On the success of a swindle: pollination by deception in orchids

A standing enigma in pollination ecology is the evolution of pollinator attraction without offering reward in about one third of all orchid species. Here I review concepts of pollination by deception, and in particular recent findings in the pollination syndromes of food deception and sexual deception in orchids. Deceptive orchids mimic floral signals of rewarding plants (food deception) or mating signals of receptive females (sexual deception) to attract pollen vectors. In some food deceptive orchids, similarities in the spectral reflectance visible to the pollinator in a model plant and its mimic, and increased reproductive success of the mimic in the presence of the model have been demonstrated. Other species do not mimic specific model plants but attract pollinators with general attractive floral signals. In sexually deceptive orchids, floral odor is the key trait for pollinator attraction, and behaviorally active compounds in the orchids are identical to the sex pheromone of the pollinator species. Deceptive orchids often show high variability in floral signals, which may be maintained by negative frequency-dependent selection, since pollinators can learn and subsequently avoid common deceptive morphs more quickly than rare ones. The evolution of obligate deception in orchids seems paradoxical in the light of the typically lower fruit set than in rewarding species. Pollination by deception, however, can reduce self-pollination and encourage pollen flow over longer distances, thus promoting outbreeding. Although some food deceptive orchids are isolated through postzygotic reproductive barriers, sexually deceptive orchids lack post-mating barriers and species isolation is achieved via specific pollinator attraction. Recent population genetic and phylogenetic investigations suggest gene-flow within subgeneric clades, but pollinator-mediated selection may maintain species-specific floral traits.     

Pollination syndromes ignored: importance of non-ornithophilous flowers to Neotropical savanna hummingbirds

Generalization prevails in flower–animal interactions, and although animal visitors are not equally effective pollinators, most interactions likely represent an important energy intake for the animal visitor. Hummingbirds are nectar-feeding specialists, and many tropical plants are specialized toward hummingbird-pollination. In spite of this, especially in dry and seasonal tropical habitats, hummingbirds may often rely on non-ornithophilous plants to meet their energy requirements. However, quantitative studies evaluating the relative importance of ornithophilous vs. non-ornithophilous plants for hummingbirds in these areas are scarce. We here studied the availability and use of floral resources by hummingbirds in two different areas of the Cerrado, the seasonal savannas in Central Brazil. Roughly half the hummingbird visited plant species were non-ornithophilous, and these contributed greatly to increase the overall nectar availability. We showed that mean nectar offer, at the transect scale, was the only parameter related to hummingbird visitation frequency, more so than nectar offer at single flowers and at the plant scale, or pollination syndrome. Centrality indices, calculated using hummingbird–plant networks, showed that ornithophilous and non-ornithophilous plants have similar importance for network cohesion. How this foraging behaviour affects reproduction of non-ornithophilous plants remains largely unexplored and is probably case specific, however, we suggest that the additional energy provided by non-ornithophilous plants may facilitate reproduction of truly ornithophilous flowers by attracting and maintaining hummingbirds in the area. This may promote asymmetric hummingbird–plant associations, i.e., pollination depends on floral traits adapted to hummingbird morphology, but hummingbird visitation is determined more by the energetic "reward" than by pollination syndromes.     

Bird pollination of Canary Island endemic plants

The Canary Islands are home to a guild of endemic, threatened bird-pollinated plants. Previous work has suggested that these plants evolved floral traits as adaptations to pollination by flower specialist sunbirds, but subsequently, they appear to have co-opted generalist passerine birds as sub-optimal pollinators. To test this idea, we carried out a quantitative study of the pollination biology of three of the bird-pollinated plants, Canarina canariensis (Campanulaceae), Isoplexis canariensis (Veronicaceae) and Lotus berthelotii (Fabaceae), on the island of Tenerife. Using colour vision models, we predicted the detectability of flowers to bird and bee pollinators. We measured pollinator visitation rates, nectar standing crops as well as seed-set and pollen removal and deposition. These data showed that the plants are effectively pollinated by non-flower specialist passerine birds that only occasionally visit flowers. The large nectar standing crops and extended flower longevities (>10 days) of Canarina and Isoplexis suggests that they have evolved a bird pollination system that effectively exploits these low frequency non-specialist pollen vectors and is in no way sub-optimal. Seed set in two of the three species was high and was significantly reduced or zero in flowers where pollinator access was restricted. In L. berthelotii, however, no fruit set was observed, probably because the plants were self-incompatible horticultural clones of a single genet. We also show that, while all three species are easily detectable for birds, the orange Canarina and the red Lotus (but less so the yellow-orange Isoplexis) should be difficult to detect for insect pollinators without specialised red receptors, such as bumblebees. Contrary to expectations if we accept that the flowers are primarily adapted to sunbird pollination, the chiffchaff (Phylloscopus canariensis) was an effective pollinator of these species.     

A novel mutualism between an ant-plant and its resident pollinator

Pollination systems in which the host plant provides breeding sites for pollinators, invariably within flowers, are usually highly specialized mutualisms. We found that the pollinating bee Braunsapis puangensis breeds within the caulinary domatia of the semi-myrmecophyte Humboldtia brunonis (Fabaceae), an unusual ant-plant that is polymorphic for the presence of domatia and harbours a diverse invertebrate fauna including protective and non-protective ants in its domatia. B. puangensis is the most common flower visitor that carries the highest proportion of H. brunonis pollen. This myrmecophyte is pollen limited and cross-pollinated by bees in the daytime. Hence, the symbiotic pollinator could provide a benefit to trees bearing domatia by alleviating this limitation. We therefore report for the first time an unspecialised mutualism in which a pollinator is housed in a plant structure other than flowers. Here, the cost to the plant is lower than for conventional brood-site pollination mutualisms where the pollinator develops at the expense of plant reproductive structures. Myrmecophytes housing resident pollinators are unusual, as ants are known to be enemies of pollinators, and housing them together may decrease the benefits that these residents could individually provide to the host plant.     

A novel role for proline in plant floral nectars

Plants offer metabolically rich floral nectar to attract visiting pollinators. The composition of nectar includes not only sugars, but also amino acids. We have examined the amino acid content of the nectar of ornamental tobacco and found that it is extremely rich (2 mM) in proline. Because insect pollinators preferentially utilize proline during the initial phases of insect flight and can reportedly taste proline, we determined whether honeybees showed a preference for synthetic nectars rich in proline. We therefore established an insect preference test and found that honeybees indeed prefer nectars rich in the amino acid proline. To determine whether this was a general phenomenon, we also examined the nectars of two insect-pollinated wild perennial species of soybean. These species also showed high levels of proline in their nectars demonstrating that plants often produce proline-rich floral nectar. Because insects such as honeybees prefer proline-rich nectars, we hypothesize that some plants offer proline-rich nectars as a mechanism to attract visiting pollinators.     

A weevil pollinating the Canary Islands date palm: between parasitism and mutualism

Palm pollination systems are highly diverse, including by wind and by several different groups of insects. Many palm species are associated with more or less specific pollinating weevils that are also floral herbivores. For many such palms, the importance of these "palm flower weevils" as pollinators has not been examined. Here we describe a new ex situ method of demonstrating insect pollination when pollinator exclusion is not possible. We show that Neoderelomus piriformis beetles carry pollen and deposit it on the stigma of Phoenix canariensis. Up until now, pollination systems in Phoenix have been unclear, despite the economic importance of the date palm P. dactylifera. We demonstrate here that small weevils that visit inflorescences and often inconspicuously hide there could be efficient pollinators.     

Why do <Emphasis Type="Italic">Manduca sexta</Emphasis> feed from white flowers? Innate and learnt colour preferences in a hawkmoth

Flower colour is an important signal used by flowering plants to attract pollinators. Many anthophilous insects have an innate colour preference that is displayed during their first foraging bouts and which could help them locate their first nectar reward. Nevertheless, learning capabilities allow insects to switch their colour preferences with experience and thus, to track variation in floral nectar availability. Manduca sexta, a crepuscular hawkmoth widely studied as a model system for sensory physiology and behaviour, visits mostly white, night-blooming flowers lacking UV reflectance throughout its range in the Americas. Nevertheless, the spectral sensitivity of the feeding behaviour of naïve moths shows a narrow peak around 450 nm wavelengths, suggesting an innate preference for the colour blue. Under more natural conditions (i.e. broader wavelength reflectance) than in previous studies, we used dual choice experiments with blue- and white-coloured feeders to investigate the innate preference of naïve moths and trained different groups to each colour to evaluate their learning capabilities. We confirmed the innate preference of M. sexta for blue and found that these moths were able to switch colour preferences after training experience. These results unequivocally demonstrate that M. sexta moths innately prefer blue when presented against white flower models and offer novel experimental evidence supporting the hypothesis that learning capabilities could be involved in their foraging preferences, including their widely observed attraction to white flowers in nature.     

Indirect interactions between invasive and native plants via pollinators

In generalised pollination systems, the presence of alien plant species may change the foraging behaviour of pollinators on native plant species, which could result in reduced reproductive success of native plant species. We tested this idea of indirect interactions on a small spatial and temporal scale in a field study in Mauritius, where the invasive strawberry guava, Psidium cattleianum, provides additional floral resources for insect pollinators. We predicted that the presence of flowering guava would indirectly and negatively affect the reproductive success of the endemic plant Bertiera zaluzania, which has similar flowers, by diverting shared pollinators. We removed P. cattleianum flowers within a 5-m radius from around half the B. zaluzania target plants (treatment) and left P. cattleianum flowers intact around the other half (control). By far, the most abundant and shared pollinator was the introduced honey bee, Apis mellifera, but its visitation rates to treatment and control plants were similar. Likewise, fruit and seed set and fruit size and weight of B. zaluzania were not influenced by the presence of P. cattleianum flowers. Although other studies have shown small-scale effects of alien plant species on neighbouring natives, we found no evidence for such negative indirect interactions in our system. The dominance of introduced, established A. mellifera indicates their replacement of native insect flower visitors and their function as pollinators of native plant species. However, the pollination effectiveness of A. mellifera in comparison to native pollinators is unknown. Christine B. Müller, deceased 7 March 2008.     

Sex-specific effects of parasites on telomere dynamics in a short-lived passerine—the blue tit

The pollination syndrome concept implies that flowers evolved with particular sets of characteristics, such as colors, shapes, orientations, and rewards, as a means of attracting pollinators. However, these traits may have also evolved to deter unwanted visitors. The North American genus Penstemon exhibits a great floral diversity that is mainly associated with bumblebee and hummingbird pollination. Evolutionary shifts from insect pollination to hummingbird pollination have occurred in Penstemon repeatedly, but some species maintain mixed-pollination systems and intermediate floral traits between bee- and hummingbird-pollination modes. The apparently intermediate floral traits of species with mixed-pollination systems might be potentially acting to deter bumblebee foragers. Then, bird-flower traits might be selected with increased hummingbird visitation over evolutionary time might, resulting in specialization to and the evolution of floral traits present in hummingbird-pollinated species. Here, we modified bee-pollination floral traits in Penstemon gentianoides with a mixed pollination system, to resemble hummingbird-pollination traits, and measured the effects of trait modification on bumblebee foraging behavior and plant female reproductive fitness. Our results showed that reduction in the width of the corolla tube and the absence of the corolla lip negatively affects bumblebee visitation and their efficiency as pollinators, and that the synergistic interaction of both traits enhanced the “anti-bee” effect. We conclude that acquisition of floral traits that resemble those of hummingbird-pollination enables Penstemon plant species to deter bumblebee visits.

     

Flower-visiting behavior of male bees is triggered by nectar-feeding insects

Bees are important pollinators for many flowering plants. Female bees are thought to be more effective pollinators than male bees because they carry much more pollen than males. Males of some solitary bee species are known to patrol near flowers that females visit. Because patrolling males visit flowers to mate or defend their territories, they may function as pollinators. However, the significance of patrolling males to pollination has not been studied. We studied males of a solitary bee, Heriades fulvohispidus (Megachilidae), patrolling near flowers and visiting flowers that attracted nectar-feeding insects, including conspecifics, on the Ogasawara (Bonin) Islands. To test the hypothesis that patrolling male bees may function as pollen vectors, we compared the frequency of visits by H. fulvohispidus to flowers of an endemic plant, Schima mertensiana (Theaceae); comparisons were made among flowers with a dead H. fulvohispidus, a dead beetle, a piece of plastic, and nothing (control flowers). Patrolling H. fulvohispidus more frequently visited flowers with a dead conspecific, a dead beetle, or a piece of plastic than the control flowers. Our experiment demonstrates that nectar-feeding insects (including conspecifics and other insects) enhance the flower-visiting frequency of patrolling H. fulvohispidus males on S. mertensiana flowers. Furthermore, we observed S. mertensiana pollen on patrolling males as well as females, suggesting that male bees may also function as pollen vectors.     

Highly modular pattern in ant-plant interactions involving specialized and non-specialized myrmecophytes

Because Tachia guianensis (Gentianaceae) is a “non-specialized myrmecophyte” associated with 37 ant species, we aimed to determine if its presence alters the ant guild associated with sympatric “specialized myrmecophytes” (i.e., plants sheltering a few ant species in hollow structures). The study was conducted in a hilly zone of a neotropical rainforest where two specialized myrmecophytes grow at the bottom of the slopes, another at mid-slope, and a fourth on the hilltops. Tachia guianensis, which occurred everywhere, had its own guild of associated ant species. A network analysis showed that its connections with the four other myrmecophytes were rare and weak, the whole resulting in a highly modular pattern of interactions with one module (i.e., subnetwork) per myrmecophyte. Three ant species parasitized three out of the four specialized myrmecophytes (low nestedness noted), but were not or barely associated with T. guianensis that therefore did not influence the parasitism of specialized myrmecophytes.     

Large pollen loads of a South African asclepiad do not interfere with the foraging behaviour or efficiency of pollinating honey bees

The pollen of asclepiads (Asclepiadoideae, Apocynaceae) and most orchids (Orchidaceae) are packaged as large aggregations known as pollinaria that are removed as entire units by pollinators. In some instances, individual pollinators may accumulate large loads of these pollinaria. We found that the primary pollinator of Cynanchum ellipticum (Apocynaceae—Asclepiadoideae), the honey bee Apis mellifera, accumulate very large agglomerations of pollinaria on their mouthparts when foraging on this species. We tested whether large pollinarium loads negatively affected the foraging behaviour and foraging efficiency of honey bees by slowing foraging speeds or causing honey bees to visit fewer flowers, and found no evidence to suggest that large pollinarium loads altered foraging behaviour. C. ellipticum displayed consistently high levels of pollination success and pollen transfer efficiency (PTE). This may be a consequence of efficiently loading large numbers of pollinaria onto pollinators even when primary points of attachment on pollinators are already occupied and doing so in a manner that does not impact the foraging behaviour of pollinating insects.     

Multicomponent floral signals elicit selective foraging in bumblebees

Flower constancy, or the tendency of individual pollinators to visit sequentially a single flower type even when other equally rewarding types are available, has important implications for animal-pollinated plants. Yet, the proximal reason for the behaviour still remains poorly understood. Here I show that bumblebees visiting equally rewarding flowers that differ in size and odour are more flower constant and less efficient (visited fewer flowers per minute) than bees visiting flowers that differ in size only and odour only. These results are consistent with the view that flower constancy in pollinators is related to their inability to perceive, process or recall multicomponent floral signals. I discuss these findings in the context of pollinator behavioural mechanisms and the evolution of floral diversity.     

More than euglossines: the diverse pollinators and floral scents of Zygopetalinae orchids

Floral volatile organic compounds (VOCs) play important roles in plant-pollinator interactions. We investigated the reproductive ecology and floral VOCs of Zygopetalinae orchids to understand the relationship between floral scents and pollinators. We performed focal observations, phenological censuses and breeding system experiments in eight species in southeast Brazil. Floral scents were collected and analysed using SPME/GC-MS. We performed multivariate analyses to group species according to affinities of their VOCs and define compounds associated to each plant. Dichaea cogniauxiana was pollinated by weevils which use their developing ovules, while D. pendula was pollinated by the same weevils and perfume-collecting male euglossine bees. The other species were deceit-pollinated by bees. Zygopetalum crinitum was pollinated by carpenter bees, while W. warreana, Z. mackayi and Z. maxillare were bumblebee-pollinated. The latter was also pollinated by Centris confusa. Breeding system varied widely with no association to any pollinator group. Most VOCs are common to other floral scents. Zygopetalum crinitum presented an exclusive blend of VOCs, mainly composed of benzenoids. The scents of Pabstia jugosa, Promenaea xanthina and the Zygopetalum spp. were similar. The bumblebee-pollinated species have flowering periods partially overlapped, thus neither phenology nor pollinators constitute hybridization barriers among these species. Euglossines are not the only pollinators of Zygopetalinae. Different VOCs, size and lifespan of flowers are associated with distinct pollinators. A distinctive VOC bouquet may determine specialisation in carpenter bees or male euglossines within bee-pollinated flowers. Finally, visitation of deceit-pollinated flowers by perfume-collecting euglossines allows us to hypothesise how pollination by this group of bees had evolved.     

Floral colour change in <Emphasis Type="Italic">Byrsonima variabilis</Emphasis> (Malpighiaceae) as a visual cue for pollen but not oil foraging by oil-collecting bees

Pollinators search for multiple flora resources throughout their life cycle. Most studies, however, only assess how bees discriminate floral cues in the context of nectar foraging. In the present study, we sought to elucidate whether oil-collecting bees discriminate flowers of Byrsonima variabilis (Malpighiaceae) with petals of different colours when foraging for pollen or oil. As the colour of the standard petal changes during anthesis, we characterised the spectral reflectance patterns of flowers throughout anthesis and modelled chromatic perceptual space to determine how these colour patterns are perceived by bees. Through the quantification of flower pollen in the different phases, we found that the colour of the standard petal is an honest cue of the presence of pollen. Centridine bees preferentially visited flowers with a yellow (bee’s green) colour when searching for pollen, but indiscriminately visited flowers with different petal colours when searching for floral oil. We suggest that standard petals, in the species studied and others of the genus, like nectar guides, act as pollen guides, which oil-collecting females use to detect pollen-rich flowers. Moreover, they use different floral clues during foraging for different resources in the same host plant.     

Nectar production dynamics and sugar composition in two <Emphasis Type="Italic">Mucuna</Emphasis> species (Leguminosae,Faboideae) with different specialized pollinators

Nectar is secreted in particular rhythms throughout the lifespan of a flower, which allows determining the nectar production dynamics. This paper compares nectar features in Mucuna japira and Mucuna urens describing: dynamics of nectar production, floral response to nectar removal, resorption, nectar sugar composition, and variation in nectar sugar composition. M. japira inflorescence bears 12–21 yellow flowers, which are in anthesis for 7 days, whereas M. urens inflorescence bears 36–54 greenish flowers, but only 1–3 flowers are in anthesis simultaneously that last one night. Nectar volume and sugar concentration were measured, and the amount of sugar was estimated. Qualitative and quantitative nectar sugar composition was determined. Both species had a constant nectar sugar concentration (ca. 10% for M. japira and ca. 16% for M. urens) and secreted high volumes of nectar (ca. 340 μl per flower for M. japira and 310 μl per flower for M. urens), during 5 days for M. japira and 6 h for M. urens, but after the first removal, i.e., when flower opening mechanism is triggered, nectar production stops immediately. Nectar resorption occurred in both species. Nectar sugar composition showed some similarities between the species. Variation in nectar sugar composition occurred in both species. The Mucuna species are dependent on their pollinators to produce fruits and seeds, and they have different strategies to promote the necessary interaction with birds or bats, especially related to nectar and flower characteristics.     

Colour mimicry and sexual deception by Tongue orchids (Cryptostylis)

Typically, floral colour attracts pollinators by advertising rewards such as nectar, but how does colour function when pollinators are deceived, unrewarded, and may even suffer fitness costs? Sexually deceptive orchids are pollinated only by male insects fooled into mating with orchid flowers and inadvertently transferring orchid pollinia. Over long distances, sexually deceptive orchids lure pollinators with counterfeit insect sex pheromones, but close-range deception with colour mimicry is a tantalising possibility. Here, for the first time, we analyse the colours of four sexually deceptive Cryptostylis orchid species and the female wasp they mimic (Lissopimpla excelsa, Ichneumonidae), from the perspective of the orchids’ single, shared pollinator, male Lissopimpla excelsa. Despite appearing different to humans, the colours of the orchids and female wasps were effectively identical when mapped into a hymenopteran hexagonal colour space. The orchids and wasps reflected predominantly red-orange wavelengths, but UV was also reflected by raised bumps on two orchid species and by female wasp wings. The orchids’ bright yellow pollinia contrasted significantly with their overall red colour. Orchid deception may therefore involve accurate and species-specific mimicry of wavelengths reflected by female wasps, and potentially, exploitation of insects’ innate attraction to UV and yellow wavelengths. In general, mimicry may be facilitated by exploiting visual vulnerabilities and evolve more readily at the peripheries of sensory perception. Many sexually deceptive orchids are predominantly red, green or white: colours that are all potentially difficult for hymenoptera to detect or distinguish from the background.     

Degeneration of sperm reservoir and the loss of mating ability in worker ants

Workers never mate in the large majority of ants, and they have usually lost the spermatheca, an organ specialized for long-term storage of sperm. Such ‘non-sexual’ workers are restricted to laying unfertilized eggs that give rise to males, and they cannot compete with the queens for the production of female offspring. In sharp contrast, workers in 200–300 species from phylogenetically basal subfamilies can reproduce sexually (‘gamergates’) because they retain a functional spermatheca like the queens. Importantly, ‘non-sexual’ workers in closely related species have a vestigial spermatheca. In this study, we compared the reservoir epithelium of ‘sexual’ workers to that of congeneric queens and ‘non-sexual’ workers using 21 species of Amblyoponinae, Ponerinae and Ectatomminae. We show that a pronounced thickening of the epithelium near the opening of the sperm duct is strictly associated with sexual reproduction in both castes. This is unlike ‘non-sexual’ workers in which this epithelium is always very thin, with few organelles; but all other structures remain intact. We discuss this evolutionary degeneration of the spermatheca and how it relates to behavioural or physiological modifications linked to mating. Our results help understand the loss of sexual reproduction by ant workers, a critical step in the extreme specialization of their phenotype.     

Effects of life-history traits on parasitism in a monogamous mammal, the eastern rock sengi (Elephantulus myurus)

The distribution of parasites is often characterised by substantial aggregation with a small proportion of hosts harbouring the majority of parasites. This pattern can be generated by abiotic and biotic factors that affect hosts and determine host exposure and susceptibility to parasites. Climate factors can change a host’s investment in life-history traits (e.g. growth, reproduction) generating temporal patterns of parasite aggregation. Similarly, host age may affect such investment. Furthermore, sex-biased parasitism is common among vertebrates and has been linked to sexual dimorphism in morphology, behaviour and physiology. Studies exploring sex-biased parasitism have been almost exclusively conducted on polygynous species where dimorphic traits are often correlated. We investigated the effects of season and life-history traits on tick loads of the monogamous eastern rock sengi (Elephantulus myurus). We found larger tick burdens during the non-breeding season possibly as a result of energetic constraints and/or climate effects on the tick. Reproductive investment resulted in increased larval abundance for females but not males and may be linked to sex-specific life-history strategies. The costs of reproduction could also explain the observed age effect with yearling individuals harbouring lower larval burdens than adults. Although adult males had the greatest larval tick loads, host sex appears to play a minor role in generating the observed parasite heterogeneities. Our study suggests that reproductive investment plays a major role for parasite patterns in the study species.     

Cells of the connective tissue differentiate and migrate into pollen sacs

In angiosperms, archesporial cells in the anther primordium undergo meiosis to form haploid pollen, the sole occupants of anther sacs. Anther sacs are held together by a matrix of parenchyma cells, the connective tissue. Cells of the connective tissue are not known to differentiate. We report the differentiation of parenchyma cells in the connective tissue of two Gordonia species into pollen-like structures (described as pseudopollen), which migrate into the anther sacs before dehiscence. Pollen and pseudopollen were distinguishable by morphology and staining. Pollen were tricolpate to spherical while pseudopollen were less rigid and transparent with a ribbed surface. Both types were different in size, shape, staining and surface architecture. The ratio of the number of pseudopollen to pollen was 1:3. During ontogeny in the connective tissue, neither cell division nor tetrad formation was observed and hence pseudopollen were presumed to be diploid. Only normal pollen germinated on a germination medium. Fixed preparations in time seemed to indicate that pseudopollen migrate from the connective tissue into the anther sac.