Abstract
During the study, the honeybee effects on wild bees were tested and hypothesized that smaller distances from beehives will increase competitions between honeybees and wild bees, while greater distances will have a deleterious effect on competition. The impact on species richness and diversity was tested with distances from beehives, considering that this may differ when large and small wild bee species are considered separately. Altogether 158 species and 13,164 individuals were collected, from which 72% (9,542 individuals) were Apis mellifera. High variation in abundances was detected from one year to another, and the species turnover by sites was 67% in site A, 66% in site V, and 63% in site F. This last one was the site with the previous contact with honeybees. Considering distances from beehives, significant decreases in small bee species diversity were detected from one year to another at each distance except site F, 250 m from hives. The changes in species diversity and community structure of small bee species are detected from one year to another.
Introduction
The current large-scale decline in the number of pollinating insects can have a negative impact on global food production and human wellbeing () since the quality and yield of many plants are based on the pollination by insects (). Nearly 45% of the most commonly grown plant species in the world depend on pollinators (). The role of bees in pollination is highly significant, as it is responsible for pollinating a large number of nutrient-rich plants important in human nutrition (). In the developed world, 14.7% of total agricultural production, and in the developing world, 22.6% (Aizen et al., 2009) are directly linked to bee activity, which is estimated to have annually a total value of €153 billion ().
It is a common practice to introduce managed pollination in order to meet the pollination need of plants by placing honeybee (Apis mellifera) colonies on specific areas (). The presence of wild bees in crop production is also significant even when the presence of honeybees is high because wild bee communities often prove to be more effective pollinators, and at the same time, interspecies interactions can increase pollination efficiency (; ; Woodcock et al., 2013). In seminatural landscapes, wild bees are the most important pollinators of flowering plants (). Diverse bee communities increase landscape biodiversity and provide steady pollination services (; ; ).
The diversity and density of wild bees are declining in many parts of the world due to habitat loss and habitat degradation, the use of chemicals, and the presence of parasites. Furthermore, due to intensive agriculture, croplands are less suitable for sustainable honey production, so professional beekeepers regularly move large apiaries to natural areas, either to exploit prosperous resources or to avoid chemical hazards or intermittent food shortages (Henry et al., 2012; ; Requier et al., 2017). As both honeybees and wild bees feed on nectar and pollen, it is not a recent concern that there might be a competition for food resources between the native wild bees and the artificially placed honeybees (Schaffer et al., 1983; ; Thomson, 2016; ; ).
Honeybees can negatively affect the reproduction of bumblebees (Thomson, 2004) and solitary bees () and can change the collection habits of bumblebees by displacing them from the area (Walther-Hellwig et al., 2006). In addition, bumblebee workers develop to a smaller size, probably due to malnutrition during the larval stage (). Due to these competitive effects, a total ban on beekeeping on nature reserves is more and more pronounced (; ; ; Saunders et al., 2018). Several studies have attempted to assess the effect of honeybees on wild bees, but some of them have failed to show significant competition (). According to this, in Europe, under natural conditions, competition between honeybees and bumblebees is unlikely, as both taxa are native. The foraging-related traits of bumblebees may differ from those of honeybees (Walther-Hellwig et al., 2006), as the tongue of the bumblebees is longer than that of the honeybees (), which allows for food niche separation (). An inclusive conservation approach would allow these conflicting hypotheses to be conciliated, involving all parties for sustainable results (). One such solution could be to regulate the density of apiaries with a maximum number of colonies of 3.1 colonies/km2 (Steffan-Dewenter and Tscharntke, 2000) or 3.5 colonies/km2 as suggested by another author (Torné-Noguera et al., 2016). Having the appropriate hive density in a given area is extremely difficult, as current apiaries often consist of 100–200 colonies. The appropriate density is furthermore influenced by the fact that honeybees can fly up to several kilometers, the hive density may depend on the density of wild pollinators, in addition, most nature reserves are not homogeneous, and available flowering plants vary seasonally and year by year.
Altogether more detailed researches are needed to test the effect of honeybees on wild bee species in “sensu lato” and effects on large and small bee species separately in highly diverse and protected habitats. By understanding these mechanisms, a better explanation of honeybee influences on wild bees and the habitat effect on these interactions can be explained. Thus, our hypotheses were as follows: H1. Honeybee effects on wild bees can be detected differently if distances from beehives are considered; smaller distances from beehives will increase competitions between honeybees and wild bees, while higher distances will have a deleterious effect on competition. H2. Exchange in species richness and diversity can be detected with distances from beehives, and this may differ when large and small wild bee species are considered separately.
Materials and Methods
Study Area and Sampling
This study was carried out between 2018 and 2019 in Central Europe (Transylvania), in Harghita and Covasna counties. Three seminatural protected, high nature value (HNV) areas were selected where extensive farming takes place, and the diversity and number of wild bees are extremely high, but the number of artificially placed honeybees (A. mellifera) is missing from two areas and is low in one area. The first area is the Vârghiş Valley area (coded as V) (N:46.2034539, E:25.5344264), which is a nature reserve, where prior to our research no artificially placed honeybees were introduced, and it is characterized by meadows and forest patches. The second one is the Almas-Meresti area (coded as A) (N:46.2394164, E:25.5322366) where again no artificially placed honeybees were present, and it is characterized by meadows, pastures, and forest patches. The third area is the Filia area (coded as F) (N:46.1731241, E:25.6236372), which was considered as the control area, honeybees have been present artificially in low density for 5 years, and this area is characterized by meadows, forest patches, and very few arable lands. The distances between the sampling areas were as follows: F–A 10 km; F–V 7 km; A–V 3.7 km. In all three areas, the average altitude is 530–630 m (Figure 1A).
FIGURE 1
The studied areas, which are located relatively far from the closest villages, and the complex natural habitat are diversely represented by small grassland-woodland-scrub mosaics. The grasslands are mainly used as meadows. Mowing on mosaic grassland patches was made at different times, providing a continuous food resource for pollinators. Although differences in plant diversity can be observed in the three areas, several plant species were common in all areas (Supplementary Material).
In all three valleys, sampling was performed four times in both 2018 and 2019 (i.e., one time in May, two times in June, and one time in July). The first assessment started in May and was made before the placement of honeybee colonies. Then, 7–10 days prior to the second assessment, 30 honeybee colonies were placed in each area; thus, during the second, third, and fourth assessments, honeybee colonies were present in all three areas. The average weight of a hive was 60–70 kg, and the bees populated 20 frames (300 mm/470 mm/37 mm) when hives were initially placed on these areas. Beehives were removed from the sites immediately after the last assessment and replaced next year in a same way.
The sampling area was a circle with a radius of 1,200 m around beehives and contained nine randomly selected subsampling sites. From these, three sampling sites were at a distance of 250 m, three at 500 m, and three at 1,500 m from beehives. Each assessment was made parallel (at each distance) by collecting for 20 min along a 200-m transect of all bee species using a sweep net. Then, the whole procedure was repeated two times at each distance (Figure 1B). All insects were stored in 70% ethanol, and species were identified in the laboratory.
Data Analyses
The collected species were divided into two groups, namely, bumblebees (referred to as large bees) and other wild bees (referred to as small bees), as these may show significant differences partly in social behavior and partly in home-range size (). The endangered status of the species was determined based on the European Red List (). To characterize the differences of wild bee communities between areas, we compared the species composition and also the k-dominance relationships. The data were averaged by sampling numbers (three sampling/distances/sampling period) and used for all analyses.
Analyses comparing abundances and diversity prior to hive placement and after hive placement in 2018 were performed. This makes sense for data collected in 2018 because the data from 2019 represent samples after hive placement in 2018. The Kruskal–Wallis test was performed to compare abundances. Alpha diversity profiles and diversity indices were computed using PAST version 4.02.
Mann–Whitney U test followed by Tukey’s pairwise comparisons were made to compare species numbers and abundances between years and distances from beehives inside each site. For this comparison, the data from the first sampling period in 2018 were incorporated. The densities of honeybees, large bees, and small bees were also compared between sites for all distances (i.e., 250, 500, and 1,500 m) using the same method. Diversity profiles at each distance and diversity T-test between years were computed for the entire wild bee community (Tóthmérész, 1995). The analyses were made using PAST version 4.02.
The effect of years, sites, and distances on honeybees, small bees, large bees, and endangered species (averaged data as mentioned above) was tested using each species group as a response variable and the sites, years, and distances as explanatory variables. Main effects as significant positive and negative relationships were defined at the level of P < 0.01.
The variation in the densities of honeybees as well as small and large bees for each site, year, and distance from beehives, respectively, were tested using repeated measures multivariate ANOVA (MANOVA). Interactions were then compared using χ2 tests on the differences between the covariance matrices and by the root mean square error of approximation. This comparison was made between the densities of honeybees and the densities of small and large bees for each distance separately. Due to the low density of endangered species, comparisons were made without statistical analyses, and differences were only mentioned according to the species and individual numbers. The statistical analyses were performed in R version 3.0.1 ().
The canonical correspondence analyses were used to test the effect of years and sites on wild bee species; in this study, sites and years were used as components and species abundances as variables. The analyses were made in PAST version 4.02.
Results
Altogether 158 species and 13,164 individuals were collected, from which 72% (9,542 individuals) were A. mellifera. Dominant large wild bee species were Bombus humilis (889 individuals), Bombus terrestris (874 individuals), Bombus pascuorum (225 individuals), Bombus hortorum (174 individuals), Bombus ruderarius (79 individuals), and Bombus sylvarum (67 individuals). Dominant small bee species were Andrena flavipes (152 individuals), Andrena ovatula (81 individuals), Lasioglossum calceatum (67 individuals), Eucera nigrescens (55 individuals), Eucera longicornis (53 individuals), and Halictus tumulorum (44 individuals).
No significant differences were detected in abundances and diversity between the first sampling period (prior to hive placement) and other sampling periods (after hive placement) in 2018 in all sites (Supplementary Material). Significant differences between abundances in the last sampling period and all others in site A 500 m, 1,500 m, and site V 250 m from hives were observed. Also, some differences in abundances at site F 250 m between the third sampling data and at 1,500 m between the fourth sampling data and all others were observed. The same differences can also be detected at diversity profiles and indices (Supplementary Material).
Some variation in species richness and abundances can be detected between sites, years, and distances from beehives when small and large bees are considered together in analyses. In site A at 250 m distances from beehives 45, at 500 m 43 species while at 1,500 m 42 wild bee species were detected in 2018, this was 43 (250 m), 30 (500 m), and 29 (1,500 m) in 2019, a significant reduction was detected at 500 and 1,500 m (Figure 2A). The same trend in site V was also detected with no differences in species numbers at 250 m (39 in 2018 and 29 in 2019), and a significant decrease was detected at 500 m (47 in 2018 and 28 in 2019) and at 1,500 m (65 in 2018 and only 18 in 2019) (Figure 2B). Again, no changes at 250 m in site F were detected (44 species in 2018 and 47 in 2019), and decreases at 500 m (50 species in 2018 and 36 in 2019) and at 1,500 m (45 in 2018 and 26 in 2019) were observed (Figure 2C). No such accentuated changes in abundances were detected; increase from 2018 to 2019 (from 181 to 228) in site A at 250 m, no changes at 500 m (208 and 200), and decrease at 1,500 m (from 256 to 171) were detected (Figure 2D). A decrease in site V at 500 m was only detected (from 336 to 214), while the same trend as in site A was observed in site F (Figures 2E,F). Significant differences in honeybee densities and any other wild bees were detected at 250 and 500 m between site A and sites V and F in both 2018 and 2019, while at 1,500 m, differences in honeybee densities in 2018 between site F and the other species in sites A and V were detected (Supplementary Material). The variations “sensu lato” of wild bee populations within years considering distances from beehives in each site separately were as follows:
FIGURE 2
Species richness by distances from beehives within years:
2018: site V small increase, no change in site A and F.
2019: site V no change, small decrease in site A, strong decrease in site F.
Abundance variations by distances from beehives within years:
2018: increase in all sites (strong in site A and small increase in sites V and F).
2019: no change in site V, small decrease in sites A and F.
The variations “sensu lato” of wild bee populations from one year to another considering distances from beehives in each site separately were as follows:
Species richness variations by distances from beehives between years:
Site A: 250 m no changes; 500 m decrease; 1,500 m decrease.
Site V: 250 m no changes; 500 m decrease; 1,500 m decrease.
Site F: 250 m no change; 500 m decrease; 1,500 m decrease.
Abundance variations by distances from beehives between years:
A: 250 m increase; 500 m no changes; 1,500 m decrease.
V: 250 m no change; 500 m decrease; 1,500 m no changes.
F: 250 m increase; 500 m no changes; 1,500 m decrease.
High change in species richness and composition and also in abundances was detected from one year to another, and the species exchange rates by sites were 67% in site A, 66% in site V, and 63% in site F. Considering again distances from beehives, a significant decrease in diversity was detected from one year to another at each distance except site F, 250 m from hives (F18/19, t = −0.35, P = 0.72) (Figures 3A–C).
FIGURE 3
Considering separately, the effects of honeybees on small and large bees for each site, year, and distance from beehives (MANOVA and χ2 test) revealed a significant decrease in small bee species richness at all distances and all sites from 2018 when experiments started in 2019. As an example, in site A, 34 species at 250 m and 500 m and 36 species at 1,500 m were detected in 2018, this was reduced to 26 species at 250, 18 at 500, and 19 at 1,500 m in 2019. No such trend in large bee species richness was observed (Figures 4A,B). More significant decreases in site V were detected from 2018 when 28, 35, and 51 species from small bees were collected in 2019, and when only 17 species at 250 and 500 m and seven species at 1,500 m were counted again, no such decreases of large bees were detected (Figures 4C,D). Also, a small decrease of small bees (38, 40, and 39 species in 2018 and 34, 24, and 16 species in 2019) and no change in large bees were observed in control site F (Figures 4E,F). Changes in abundances at small bees can also be detected from one year to another and no changes at large bees. No clear trend in species and abundance variations for endangered species was observed. Altogether the data present that honeybees, in general, had a negative effect on both small and large bees and on endangered species, but if years and distances from beehives are considered in analyses as explanatory variables and species group as a response variable, a significant negative effect on only small bees can be detected (Table 1).
FIGURE 4
TABLE 1
| Variables | Honeybees | Large bee species | Small bee species | Endangered bee species |
| Year | F = 0.19NS | F = 1.21NS | ↓F = 19.92*** | ↓F = 12.56*** |
| Sites | F = 1.01NS | F = 1.32NS | F = 0.78NS | F = 0.91NS |
| 250 m from hives | F = 0.81NS | F = 1.05NS | ↓F = 2.45** | ↑F = 2.67** |
| 500 m from hives | F = 1.34NS | F = 1.45NS | ↓F = 3.88** | F = 1.34NS |
| 1,500 m from hives | F = 1.78NS | F = 1.87NS | ↓F = 2.99** | F = 1.54NS |
| Honeybees | - | ↓F = 5.91** | ↓F = 10.18*** | ↓F = 4.89** |
| Large spec. | F = 0.79NS | - | F = 1.09NS | F = 0.33NS |
| Small spec. | F = 0.48NS | F = 0.38NS | - | F = 0.89NS |
| Endangered sp. | F = 0.71NS | F = 0.56NS | F = 0.34NS | - |
The effect of years, sites, and distances on honeybee, small bees, and large bees, respectively, on endangered species (relative proportion found in each sampling data) using each species group as a response variable and the sites, years, and distances as explanatory variables.
Arrows before value show the direction of main effects: ↑ indicates a positive relationship, and ↓ indicates a negative relationship. “-” shows where a term was not retained in the minimum adequate model. ***P < 0.001, **P < 0.01, NSdenotes not significant.
The canonical correspondence analyses revealed again high species richness variation between years when sites were considered as grouping factors (Figure 5A) but also when distances from beehives were considered as grouping factors (Figure 5B). In both cases, year effect determined 30% species distributions, while site effect was only representative at 20%.
FIGURE 5
Discussion
Altogether no general trend in decrease or increase in wild bee species richness and abundances was detected; however, wild bee abundances increased in 2018 with distances from beehives in all sites. While other similar researches clearly detected the negative influence of honeybees on wild bee species (), we cannot conclude such a very clear effect for all distances from beehives (especially when large wild bees are considered). This finding comes partially in concordance with our first hypothesis, such as wild bee species richness increasing with distances from beehives. This was clearly detected in 2018 at site V and less obvious in sites A and F. This can be due to the competition with honeybees; however, the trend has changed in 2019, decreases in abundances in sites A and F were detected with distances, and no changes in site V observed. The rapid change in the first year of contact with honeybees was observed, and the change in species diversity and community structure of wild bees (mostly small bee species) was detected. This new community structure in the next year was less sensible to the honeybees, and the effect with distances was not significant. This can be because European wild bee communities are more tolerant to honeybees, because A. mellifera is native in Eurasia. Even if no previous interactions were reported (in two of our sites), still the habitat and floral diversity may have delaying effects on competition. The long-term presence of honeybees in other habitats (our F site) has no significant negative effect in all cases on wild bee populations as niche overlap is not a forcing effect for food competition (; ).
Considering separately large and small bee species richness, a significant decay in species numbers can be detected only at small bee species but not at large ones. However, in the control area, we examined that (site F), where 60 families of honeybees have been regularly displaced during the season, the number of bumblebees was 70 and 48% lower in 2018 and 2019, respectively, compared to the other two study areas. In light of this research, it is possible that the long-term presence of the honeybee hive at the control site (site F) led to a decreased abundance of bumblebees. Generalist bees tend to be more significantly affected by honeybees than oligolectic bees (Wojcik et al., 2018). Thus, honeybees, which have been present in area F for a long time and in smaller numbers, were more likely to have a greater effect on bumblebees, reducing their numbers (Thomson, 2004) and causing bumblebees to avoid foraging areas where the numbers of honeybees were high, and thus, the lack of food sources or interference is also significant (Rogers et al., 2013). Other studies suggest that bumblebees are forced to select suboptimal foraging areas to avoid honeybees (Walther-Hellwig et al., 2006). In addition to the short-term and direct competitive effects mentioned above, competition with honeybees may have the long-term, multiyear effects on the bumblebee community through body size reduction and consequent changes in fecundity. Such an effect can be, for example, a slowing of the weight gain of the bumblebee colony and a decrease in the body size of queens and workers (). Body size plays an important role in winter hibernation in bumblebee queens, so a decrease in body size can also lead to a decrease in reproductive capacity in the long run ().
In addition to the decline in species number of small bees, a high exchange in species richness composition has been observed, and differences in species richness and diversity can also be detected from one year to another. This may be due to the competition, but the confirmation of this would require further research. However, in the case of small bees, even if their numbers have not decreased near apiaries, low levels of nectar and pollen can have a negative effect. found that the growth of Osmia bicornis was reduced in the presence of honeybees. The adult body size is directly determined by the amount of pollen and nectar consumed by the larva (). Smaller offsprings are more likely to die during development () and wintering (), and smaller individuals are less likely to find a nesting site (). Low levels of food sources can also increase the number of parasites in the nest (), as females spend more time obtaining food and therefore leave nests unattended for longer periods of time (Seidelmann, 2006).
In contrast, smaller bee species require less energy to fly and maintain nesting sites (). In addition, they require less pollen and nectar to raise offspring (). In areas where there are large apiaries, the amount of pollen and nectar may be sufficient for small bees but not sufficient for larger species, so these are forced to look for sufficient food somewhere further away or to broaden their food spectrum to other plants (; ), and thus, the wild bee community structure and species composition may change near the hives.
Other studies that are examining competition as a function of honeybee abundance found that competition was strongest near honeybees (usually within 800 m). Less or no effect was observed with increasing distance, suggesting that the effect of honeybees may be local (Steffan-Dewenter and Kuhn, 2003; Thomson, 2004; Walther-Hellwig et al., 2006). In this study, we did not find significant effects on abundance or species richness as a function of distance. The degree of competition and thus its direct effects may depend on the availability of resources, with significant impacts occurring only where resources are scarce, such as in the homogeneous agricultural intensification landscapes. However, competition can have less effect when abundant resources are available or when we study heterogeneous landscapes (Thomson, 2006; ; ). In addition to the heterogeneity of the landscape, the Apiary Influence Range (AIR) can vary seasonally depending on the amount of the flowering plants in the area (). Our study areas are characterized by high heterogeneity, and due to the extensive pasture and meadow farming, the naturalness and plant species richness of the areas are quite high (). Probably due to this, the direct short-term effects (i.e., variations from one year to another) of the competition (i.e., a decline in abundance and species richness) are not noticeable in the results of our studies. Also, no differences in abundances and diversity can be detected in 2018, comparing data prior to and after hive placement. Nevertheless, it is important to know that the mass presence of honeybees may have not only the short-term effects on wild bees: through offspring body size () and reducing fecundity (), possible food shortages may have the long-term negative effects on populations (similar to large bees, refer to the abovementioned contents).
In general, the effects of honeybees on wild bees are measured through which diversity and community structure from one year to another can be considered drastic (i.e., diversity values changed 63–67% between years depending on the site). In contrast, the honeybee can be considered native to the studied areas, so the community structure of the wild bees at the study sites probably was less sensible to the honeybee invasion. It may also be important that the relatively small number of bee colonies deployed for the experiments may not have been sufficient to exert a truly significant competitive effect. Some studies suggest that small apiaries have virtually no effect () or may develop a much less competitive situation (Requier et al., 2017). In such circumstances, the impact of honeybees on the wild bee community would probably be observed only in long term in such areas, so the long-term monitoring of the wild bee communities would be essential, even if only the 2-year assessments were allowed in these protected areas. It would also be important to examine whether the deployment of larger apiaries (100–200 families) has similarly mild consequences. Such studies could potentially determine the approximate amount of honeybee load in nature reserves that can still be tolerated by wild bee communities.
Publisher’s Note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Statements
Data availability statement
The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author/s.
Ethics statement
Ethical review and approval was not required for the animal study because working with bees does not require such approval.
Author contributions
AB took the lead in writing the manuscript, conducted the statistical analyses, and created the figures. ID and MS contributed to the writing and provided critical feedback on the manuscript, and planned and conducted the field experiments. All authors contributed to the article and approved the submitted version.
Funding
During the study, ID had a Ph.D. “Collegium Talentum” research grant from the Sapientia Hungariae Foundation. The research was also funded by TKP2020-NKA-16_One Health.
Acknowledgments
We would like to thank Zsolt Józan for identifying the sampled insects and the Asociaţia Speo-Turistică şi de Protecţia Naturii “Lumea Pierdută” Baraolt and Agenţia Naţională pentru Arii Naturale Protejate for the research permissions in the protected areas.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Supplementary material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fevo.2021.750236/full#supplementary-material
References
1
AizenM. A.GaribaldiL. A.CunninghamS. A.KleinA. M. (2009). How much does agriculture depend on pollinators? Lessons from long-term trends in crop production.Ann. Bot.1031579–1588. 10.1093/aob/mcp076
2
BabaiD.MolnárZ. (2014). Small-scale traditional management of highly species-rich grasslands in the Carpathians.Agric. Ecosyst. Environ.182123–130. 10.1016/j.agee.2013.08.018
3
BalfourN. J.GarbuzovM.RatnieksF. L. W. (2013). Longer tongues and swifter handling: why do more bumble bees (Bombus spp.) than honey bees (Apis mellifera) forage on lavender (Lavandula spp.)?Ecol. Entomol.38323–329. 10.1111/een.12019
4
BoschJ. (2008). Production of undersized offspring in a solitary bee.Anim. Behav.75809–816. 10.1016/j.anbehav.2007.06.018
5
BoschJ.KempW. (2002). Developing and establishing bee, species as crop pollinators: the example of Osmia spp. (Hymenoptera: Megachilidae) and fruit trees.Bull. Entomol. Res.923–16. 10.1079/BER2001139
6
BoschJ.VicensN. (2006). Relationship between body size, provisioning rate, longevity and reproductive success in females of the solitary bee Osmia cornuta.Behav. Ecol. Sociobiol.6026–33. 10.1007/s00265-005-0134-4
7
BrittainC.WilliamsN.KremenC.KleinA.-M. (2013). Synergistic effects of non-apis bees and honey bees for pollination services.Proc. R. Soc. B Biol. Sci.280:20122767. 10.1098/rspb.2012.2767
8
CouvillonM. J.SchürchR.RatnieksF. L. W. (2014). Waggle dance distances as integrative indicators of seasonal foraging challenges.PLoS One9:e93495. 10.1371/journal.pone.0093495
9
DannerN.MolitorA. M.SchieleS.HärtelS.Steffan-DewenterI. (2016). Season and landscape composition affect pollen foraging distances and habitat use of honey bees.Ecol. Appl.261920–1929. 10.1890/15-1840.1
10
EeraertsM.VanderhaegenR.SmaggheG.MeeusI. (2020). Pollination efficiency and foraging behaviour of honey bees and non-Apis bees to sweet cherry.Agric. For. Entomol.2275–82. 10.1111/afe.12363
11
ElbgamiT.KuninW. E.HughesW. O. H.BiesmeijerJ. C. (2014). The effect of proximity to a honeybee apiary on bumblebee colony fitness, development, and performance.Apidologie45504–513. 10.1007/s13592-013-0265-y
12
EllisA. M.MyersS. S.RickettsT. H. (2015). Do pollinators contribute to nutritional health?PLoS One10:e114805. 10.1371/journal.pone.0114805
13
GallaiN.SallesJ.-M.SetteleJ.VaissièreB. E. (2009). Economic valuation of the vulnerability of world agriculture confronted with pollinator decline.Ecol. Econ.68810–821. 10.1016/j.ecolecon.2008.06.014
14
GaribaldiL. A.RequierF.RollinO.AnderssonG. K. (2017). Towards an integrated species and habitat management of crop pollination.Curr. Opin. Insect Sci.21105–114. 10.1016/j.cois.2017.05.016
15
GaribaldiL. A.Steffan-DewenterI.WinfreeR.AizenM. A.BommarcoR.CunninghamS. A.et al (2013). Wild pollinators enhance fruit set of crops regardless of honey bee abundance.Science3391608–1611. 10.1126/science.1230200
16
GathmannA.GreilerH.-J.TscharntkeT. (1994). Trap-nesting bees and wasps colonizing set-aside fields: succession and body size, management by cutting and sowing.Oecologia988–14. 10.1007/BF00326084
17
GeldmannJ.González-VaroJ. P. (2018). Conserving honey bees does not help wildlife.Science359392–393. 10.1126/science.aar2269
18
GeslinB.GauzensB.BaudeM.DajozI.FontaineC.HenryM.et al (2017). “Chapter four - massively introduced managed species and their consequences for plant–pollinator interactions,” in Advances in Ecological Research Networks of Invasion: Empirical Evidence and Case Studies, edsBohanD. A.DumbrellA. J.MassolF. (Cambridge, MA: Academic Press), 147–199. 10.1016/bs.aecr.2016.10.007
19
González-VaroJ. P.GeldmannJ. (2018). Response—“Bee conservation: key role of managed bees” and “Bee conservation: inclusive solutions.”Science360390–390. 10.1126/science.aat3746
20
GoodellK. (2003). Food availability affects Osmia pumila (Hymenoptera: Megachilidae) foraging, reproduction, and brood parasitism.Oecologia134518–527. 10.1007/s00442-002-1159-2
21
GoulsonD.SparrowK. R. (2009). Evidence for competition between honeybees and bumblebees; effects on bumblebee worker size.J. Insect Conserv.13177–181. 10.1007/s10841-008-9140-y
22
GreenleafS. S.WilliamsN. M.WinfreeR.KremenC. (2007). Bee foraging ranges and their relationship to body size.Oecologia153589–596. 10.1007/s00442-007-0752-9
23
GuedotC.BoschJ.KempW. (2009). Relationship between body size and homing ability in the genus Osmia (Hymenoptera; Megachilidae).Ecol. Entomol.34158–161. 10.1111/j.1365-2311.2008.01054.x
24
HabelJ. C.SamwaysM. J.SchmittT. (2019). Mitigating the precipitous decline of terrestrial European insects: requirements for a new strategy.Biodivers. Conserv.281343–1360. 10.1007/s10531-019-01741-8
25
HeinrichB. (1975). Energetics of pollination.Annu. Rev. Ecol. Syst.6139–170. 10.1146/annurev.es.06.110175.001035
26
HenryM.RodetG. (2020). The apiary influence range: a new paradigm for managing the cohabitation of honey bees and wild bee communities.Acta Oecol.105:103555. 10.1016/j.actao.2020.103555
27
HenryM.BéguinM.RequierF.RollinO.OdouxJ.-F.AupinelP.et al (2012). A common pesticide decreases foraging success and survival in honey bees.Science336348–350. 10.1126/science.1215039
28
HerbertssonL.LindströmS. A. M.RundlöfM.BommarcoR.SmithH. G. (2016). Competition between managed honeybees and wild bumblebees depends on landscape context.Basic Appl. Ecol.17609–616. 10.1016/j.baae.2016.05.001
29
HoehnP.TscharntkeT.TylianakisJ. M.Steffan-DewenterI. (2008). Functional group diversity of bee pollinators increases crop yield.Proc. R. Soc. B Biol. Sci.2752283–2291. 10.1098/rspb.2008.0405
30
HudewenzA.KleinA.-M. (2015). Red mason bees cannot compete with honey bees for floral resources in a cage experiment.Ecol. Evol.55049–5056. 10.1002/ece3.1762
31
KleijnD.BiesmeijerK.DupontY. L.NielsenA.PottsS. G.SetteleJ. (2018). Bee conservation: inclusive solutions.Science360389–390. 10.1126/science.aat2054
32
KleinA.-M.VaissièreB. E.CaneJ. H.Steffan-DewenterI.CunninghamS. A.KremenC.et al (2007). Importance of pollinators in changing landscapes for world crops.Proc. R. Soc. B Biol. Sci.274303–313. 10.1098/rspb.2006.3721
33
LindströmS. A. M.HerbertssonL.RundlöfM.BommarcoR.SmithH. G. (2016). Experimental evidence that honeybees depress wild insect densities in a flowering crop.Proc. R. Soc. B Biol. Sci.283:20161641. 10.1098/rspb.2016.1641
34
MacInnisG.ForrestJ. R. K. (2020). Field design can affect cross-pollination and crop yield in strawberry (Fragaria x ananassa D.).Agric. Ecosyst. Environ.289:106738. 10.1016/j.agee.2019.106738
35
MagrachA.González-VaroJ. P.BoiffierM.VilàM.BartomeusI. (2017). Honeybee spillover reshuffles pollinator diets and affects plant reproductive success.Nat. Ecol. Evol.11299–1307. 10.1038/s41559-017-0249-9
36
MallingerR. E.Gaines-DayH. R.GrattonC. (2017). Do managed bees have negative effects on wild bees?: a systematic review of the literature.PLoS One12:e0189268. 10.1371/journal.pone.0189268
37
MüllerA.ProsiR.PrazC.RichterH. (2019). Nesting in bark – the peculiar life history of the rare boreoalpine osmiine bee Osmia (Melanosmia) nigriventris (Hymenoptera, Megachilidae).Alp. Entomol.3105–119. 10.3897/alpento.3.34409
38
NietoA.RobertsS.KempJ.RasmontP.KuhlmannM.García CriadoM.et al (2014). European Red List of Bees.Luxembourg: Publication Office of the European Union, 10.2779/77003
39
OdouxJ.-F.AupinelP.GateffS.RequierF.HenryM.BretagnolleV. (2014). ECOBEE: a tool for long-term honey bee colony monitoring at the landscape scale in West European intensive agroecosystems.J. Apic. Res.5357–66. 10.3896/IBRA.1.53.1.05
40
PainiD. (2004). Impact of the introduced honey bee (Apis mellifera) (Hymenoptera: Apidae) on native bees: a review.Austral Ecol.29399–407. 10.1111/j.1442-9993.2004.01376.x
41
PottsS. G.BiesmeijerJ. C.KremenC.NeumannP.SchweigerO.KuninW. E. (2010). Global pollinator declines: trends, impacts and drivers.Trends Ecol. Evol.25345–353. 10.1016/j.tree.2010.01.007
42
PottsS. G.Imperatriz-FonsecaV.NgoH. T.AizenM. A.BiesmeijerJ. C.BreezeT. D.et al (2016). Safeguarding pollinators and their values to human well-being.Nature540220–229. 10.1038/nature20588
43
R Core Team (2013). A Language and Environment for Statistical Computing.Vienna: R Foundation for Statistical Computing.
44
RantaE.LundbergH. (1980). Resource partitioning in bumblebees: the significance of differences in proboscis length.Oikos35298–302. 10.2307/3544643
45
RequierF.OdouxJ.-F.HenryM.BretagnolleV. (2017). The carry-over effects of pollen shortage decrease the survival of honeybee colonies in farmlands.J. Appl. Ecol.541161–1170. 10.1111/1365-2664.12836
46
RogersS.CajamarcaP.TarpyD.BurrackH. (2013). Honey bees and bumble bees respond differently to inter- and intra-specific encounters.Apidologie44621–629. 10.1007/s13592-013-0210-0
47
SaundersM. E.SmithT. J.RaderR. (2018). Bee conservation: key role of managed bees.Science360389–389. 10.1126/science.aat1535
48
SchafferW. M.ZehD. W.BuchmannS. L.KleinhansS.SchafferM. V.AntrimJ. (1983). Competition for nectar between Introduced honey bees and native North American bees and ants.Ecology64564–577. 10.2307/1939976
49
SeidelmannK. (2006). Open-cell parasitism shapes maternal investment patterns in the Red Mason bee Osmia rufa.Behav. Ecol.17839–848. 10.1093/beheco/arl017
50
Steffan-DewenterI.KuhnA. (2003). Honeybee foraging in differentially structured landscapes.Proc. Biol. Sci.270569–575. 10.1098/rspb.2002.2292
51
Steffan-DewenterI.TscharntkeT. (2000). Resource overlap and possible competition between honey bees and wild bees in central Europe.Oecologia122288–296. 10.1007/s004420050034
52
ThomsonD. (2004). Competitive interactions between the invasive european honey bee and native bumble bees.Ecology85458–470.
53
ThomsonD. M. (2006). Detecting the effects of introduced species: a case study of competition between Apis and Bombus.Oikos114407–418. 10.1111/j.2006.0030-1299.14604.x
54
ThomsonD. M. (2016). Local bumble bee decline linked to recovery of honey bees, drought effects on floral resources.Ecol. Lett.191247–1255. 10.1111/ele.12659
55
Torné-NogueraA.RodrigoA.OsorioS.BoschJ. (2016). Collateral effects of beekeeping: Impacts on pollen-nectar resources and wild bee communities.Basic Appl. Ecol.17199–209. 10.1016/j.baae.2015.11.004
56
TóthmérészB. (1995). Comparison of different methods for diversity ordering.J. Veg. Sci.6283–290. 10.2307/3236223
57
Walther-HellwigK.FokulG.FranklR.BüchlerR.EkschmittK.WoltersV. (2006). Increased density of honeybee colonies affects foraging bumblebees.Apidologie37517–532. 10.1051/apido:2006035
58
WojcikV. A.MorandinL. A.Davies AdamsL.RourkeK. E. (2018). Floral resource competition between honey bees and wild bees: is there clear evidence and can we guide management and conservation?Environ. Entomol.47822–833. 10.1093/ee/nvy077
59
WoodcockB. A.EdwardsM.RedheadJ.MeekW. R.NuttallP.FalkS.et al (2013). Crop flower visitation by honeybees, bumblebees and solitary bees: behavioural differences and diversity responses to landscape.Agric. Ecosyst. Environ.1711–8. 10.1016/j.agee.2013.03.005
Summary
Keywords
Apis mellifera, small bees, large bees, diversity, change in community structure, high natural value habitats
Citation
Demeter I, Balog A and Sárospataki M (2021) Variation of Small and Large Wild Bee Communities Under Honeybee Pressure in Highly Diverse Natural Habitats. Front. Ecol. Evol. 9:750236. doi: 10.3389/fevo.2021.750236
Received
30 July 2021
Accepted
03 November 2021
Published
02 December 2021
Volume
9 - 2021
Edited by
Michael Hrncir, University of São Paulo, Brazil
Reviewed by
Victoria Wojcik, Pollinator Partnership Canada, Canada; Sándor Keszthelyi, University of Kaposvár, Hungary
Updates
Copyright
© 2021 Demeter, Balog and Sárospataki.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Adalbert Balog, adalbert.balog@ms.sapientia.roMiklós Sárospataki, Sarospataki.Miklos@uni-mate.hu
This article was submitted to Conservation and Restoration Ecology, a section of the journal Frontiers in Ecology and Evolution
Disclaimer
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.