Sarah E. J. Arnold

Angiosperm wood structure: Global patterns in vessel anatomy and their relation to wood density and potential conductivity

Woody stems comprise a large biological carbon fraction and determine water transport between roots and leaves; their structure and function can influence both carbon and hydrological cycles. While angiosperm wood anatomy and density determine hydraulic conductivity and mechanical strength, little is known about interrelations across many species. We compiled a global data set comprising two anatomical traits for 3005 woody angiosperms: mean vessel lumen area (Ā) and number per unit area (N). From these, we calculated vessel lumen fraction (F = ĀN) and size to number ratio (S = Ā/N), a new vessel composition index. We examined the extent to which F and S influenced potential sapwood specific stem conductivity (K(S)) and wood density (D; dry mass/fresh volume). F and S varied essentially independently across angiosperms. Variation in K(S) was driven primarily by S, and variation in D was virtually unrelated to F and S. Tissue density outside vessel lumens (D(N)) must predominantly influence D. High S should confer faster K(S) but incur greater freeze-thaw embolism risk. F should also affect K(S), and both F and D(N) should influence mechanical strength, capacitance, and construction costs. Improved theory and quantification are needed to better understand ecological costs and benefits of these three distinct dimensions.

Mutations perturbing petal cell shape and anthocyanin synthesis influence bumblebee perception of Antirrhinum majus flower colour

We wished to understand the effects on pollinator behaviour of single mutations in plant genes controlling flower appearance. To this end, we analysed snapdragon flowers (Antirrhinum majus), including the mixta and nivea mutants, in controlled laboratory conditions using psychophysical tests with bumblebees. The MIXTA locus controls petal epidermal cell shape, and thus the path that incident light takes within the pigment-containing cells. The effect is that mixta mutant flowers are pink in comparison to the wild type purple flowers, and mutants lack the sparkling sheen of wild type flowers that is clearly visible to human observers. Despite their fundamentally different appearance to humans, and even though bees could discriminate the flowers, inexperienced bees exhibited no preference for either type, and the flowers did not differ in their detectability in a Y-maze—either when the flowers appeared in front of a homogeneous or a dappled background. Equally counterintuitive effects were found for the non-pigmented, UV reflecting nivea mutant: even though the overall reflectance intensity and UV signal of nivea flowers is several times that of wild type flowers, their detectability was significantly reduced relative to wild type flowers. In addition, naïve foragers preferred wild type flowers over nivea mutants, even though these generated a stronger signal in all receptor types. Our results show that single mutations affecting flower signal can have profound effects on pollinator behaviour—but not in ways predictable by crude assessments via human perception, nor simple quantification of UV signals. However, current models of bee visual perception predict the observed effects very well.

Flower colours along an alpine altitude gradient, seen through the eyes of fly and bee pollinators

Alpine flowers face multiple challenges in terms of abiotic and biotic factors, some of which may result in selection for certain colours at increasing altitude, in particular the changing pollinator species composition, which tends to move from bee-dominated at lower elevations to fly-dominated in high-alpine regions. To evaluate whether growing at altitude—and the associated change in the dominant pollinator groups present—has an effect on the colour of flowers, we analysed data collected from the Dovrefjell National Park in Norway. Unlike previous studies, however, we considered the flower colours according to ecologically relevant models of bee and fly colour vision and also their physical spectral properties independently of any colour vision system, rather than merely looking at human colour categories. The shift from bee to fly pollination with elevation might, according to the pollination syndrome hypothesis, lead to the prediction that flower colours should shift from more bee-blue and UV-blue flowers (blue/violet to humans, i.e. colours traditionally associated with large bee pollinators) at low elevations to more bee-blue-green and green (yellow and white to humans—colours often linked to fly pollination) flowers at higher altitude. However, although there was a slight increase in bee-blue-green flowers and a decrease in bee-blue flowers with increasing elevation, there were no statistically significant effects of altitude on flower colour as seen either by bees or by flies. Although flower colour is known to be constrained by evolutionary history, in this sample we also did not find evidence that phylogeny and elevation interact to determine flower colours in alpine areas.

FReD: The Floral Reflectance Database — A Web Portal for Analyses of Flower Colour

Background Flower colour is of great importance in various fields relating to floral biology and pollinator behaviour. However, subjective human judgements of flower colour may be inaccurate and are irrelevant to the ecology and vision of the flowers pollinators. For precise, detailed information about the colours of flowers, a full reflectance spectrum for the flower of interest should be used rather than relying on such human assessments. Methodology/Principal Findings The Floral Reflectance Database (FReD) has been developed to make an extensive collection of such data available to researchers. It is freely available at http://www.reflectance.co.uk. The database allows users to download spectral reflectance data for flower species collected from all over the world. These could, for example, be used in modelling interactions between pollinator vision and plant signals, or analyses of flower colours in various habitats. The database contains functions for calculating flower colour loci according to widely-used models of bee colour space, reflectance graphs of the spectra and an option to search for flowers with similar colours in bee colour space. Conclusions/Significance The Floral Reflectance Database is a valuable new tool for researchers interested in the colours of flowers and their association with pollinator colour vision, containing raw spectral reflectance data for a large number of flower species.

Herbivore defence compounds occur in pollen and reduce bumblebee colony fitness.

Herbivory defence chemicals in plants can affect higher trophic levels such as predators and parasitoids, but the impact on pollinators has been overlooked. We show that defensive plant chemicals can damage pollinator fitness when expressed in pollen. Crop lupins (Lupinus species from Europe and South America) accumulate toxic quinolizidine alkaloids in vegetative tissues, conferring resistance to herbivorous pests such as aphids. We identified the alkaloid lupanine and its derivatives in lupin pollen, and then provided this compound at ecologically-relevant concentrations to queenless microcolonies of bumblebees (Bombus terrestris) in their pollen to determine how foraging on these crops may impact bee colony health and fitness. Fewer males were produced by microcolonies provided with lupanine-treated pollen and they were significantly smaller than controls. This impact on males was not linked to preference as workers willingly fed lupanine-treated pollen to larvae, even though it was deleterious to colony health. Agricultural systems comprising large monocultures of crops bred for herbivore resistance can expose generalist pollinators to deleterious levels of plant compounds, and the broader environmental impacts of crop resistance must thus be considered.

Flower color phenology in European grassland and woodland habitats, through the eyes of pollinators

Some studies have claimed that flowers in bloom at particular times of year are more likely to be of particular colors to better attract pollinating insects. To test this, we analyzed a data set collected from five field sites near Strausberg, Germany, which included information on flower color and months of blooming. However, we chose to consider flower color as perceived by bee as well as human visual systems, as well as independent of any color vision system, to reveal whether trends, if present, have any ecological relevance. Using randomization analyses, we were able to consider whether blooming time interacts with flower color, and how this interaction depends upon other factors. Our results show that there is an association between the months of flowering and the colors of flowers — but only when flowers are considered according to human color categories. Further analysis showed that this is merely a consequence of flowers from the same family being more likely to flower at the same time and have similar colors. All these effects disappeared when flowers were considered using bee color categories, and in the analyses of physical spectral reflectances.

The effect of polyploidy and hybridization on the evolution of floral colour in Nicotiana (Solanaceae).

Background and Aims Speciation in angiosperms can be accompanied by changes in floral colour that may influence pollinator preference and reproductive isolation. This study investigates whether changes in floral colour can accompany polyploid and homoploid hybridization, important processes in angiosperm evolution. Methods Spectral reflectance of corolla tissue was examined for 60 Nicotiana (Solanaceae) accessions (41 taxa) based on spectral shape (corresponding to pigmentation) as well as bee and hummingbird colour perception in order to assess patterns of floral colour evolution. Polyploid and homoploid hybrid spectra were compared with those of their progenitors to evaluate whether hybridization has resulted in floral colour shifts. Key Results Floral colour categories in Nicotiana seem to have arisen multiple times independently during the evolution of the genus. Most younger polyploids displayed an unexpected floral colour, considering those of their progenitors, in the colour perception of at least one pollinator type, whereas older polyploids tended to resemble one or both of their progenitors. Conclusions Floral colour evolution in Nicotiana is weakly constrained by phylogeny, and colour shifts do occur in association with both polyploid and homoploid hybrid divergence. Transgressive floral colour in N. tabacum has arisen by inheritance of anthocyanin pigmentation from its paternal progenitor while having a plastid phenotype like its maternal progenitor. Potentially, floral colour evolution has been driven by, or resulted in, pollinator shifts. However, those polyploids that are not sympatric (on a regional scale) with their progenitor lineages are typically not divergent in floral colour from them, perhaps because of a lack of competition for pollinators.

Optimizing the Colour and Fabric of Targets for the Control of the Tsetse Fly Glossina fuscipes fuscipes

Background Most cases of human African trypanosomiasis (HAT) start with a bite from one of the subspecies of Glossina fuscipes. Tsetse use a range of olfactory and visual stimuli to locate their hosts and this response can be exploited to lure tsetse to insecticide-treated targets thereby reducing transmission. To provide a rational basis for cost-effective designs of target, we undertook studies to identify the optimal target colour. Methodology/Principal Findings On the Chamaunga islands of Lake Victoria , Kenya, studies were made of the numbers of G. fuscipes fuscipes attracted to targets consisting of a panel (25 cm square) of various coloured fabrics flanked by a panel (also 25 cm square) of fine black netting. Both panels were covered with an electrocuting grid to catch tsetse as they contacted the target. The reflectances of the 37 different-coloured cloth panels utilised in the study were measured spectrophotometrically. Catch was positively correlated with percentage reflectance at the blue (460 nm) wavelength and negatively correlated with reflectance at UV (360 nm) and green (520 nm) wavelengths. The best target was subjectively blue, with percentage reflectances of 3%, 29%, and 20% at 360 nm, 460 nm and 520 nm respectively. The worst target was also, subjectively, blue, but with high reflectances at UV (35% reflectance at 360 nm) wavelengths as well as blue (36% reflectance at 460 nm); the best low UV-reflecting blue caught 3× more tsetse than the high UV-reflecting blue. Conclusions/Significance Insecticide-treated targets to control G. f. fuscipes should be blue with low reflectance in both the UV and green bands of the spectrum. Targets that are subjectively blue will perform poorly if they also reflect UV strongly. The selection of fabrics for targets should be guided by spectral analysis of the cloth across both the spectrum visible to humans and the UV region.

Odour-mediated orientation of beetles is influenced by age, sex and morph.

The behaviour of insects is dictated by a combination of factors and may vary considerably between individuals, but small insects are often considered en masse and thus these differences can be overlooked. For example, the cowpea bruchid Callosobruchus maculatus F. exists naturally in two adult forms: the active (flight) form for dispersal, and the inactive (flightless), more fecund but shorter-lived form. Given that these morphs show dissimilar biology, it is possible that they differ in odour-mediated orientation and yet studies of this species frequently neglect to distinguish morph type, or are carried out only on the inactive morph. Along with sex and age of individual, adult morph could be an important variable determining the biology of this and similar species, informing studies on evolution, ecology and pest management. We used an olfactometer with motion-tracking to investigate whether the olfactory behaviour and orientation of C. maculatus towards infested and uninfested cowpeas and a plant-derived repellent compound, methyl salicylate, differed between morphs or sexes. We found significant differences between the behaviour of male and female beetles and beetles of different ages, as well as interactive effects of sex, morph and age, in response to both host and repellent odours. This study demonstrates that behavioural experiments on insects should control for sex and age, while also considering differences between adult morphs where present in insect species. This finding has broad implications for fundamental entomological research, particularly when exploring the relationships between physiology, behaviour and evolutionary biology, and the application of crop protection strategies.

Shades of yellow: interactive effects of visual and odour cues in a pest beetle

Background: The visual ecology of pest insects is poorly studied compared to the role of odour cues in determining their behaviour. Furthermore, the combined effects of both odour and vision on insect orientation are frequently ignored, but could impact behavioural responses. Methods: A locomotion compensator was used to evaluate use of different visual stimuli by a major coleopteran pest of stored grains (Sitophilus zeamais), with and without the presence of host odours (known to be attractive to this species), in an open-loop setup. Results: Some visual stimuli—in particular, one shade of yellow, solid black and high-contrast black-against-white stimuli—elicited positive orientation behaviour from the beetles in the absence of odour stimuli. When host odours were also present, at 90° to the source of the visual stimulus, the beetles presented with yellow and vertical black-on-white grating patterns changed their walking course and typically adopted a path intermediate between the two stimuli. The beetles presented with a solid black-on-white target continued to orient more strongly towards the visual than the odour stimulus. Discussion: Visual stimuli can strongly influence orientation behaviour, even in species where use of visual cues is sometimes assumed to be unimportant, while the outcomes from exposure to multimodal stimuli are unpredictable and need to be determined under differing conditions. The importance of the two modalities of stimulus (visual and olfactory) in food location is likely to depend upon relative stimulus intensity and motivational state of the insect.