Imidacloprid-induced impairment of mushroom bodies and behavior of the native stingless bee Melipona quadrifasciata anthidioides

Declines in pollinator colonies represent a worldwide concern. The widespread use of agricultural pesticides is recognized as a potential cause of these declines. Previous studies have examined the effects of neonicotinoid insecticides such as imidacloprid on pollinator colonies, but these investigations have mainly focused on adult honey bees. Native stingless bees (Hymenoptera: Apidae: Meliponinae) are key pollinators in neotropical areas and are threatened with extinction due to deforestation and pesticide use. Few studies have directly investigated the effects of pesticides on these pollinators. Furthermore, the existing impact studies did not address the issue of larval ingestion of contaminated pollen and nectar, which could potentially have dire consequences for the colony. Here, we assessed the effects of imidacloprid ingestion by stingless bee larvae on their survival, development, neuromorphology and adult walking behavior. Increasing doses of imidacloprid were added to the diet provided to individual worker larvae of the stingless bee Melipona quadrifasciata anthidioides throughout their development. Survival rates above 50% were only observed at insecticide doses lower than 0.0056 μg active ingredient (a.i.)/bee. No sublethal effect on body mass or developmental time was observed in the surviving insects, but the pesticide treatment negatively affected the development of mushroom bodies in the brain and impaired the walking behavior of newly emerged adult workers. Therefore, stingless bee larvae are particularly susceptible to imidacloprid, as it caused both high mortality and sublethal effects that impaired brain development and compromised mobility at the young adult stage. These findings demonstrate the lethal effects of imidacloprid on native stingless bees and provide evidence of novel serious sublethal effects that may compromise colony survival. The ecological and economic importance of neotropical stingless bees as pollinators, their susceptibility to insecticides and the vulnerability of their larvae to insecticide exposure emphasize the importance of studying these species.     

Honey bees and wild pollinators differ in their preference for and use of introduced floral resources

Introduced plants may be important foraging resources for honey bees and wild pollinators, but how often and why pollinators visit introduced plants across an entire plant community is not well understood. Understanding the importance of introduced plants for pollinators could help guide management of these plants and conservation of pollinator habitat. We assessed how floral abundance and pollinator preference influence pollinator visitation rate and diversity on 30 introduced versus 24 native plants in central New York. Honey bees visited introduced and native plants at similar rates regardless of floral abundance. In contrast, as floral abundance increased, wild pollinator visitation rate decreased more strongly for introduced plants than native plants. Introduced plants as a group and native plants as a group did not differ in bee diversity or preference, but honey bees and wild pollinators preferred different plant species. As a case study, we then focused on knapweed (Centaurea spp.), an introduced plant that was the most preferred plant by honey bees, and that beekeepers value as a late‐summer foraging resource. We compared the extent to which honey bees versus wild pollinators visited knapweed relative to coflowering plants, and we quantified knapweed pollen and nectar collection by honey bees across 22 New York apiaries. Honey bees visited knapweed more frequently than coflowering plants and at a similar rate as all wild pollinators combined. All apiaries contained knapweed pollen in nectar, 86% of apiaries contained knapweed pollen in bee bread, and knapweed was sometimes a main pollen or nectar source for honey bees in late summer. Our results suggest that because of diverging responses to floral abundance and preferences for different plants, honey bees and wild pollinators differ in their use of introduced plants. Depending on the plant and its abundance, removing an introduced plant may impact honey bees more than wild pollinators.     

Neighborhood‐contingent indirect interactions between native and exotic plants: multiple shared pollinators mediate reproductive success during invasions

Native and exotic plants can influence one another's fecundity through their influence on shared pollinators. Specifically, invasion may alter abundance and composition of local floral resources, affecting pollinator visitation and ultimately causing seedset of natives in more‐invaded and less‐invaded floral neighborhoods to differ. Such pollinator‐mediated effects of exotic plants on natives are common, but native and exotic plants often share multiple pollinators, which may differ in their responses to altered floral neighborhoods. We quantified pollinator‐mediated interactions between three common forbs of western Washington prairies (native Microseris laciniata and Eriophyllum lanatum and European Hypochaeris radicata) in three floral neighborhoods: 1) high native and low exotic floral density, 2) high exotic floral density and low native density, and 3) experimentally manipulated low exotic floral density. Pollinator visitation rates varied by floral neighborhood, plant species identity, and their interaction for all three plant species. Similarly, pollinator functional groups (eusocial bees, solitary bees, and syrphid flies) contributed differing proportions of total visitation to each species depending upon neighborhood context. Consequently, in exotic neighborhoods H. radicata competed with native M. laciniata, reducing seed set, while simultaneously facilitating visitation and seed set for native E. lanatum. Seed set of H. radicata was also highest in exotic neighborhoods (with high densities of conspecifics), raising the possibility of a positive feedback between exotic abundance and success. Our results suggest that the outcome of indirect interactions between native and exotic plants depends on the density and the composition of the floral neighborhood and of the pollinator fauna, and on context‐dependent pollinator foraging.     

The relative importance of birds and bees in the pollination of Metrosideros excelsa (Myrtaceae)

Exclusion experiments were used to assess the effect of different pollinator groups on outcrossing and seed production in Metrosideros excelsa. The main study site was Little Barrier Island, New Zealand where indigenous bird and native solitary bees are the main flower visitors. Our results showed that native birds were more important pollinators of M. excelsa than native bees. Seed production was much higher in open pollination than in two exclusion experiments where either birds were excluded and native bees only had access to flowers, or where all pollinators had been excluded. The number of fertile seeds per capsule was 45% higher after open pollination than in treatments with bee visitation only and 28% higher than in treatments where all flower visitors were excluded. Estimated outcrossing rates were significantly higher (t_m = 0.71) for open pollination in the upper canopy (>4 m above‐ground level) where bird visitation is presumed to be more frequent than for a treatment with native bee access only (t_m = 0.40). Our results also suggest that a large proportion of seeds (66%) arise from autonomous self‐pollination when all pollinators are excluded. In four trees of a modified mainland population with predominantly introduced birds and a mixture of introduced and native bees there was no decrease in seed production for the treatment allowing bee access only, indicating that – in contrast to native bees – honeybees may be more efficient pollinators of M. excelsa. Observation of the foraging behaviour of both groups of bees showed that native bees contact the stigma of flowers less frequently than honeybees. This is likely to be a consequence of their smaller body size relative to honeybees.     

Sublethal neonicotinoid insecticide exposure reduces solitary bee reproductive success

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Potential negative effects of exotic honey bees on the diversity of native pollinators and yield of highland coffee plantations

• 1 The honey bee Apis mellifera is native to Eurasia and Africa, although it is commonly introduced into crop fields of different parts of the world because of the assumption that it improves yield. This bee is, however, a poor pollinator of several crops compared with native insects. Indeed, honey bees can displace native pollinators and reduce their diversity. The present study evaluated the potential impacts of A. mellifera on the diversity of native pollinators of highland coffee (Coffea arabica) and its putative consequences for coffee production at the state of Veracruz, Mexico.
• 2 The abundance of A. mellifera and diversity of native pollinators were assessed during blooming at 12 shade coffee plantations and pollination experiments were conducted to determine the impacts of pollinators on coffee fruit production. Regression analyses were used to assess whether the abundance of honey bees was related to native pollinator diversity, and whether fruit production was influenced by both the diversity of pollinators and the abundance of A. mellifera.
• 3 Native pollinator diversity decreased as the number of honey bees increased. Furthermore, although coffee fruit production was positively related to the diversity of native pollinators, an increasing abundance of A. mellifera was correlated with a decrease in fruit production.
• 4 Highland shade coffee plantations are considered as reservoirs of the Mexican insect fauna. Thus, native pollinator diversity could be better preserved if beekeepers reduced the number of managed hives that they brought into plantations. This may also help to increase coffee yield by decreasing the putative negative effects of A. mellifera on native pollinators.

     

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.     

Insecticide resistance and control failure likelihood of the whitefly Bemisia tabaci (MEAM1; B biotype): a Neotropical scenario

Insecticide resistance is a standing concern for arthropod pest species, which may result in insecticide control failure. Nonetheless, while insecticide resistance has remained a focus of attention for decades, the incurring risk of insecticide control failure has been neglected. The recognition of both problems is paramount for arthropod pest management and particularly so when invasive species notoriously difficult to control and exhibiting frequent cases of insecticide resistance are considered. Such is the case of the putative whitefly species Middle East‐Asia Minor I (MEAM1) (Bemisia tabaci B‐biotype), for which little information is available in the Neotropics. Thus, the likely occurrence and levels of resistance to seven insecticides were surveyed among Brazilian populations of this species. The likelihood of control failure to the five insecticides registered for this species was also determined. Resistance was detected to all insecticides assessed reaching instances of high (i.e. >100×) to very high levels (>1000×) in all of them. Overall efficacy was particularly low (<60%) and the control failure likelihood was high (>25%) and frequent (70%) for the bioinsecticide azadirachtin, followed by spiromesifen and lambda‐cyhalothrin. In contrast, the likelihood of control failure was low for diafenthiuron, and mainly imidacloprid. As cartap and chlorantraniliprole are not used against whiteflies, but are frequently applied on the same host plants, inadvertent selection probably took place leading to high levels of resistance, particularly for the latter. The resistance levels of cartap and chlorantraniliprole correlated with imidacloprid resistance (r > 0.65, P < 0.001), suggesting that the latter use may have somewhat favoured inadvertent selection for resistance to both compounds not used against the whitefly. A further concern is that chlorantraniliprole use in the reported scenario may allow cross selection to cyantraniliprole, a related diamide with recent registration against whiteflies demanding attention in designing resistance management programmes.     

Fidelity of Hymenoptera and Diptera pollinators in onion (Allium cepa L.) pollination

Onion (Allium cepa L.) is protandrous in nature and requires cross‐pollination to avoid inbreeding. The pollination potential of native bees (Hymenoptera) and true flies (Diptera) was assessed in the perspective of finding the best pollinators for onion cross‐pollination and seed multiplication. The community of pollinators was composed of four bee species and twelve true fly species. Episyrphus balteatus, Eupeodes sp., Musca domestica and Eristalinus aeneus were the most abundant pollinators. The maximum pollinator activity was observed from 12 to 24 days after opening of the flowers. The pollination effectiveness of tested bees (Apis dorsata and Apis florea) was greater than true flies (E. balteatus, Eupeodes sp., M. domestica, E. aeneus and Callihoridae sp.) in terms of Spears values.     

Urban land use limits regional bumble bee gene flow

Potential declines in native pollinator communities and increased reliance on pollinator‐dependent crops have raised concerns about native pollinator conservation and dispersal across human‐altered landscapes. Bumble bees are one of the most effective native pollinators and are often the first to be extirpated in human‐altered habitats, yet little is known about how bumble bees move across fine spatial scales and what landscapes promote or limit their gene flow. In this study, we examine regional genetic differentiation and fine‐scale relatedness patterns of the yellow‐faced bumble bee, Bombus vosnesenskii, to investigate how current and historic habitat composition impact gene flow. We conducted our study across a landscape mosaic of natural, agricultural and urban/suburban habitats, and we show that B. vosnesenskii exhibits low but significant levels of differentiation across the study system (F_ST = 0.019, D_est = 0.049). Most importantly, we reveal significant relationships between pairwise F_ST and resistance models created from contemporary land use maps. Specifically, B. vosnesenskii gene flow is most limited by commercial, industrial and transportation‐related impervious cover. Finally, our fine‐scale analysis reveals significant but declining relatedness between individuals at the 1–9 km spatial scale, most likely due to local queen dispersal. Overall, our results indicate that B. vosnesenskii exhibits considerable local dispersal and that regional gene flow is significantly limited by impervious cover associated with urbanization.     

Imidacloprid Alters Foraging and Decreases Bee Avoidance of Predators

Concern is growing over the effects of neonicotinoid pesticides, which can impair honey bee cognition. We provide the first demonstration that sublethal concentrations of imidacloprid can harm honey bee decision-making about danger by significantly increasing the probability of a bee visiting a dangerous food source. Apis cerana is a native bee that is an important pollinator of agricultural crops and native plants in Asia. When foraging on nectar containing 40 µg/L (34 ppb) imidacloprid, honey bees (Apis cerana) showed no aversion to a feeder with a hornet predator, and 1.8 fold more bees chose the dangerous feeder as compared to control bees. Control bees exhibited significant predator avoidance. We also give the first evidence that foraging by A. cerana workers can be inhibited by sublethal concentrations of the pesticide, imidacloprid, which is widely used in Asia. Compared to bees collecting uncontaminated nectar, 23% fewer foragers returned to collect the nectar with 40 µg/L imidacloprid. Bees that did return respectively collected 46% and 63% less nectar containing 20 µg/L and 40 µg/L imidacloprid. These results suggest that the effects of neonicotinoids on honey bee decision-making and other advanced cognitive functions should be explored. Moreover, research should extend beyond the classic model, the European honey bee (A. mellifera), to other important bee species.     

Azadirachtin-mediated reproductive response of the predatory pirate bug Blaptostethus pallescens

The little-known pirate bug Blaptostethus pallescens Poppius is a biocontrol agent observed in tropical tomato fields in Brazil regulating fruit borer populations. In this study, the lethal response of B. pallescens to the bioinsecticide azadirachtin and to two synthetic insecticides, chlorpyrifos and deltamethrin, was assessed. The mild effect of the azadirachtin label rate (0.006 mg a.i. ml^?1) on the predator (median lethal time (LT₅₀) of 27 days), relative to label rates of deltamethrin (0.02 mg a.i. ml^?1) and chlorpyrifos (1.44 mg a.i. ml^?1) (with LT₅₀ of 25 and 60 min, respectively) led to the assessment of its potential sublethal effects. Azadirachtin did not cause behavioral avoidance in the pirate bug, but the daily fecundity, adult progeny production and sex ratio were impaired when both male and female parents were exposed. These effects reduced the population growth of the predator in subsequent generations. Therefore, although safer than the conventional synthetic insecticides tested, the bioinsecticide azadirachtin does impair predator reproduction requiring attention when used in fields with this biological control agent.     

Susceptibility of the eggs of the field slug Deroceras reticulatum to contact with pesticides and substances of biological origin on artificial soil

The toxicity of 14 substances, including a number of pesticides, to the eggs of the pest slug Deroceras reticulatum was determined in laboratory experiments. Eggs were kept in contact with a precisely defined artificial soil to which a range of concentrations of the test substances had been applied. Mortality of the eggs was assessed every 24 h and the median lethal doses (LD₅₀) were determined. The herbicides bromoxynil, ioxynil and pyridate + bromoxynil, the insecticides thiocyclam, diflubenzuron and azadirachtin, the molluscicides metaldehyde and methiocarb, and other compounds such as carvone, iron‐EDDHA, saponin, and an extract of Pongamia pinnata, killed the eggs after periods of exposure ranging from 2 to 14 days, depending on the compound and the dose. Only two compounds, the insecticides imidacloprid and teflubenzuron, failed to kill the eggs of D. reticulatum at any of the doses tested. Values of LD₅₀ below 0.01 mg a.i. cm^?2 were obtained for the herbicides bromoxynil, ioxynil and pyridate + bromoxynil, and for the biological pesticide azadirachtin. The feasibility of slug egg control in different contexts is discussed.     

Molecular assays of pollen use consistently reflect pollinator visitation patterns in a system of flowering plants

Determining how pollinators visit plants vs. how they carry and transfer pollen is an ongoing project in pollination ecology. The current tools for identifying the pollens that bees carry have different strengths and weaknesses when used for ecological inference. In this study we use three methods to better understand a system of congeneric, coflowering plants in the genus Clarkia and their bee pollinators: observations of plant–pollinator contact in the field, and two different molecular methods to estimate the relative abundance of each Clarkia pollen in samples collected from pollinators. We use these methods to investigate if observations of plant–pollinator contact in the field correspond to the pollen bees carry; if individual bees carry Clarkia pollens in predictable ways, based on previous knowledge of their foraging behaviors; and how the three approaches differ for understanding plant–pollinator interactions. We find that observations of plant–pollinator contact are generally predictive of the pollens that bees carry while foraging, and network topologies using the three different methods are statistically indistinguishable from each other. Results from molecular pollen analysis also show that while bees can carry multiple species of Clarkia at the same time, they often carry one species of pollen. Our work contributes to the growing body of literature aimed at resolving how pollinators use floral resources. We suggest our novel relative amplicon quantification method as another tool in the developing molecular ecology and pollination biology toolbox.     

Pollinator effectiveness of native and non‐native flower visitors to an apparently generalist Andean shrub,Duranta mandonii (Verbenaceae)

Not all visitors to flowers are pollinators and pollinating taxa can vary greatly in their effectiveness. Using a combination of observations and experiments we compared the effectiveness of introduced honeybees with that of hummingbirds, native bees and moths on both the male and female components of fitness of the Andean shrub Duranta mandonii (Verbenaceae). Our results demonstrated significant variation among flower visitors in rates of visitation, pollen removal ability and contribution to fruit set. This variation was not always correlated; that is, taxa that regularly visited flowers did not remove the most pollen or contribute to fruit set. Despite the taxonomic diversity of visitors, the main natural pollinators of this shrub are large native bees, such as Bombus spp. Introduced honeybees were found to be as effective as native bees at pollinating this species. Duranta mandonii has high apparent generalization, but low realized generalization and can be considered to be a moderate ecological generalist (a number of species of large bees provide pollination services), but a functional specialist (most pollinators belong to a single functional group). The present study has highlighted the importance of measuring efficiency components when documenting plant–pollinator interactions, and has also demonstrated that visitation rates may give little insight into the relative importance of flower visitors.     

Foraging at a safe distance: crab spider effects on pollinators

1. The ability of pollinating insects to discover and evade their predators can affect plant–pollinator mutualisms and have cascading ecosystem effects. Pollinators will avoid flowers with predators, but it is not clear how far away they will move to continue foraging. If these distances are relatively small, the impact of predators on the plant–pollinator mutualism may be lessened. The plant could continue to receive some pollination, and pollinators would reduce the time and energy needed to search for another patch. 2. A native crab spider, Xysticus elegans, was placed on one cluster in a small array of Baccharis pilularis inflorescence clusters, and the preferred short‐range foraging distances of naturally visiting pollinators was determined. 3. Nearly all pollinator taxa (honey bees, wasps, other Hymenoptera, and non‐bombyliid flies) spent less time foraging on the predator cluster. 4. The key result of this study is that inflorescences within 90 mm of the crab spider were avoided by visiting honey bees and wasps, which spent three‐ and 18‐fold more time, respectively, foraging on more distant flower clusters. 5. Whether honey bees can use olfaction to detect spiders was then tested, and this study provides the first demonstration that honey bees will avoid crab spider odour alone at a food source.     

Compatibility and interaction between Bacillus thuringiensis and certain insecticides: perspective in management of Tuta absoluta (Lepidoptera: Gelechiidae)

Bacillus thuringiensis var. kurstaki (Berliner) (Bt) has been suggested as a biological control agent for Tuta absoluta (Meyrick). The objective of this study was to determine the interaction between abamectin, azadirachtin, indoxacarb, chlorantraniliprole, dichlorvos and metaflumizone with Bt. Effect of recommended doses of the chemical insecticides on colonisation of Bt was also investigated in culture medium. Except for metaflumizone, none of the chemicals tested reduced the colonisation of Bt compared with control. Interaction between Bt and the chemical insecticides on 2nd-instar larvae was also assessed. In interaction tests, Bt was applied at LC₅₀ level, 0, 12, 24 or 36 h after treating the larvae with LC₁₀ or LC₂₅ of the chemical insecticides. An antagonistic effect was observed in all treatments where Bt was applied immediately after the chemical insecticide. Also, antagonism was observed when treatment with Bt was done 12 h after azadirachtin and metaflumizone applications. Applying Bt 12 and 24 h after treatment with LC₂₅ of chlorantraniliprole, dichlorvos and abamectin resulted in synergism. But, synergism with LC₁₀ of dichlorvos and abamectin was observed only after 12 h. Additive effect was observed in the rest of the time and concentration combinations. Based on the results obtained, simultaneous use of the chemical insecticides tested and Bt is not recommended for T. absoluta control; and an appropriate time interval should be taken into consideration accordingly.     

Generalized food deception: colour signals and efficient pollen transfer in bee‐pollinated species of Eulophia (Orchidaceae)

Non‐rewarding plants use a variety of ruses to attract their pollinators. One of the least understood of these is generalized food deception, in which flowers exploit non‐specific food‐seeking responses in their pollinators. Available evidence suggests that colour signals, scent and phenology may all play key roles in this form of deception. Here we investigate the pollination systems of five Eulophia spp. (Orchidaceae) lacking floral rewards. These species are pollinated by bees, notably Xylocopa (Anthophorinae, Apidae) or Megachile (Megachilidae) for the large‐flowered species and anthophorid (Anthophorinae, Apidae) or halictid (Halictidae) bees for the small‐flowered species. Spectra of the lateral petals and ultraviolet‐absorbing patches on the labella are strongly contrasting in a bee visual system, which may falsely signal the presence of pollen to bees. All five species possess pollinarium‐bending mechanisms that are likely to limit pollinator‐mediated self‐pollination. Flowering times extend over 3–4 months and the onset of flowering was not associated with the emergence of pollinators, some of which fly year round. Despite sharing pollinators with other plants and lacking rewards that would encourage fidelity, the Eulophia spp. exhibited relatively high levels of pollen transfer efficiency compared with other rewarding and deceptive orchids. We conclude that the study species employ generalized food deception and exploit food‐seeking bees. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013 , 171 , 713–729.     

Supporting crop pollinators with floral resources: network‐based phenological matching

The production of diverse and affordable agricultural crop species depends on pollination services provided by bees. Indeed, the proportion of pollinator‐dependent crops is increasing globally. Agriculture relies heavily on the domesticated honeybee; the services provided by this single species are under threat and becoming increasingly costly. Importantly, the free pollination services provided by diverse wild bee communities have been shown to be sufficient for high agricultural yields in some systems. However, stable, functional wild bee communities require floral resources, such as pollen and nectar, throughout their active season, not just when crop species are in flower. To target floral provisioning efforts to conserve and support native and managed bee species, we apply network theoretical methods incorporating plant and pollinator phenologies. Using a two‐year dataset comprising interactions between bees (superfamily Apoidea, Anthophila) and 25 native perennial plant species in floral provisioning habitat, we identify plant and bee species that provide a key and central role to the stability of the structure of this community. We also examine three specific case studies: how provisioning habitat can provide temporally continuous support for honeybees (Apis mellifera) and bumblebees (Bombus impatiens), and how resource supplementation strategies might be designed for a single genus of important orchard pollinators (Osmia). This framework could be used to provide native bee communities with additional, well‐targeted floral resources to ensure that they not only survive, but also thrive.