Measuring bee diversity in different European habitats and biogeographical regions

Bee pollinators are currently recorded with many different sampling methods. However, the relative performances of these methods have not been systematically evaluated and compared. In response to the strong need to record ongoing shifts in pollinator diversity and abundance, global and regional pollinator initiatives must adopt standardized sampling protocols when developing large-scale and long-term monitoring schemes. We systematically evaluated the performance of six sampling methods (observation plots, pan traps, standardized and variable transect walks, trap nests with reed internodes or paper tubes) that are commonly used across a wide range of geographical regions in Europe and in two habitat types (agricultural and seminatural). We focused on bees since they represent the most important pollinator group worldwide. Several characteristics of the methods were considered in order to evaluate their performance in assessing bee diversity: sample coverage, observed species richness, species richness estimators, collector biases (identified by subunit-based rarefaction curves), species composition of the samples, and the indication of overall bee species richness (estimated from combined total samples). The most efficient method in all geographical regions, in both the agricultural and seminatural habitats, was the pan trap method. It had the highest sample coverage, collected the highest number of species, showed negligible collector bias, detected similar species as the transect methods, and was the best indicator of overall bee species richness. The transect methods were also relatively efficient, but they had a significant collector bias. The observation plots showed poor performance. As trap nests are restricted to cavity-nesting bee species, they had a naturally low sample coverage. However, both trap nest types detected additional species that were not recorded by any of the other methods. For large-scale and long-term monitoring schemes with surveyors with different experience levels, we recommend pan traps as the most efficient, unbiased, and cost-effective method for sampling bee diversity. Trap nests with reed internodes could be used as a complementary sampling method to maximize the numbers of collected species. Transect walks are the principal method for detailed studies focusing on plant-pollinator associations. Moreover, they can be used in monitoring schemes after training the surveyors to standardize their collection skills.

Comparative micromorphology of nectariferous and nectarless labellar spurs in selected clades of subtribe Orchidinae (Orchidaceae)

Floral nectar spurs are widely considered to influence pollinator behaviour in orchids. Spurs of 21 orchid species selected from within four molecularly circumscribed clades of subtribe Orchidinae (based on Platanthera s.l., Gymnadenia-Dactylorhiza s.l., Anacamptis s.l., Orchis s.s.) were examined under light and scanning electron microscopes in order to estimate correlations between nectar production (categorized as absent, trace, reservoir), interior epidermal papillae (categorized as absent, short, medium, long) and epidermal cell striations (categorized as apparently absent, weak, moderate, strong). Closely related congeneric species scored similarly, but more divergent species showed less evidence of phylogenetic constraints. Nectar secretion was negatively correlated with striations and positively correlated with papillae, which were especially frequent and large in species producing substantial reservoirs of nectar. We speculate that the primary function of the papillae is conserving energy through nectar resorption and explain the presence of large papillae in a minority of deceit-pollinated species by arguing that the papillae improve pollination because they are a tactile expectation of pollinating insects. In contrast, the prominence of striations may be a 'spandrel', simply reflecting the thickness of the overlying cuticle. Developmentally, the spur is an invagination of the labellum; it is primarily vascularized by a single 'U'-shaped primary strand, with smaller strands present in some species. Several suggestions are made for developing further, more targeted research programmes. (C) 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 160, 369-387.

Reconstruction of historical pollination rates reveals linked declines of pollinators and plants

Widespread reports of low pollination rates suggest a recent anthropogenic decline in pollination that could threaten natural and agricultural ecosystems. Nevertheless, unequivocal evidence for a decline in pollination over time has remained elusive because it was not possible to determine historical pollination rates. Here we demonstrate a widely applicable method for reconstructing historical pollination rates, thus allowing comparison with contemporary rates from the same sites. We focused on the relationship between the oil-collecting bee Rediviva peringueyi (Melittidae) and the guild of oil-secreting orchid species (Coryciinae) that depends on it for pollination. The guild is distributed across the highly transformed and fragmented lowlands of the Cape Region of South Africa. We show that rehydrated herbarium specimens of Pterygodium catholicum, the most abundant member of the guild, contain a record of past pollinator activity in the form of pollinarium removal rates. Analysis of a pollination time series showed a recent decline in pollination on Signal Hill, a small urban conservation area. The same herbaria contain historical species occurrence data. We analyzed this data and found that there has been a contemporaneous shift in orchid guild composition in urban areas due to the local extirpation of the non-clonal species, consistent with their greater dependence on seeds and pollination for population persistence.

Stability of pollination services decreases with isolation from natural areas despite honey bee visits

Sustainable agricultural landscapes by definition provide high magnitude and stability of ecosystem services, biodiversity and crop productivity. However, few studies have considered landscape effects on the stability of ecosystem services. We tested whether isolation from florally diverse natural and semi-natural areas reduces the spatial and temporal stability of flower-visitor richness and pollination services in crop fields. We synthesised data from 29 studies with contrasting biomes, crop species and pollinator communities. Stability of flower-visitor richness, visitation rate (all insects except honey bees) and fruit set all decreased with distance from natural areas. At 1 km from adjacent natural areas, spatial stability decreased by 25, 16 and 9% for richness, visitation and fruit set, respectively, while temporal stability decreased by 39% for richness and 13% for visitation. Mean richness, visitation and fruit set also decreased with isolation, by 34, 27 and 16% at 1 km respectively. In contrast, honey bee visitation did not change with isolation and represented > 25% of crop visits in 21 studies. Therefore, wild pollinators are relevant for crop productivity and stability even when honey bees are abundant. Policies to preserve and restore natural areas in agricultural landscapes should enhance levels and reliability of pollination services.

Quantifying the value of ecosystem services: a case study of honeybee pollination in the UK

There is concern that insect pollinators, such as honey bees, are currently declining in abundance, and are under serious threat from environmental changes such as habitat loss and climate change; the use of pesticides in intensive agriculture, and emerging diseases. This paper aims to evaluate how much public support there would be in preventing further decline to maintain the current number of bee colonies in the UK. The contingent valuation method (CVM) was used to obtain the willingness to pay (WTP) for a theoretical pollinator protection policy. Respondents were asked whether they would be WTP to support such a policy and how much would they pay? Results show that the mean WTP to support the bee protection policy was £1.37/week/household. Based on there being 24.9 million households in the UK, this is equivalent to £1.77 billion per year. This total value can show the importance of maintaining the overall pollination service to policy makers. We compare this total with estimates obtained using a simple market valuation of pollination for the UK.

Assessing bee species richness in two Mediterranean communities: importance of habitat type and sampling techniques

The decline of bees has raised concerns regarding their conservation and the maintenance of ecosystem services they provide to bee-pollinated wild flowers and crops. Although the Mediterranean region is a hotspot for bee species richness, their status remains poorly studied. There is an urgent need for cost-effective, reliable, and unbiased sampling methods that give good bee species richness estimates. This study aims: (a) to assess bee species richness in two common Mediterranean habitat types: semi-natural scrub (phrygana) and managed olive groves; (b) to compare species richness in those systems to that of other biogeographic regions, and (c) to assess whether six different sampling methods (pan traps, variable and standardized transect walks, observation plots and trap nests), previously tested in other European biogeographic regions, are suitable in Mediterranean communities. Eight study sites, four per habitat type, were selected on the island of Lesvos, Greece. The species richness observed was high compared to other habitat types worldwide for which comparable data exist. Pan traps collected the highest proportion of the total bee species richness across all methods at the scale of a study site. Variable and standardized transect walks detected the highest total richness over all eight study sites. Trap nests and observation plots detected only a limited fraction of the bee species richness. To assess the total bee species richness in bee diversity hotspots, such as the studied habitats, we suggest a combination of transect walks conducted by trained bee collectors and pan trap sampling

Pollinator community responses to the spatial population structure of wild plants: A pan-European approach

Land-use changes can alter the spatial population structure of plant species, which may in turn affect the attractiveness of flower aggregations to different groups of pollinators at different spatial scales. To assess how pollinators respond to spatial heterogeneity of plant distributions and whether honeybees affect visitation by other pollinators we used an extensive data set comprising ten plant species and their flower visitors from five European countries. In particular we tested the hypothesis that the composition of the flower visitor community in terms of visitation frequencies by different pollinator groups were affected by the spatial plant population structure, viz. area and density measures, at a within-population (‘patch’) and among-population (‘population’) scale. We found that patch area and population density were the spatial variables that best explained the variation in visitation frequencies within the pollinator community. Honeybees had higher visitation frequencies in larger patches, while bumblebees and hoverflies had higher visitation frequencies in sparser populations. Solitary bees had higher visitation frequencies in sparser populations and smaller patches. We also tested the hypothesis that honeybees affect the composition of the pollinator community by altering the visitation frequencies of other groups of pollinators. There was a positive relationship between visitation frequencies of honeybees and bumblebees, while the relationship with hoverflies and solitary bees varied (positive, negative and no relationship) depending on the plant species under study. The overall conclusion is that the spatial structure of plant populations affects different groups of pollinators in contrasting ways at both the local (‘patch’) and the larger (‘population’) scales and, that honeybees affect the flower visitation by other pollinator groups in various ways, depending on the plant species under study. These contrasting responses emphasize the need to investigate the entire pollinator community when the effects of landscape change on plant–pollinator interactions are studied.

Wild pollinators enhance fruit set of crops regardless of honey bee abundance

Diversity and abundance of wild-insect pollinators have declined in many agricultural landscapes. Whether such declines reduce crop yields, or are mitigated by managed pollinators such as honey bees, is unclear. Here, we show universally positive associations of fruit set with wild-insect visits to flowers in 41 crop systems worldwide, and thus clearly demonstrate their agricultural value. In contrast, fruit set increased significantly with visitation by honey bees in only 14% of the systems surveyed. Overall, wild insects pollinated crops more effectively, because increase in their visitation enhanced fruit set by twice as much as an equivalent increase in honey bee visitation. Further, visitation by wild insects and honey bees promoted fruit set independently, so high abundance of managed honey bees supplemented, rather than substituted for, pollination by wild insects. Our results suggest that new practices for integrated management of both honey bees and diverse wild-insect assemblages will enhance global crop yields.

Detecting insect pollinator declines on regional and global scales.

Recently there has been considerable concern about declines in bee communities in agricultural and natural habitats. The value of pollination to agriculture, provided primarily by bees, is >$200 billion/year worldwide, and in natural ecosystems it is thought to be even greater. However, no monitoring program exists to accurately detect declines in abundance of insect pollinators; thus, it is difficult to quantify the status of bee communities or estimate the extent of declines. We used data from 11 multiyear studies of bee communities to devise a program to monitor pollinators at regional, national, or international scales. In these studies, 7 different methods for sampling bees were used and bees were sampled on 3 different continents. We estimated that a monitoring program with 200–250 sampling locations each sampled twice over 5 years would provide sufficient power to detect small (2–5%) annual declines in the number of species and in total abundance and would cost U.S.$2,000,000. To detect declines as small as 1% annually over the same period would require >300 sampling locations. Given the role of pollinators in food security and ecosystem function, we recommend establishment of integrated regional and international monitoring programs to detect changes in pollinator communities.

Enhancement of buffer strips can improve provision of multiple ecosystem services

Farmland invertebrates play a pivotal role in the provision of ecosystem services, i.e. services that benefit humans. For example, bumblebees, solitary bees and honeybees, are crucial to the pollination of many of the world's crops and wildflowers, with over 70% of the world's major food crops dependent on the pollination services provided by these insects. The larvae of some butterfly species are considered to be pests; however, together with moth and sawfly larvae, they represent a key dietary component for many farmland birds. Spiders and ground beetles predate on crop pests including aphids, whilst soil macrofauna such as earthworms are vital for soil fertility services and nutrient recycling. Despite their importance, population declines of invertebrates have been observed during the last sixty years in the UK and NW Europe. For example, seven UK bumblebee species are in decline, and in the last 20 years, the species Bombus subterraneus (short-haired bumblebee) has become extinct, whilst there was a 54% decline in honeybee colony numbers in England from 1985 to 2005. Comparable trends have been documented for butterflies with a 23% decline in UK farmland species such as Anthocharis cardamines (orange tip) between 1990 and 2007. These declines have been widely attributed to the modern intensive arable management practices that have been developed to maximise crop yield. For example, loss and fragmentation of foraging and nesting habitats, including species-rich meadows and hedgerows, have been implicated in the decline of bees and butterflies. Increased use of herbicides and fertilisers has caused detrimental effects on many plant species with negative consequences for predatory invertebrates such as spiders and beetles which rely on plants for food and shelter.

Assessing continental-scale risks for generalist and specialist pollinating bee species under climate change

Increased risks of extinction to populations of animals and plants under changing climate have now been demonstrated for many taxa. This study assesses the extinction risks to species within an important genus of pollinating bees (Colletes: Apidae) by estimating the expected changes in the area and isolation of suitable habitat under predicted climatic condition for 2050. Suitable habitat was defined on the basis of the presence of known forage plants as well as climatic suitability. To investigate whether ecological specialisation was linked to extinction risk we compared three species which were generalist pollen foragers on several plant families with three species which specialised on pollen from a single plant species. Both specialist and generalist species showed an increased risk of extinction with shifting climate, and this was particularly high for the most specialised species (Colletes anchusae and C. wolfi). The forage generalist C. impunctatus, which is associated with Boreo-Alpine environments, is potentially threatened through significant reduction in available climatic niche space. Including the distribution of the principal or sole pollen forage plant, when modelling the distribution of monolectic or narrowly oligolectic species, did not improve the predictive accuracy of our models as the plant species were considerably more widespread than the specialised bees associated with them.

Convergent evolution of floral signals underlies the success of Neotropical orchids

The great majority of plant species in the tropics require animals to achieve pollination, but the exact role of floral signals in attraction of animal pollinators is often debated. Many plants provide a floral reward to attract a guild of pollinators, and it has been proposed that floral signals of non-rewarding species may converge on those of rewarding species to exploit the relationship of the latter with their pollinators. In the orchid family (Orchidaceae), pollination is almost universally animal-mediated, but a third of species provide no floral reward, which suggests that deceptive pollination mechanisms are prevalent. Here, we examine floral colour and shape convergence in Neotropical plant communities, focusing on certain food-deceptive Oncidiinae orchids (e.g. Trichocentrum ascendens and Oncidium nebulosum) and rewarding species of Malpighiaceae. We show that the species from these two distantly related families are often more similar in floral colour and shape than expected by chance and propose that a system of multifarious floral mimicry—a form of Batesian mimicry that involves multiple models and is more complex than a simple one model–one mimic system—operates in these orchids. The same mimetic pollination system has evolved at least 14 times within the species-rich Oncidiinae throughout the Neotropics. These results help explain the extraordinary diversification of Neotropical orchids and highlight the complexity of plant–animal interactions.