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Featured researches published by Adam Shuttleworth.


Proceedings of the Royal Society of London. Series B, Biological Sciences | 2010

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

Adam Shuttleworth; Steven D. Johnson

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.


Ecology Letters | 2013

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

Andreas Jürgens; Suk Ling Wee; Adam Shuttleworth; Steven D. Johnson

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.


Annals of Botany | 2014

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

Timotheüs van der Niet; Michael D. Pirie; Adam Shuttleworth; Steven D. Johnson; Jeremy J. Midgley

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.


Annals of Botany | 2009

A key role for floral scent in a wasp-pollination system in Eucomis (Hyacinthaceae)

Adam Shuttleworth; Steven D. Johnson

BACKGROUND AND AIMS Floral scent may play a key role as a selective attractant in plants with specialized pollination systems, particularly in cases where floral morphology does not function as a filter of flower visitors. The pollination systems of two African Eucomis species (E. autumnalis and E. comosa) were investigated and a test was made of the importance of scent and visual cues as floral attractants. METHODS AND KEY RESULTS Visitor observations showed that E. autumnalis and E. comosa are visited primarily by pompilid wasps belonging to the genus Hemipepsis. These wasps carry considerably more Eucomis pollen and are more active on flowers than other visiting insects. Furthermore, experiments involving virgin flowers showed that these insects are capable of depositing pollen on the stigmas of E. autumnalis, and, in the case of E. comosa, pollen deposited during a single visit is sufficient to result in seed set. Experimental hand-pollinations showed that both species are genetically self-incompatible and thus reliant on pollinators for seed set. Choice experiments conducted in the field and laboratory with E. autumnalis demonstrated that pompilid wasps are attracted to flowers primarily by scent and not visual cues. Measurement of spectral reflectance by flower petals showed that flowers are cryptically coloured and are similar to the background vegetation. Analysis of headspace scent samples using coupled gas chromatography-mass spectrometry revealed that E. autumnalis and E. comosa scents are dominated by aromatic and monoterpene compounds. One hundred and four volatile compounds were identified in the floral scent of E. autumnalis and 83 in the floral scent of E. comosa, of which 57 were common to the scents of both species. CONCLUSIONS This study showed that E. autumnalis and E. comosa are specialized for pollination by pompilid wasps in the genus Hemipepsis and achieve specialization through cryptic colouring and the use of scent as a selective floral attractant.


International Journal of Plant Sciences | 2006

SPECIALIZED POLLINATION BY LARGE SPIDER-HUNTING WASPS AND SELF-INCOMPATIBILITY IN THE AFRICAN MILKWEED PACHYCARPUS ASPERIFOLIUS

Adam Shuttleworth; Steven D. Johnson

Specialized pollination systems in flowers with exposed nectar are difficult to explain because there are usually no morphological traits, such as long spurs, that could function to exclude particular flower visitors. Observations of the milkweed Pachycarpus asperifolius in KwaZulu‐Natal, South Africa, showed that its flowers are visited mainly by large spider‐hunting wasps belonging to the genus Hemipepsis (Hymenoptera: Pompilidae), despite producing copious amounts of nectar in an exposed position. Cage experiments showed that these wasps are effective in removing and depositing P. asperifolius pollinaria. Pollinaria become attached to the palps (and, to a lesser extent, the legs) of wasps. Palps are frequently broken, either when they become jammed in the guide rails or when pollinia are inserted. To try to understand why P. asperifolius flowers are visited almost exclusively by wasps, we presented droplets of nectar and control sugar solutions of the same concentration (ca. 70%) to honeybees (Apis mellifera scutellata). Honeybees readily consumed the sugar solutions but rejected P. asperifolius nectar, suggesting that secondary compounds in P. asperifolius nectar may deter insects other than pompilid wasps. Experimental hand pollinations conducted in the field showed that P. asperifolius is genetically self‐incompatible and thus completely reliant on pollinators for seed production. We conclude that P. asperifolius is specialized for pollination by large pompilid wasps and that its nectar functions as the primary filter of flower visitors.


Plant Systematics and Evolution | 2009

Specialized pollination in the African milkweed Xysmalobium orbiculare: a key role for floral scent in the attraction of spider-hunting wasps

Adam Shuttleworth; Steven D. Johnson

Specialized pollination by prey-hunting wasps is poorly documented in rewarding plants. Furthermore, the mechanisms of achieving specialization are not clear since flowers typically produce exposed nectar and have no morphological adaptations (such as long spurs) to exclude non-pollinating visitors. We investigated the pollination of Xysmalobium orbiculare and explored the functional roles of floral scent and nectar in attracting pollinators and deterring nectar robbers. Floral visitor observations showed that this milkweed is visited almost exclusively by pompilid wasps in the genus Hemipepsis. These wasps were the only insects to carry pollinia, and a cage experiment confirmed their effectiveness in removing and inserting pollinia on flowers. Hand-pollinations showed that plants are genetically self-incompatible and thus reliant on pollinators for seed set. Palatability experiments with honeybees showed that nectar is distasteful to non-pollinating insects and is therefore likely to play a functional role in deterring nectar thieves. Choice experiments in the field showed that the wasp pollinators are attracted primarily by floral scent rather than visual cues. Analysis of spectral reflectance of flowers revealed that flowers are dull colored and are unlikely to stand out from the background vegetation. We conclude that X. orbiculare is specialized for pollination by spider-hunting wasps in the genus Hemipepsis and utilizes floral scent to selectively attract its pollinators and unpalatable nectar to deter non-pollinating visitors.


Environmental Entomology | 2009

Palp-Faction: An African Milkweed Dismembers Its Wasp Pollinators

Adam Shuttleworth; Steven D. Johnson

ABSTRACT 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.


Annals of Botany | 2018

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

Jeff Ollerton; Sigrid Liede-Schumann; Mary E. Endress; Ulrich Meve; André Rodrigo Rech; Adam Shuttleworth; Héctor A. Keller; Mark Fishbein; Leonardo O. Alvarado-Cárdenas; Felipe W. Amorim; Peter Bernhardt; Ferhat Celep; Yolanda Chirango; Fidel Chiriboga-Arroyo; Laure Civeyrel; Andrea A. Cocucci; Louise Cranmer; Inara Carolina da Silva-Batista; Linde de Jager; Mariana Scaramussa Deprá; Arthur Domingos-Melo; Courtney Dvorsky; Kayna Agostini; Leandro Freitas; Maria Cristina Gaglianone; Leo Galetto; Mike Gilbert; Ixchel González-Ramírez; Pablo Gorostiague; David J. Goyder

Abstract 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.


Animal Behaviour | 2018

African elephants use plant odours to make foraging decisions across multiple spatial scales

Melissa H. Schmitt; Adam Shuttleworth; David Ward; Adrian M. Shrader

The National Research Foundation of South Africa (grant numbers: 90448, 90691, 97262, & 77582) and the Gay Langmuir Bursary from the University of KwaZulu-Natal, School of Life Sciences.


Functional Ecology | 2009

The importance of scent and nectar filters in a specialized wasp-pollination system.

Adam Shuttleworth; Steven D. Johnson

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Steven D. Johnson

University of KwaZulu-Natal

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Andreas Jürgens

University of KwaZulu-Natal

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Colleen T. Downs

University of KwaZulu-Natal

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Amy-Leigh Wilson

University of KwaZulu-Natal

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Adrian M. Shrader

University of KwaZulu-Natal

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David Ward

University of KwaZulu-Natal

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K. Govender

University of KwaZulu-Natal

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