Almost three-quarters of species are pollinated by a single higher taxon (e.g. flies or moths); 7 % have bimodal pollination systems, whilst the remaining approx. 20 % are insect generalists. The less phenotypically specialized flowers of the Rauvolfioids are pollinated by a more restricted set of pollinators than are more complex flowers within the Apocynoids + Periplocoideae + Secamonoideae + Asclepiadoideae (APSA) clade. Certain combinations of bimodal pollination systems are more common than others. Some pollination systems are missing from particular regions, whilst others are over-represented. Conclusions: Within Apocynaceae, interactions with pollinators are highly structured both phylogenetically and biogeographically. Variation in transition rates between pollination systems suggest constraints on their evolution, whereas regional differences point to environmental effects such as filtering of certain pollinators from habitats. This is the most extensive analysis of its type so far attempted and gives important insights into the diversity and evolution of pollination systems in large clades.

Generalist birds outperform specialist sunbirds as pollinators of an African Aloe.

Bird pollination systems are dominated by specialist nectarivores, such as hummingbirds in the Americas and sunbirds in Africa. Opportunistic (generalist) avian nectarivores such as orioles, weavers and bulbuls have also been implicated as plant pollinators, but their effectiveness as agents of pollen transfer is poorly known. Here, we compare the single-visit effectiveness of specialist and opportunistic avian nectarivores as pollinators of Aloe ferox, a plant that relies almost exclusively on birds for seed production. We found that the number of pollen grains on stigmas of flowers receiving single visits by opportunistic avian nectarivores was approximately threefold greater than on those receiving single visits by specialist sunbirds and about twofold greater than on those that received single visits by honeybees. The number of pollen grains on stigmas of flowers visited by sunbirds was similar to that on stigmas of unvisited flowers. These results show that opportunistic birds are highly effective pollinators of A. ferox, supporting the idea that some plants are specialized for pollination by opportunistic birds.