'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.

Sexual deception of a beetle pollinator through floral mimicry.

Sexual mimicry is a complex multimodal strategy used by some plants to lure insects to flowers for pollination.1-4 It is notable for being highly species-specific and is typically mediated by volatiles belonging to a restricted set of chemical compound classes.3,4 Well-documented cases involve exploitation of bees and wasps (Hymenoptera)5,6 and flies (Diptera).7-9 Although beetles (Coleoptera) are the largest insect order and are well known as pollinators of both early and modern plants,10,11 it has been unclear whether they are sexually deceived by plants during flower visits.12,13 Here we report the discovery of an unambiguous case of sexual deception of a beetle: male longhorn beetles (Chorothyse hessei, Cerambycidae) pollinate the elaborate insectiform flowers of a rare southern African orchid (Disa forficaria), while exhibiting copulatory behavior including biting the antennae-like petals, curving the abdomen into the hairy lip cleft, and ejaculating sperm. The beetles are strongly attracted by (16S,9Z)-16-ethyl hexadec-9-enolide, a novel macrolide that we isolated from the floral scent. Structure-activity studies14,15 confirmed that chirality and other aspects of the structural geometry of the macrolide are critical for the attraction of the male beetles. These results demonstrate a new biological function for plant macrolides and confirm that beetles can be exploited through sexual deception to serve as pollinators.

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.

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.

Survey-based pilot study into the chosen therapy and prophylaxis used by UK primary care veterinary surgeons against canine angiostrongylosis.

Canine Angiostrongylosis (CA), a gastropod-borne parasitic infection caused by the metastrongyloid nematode Angiostrongylus vasorum, is an important cause of significant morbidity to domestic dogs across the UK as well as in other European countries. This study aimed to ascertain the frequency at which particular drugs were used by primary care practitioners in the UK for therapy against and prophylaxis for CA. Primary care veterinary clinicians were surveyed using an online questionnaire and face-to-face or telephone interviews. Eighty-six veterinary surgeons responded. The majority of practices (n = 52) included lungworm in their standard anthelmintic protocols; moxidectin was the most common drug used for prophylaxis (n = 71). Fenbendazole was the most frequently selected drug, by 45% of vets, for treatment of confirmed cases of CA despite it being unlicensed for this purpose in the UK and the absence of a clear treatment protocol. The results of this pilot study provide an initial insight into the approach taken by primary care practitioners in their approach to CA. This provides an important starting point for future studies investigating the decision-making for CA amongst UK veterinary surgeons, particularly to clarify whether in a larger cohort an unlicensed drug remains the treatment of choice. The absence of a clear protocol for fenbendazole means that treatment of dogs affected by CA may be suboptimal, increasing the risk of morbidity and mortality.

Do pollinator distributions underlie the evolution of pollination ecotypes in the Cape shrub Erica plukenetii?

BACKGROUND AND AIMS: According to the Grant-Stebbins model of pollinator-driven divergence, plants that disperse beyond the range of their specialized pollinator may adapt to a new pollination system. Although this model provides a compelling explanation for pollination ecotype formation, few studies have directly tested its validity in nature. Here we investigate the distribution and pollination biology of several subspecies of the shrub Erica plukenetii from the Cape Floristic Region in South Africa. We analyse these data in a phylogenetic context and combine these results with information on pollinator ranges to test whether the evolution of pollination ecotypes is consistent with the Grant-Stebbins model. METHODS AND KEY RESULTS: Pollinator observations showed that the most common form of E. plukenetii with intermediate corolla length is pollinated by short-billed Orange-breasted sunbirds. Populations at the northern fringe of the distribution are characterized by long corollas, and are mainly pollinated by long-billed Malachite sunbirds. A population with short corollas in the centre of the range was mainly pollinated by insects, particularly short-tongued noctuid moths. Bird exclusion in this population did not have an effect on fruit set, while insect exclusion reduced fruit set. An analysis of floral scent across the range, using coupled gas chromatography-mass spectrometry, showed that the scent bouquets of flowers from moth-pollinated populations are characterized by a larger number of scent compounds and higher emission rates than those in bird-pollinated populations. This was also reflected in clear separation of moth- and bird-pollinated populations in a two-dimensional phenotype space based on non-metric multidimensional scaling analysis of scent data. Phylogenetic analyses of chloroplast and nuclear DNA sequences strongly supported monophyly of E. plukenetii, but not of all the subspecies. Reconstruction of ancestral character states suggests two shifts from traits associated with short-billed Orange-breasted sunbird pollination: one towards traits associated with moth pollination, and one towards traits associated with pollination by long-billed Malachite sunbirds. The latter shift coincided with the colonization of Namaqualand in which Orange-breasted sunbirds are absent. CONCLUSIONS: Erica plukenetii is characterized by three pollination ecotypes, but only the evolutionary transition from short- to long-billed sunbird pollination can be clearly explained by the Grant-Stebbins model. Corolla length is a key character for both ecotype transitions, while floral scent emission was important for the transition from bird to moth pollination.

Chemical mimicry of insect oviposition sites: a global analysis of convergence in angiosperms.

Floral mimicry of decaying plant or animal material has evolved in many plant lineages and exploits, for the purpose of pollination, insects seeking oviposition sites. Existing studies suggest that volatile signals play a particularly important role in these mimicry systems. Here, we present the first large-scale phylogenetically informed study of patterns of evolution in the volatile emissions of plants that mimic insect oviposition sites. Multivariate analyses showed strong convergent evolution, represented by distinct clusters in chemical phenotype space of plants that mimic animal carrion, decaying plant material, herbivore dung and omnivore/carnivore faeces respectively. These plants deploy universal infochemicals that serve as indicators for the main nutrients utilised by saprophagous, coprophagous and necrophagous insects. The emission of oligosulphide-dominated volatile blends very similar to those emitted by carrion has evolved independently in at least five plant families (Annonaceae, Apocynaceae, Araceae, Orchidaceae and Rafflesiaceae) and characterises plants associated mainly with pollination by necrophagous flies and beetles.

The missing stink: sulphur compounds can mediate a shift between fly and wasp pollination systems.

The radiation of the angiosperms is often attributed to repeated evolutionary shifts between different pollinators, as this process drives diversification of floral forms and can lead to reproductive isolation. Floral scent is an important functional trait in many pollination systems but has seldom been implicated as a key mechanism in pollinator transitions. In this study, we suggest a role for sulphur compounds in mediating a shift between specialized carrion-fly and pompilid-wasp pollination systems in Eucomis (Hyacinthaceae). Flowers of closely related Eucomis species pollinated by carrion flies or pompilid wasps have very similar greenish-white flowers, but differ markedly in floral scent chemistry (determined by GC-MS analysis of headspace extracts). Comparison of the floral colours of the four Eucomis species in the visual systems of flies and wasps suggests that colour plays little role in pollinator discrimination. Nectar properties and morphology also do not differ strongly between fly- and wasp-pollinated flowers. By comparing floral scent bouquets and experimentally manipulating the scent of plants in the field, we demonstrate that shifts between wasp and fly pollination in these four congeners can depend on the production or suppression of sulphur compounds (dimethyl disulphide and dimethyl trisulphide) in the fragrance bouquet. This suggests that mutations affecting the production of particular scent compounds could precipitate shifts between pollinators, independently of floral morphology, colour or nectar properties.

Palp-faction: an African milkweed dismembers its wasp pollinators.

Interactions between pollinators and nectar-producing flowers are usually assumed to be mutualistic, but the exploitative basis of these relationships can lead to antagonistic interactions. Flowers of the African milkweed, Pachycarpus appendiculatus E. Mey, produce concentrated nectar that is consumed primarily by the large spider-hunting wasp Hemipepsis dedjas Guerin (Hymenoptera: Pompilidae). Pollinaria of this milkweed become attached to the palps of these wasps during nectar feeding. Broken wasp palps were found between guide rails, attached to corpuscula that were trapped behind the guide rails, and attached to pollinia that were inserted into the stigmatic chambers of the flowers. Approximately 85% of wasps captured on flowers of P. appendiculatus were missing one or more palps, whereas only 9% of wasps captured on flowers of another asclepiad species were missing any palps. It thus seems that wasps face a high risk of losing their palps when foraging on these flowers. The interaction may thus be antagonistic for the wasps if the cost of losing their sensory palps (not yet established) is greater than the benefits of the nectar reward. The plants, however, gain clear benefit from the interaction, as verified by the removal and insertion of pollinia in flowers exposed solely to visits by pompilid wasps.