Pollination Strategies Research Articles

Evidence for a food-deceptive pollination system using Hylaeus bees in Caladenia hildae (Orchidaceae)

Numerous orchid species are pollinated by food deception, where rewardless flowers attract foraging pollinators through the mimicry of other flowers or the use of non-specific floral signals. Here we investigate the pollination of Caladenia hildae, a member of a diverse Australian genus containing species pollinated by sexual deception, and species pollinated by food foraging pollinators. Despite eight bee species occurring at the main study site, only food foraging bees of a single species of Hylaeus (Colletidae) were observed to remove and deposit pollen of C. hildae. Spectral reflectance of C. hildae flowers differed from co-flowering rewarding species in terms of both the wavelengths of light reflected, and the pattern of colouration. As such, there was no evidence that C. hildae uses a pollination strategy based on floral mimicry. However, the attraction of only a single bee species at this site suggests that C. hildae may use a deceptive strategy that exploits sensory biases or behaviours that differ between Hylaeus sp. and the remainder of the bee community. While Hylaeus have been recorded visiting orchid flowers in several parts of the world, C. hildae may represent the first documented case of an orchid species specialised on pollination by Hylaeus bees.

A specialised pollination system using nectar-seeking thynnine wasps in Caladenia nobilis (Orchidaceae).

Caladenia is a diverse Australian genus that is exceptional among orchids in having both species pollinated by food-seeking and sexually deceived insects. Here, we investigated the pollination of Caladenia nobilis, a species predicted to be food-deceptive due to its large, cream-coloured and apparently nectarless flowers. Pollinator observations were made using experimental clumps of flowers. Measurements of floral colour were undertaken with a spectrometer, nectar was tested using GC-MS, and reproductive success was quantified for 2years. While C.nobilis attracted nine species of insect, only males of the thynnine wasp Rhagigaster discrepans exhibited the correct size and behaviour to remove and deposit pollen. Male R.discrepans attempted to feed from the surface of the labellum, often crawling to multiple flowers, but showed no evidence of sexual attraction. Most flowers produced little or no nectar, although some may provide enough sucrose to act as a meagre reward to pollinators. Floral colouration was similar to a related Caladenia species pollinated by sexual deception, although the sexually deceptive species had a dull-red labellum. Reproductive success was generally low and highly variable between sites and years. In addition to most visitors being of inappropriate size for pollinia removal, the lack of response to the orchid by several co-occurring species of thynnine wasp suggests filtering of potential pollinators at the attraction phase. Our discovery of a pollination strategy that may be intermediate between food deception and food reward raises the question, how many putatively rewardless orchids actually produce meagre amounts of nectar?

The effect of seasonality on developmental stages of anthetic ovule integuments in Mediterranean orchids.

Orchids, differently from most flowering plants, have under-differentiated ovules at anthesis that require pollination to complete differentiation. This ovule developmental stage has been often observed in tropical species in which the absence of an evident seasonality may allow plants to extend their phenology beneficiating of a long time for post-pollination events. Here, we used scanning electron microscopy (SEM) to detect ovule integument developmental stages in 21 species of Mediterranean Orchidoideae and Epidendroideae and in 11 tropical Epidendroideae with the aim of understanding whether species with a seasonal constraint and shorter time for post-pollination ovule maturation are characterized by different stages of ovule development at anthesis. We found that Mediterranean orchids (both Orchidoideae and Epidendroideae) have more developed ovule integuments than tropical orchids. Most species show partially to fully developed ovules at anthesis with the exception of Cephalanthera where ovules are arrested in a very early developmental stage. Despite the phylogenetic signal, anthetic ovule integument development differs between related species (with different pollination strategies or blooming times), suggesting the presence of some ecological constraints. The synchronization between ovule integuments and megagametophyte development, as found in tropical orchids, is also confirmed in Mediterranean orchids. Our data show that Mediterranean and tropical orchids clearly differ in anthetic ovule developmental stages, likely depending on seasonality.

A Specific Blend of Drakolide and Hydroxymethylpyrazines: An Unusual Pollinator Sexual Attractant Used by the Endangered Orchid Drakaea micrantha.

Bioactive natural products underpin the intriguing pollination strategy used by sexually deceptive orchids. These compounds, which mimic the sex pheromones of the female insect, are emitted in particular blends to lure male insect pollinators of specific species. By combining methods from field biology, analytical chemistry, electrophysiology, crystallography, and organic synthesis, we report that an undescribed β-hydroxylactone, in combination with two specific hydroxymethylpyrazines, act as pollinator attractants in the rare hammer orchid Drakaea micrantha. This discovery represents an unusual case of chemically unrelated compounds being used together as a sexual attractant. Furthermore, this is the first example of the identification of pollinator attractants in an endangered orchid, enabling the use of chemistry in orchid conservation. Our synthetic blend is now available to be used in pollinator surveys to locate suitable sites for plant conservation translocations.

A Specific Blend of Drakolide and Hydroxymethylpyrazines: An Unusual Pollinator Sexual Attractant Used by the Endangered Orchid Drakaea micrantha

AbstractBioactive natural products underpin the intriguing pollination strategy used by sexually deceptive orchids. These compounds, which mimic the sex pheromones of the female insect, are emitted in particular blends to lure male insect pollinators of specific species. By combining methods from field biology, analytical chemistry, electrophysiology, crystallography, and organic synthesis, we report that an undescribed β‐hydroxylactone, in combination with two specific hydroxymethylpyrazines, act as pollinator attractants in the rare hammer orchid Drakaea micrantha. This discovery represents an unusual case of chemically unrelated compounds being used together as a sexual attractant. Furthermore, this is the first example of the identification of pollinator attractants in an endangered orchid, enabling the use of chemistry in orchid conservation. Our synthetic blend is now available to be used in pollinator surveys to locate suitable sites for plant conservation translocations.

A literature review of the pollination strategies and breeding systems in Oncidiinae orchids

ABSTRACT Oncidiinae is an exclusively Neotropical orchid subtribe with about 1600 described species and an impressive array of vegetative and floral morphological adaptations. We present the results of a literature survey on the pollination strategies and breeding systems of this orchid subtribe. The flowers are pollinated by a wide range of insects (mostly bees) and, sometimes, hummingbirds. Several genera reward their pollinators with floral resources such as oils, nectar or perfumes. Whereas pollination by oil-gathering bees likely evolved several times within Oncidiinae, exclusive pollination by perfume-gathering male Euglossine bees is likely restricted to a set of closely-related genera. Pollination by food or sexual deception is also present within the subtribe. Up to date, the pollen-vectors of the 92 species of Oncidiinae studied so far are as follows: 84.7 % are pollinated by bees, 6.5 % by wasps, 4.3 % by hummingbirds, 3.2 % by butterflies and 3.2 % by flies. Oncidiinae orchids are preferentially self-incompatible (69.4 % of the species studied so far), some may also present protandry as a mechanism to promote cross-pollination. Fruiting success is generally low. The rate of visitation with subsequent pollination is low, in general, which contributes to the low reproductive success of this plant group.

A Phylogenomic Analysis of the Floral Transcriptomes of Sexually Deceptive and Rewarding European Orchids, Ophrys and Gymnadenia.

The orchids (Orchidaceae) constitute one of the largest and most diverse families of flowering plants. They have evolved a great variety of adaptations to achieve pollination by a diverse group of pollinators. Many orchids reward their pollinators, typically with nectar, but the family is also well-known for employing deceptive pollination strategies in which there is no reward for the pollinator, in the most extreme case by mimicking sexual signals of pollinators. In the European flora, two examples of these different pollination strategies are the sexually deceptive genus Ophrys and the rewarding genus Gymnadenia, which differ in their level of pollinator specialization; Ophrys is typically pollinated by pseudo-copulation of males of a single insect species, whilst Gymnadenia attracts a broad range of floral visitors. Here, we present and describe the annotated floral transcriptome of Ophrys iricolor, an Andrena-pollinated representative of the genus Ophrys that is widespread throughout the Aegean. Furthermore, we present additional floral transcriptomes of both sexually deceptive and rewarding orchids, specifically the deceptive Ophrys insectifera, Ophrys aymoninii, and an updated floral transcriptome of Ophrys sphegodes, as well as the floral transcriptomes of the rewarding orchids Gymnadenia conopsea, Gymnadenia densiflora, Gymnadenia odoratissima, and Gymnadenia rhellicani (syn. Nigritella rhellicani). Comparisons of these novel floral transcriptomes reveal few annotation differences between deceptive and rewarding orchids. Since together, these transcriptomes provide a representative sample of the genus-wide taxonomic diversity within Ophrys and Gymnadenia (Orchidoideae: Orchidinae), we employ a phylogenomic approach to address open questions of phylogenetic relationships within the genera. Specifically, this includes the controversial placement of O. insectifera within the Ophrys phylogeny and the placement of “Nigritella”-type morphologies within the phylogeny of Gymnadenia. Whereas in Gymnadenia, several conflicting topologies are supported by a similar number of gene trees, a majority of Ophrys gene topologies clearly supports a placement of O. insectifera as sister to a clade containing O. sphegodes.

Cretaceous beetles (Insecta: Coleoptera) in amber: the palaeoecology of this most diverse group of insects

AbstractBeetles, the most successful group of invertebrates on Earth, have a worldwide distribution and an outstanding fossil record. In addition, they are well known as inclusions in fossil resin. In historical studies of fossil material, specimens were often named and described without placing the taxa in an ecological context. However, the research philosophy for fossil beetles has changed over the past few years. In this article, we summarize the palaeoecological interpretations of fossil beetles from Cretaceous ambers, which includes species from 69 families, most of which were described during the last 3 years. By analysing current habits of those families, we argue that saproxylicity was the most common feeding strategy for these fossil beetles. More specifically, fungivorous species appear to dominate. In contrast, we find only anecdotal evidence for the presence of wood-boring groups, and it is thus necessary to identify alternative abiotic or biotic processes that are responsible for the copious resin production at this time. Finally, the recent description of some beetles as gymnosperm pollinators during the Cretaceous lends more weight to the importance of amber studies in addressing the role of beetles in the evolution of pollination strategies.

In-situ and ex situ pollination biology of the four threatened plant species and the significance for conservation

Both in situ and ex situ conservation are important strategies for protecting threatened plant species. Nevertheless, the success of conservation depends on whether the plant species can naturally regenerate and accomplish its life cycle over a long-term. Here we studied the pollination biology of the threatened species Hibiscus aridicola, Amorphophallus albus, Stemona parviflora and S. japonica aiming to get data about pollination strategies, pollinators as well as mating systems. These experiments were performed at Kunming Botanical Garden (KBG) for ex situ and the plant species’ natural habitat for in situ conservation. The results indicated that H. aridicola is self-compatible and had pollinators under both ex situ and in situ conditions. The other three species are all self-incompatible and a limited number of pollinators for S. parviflora and S. japonica were observed at cultivated and natural habitats. Amorphophallus albus had no pollinators at KBG but a large number of rove beetles (Atheta sp.) could be observed in the plant species’ natural habitat. This resulted in a high fruit set under natural conditions (73.3%, n = 30). The results showed clearly, that appropriate pollinators for the four plant species are not present all the time and all localities, which further influences the reproduction success of a plant species. Hence, for a successful conservation, it is vital to assess the species reproduction strategy prior deciding whether in situ and/or ex situ conservation should be carried out.

Flower nectar trichome structure of carnivorous plants from the genus butterworts Pinguicula L. (Lentibulariaceae)

Pinguicula (Lentibulariaceae) is a genus comprising around 96 species of herbaceous, carnivorous plants, which are extremely diverse in flower size, colour and spur length and structure as well as pollination strategy. In Pinguicula, nectar is formed in the flower spur; however, there is a gap in the knowledge about the nectary trichome structure in this genus. Our aim was to compare the nectary trichome structure of various Pinguicula species in order to determine whether there are any differences among the species in this genus. The taxa that were sampled were Pinguicula moctezumae, P. moranensis, P. rectifolia, P. emarginata and P. esseriana. We used light microscopy, histochemistry, scanning and transmission electron microscopy to address those aims. We show a conservative nectary trichome structure and spur anatomy in various Mexican Pinguicula species. The gross structural similarities between the examined species were the spur anatomy, the occurrence of papillae, the architecture of the nectary trichomes and the ultrastructure characters of the trichome cells. However, there were some differences in the spur length, the size of spur trichomes, the occurrence of starch grains in the spur parenchyma and the occurrence of cell wall ingrowths in the terminal cells of the nectary trichomes. Similar nectary capitate trichomes, as are described here, were recorded in the spurs of species from other Lentibulariaceae genera. There are many ultrastructural similarities between the cells of nectary trichomes in Pinguicula and Utricularia.

Development of sweet cherry (Prunus avium L.) and apricot (Prunus armeniaca L.) cultivars and production systems in California and Europe

There is an ongoing need for sweet cherries and apricots that are improved over those existing. Improved and regular production, fruit size, firmness, time of maturity, packing, shipping and organoleptic characteristics are some traits that can be improved within the varietal maturity window. Over the last several years, we have released several sweet cherry cultivars (4 patented in Europe and others pending in the world) with early fruit ripening characteristics that are productive, with large fruit size, over a range of geographic locations with commercial potential. A number of apricots have been patented in Europe and the world and commercialized. We have identified pollination and production strategies toward maximizing the potential of these selections. The development of these cultivars and production strategies in Europe and worldwide will be discussed and reviewed as will future developments.

Pollination Strategies to Improve Fruit Set in Orchards of ‘Manzanilloʼ Olive in a Nontraditional Producing Country, Mexico

In countries new to producing ‘Manzanillo’ olive trees (Olea europaea), free cross-pollination is often insufficient to obtain high levels of fruit set. An appropriate pollination design is therefore essential to ensure a timely, abundant, and compatible pollen supply. With a view to determining whether a pollination deficit exists in a nontraditional olive area such as the northern Mexico, pollination experiments were carried out in two consecutive seasons in both a monovarietal and a multivarietal Manzanillo orchard, where Sevillano, Barouni, Picual, Pendolino, Mission, Nevadillo, and Frantoio trees were growing nearby. The pollination treatments were self-, open, and cross-pollination with ‘Barouni’ and ‘Sevillano’ pollen, the latter only in the multivarietal orchard. The results confirmed the full self-incompatible condition of ‘Manzanillo’. Open-pollination did not improve fruit set in the monovarietal orchard, but it did so significantly in the multivarietal plot, where fruit set levels under open-pollination matched those of cross-pollination. Lower pollen adhesion, as well as occasional decreased germination, and reduced and delayed pollen tube growth were observed under self-pollination, highlighting self-incompatibility reactions. The reduction in fertilization rates led to low fruit set under self-pollination. Positive effects of open- and cross-pollination treatments were also noted on fruit weight (despite higher crop loads) and pulp-to-pit ratios. A strategic plantation design, including appropriate pollinizers in the right number and position, is therefore suggested for increasing ‘Manzanillo’ fruit quality and yield in Mexico. Both ‘Barouni’ and ‘Sevillano’ served as efficient pollinizers for ‘Manzanillo’, although we recommend ‘Barouni’ as a more efficient because the bloom periods of them matched that of ‘Manzanillo’

Pollinators and visitors of the generalized food-deceptive orchid Dactylorhiza majalis in North-Eastern Poland

Pollinator foraging behavior plays a key role in breeding and therefore affects the evolution of the orchid reproductive strategy. Food-deceptive orchids usually implement a generalized plant pollination strategy and a relatively diverse group of pollinators visit them. Dactylorhiza majalis is a food-deceptive, early-flowering orchid that relies on insect-mediated pollination. This study’s objectives were to identify D. majalis’ pollinators and flower visitors and their foraging behaviors on D. majalis inflorescences. We also assessed the bending movement time to determine the relationship between bending time and the duration of pollinators’ visits. To assess pollination efficiency, we measured the spur length of D. majalis flowers, which is expected to affect the mechanical fit to pollinators/“potential” pollinators. The arthropod fauna were investigated to examine the availability of “potential” pollinators in populations. We identified Apis mellifera as this orchid’s main pollinator and confirmed that few of the flower visitors belonged to Diptera (12 individuals, 9 taxa), Hymenoptera (3 individuals, 3 taxa), or Coleoptera (2 individuals, 2 taxa) in our dataset, which was collected over a 2-year period and includes 360 h of video. The arthropods were collected by a sweep net in D. majalis populations and there were fewer Hymenoptera (2.9–23.2%) and Coleoptera (4.4–23.8%) visitors but more Diptera (23.3–58.6%) visitors. We found that A. mellifera foraged in different ways on D. majalis inflorescences, thereby resulting in cross-pollination and/or geitonogamy; however, the bending time data supported the hypothesis about promoting cross-pollination while decreasing self-pollination, but these data do not exclude the possibility of geitonogamy.

Random search with resetting as a strategy for optimal pollination.

The problem of pollination is unique among a wide scope of search problems, since it requires optimization of benefits for both the searcher (pollinator) and its targets (plants). To address this challenge, we propose a pollination model which is based on a framework of first passage under stochastic restart. We derive equations for the search time and number of visited plants as functions of the distribution of nectar in the plant population and of the probability that a pollinator will leave the plant after examining a flower, thus effectively restarting the search. We demonstrate that nectar variation in plants serves as a driving force for pollination and establish conditions required for optimal pollination, which provides an efficient pollinator search strategy and the maximum number of plants visited by the pollinator.

Mechanisms in mutualisms: a chemically mediated thrips pollination strategy in common elder

Main conclusionThis study provides first evidence of a thrips species pollinating Sambucus nigra and describes how interactions are driven by plant biochemical signalling and moderated by temporal changes in floral chemistry.The concept of flower-feeding thrips as pollinating insects in temperate regions is rarely considered as they are more frequently regarded to be destructive florivores feeding on pollen and surrounding plant tissue. Combining laboratory and field-based studies we examined interactions between Sambucus nigra (elderflower) and Thrips major within their native range to ascertain the role of thrips in the pollination of this species and to determine if floral chemicals mediated flower visits. If thrips provide a pollination service to S. nigra, then this will likely manifest in traits that attract the pollinating taxa at temporally critical points in floral development. T. major were highly abundant in inflorescences of S. nigra, entering flowers when stigmas were pollen-receptive and anthers were immature. When thrips were excluded from the inflorescences, fruit-set failed. Linalool was the major component of the inflorescence headspace with peak abundance coinciding with the highest number of adult thrips visiting flowers. Thrips were absent in buds and their numbers declined again in senescing flowers inversely correlating with the concentration of cyanogenic glycosides recorded in the floral tissue. Our data show that S. nigra floral chemistry mediates the behaviour of pollen-feeding thrips by attracting adults in high numbers to the flowers at pre-anthesis stage, while producing deterrent compounds prior to fruit development. Taking an integrative approach to studying thrips behaviour and floral biology we provide a new insight into the previously ambiguously defined pollination strategies of S. nigra and provide evidence suggesting that the relationship between T. major and S. nigra is mutualistic.

Flower scent of Ceropegia stenantha: electrophysiological activity and synthesis of novel components

In specialized pollination systems, floral scents are crucial for flower–pollinator communication, but key volatiles that attract pollinators are unknown for most systems. Deceptive Ceropegia trap flowers are famous for their elaborate mechanisms to trap flies. Recent studies revealed species-specific floral chemistry suggesting highly specialized mimicry strategies. However, volatiles involved in fly attraction were until now identified in C. dolichophylla and C. sandersonii, only. We here present data on C. stenantha for which flower scent and pollinators were recently described, but volatiles involved in flower–fly communication stayed unknown. We performed electrophysiological measurements with scatopsid fly pollinators (Coboldia fuscipes) and identified 12 out of 13 biologically active floral components. Among these volatiles some were never described from any organism but C. stenantha. We synthesized these components, tested them on antennae of male and female flies, and confirmed their biological activity. Overall, our data show that half of the volatiles emitted from C. stenantha flowers are perceived by male and female fly pollinators and are potentially important for flower–fly communication in this pollination system. Further studies are needed to clarify the role of the electrophysiologically active components in the life of scatopsid fly pollinators, and to fully understand the pollination strategy of C. stenantha.

Linking the foraging behavior of three bee species to pollen dispersal and gene flow.

Foraging behaviors that impact gene flow can guide the design of pollinator strategies to mitigate gene flow. Reduced gene flow is expected to minimize the impact of genetically engineered (GE) crops on feral and natural populations and to facilitate the coexistence of different agricultural markets. The goal of this study is to link foraging behavior to gene flow and identify behaviors that can help predict gene flow for different bee species. To reach this goal, we first examined and compared the foraging behaviors of three distinct bee species, the European honey bee, Apis mellifera L., the common eastern bumble bee, Bombus impatiens Cr., and the alfalfa leafcutting bee, Megachile rotundata F., foraging on Medicago sativa flowers. Each foraging behavior investigated differed among bee species. Both social bees exhibited directionality of movement and had similar residence, in contrast to the random movement and shorter residence of the solitary bee. Tripping rate and net distance traveled differed among the three bee species. We ranked each behavior among bee species and used the relative ranking as gene flow predictor before testing the predictions against empirical gene flow data. Tripping rate and net distance traveled, but not residence, predicted relative gene dispersal among bee species. Linking specific behaviors to gene flow provides mechanisms to explain differences in gene flow among bee species and guides the development of management practices to reduce gene flow. Although developed in one system, the approach developed here can be generalized to different plant/pollinator systems.

Sebaea solaris (Gentianaceae), a new species from the Western cape of South Africa

Sebaea solaris (Gentianaceae) is here described as a new species from the Overberg region, Western Cape, South Africa. This new species is at first glance very distinct from all others in the genus mainly due to its relative large yellow flowers of c. 2.5 cm diameter with oblanceolate to obdeltoid erose corolla lobes. The petal ornamentation with several orange lines indicating the flower centre (versus two lines per petal for a few other Sebaea species) and a conspicuous undulated calyx wing are also unique in the genus. Furthermore, the position of large secondary stigmas above the middle of the style (versus at the base of the style for its morphologically closest relative: S. exacoides) possibly indicates differences in pollination strategies.

Quantitative representation of floral colors

AbstractHuman and insect pollinator perceived floral colors of 81 species of angiosperms (flowering plants) from Trivandrum (Kerala, India) was represented using the CIE 1976 L*a*b* color space and color hexagon, respectively. The floral color difference among human perceived red, yellow, and blue‐hued flowers and that of each flower from its respective pure hue was calculated using the CIE ΔE 2000 formula. Human perceived floral color difference values were consistently higher than 3.5, indicating the uniqueness of floral colors. Flowers perceived red and yellow by humans were dominant and of comparable proportions. Insect pollinators perceive most of the flowers as blue‐green. Quantitative representation of human and pollinator perceived floral colors would be invaluable to understand the information broadcasted by flowers. It can form the basis of flower grading in the floriculture industry and underpin objectivity in evolving the framework for national pollinator strategies.

Pollination by nectar-foraging thynnine wasps in the endangered Caladenia arenaria and Caladenia concolor (Orchidaceae)

Prior to undertaking conservation translocations of plants with specialised pollination systems, it is important to ensure the presence of pollinators at recipient sites. Here, for two threatened species, Caladenia concolor Fitzg. and Caladenia arenaria Fitzg. (Orchidaceae), we determine (i) the pollination strategy used, (ii) which floral visitors are involved in pollination, and (iii) whether the pollinator species are present at potential translocation sites. For both orchid species, pollination was primarily achieved by nectar-foraging thynnine wasps, with a single species responsible for pollination in C. concolor, whereas C. arenaria utilised at least two species to achieve pollination. Both orchid species secreted meagre quantities of sucrose on the upper surface of the labellum. Visits to C. concolor occurred primarily in the late afternoon, with some wasps perching on the flowers overnight. Surveys revealed that pollinators were present at all extant populations and most potential translocation sites for both orchids. The specialisation on one pollinator species in C. concolor means that the distribution of the pollinator needs to be considered for conservation translocations. With C. arenaria, the risk of hybridisation with other Caladenia that are known to share one of its pollinator species needs to be taken into account when selecting translocation sites.