The effect of insecticide application by dropleg sprayers on pollen beetle parasitism in oilseed rape

Dropleg sprayers apply pesticides below the flower horizon of oilseed rape plants and thus reduce unwanted side effects on pollinating insects. Whether this technique benefits parasitoids of seed and pollen feeding insect pests has not been studied earlier. To answer this question, we first assessed the vertical distribution of pests and parasitoids using a portable aspirator. In addition, parasitism rates of pollen beetle, Brassicogethes aeneus Fabricius (Coleoptera: Nitidulidae), by the larval parasitoid Tersilochus heterocerus Thomson (Hymenoptera: Ichneumonidae) were compared in conventional and dropleg sprayed fields over four years (2016–2019), using the neonicotinoids thiacloprid and acetamiprid. Our results show that seed and pollen feeders were mainly found in the flowering canopy, while the predominant location of parasitoids was species-specific. Among pollen beetle parasitoids, Phradis interstitialis Thomson (Hymenoptera: Ichneumonidae) was more abundant below flowering canopy (63% of total catch), whereas T. heterocerus was mainly caught in the flowering canopy (84% of total catch). In the spraying experiments, average parasitism rates of pollen beetles by T. heterocerus ranged between 55 and 82% in the untreated controls. In the dropleg spray treatments, parasitism rates did not differ significantly from control levels, with the exception of thiacloprid application in 2019. In contrast, conventional spray applications resulted in a reduction of parasitism rates by up to 37% compared to the control for at least one of the insecticides in three out of four years. The impact of conventional application differed between years, which may be explained by the temporal coincidence between spray application and the immigration of parasitoids into the crop. We conclude that dropleg spraying exerts lower non-target effects on the main biological control agent of pollen beetle.

     

Local and landscape determinants of pollen beetle abundance in overwintering habitats

• 1 The development of integrated pest management strategies requires that the semi‐natural habitats scattered across the landscape are taken into account. Particular determinants of insect pest abundance in overwintering habitats just before they migrate onto crops appear to be poorly known and of crucial importance for understanding patterns of crop colonization and pest population dynamics at the landscape scale.
• 2 The emergence of pollen beetle Meligethes aeneus F. was studied in grassland, woodland edge and woodland interior over a 3‐year survey in France using macro‐emergence traps. A suite of variables at the local and the landscape scale was assessed for each trap, aiming to identify potential relevant habitat indicators. The effects of habitat characteristics were evaluated using partial least square regressions.
• 3 It was found that M. aeneus can overwinter in all types of habitat but that particular habitat characteristics at the local and landscape scales may explain their abundance in overwintering sites more than the types of habitat: relative altitude, litter thickness, soil moisture and proximity to the previous year's oilseed rape fields appear to be positively correlated with abundance of adults over the 3 years.
• 4 Hence, the abundance of emerged pollen beetles depends on both the landscape configuration of the previous year's oilseed rape fields around overwintering sites and local habitat characteristics. Landscape configuration may determine population flow towards overwintering sites in the late summer, and local habitat characteristics may influence survival rates during the winter. The findings of the present study provide valuable insight into the role of semi‐natural habitats as a source of pests, patterns of crop colonization in the spring, and the influence of landscape on pollen beetle abundance.

     

Effects of host plant species on the interaction between the parasitic wasp Diospilus capito and pollen beetles (Meligethes spp.)

1 Field studies were conducted in central Sweden to establish whether two host plants with high and low suitability for pollen beetles (Meligethes aeneus Fabr. [Coleoptera: Nitidulidae] and Meligethes viridescens Fabr.) affected the parasitoid Diospilus capito Nees [Hymenoptera: Braconidae]. 2 Samples of larvae were taken from fields with plots of white mustard, Sinapis alba L. and spring rape, Brassica napus L. in 1997 and 1998. Levels of parasitism and the survival and size of D. capito were measured to determine any influence of the host plant species. Survival and weights of pollen beetles from S. alba and B. napus were also measured. 3 Levels of parasitism between 8% and 29% were recorded. There was a significantly higher likelihood of being parasitized by D. capito for beetle larvae developing on S. alba than on B. napus. We argue that semiochemical or morphological properties of plant species could be responsible for differential parasitism by D. capito. 4 Neither survival of D. capito nor parasitoid size differed from hosts developing on S. alba or B. napus. Pollen beetle emergence was the same for both plant species, but beetles that developed on S. alba weighed less than those from B. napus. Results suggest that the partial resistance of S. alba to the pollen beetle will have no negative effects on the parasitoid D. capito.     

Agri‐environment schemes targeting farmland bird populations also provide food for pollinating insects

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Crop–noncrop spillover: arable fields affect trophic interactions on wild plants in surrounding habitats

Ecosystem processes in agricultural landscapes are often triggered by resource availability in crop and noncrop habitats. We investigated how oilseed rape (OSR; Brassica napus, Brassicaceae) affects noncrop plants in managed systems and semi-natural habitat, using trophic interactions among wild mustard (Sinapis arvensis, Brassicaceae), rape pollen beetles (Meligethes aeneus, Nitidulidae) and their parasitoids (Tersilochus heterocerus, Ichneumonidae). We exposed wild mustard as phytometer plants in two cropland habitat types (wheat field, field margin) and three noncrop habitat types (fallow, grassland, wood margin) across eight landscapes along a gradient from simple to complex (quantified as % arable land). Both landscape and local factors affected the abundance of rape pollen beetles and parasitoids. Rape pollen beetle infestation and parasitism rates on these plants were lower in noncrop habitats and higher in wheat fields and field margins, whereas beetles and parasitoids responded differently to landscape scale parameters. We found the hypothesized spillover from OSR crop onto wild plants in surrounding habitats only for parasitoids, but not for pollen beetles. Parasitism rates were not related to landscape simplification, but benefited from increasing proportions of OSR. In contrast, rape pollen beetles benefited from simple landscape structures, presumably due to multi-annual population build-ups resulting from long-term OSR planting (as part of the crop rotation). In conclusion, we showed that spillover from cropland affects parasitism rates on related wild plants outside cropland, which has not been shown so far, but can be expected to be a widespread effect shaping noncrop food webs.     

Heteranthery as a solution to the demand for pollen as food and for pollination – Legitimate flower visitors reject flowers without feeding anthers

• Heteranthery, the presence of feeding and pollinating anthers in the same flower, seems to mediate the evolutionary dilemma for plants to protect their gametes and yet provide food for pollinators. This study aims to elucidate the role of heteranthery in the buzz‐pollinated Senna reniformis.
• The fecundity of pollen from long‐, medium‐ and short‐sized anthers was determined by hand cross‐pollination experiments, and the quantity, size, ornamentation and viability of pollen of different anthers were compared. Rates of flower rejection by bees were measured in anther removal experiments to assess the preferences of flower visitors for feeding or pollinating anthers.
• Large bees, which were the effective pollinators of self‐incompatible S. reniformis, avoided flowers without short feeding anthers, but not those without medium or long anthers. Illegitimate small and medium‐sized bees were unresponsive to anther exclusion experiments. Long anthers deposited pollen on the back and short anthers on the venter of large bees. Pollen from long anthers had higher in vitro viability and higher fruit and seed set after cross‐pollination than pollen from other sized anthers.
• Short anthers produce feeding pollen to effective pollinators and long anthers are related to pollination of S. reniformis. Bee behaviour and size was found to directly influence the role of anthers in the ‘division of labour’. Only large bee pollinators that carry the pollinating pollen from long anthers in ‘safe sites’ associated short anthers with the presence of food. In the absence of these larger bee pollinators, the role of heteranthery in S. reniformis would be strongly compromised and its function would be lost.

     

Hoverflies (Diptera: Syrphidae) benefit from a cultivation of the bioenergy crop Silphium perfoliatum L. (Asteraceae) depending on larval feeding type,landscape composition and crop management

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Do native and invasive herbivores have an effect on Brassica rapa pollination?

• Mutualistic (e.g. pollination) and antagonistic (e.g. herbivory) plant–insect interactions shape levels of plant fitness and can have interactive effects.
• By using experimental plots of Brassica rapa plants infested with generalist (Mamestra brassicae) and specialised (Pieris brassicae) native herbivores and with a generalist invasive (Spodoptera littoralis) herbivore, we estimated both pollen movement among treatments and the visiting behaviour of honeybees versus other wild pollinators.
• Overall, we found that herbivory has weak effects on plant pollen export, either in terms of inter‐treatment movements or of dispersion distance. Plants infested with the native specialised herbivore tend to export less pollen to other plants with the same treatment. Other wild pollinators preferentially visit non‐infested plants that differ from those of honeybees, which showed no preferences. Honeybees and other wild pollinators also showed different behaviours on plants infested with different herbivores, with the former tending to avoid revisiting the same treatment and the latter showing no avoidance behaviour. When taking into account the whole pollinator community, i.e. the interactive effects of honeybees and other wild pollinators, we found an increased avoidance of plants infested by the native specialised herbivore and a decreased avoidance of plants infested by the invasive herbivore.
• Taken together, our results suggest that herbivory may have an effect on B. rapa pollination, but this effect depends on the relative abundance of honeybees and other wild pollinators.

     

Targeted sugar provision promotes parasitism of the cereal leaf beetle Oulema melanopus

• 1 Parasitoids may often lack access to sugar (e.g. floral nectar) in agricultural settings. Strategically timed spraying of host plants with sugar solution may provide one means of enhancing parasitism at the same time as minimizing nontarget effects (e.g. benefiting the pest itself).
• 2 Sucrose was sprayed in wheat fields of northern Utah (U.S.A.) to assess the effects on parasitism of the cereal leaf beetle Oulema melanopus by the larval parasitoid Tetrastichus julis.
• 3 Early‐season sugar provisioning, when larvae of the pest were first hatching and parasitoid adults were newly emerged, did not affect the numbers of cereal leaf beetle larvae that matured in treated plots but increased parasitism rates of beetle larvae by four‐fold in 2006 and by seven‐fold in 2007.
• 4 No net influx of adult parasitoids into plots was detected after the application of sugar. Locally‐emerging parasitoids may have spent less time searching for their own food needs versus hosts. A laboratory experiment also confirmed that access to sucrose significantly increased parasitoid longevity.
• 5 The field experimental results obtained demonstrate that applications of sugar, implemented to target a key time of the growing season when benefits are maximized for parasitoids and minimized for their hosts, can strongly promote parasitism of the cereal leaf beetle in wheat fields.

     

Specialised protagonists in a plant–pollinator interaction: the pollination of Blumenbachia insignis (Loasaceae)

• Analyses of resource presentation, floral morphology and pollinator behaviour are essential for understanding specialised plant‐pollinator systems. We investigated whether foraging by individual bee pollinators fits the floral morphology and functioning of Blumenbachia insignis, whose flowers are characterised by a nectar scale‐staminode complex and pollen release by thigmonastic stamen movements.
• We described pollen and nectar presentation, analysed the breeding system and the foraging strategy of bee pollinators. We determined the nectar production pattern and documented variations in the longevity of floral phases and stigmatic pollen loads of pollinator‐visited and unvisited flowers.
• Bicolletes indigoticus (Colletidae) was the sole pollinator with females revisiting flowers in staminate and pistillate phases at short intervals, guaranteeing cross‐pollen flow. Nectar stored in the nectar scale‐staminode complex had a high sugar concentration and was produced continuously in minute amounts (~0.09 μl·h^?1). Pushing the scales outward, bees took up nectar, triggering stamen movements and accelerating pollen presentation. Experimental simulation of this nectar uptake increased the number of moved stamens per hour by a factor of four. Flowers visited by pollinators received six‐fold more pollen on the stigma than unvisited flowers, had shortened staminate and pistillate phases and increased fruit and seed set.
• Flower handling and foraging by Bicolletes indigoticus were consonant with the complex flower morphology and functioning of Blumenbachia insignis. Continuous nectar production in minute quantities but at high sugar concentration influences the pollen foraging of the bees. Partitioning of resources lead to absolute flower fidelity and stereotyped foraging behaviour by the sole effective oligolectic bee pollinator.

     

Parasitism of a pollinator fig wasp: mortalities are higher in figs with more pollinators,but are not related to local densities of figs

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Pollination and breeding system of the enigmatic South African parasitic plant Mystropetalon thomii (Mystropetalaceae): rodents welcome,but not needed

• Unrelated plants adapted to particular pollinator types tend to exhibit convergent evolution in floral traits. However, inferences about likely pollinators from ‘pollination syndromes’ can be problematic due to trait overlap among some syndromes and unusual floral architecture in some lineages. An example is the rare South African parasitic plant Mystropetalon thomii (Mystropetalaceae), which has highly unusual brush‐like inflorescences that exhibit features of both bird and rodent pollination syndromes.
• We used camera traps to record flower visitors, quantified floral spectral reflectance and nectar and scent production, experimentally determined self‐compatibility and breeding system, and studied pollen dispersal using fluorescent dyes.
• The dark‐red inflorescences are usually monoecious, with female flowers maturing before male flowers, but some inflorescences are purely female (gynoecious). Inflorescences were visited intensively by several rodent species that carried large pollen loads, while visits by birds were extremely rare. Rodents prefer male‐ over female‐phase inflorescences, likely because of the male flowers’ higher nectar and scent production. The floral scent contains several compounds known to attract rodents. Despite the obvious pollen transfer by rodents, we found that flowers on both monoecious and gynoecious inflorescences readily set seed in the absence of rodents and even when all flower visitors are excluded.
• Our findings suggest that seed production occurs at least partially through apomixis and that M. thomii is not ecologically dependent on its rodent pollinators. Our study adds another species and family to the growing list of rodent‐pollinated plants, thus contributing to our understanding of the floral traits associated with pollination by non‐flying mammals.

     

Responses of <Emphasis Type="Italic">Phradis</Emphasis> parasitoids to volatiles of lavender, <Emphasis Type="Italic">Lavendula angustifolia</Emphasis>—a possible repellent for their host, <Emphasis Type="Italic">Meligethes aeneus</Emphasis>

Hymenopterous parasitoids of herbivorous insects can be useful biocontrol agents in integrated pest management strategies. However, the potential effects on these beneficials of new components in such strategies are often neglected. Essential oil of lavender, Lavendula angustifolia (Miller) (Lamiaceae), has recently been identified as a potential repellent in new control strategies being developed for the pollen beetle Meligethes aeneus (Fabricius) (Coleoptera: Nitidulidae), a major pest of oilseed rape, Brassica napus L. (Brassicaceae). We tested the electrophysiological and behavioural responses of two common parasitoids of M. aeneus: Phradis interstitialis (Thomson) and P. morionellus (Holmgren) (both Ichneumonidae) using coupled gas chromatography-electroantennodetection (GC-EAD) and olfactometry techniques. Both species elicited electrophysiological responses to lavender oil volatiles, including two compounds known to be repellent to M. aeneus. However, the parasitoids gave no significant responses to the odours of lavender oil in behavioural bioassays and there was no evidence to suggest that lavender-treated oilseed rape plants would reduce host habitat location by parasitoids of the target pest.     

The relative attractiveness of Brassica napus,B. rapa,B. juncea and Sinapis alba to pollen beetles

It is often suggested that weeds from the same family as the crop plant may increase insect pest damages by providing shelter and additional oviposition opportunities. We compared the relative attractiveness of Brassica rapa L., B. juncea L., Sinapis alba L. and B. napus L. (Capparales: Brassicaceae) to the pollen beetle and its hymenopteran parasitoids in field conditions. Our results revealed that none of the investigated plants increased the pest abundance on B. napus plants. On the contrary, B. juncea and S. alba lured beetles away from B. napus during its damage-susceptible stage. The parasitism rate of pollen beetle larvae was the highest on B. juncea plants, indicating that cruciferous weeds could improve the natural control of the pollen beetle by providing additional hosts for parasitoids. Therefore, close relatives of oilseed rape might be used to trap pollen beetle adults, but also to support populations of natural enemies that could decrease the number of beetles.     

Effect of pollen and resource limitation on reproduction of Zygophyllum xanthoxylum in fragmented habitats

Limitations on pollen and resources may significantly affect plant reproduction in fragmented habitats. In this study, phenology and pollinator frequency and activity were investigated to estimate the role of pollinators in Zygophyllum xanthoxylum reproduction, and this species is ecologically important in northwest China. In addition, the relative impact of restrictive amounts of pollen and resources on the seed set per flower was evaluated. It was found that adding pollen boosted the size of the seed set per flower, but had no significant effect on the number of flowers. By contrast, the addition of resources increased flower numbers as well as had a slight impact on the seed set per flower. These results indicate the amount of available pollen is a limiting factor for reproductive success. Moreover, Apis mellifera was identified as the most effective pollinator of Z. xanthoxylum, and there were more overall pollinators and visitations in the control than in the fragmented habitats. Furthermore, the limitations in pollen were more restrictive in the fragmented area than in the control. This was due to increased pollinator visitations in the control that could ameliorate the effects of lower pollen levels. When there is a limited availability of suitable pollinators, self‐pollination is critical in fragmented habitats. Z. xanthoxylum has reproductive strategies that aid in adapting to harsh environments, including protogyny and delayed selfing.     

Effects of insecticide application on parasitism rates of pollen beetle larvae (<Emphasis Type="Italic">Brassicogethes aeneus</Emphasis> (Fabricius)) by tersilochine parasitoids

Larval parasitoids can substantially reduce the population density of the pollen beetle [Brassicogethes aeneus (Fabricius), syn. Meligethes aeneus (Fabricius)]. The most abundant tersilochine parasitoids of pollen beetle are Tersilochus heterocerus, Phradis interstitialis and P. morionellus. The main activity of these parasitoids was observed in the period shortly before flowering to full flowering of oilseed rape. Insecticide applications during this period may have negative effects on parasitoids. In the present study, the effects of the insecticides Biscaya (a.i. thiacloprid), Mavrik (a.i. tau-fluvalinate) and Karate Zeon (a.i. lambda-cyhalothrin) applied during the bud or flowering stage of winter oilseed rape on parasitization of pollen beetle larvae by T. heterocerus were studied in 12 field trials at different locations in Germany in 2013–2015. The effects on parasitism by Phradis spp. were assessed in 2015. Parasitism of pollen beetle larvae by T. heterocerus was found in all field trials in all experimental years, but in most trials not before full flowering. Maximum percentage of parasitized larvae at different locations ranged between 3.4 and 16.8% in 2013, 8.3 and 22.4% in 2014 and from 11.1 to 29.1% in 2015. Levels of parasitism were not significantly different between the untreated control and insecticide treatments within each location. In contrast to T. heterocerus, Phradis spp. was not detected at all locations and not before flowering declining. In field trials at Lucklum and Puch, the maximum level of parasitism by Phradis spp. was 9.4 and 18.3%, respectively. No significant effect of insecticide application on parasitism by Phradis spp. was observed between the treatments. The results of this study showed that the insecticides used in the field trials did not affect parasitization of pollen beetle larvae by T. heterocerus and Phradis spp., regardless whether applied at the bud stage, at the beginning of flowering or full flowering.     

Intra‐floral resource partitioning between endemic and invasive flower visitors: consequences for pollinator effectiveness

1. Sympatric flower visitor species often partition nectar and pollen and thus affect each other's foraging pattern. Consequently, their pollination service may also be influenced by the presence of other flower visiting species. Ants are solely interested in nectar and frequent flower visitors of some plant species but usually provide no pollination service. Obligate flower visitors such as bees depend on both nectar and pollen and are often more effective pollinators. 2. In Hawaii, we studied the complex interactions between flowers of the endemic tree Metrosideros polymorpha (Myrtaceae) and both, endemic and introduced flower‐visiting insects. The former main‐pollinators of M. polymorpha were birds, which, however, became rare. We evaluated the pollinator effectiveness of endemic and invasive bees and whether it is affected by the type of resource collected and the presence of ants on flowers. 3. Ants were dominant nectar‐consumers that mostly depleted the nectar of visited inflorescences. Accordingly, the visitation frequency, duration, and consequently the pollinator effectiveness of nectar‐foraging honeybees (Apis mellifera) strongly decreased on ant‐visited flowers, whereas pollen‐collecting bees remained largely unaffected by ants. Overall, endemic bees (Hylaeus spp.) were ineffective pollinators. 4. The average net effect of ants on pollination of M. polymorpha was neutral, corresponding to a similar fruit set of ant‐visited and ant‐free inflorescences. 5. Our results suggest that invasive social hymenopterans that often have negative impacts on the Hawaiian flora and fauna may occasionally provide neutral (ants) or even beneficial net effects (honeybees), especially in the absence of native birds.     

Effect of flower traits and hosts on the abundance of parasitoids in perennial multiple species wildflower strips sown within oilseed rape (<Emphasis Type="Italic">Brassica napus</Emphasis>) crops

Reducing the use of insecticides is an important issue for agriculture today. Sowing wildflower strips along field margins or within crops represents a promising tool to support natural enemy populations in agricultural landscapes and, thus, enhance conservation biological control. However, it is important to sow appropriate flower species that attract natural enemies efficiently. The presence of prey and hosts may also guide natural enemies to wildflower strips, potentially preventing them from migrating into adjacent crops. Here, we assessed how seven flower traits, along with the abundance of pollen beetles (Meligethes spp., Coleoptera: Nitidulidae) and true weevils (Ceutorhynchus spp., Coleoptera: Curculionidae), affect the density of parasitoids of these two coleopterans in wildflower strips sown in an oilseed rape field in Gembloux (Belgium). Only flower traits, not host (i.e. pollen beetles and true weevils) abundance, significantly affected the density of parasitoids. Flower colour, ultraviolet reflectance and nectar availability were the main drivers affecting parasitoids. These results demonstrate how parasitoids of oilseed rape pests react to flower cues under field conditions. Similar analyses on the pests and natural enemies of other crops are expected to help to develop perennial flower mixtures able to enhance biological control throughout a rotation system.     

High levels of fecundity in small and isolated populations of a self‐compatible Aloe pollinated by opportunistic birds and bees

• Plant species that are effective colonisers of transient habitats are expected to have a capacity for uniparental reproduction and show flexibility in pollination systems. Such traits may enable populations to be established from a small number of founding individuals without these populations succumbing to reductions in fecundity arising from pollinator limitation.
• We tested these predictions for Aloe thraskii (Xanthorrhoeaceae), a succulent treelet that colonises shifting coastal dunes and has both bird and bee pollinators. We performed hand‐pollination experiments, and selectively excluded bird visitors to determine differences in pollinator effectiveness. We measured pollinator visitation rates and fecundity in populations varying in their size, density and isolation distance.
• Controlled hand‐pollinations revealed that unlike most other Aloe species, A. thraskii is self‐compatible and thus capable of uniparental reproduction. The species does however depend on pollinators and is visited by various bird species as well as by bees. Fruit and seed set are not affected by selective exclusion of birds, thus indicating that bees are effective pollinators. Bird visitation rates increased with increasing plant height and population size, while bee visitation rates increased with increasing population size and density. We found that seed set per flower was lower in large populations than in small populations.
• These results suggest that establishment of populations of A. thraskii from a small number of individuals is unlikely to be limited by the fecundity of individual plants.

     

A model of pollinator‐mediated gene flow between plant populations with numerical solutions for bumblebees pollinating oilseed rape

We present a model that predicts the level of gene flow mediated by animal pollinators from a source population to a sink population. The model requires specification of three elements: (1) the paternity that originates from a single flower, the paternity shadow; (2) the mean number of flowers that pollinators visit during stays in the sink population, the residence; (3) the proportion of pollinators arriving at the sink that carry pollen from the source population. Provided that pollinators visit enough flowers in the sink to exhaust the paternity shadows from the source, the general results are that gene flow is inversely proportional to the mean pollinator residence in the sink population, and is proportional to the fraction of pollinators arriving with pollen from the source. These results are used to propose explanations for two of the widely observed patterns in gene flow among plant populations. Numerical solutions to the model are derived using experimentally determined values of elements (1) and (2) that represent bumblebees, Bombus spp., visiting agricultural fields of oilseed rape, Brassica napus L. In B. napus, the paternity shadow attenuates rapidly over approximately 20 recipient flowers. Mean bumblebee residences in the fields studied varied between 490 and 720 flowers. In the absence of a direct measurement of element (3), we calculated the maximum level of bumblebee‐mediated gene flow by assuming that all bees arrived at the sink saturated with pollen from extrinsic sources. In this case, the model predicts that bumblebee‐mediated gene flow accounted for between 0.1% and 0.5% of the progeny in the agricultural fields studied. A likelihood analysis of our observations is unable to reveal convincingly the proportion of bees arriving at the sink via a source population, but the literature suggests that bumblebees have high site fidelity, which implies that bee‐mediated gene flow may be substantially less than our estimated maximum. We consider the role of various factors, including wind pollination, in accounting for the differences between the model's predictions and the generally higher levels of gene flow observed in previous studies of oilseed rape.