Ecological and life-history traits predict bee species responses to environmental disturbances

The ability to predict the responses of ecological communities and individual species to human-induced environmental change remains a key issue for ecologists and conservation managers alike. Responses are often variable among species within groups making general predictions difficult. One option is to include ecological trait information that might help to disentangle patterns of response and also provide greater understanding of how particular traits link whole clades to their environment. Although this ‘‘trait-guild” approach has been used for single disturbances, the importance of particular traits on general responses to multiple disturbances has not been explored. We used a mixed model analysis of 19 data sets from throughout the world to test the effect of ecological and life-history traits on the responses of bee species to different types of anthropogenic environmental change. These changes included habitat loss, fragmentation, agricultural intensification, pesticides and fire. Individual traits significantly affected bee species responses to different disturbances and several traits were broadly predictive among multiple disturbances. The location of nests – above vs. below ground – significantly affected response to habitat loss, agricultural intensification, tillage regime (within agriculture) and fire. Species that nested above ground were on average more negatively affected by isolation from natural habitat and intensive agricultural land use than were species nesting below ground. In contrast below-ground-nesting species were more negatively affected by tilling than were above-ground nesters. The response of different nesting guilds to fire depended on the time since the burn. Social bee species were more strongly affected by isolation from natural habitat and pesticides than were solitary bee species. Surprisingly, body size did not consistently affect species responses, despite its importance in determining many aspects of individuals’ interaction with their environment. Although synergistic interactions among traits remain to be explored, individual traits can be useful in predicting and understanding responses of related species to global change.

Convergent evolution: floral guides, stingless bee nest entrances, and insectivorous pitchers

Several recent hypotheses, including sensory drive and sensory exploitation, suggest that receiver biases may drive selection of biological signals in the context of sexual selection. Here we suggest that a similar mechanism may have led to convergence of patterns in flowers, stingless bee nest entrances, and pitchers of insectivorous plants. A survey of these non-related visual stimuli shows that they share features such as stripes, dark centre, and peripheral dots. Next, we experimentally show that in stingless bees the close-up approach to a flower is guided by dark centre preference. Moreover, in the approach towards their nest entrance, they have a spontaneous preference for entrance patterns containing a dark centre and disrupted ornamentation. Together with existing empirical evidence on the honeybee's and other insects' orientation to flowers, this suggests that the signal receivers of the natural patterns we examined, mainly Hymenoptera, have spontaneous preferences for radiating stripes, dark centres, and peripheral dots. These receiver biases may have evolved in other behavioural contexts in the ancestors of Hymenoptera, but our findings suggest that they have triggered the convergent evolution of visual stimuli in floral guides, stingless bee nest entrances, and insectivorous pitchers.

Landscape context and habitat type as drivers of bee diversity in European annual crops

To better understand the dynamics of bee populations in crops, we assessed the effect of landscape context and habitat type on bee communities in annual entomophilous crops in Europe. We quantified bee communities in five pairs of crop-country: buckwheat in Poland, cantaloupe in France, field beans in the UK, spring oilseed rape in Sweden, and strawberries in Germany. For each country, 7-10 study fields were sampled over a gradient of increasing proportion of semi-natural habitats in the surrounding landscape. The CORINE land cover classification was used to characterize the landscape over a 3 km radius around each study field and we used multivariate and regression analyses to quantify the impact of landscape features on bee abundance and diversity at the sub-generic taxonomic level. Neither overall wild bee abundance nor diversity, taken as the number of sub-genera. was significantly affected by the proportion of semi-natural habitat. Therefore, we used the most precise level of the CORINE classification to examine the possible links between specific landscape features and wild bee communities. Bee community composition fell into three distinct groups across Europe: group I included Poland, Germany, and Sweden, group 2 the UK, and group 3 France. Among all three groups, wild bee abundance and sub-generic diversity were affected by 17 landscape elements including some semi-natural habitats (e.g., transitional wood land-shrub), some urban habitats (e.g., sport and leisure facilities) and some crop habitats (e.g., non-irrigated arable land). Some bee taxa were positively affected by urban habitats only, others by semi-natural habitats only, and others by a combination of semi-natural, urban and crop habitats. Bee sub-genera favoured by urban and crop habitats were more resistant to landscape change than those favoured only by semi-natural habitats. In agroecosystems, the agricultural intensification defined as the loss of semi-natural habitats does not necessarily cause a decline in evenness at the local level, but can change community composition towards a bee fauna dominated by common taxa. (C) 2009 Elsevier B.V. All rights reserved.

Taxonomical vs. functional responses of bee communities to fire in two contrasting climatic regions

Valuable insights into mechanisms of community responses to environmental change can be gained by analysing in tandem the variation in functional and taxonomic composition along environmental gradients. We assess the changes in species and functional trait composition (i.e. dominant traits and functional diversity) of diverse bee communities in contrasting fire-driven systems in two climatic regions: Mediterranean (scrub habitats in Israel) and temperate (chestnut forests in southern Switzerland). In both climatic regions, there were shifts in species diversity and composition related to post-fire age. In the temperate region, functional composition responded markedly to fire; however, in the Mediterranean, the taxonomic response to fire was not matched by functional replacement. These results suggest that greater functional stability to fire in the Mediterranean is achieved by replacement of functionally similar species (i.e. functional redundancy) which dominate under different environmental conditions in the heterogeneous landscapes of the region. In contrast, the greater functional response in the temperate region was attributed to a more rapid post-fire vegetation recovery and shorter time-window when favourable habitat was available relative to the Mediterranean. Bee traits can be used to predict the functional responses of bee communities to environmental changes in habitats of conservation importance in different regions with distinct disturbance regimes. However, predictions cannot be generalized from one climatic region to another where distinct habitat configurations occur.

Role of nesting resources in organising diverse bee communities in a Mediterranean landscape

1. The habitat components determining the structure of bee communities are well known when considering foraging resources; however, there is little data with respect to the role of nesting resources. 2. As a model system this study uses 21 diverse bee communities in a Mediterranean landscape comprising a variety of habitats regenerating after fire. The findings clearly demonstrate that a variety of nesting substrates and nest building materials have key roles in organising the composition of bee communities. 3. The availability of bare ground and potential nesting cavities were the two primary factors influencing the structure of the entire bee community, the composition of guilds, and also the relative abundance of the dominant species. Other nesting resources shown to be important include availability of steep and sloping ground, abundance of plant species providing pithy stems, and the occurrence of pre-existing burrows. 4. Nesting resource availability and guild structure varied markedly across habitats in different stages of post-fire regeneration; however, in all cases, nest sites and nesting resources were important determinants of bee community structure.

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.

Effect of water stress on infection by species of honey fungus (Armillaria mellea and A. gallica)

Isolates of Armillaria mellea and A. gallica that differed in virulence to healthy blackcurrant, strawberry, Lawson cypress and privet were used to inoculate plants exposed to different watering regimes. Host plants from which water had either been withheld or their roots kept constantly flooded with water, both showed increased susceptibility compared to those plants, which had been watered regularly. At the end of the period of stress, roots from randomly selected plants from each treatment were harvested. Following chemical analysis of the roots for protein, lipids, and carbohydrates including starch, in vitro assays were carried out with these substances. The increased amounts of these nutrients in both groups of stressed plants are sufficient to stimulate the growth of both A. mellea and A. gallica and enhance their virulence.

In vitro investigation into the potential prebiotic activity of honey oligosaccharides

The effect of honey oligosaccharides on the growth of fecal bacteria was studied using an in vitro fermentation system. Prior to treatment, glucose and fructose (31.73 and 21.41 g/100 g of product, respectively) present in honey, which would be digested in the upper gut, were removed to avoid any influence on bacterial populations in the fermentations. Nanofiltration, yeast (Saccharomyces cerevisiae) treatment, and adsorption onto activated charcoal were used to remove monosaccharides. Prebiotic (microbial fermentation) activities of the three honey oligosaccharide fractions and the honey sample were studied and compared with fructooligosaccharide (FOS), using 1% (w/v) fecal bacteria in an in vitro fermentation system (10 mg of carbohydrate, 1.0 mL of basal medium). A prebiotic index (PI) was calculated for each carbohydrate source. Honey oligosaccharides seem to present potential prebiotic activity (PI values between 3.38 and 4.24), increasing the populations of bifidobacteria and lactobacilli, although not to the levels of FOS (PI of 6.89).

A contribution to the differentiation between nectar honey and honeydew honey

Thirty genuine honey samples were analyzed for pH, acidity, water, ash, net absorbance, total polyphenols (Folin-Ciocalteau method) and glucose, fructose, melezitose and erlose (as their trimethylsilyl oximes and trimethylsilyl ethers) by capillary gas chromatography. The resulting data were used, along with palynological analysis, to characterize the samples in relation to their possible source (nectar, honeydew and mixture honeys). Some minor components (carboxylic acids and cyclitols), eluting before monosaccharides, were also determined. One of these compounds was quercitol (1,3,4/2,5-cyclohexane-pentol), a deoxyinositol which has been previously determined in Quercus sp. samples. Quercitol was present in a broad concentration range (0.01-1.50 g/100 g) in honeys whose major source was honeydew but it was never higher than 0.01 g/100 g in samples characterized as nectar honeys. Quercitol concentrations appear to be related to the presence and amount of Quercus sp. honeydew as honey source, although further research is required to confirm this. (C) 2004 Elsevier Ltd. All rights reserved.

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

Altitude acts as an environmental filter on phylogenetic composition, traits and diversity in bee communities.

Knowledge about the phylogeny and ecology of communities along environmental gradients helps to disentangle the role of competition-driven processes and environmental filtering for community assembly. In this study, we evaluated patterns in species richness, phylogenetic structure and life-history traits of bee communities along altitudinal gradients in the Alps, Germany. We found a linear decline in species richness and abundance but increasing phylogenetic clustering in communities with increasing altitude. The proportion of social- and ground-nesting species, as well as mean body size and altitudinal range of bee communities, increased with increasing altitude, whereas the mean geographical distribution decreased. Our results suggest that community assembly at high altitudes is dominated by environmental filtering effects, whereas the relative importance of competition increases at low altitudes. We conclude that inherent phylogenetic and ecological species attributes at high altitudes pose a threat for less competitive alpine specialists with ongoing climate change.

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.