Non-Apis bees as model organisms in laboratory, semi-field and field experiments
Non-Apis Bienen als Modelorganismen in Labor-, Halbfreiland- und Freilandversuchen
Journal für Kulturpflanzen, 72 (5). S. 162–172, 2020, ISSN 1867-0911, DOI: 10.5073/JfK.2020.05.06, Verlag Eugen Ulmer KG, Stuttgart
As part of the registration process of plant protection products (PPPs) and their active substances in the EU, the risk of PPPs for bees has been assessed so far by using the European honey bee (Apis mellifera L.) as a surrogate species. In the past few years other bee species have been discussed to augment data on honey bees. The addition of bee species in the registration process goes along with adapting test methodologies to new bee species and understanding how to use these species at different tiers (laboratory, semi-field and field levels). Here we first discuss the importance of bees as test organisms, outline the current state of research relevant to the methodology and design of experiments with bees and highlight recent activities in the standardization of test procedures.
Key words: honey bee, bumble bees, solitary bees, ecotoxicology, risk assessment, sensitivity, method development
Im Rahmen der Zulassung von Pflanzenschutzmitteln und ihren Wirkstoffen in der EU wurde das Risiko für Bienen bisher anhand der Westlichen Honigbiene (Apis mellifera L.) als Modellorganismus für alle Bienenarten bewertet. In den letzten Jahren wurde kontrovers diskutiert, ob Wildbienenarten in der Risikobewertung ebenfalls berücksichtigt werden sollten, um die bisherigen Datenanforderungen für Honigbienen zu erweitern. Dies geht damit einher, etablierte, standardisierte Methoden für die Honigbiene an zusätzliche Wildbienenarten anzupassen und zu verstehen, wie diese Arten auf den verschiedenen Testebenen (Labor-, Halbfreiland- und Freilandtests) eingesetzt werden können. In diesem Artikel gehen wir zunächst auf die Bedeutung von Bienen als Testorganismen ein, diskutieren den derzeitigen Stand der Forschung, die für die Methodenentwicklung und das experimentelle Design für das Arbeiten mit Bienen wichtig ist, um abschließend einen Ausblick auf aktuelle Aktivitäten in der Standardisierung von Testmethoden zu geben.
Stichwörter: Honigbiene, Hummeln, Solitärbienen, Ökotoxikologie, Risikobewertung, Sensitivität, Methodenentwicklung
Pollinators are an integral part of global biodiversity; insects – primarily bees – are the most prominent pollinator group of many crops and wild plants (Potts et al., 2010). As a domesticated species, European honey bees (Apis mellifera L., Hymenoptera: Apidae) are economically important pollinators (Morse and Calderone, 2000; Mwebaze et al., 2010; Bartomeus et al., 2014; Oré Barrios et al., 2017). However, the great majority of bee species are non-Apis bees that display varying levels of sociality (Michener, 2007). Germany hosts almost 600 wild bee species (Westrich et al., 2011) including colony-building bumble bees as well as ground-nesting and hole-nesting solitary bee species. Wild bee species contribute significantly to crop pollination (Klein et al., 2007; Garibaldi et al., 2013), and many of them forage and nest in agricultural landscapes. An increase in their abundance and diversity can increase crop productivity (Venturini et al., 2017; Catarino et al., 2019 but Bartomeus et al., 2014). The exact number of wild bee species using agricultural landscapes has yet to be estimated for the different regions of Germany (and worldwide). Bees in agricultural landscapes are exposed to a variety of stressors, which are recognized as drivers of wild bee declines and honey bee colony losses (Goulson et al., 2015). It is essential to reduce and regulate these factors in order to maintain or increase ecological and economic benefits.
Plant protection products (PPPs) are one of the stressors identified as a major driver for bee declines (Sánchez-Bayo and Wyckhuys, 2019). Depending on the geographical and political region, their legalization and use with respect to their environmental impact is policed by regulatory authorities, e.g. the United States Environmental Protection Agency (USEPA), Brazilian Institute of the Environment and Renewable Natural Resources (IBAMA) and Australian Pesticide and Veterinary Medicines Authority (APVMA) (Handford et al., 2015). In this review, we focus on the legislative framework and schemes applied in Europe. Within the European Union, PPPs are regulated by means of the registration process of plant protection products and their active substances (European Parliament, Council of the European Union, 2009). This process involves the evaluation of hazards of PPPs to beneficial insects, including bees, based on a specific use and employing standardized test procedures. So far, these tests are designed to use the European honey bee as a surrogate species for all bee species.
After the publication of the EFSA Bee Guidance Document (European Food Safety Authority, 2013) and of a growing number of studies that showed losses of insect diversity and abundance (Biesmeijer et al., 2006; Hallmann et al., 2017; Seibold et al., 2019), the discussion about other surrogate species in the risk assessment procedure became more intense (e.g. Boyle et al., 2019). First attempts were made to expand and adapt the existing guidelines to other bee species, especially bumble bees and solitary bees (Fischer and Moriarty, 2011; Rortais et al., 2017). While the process has not implemented the use of other bee species on a regular basis, new guidelines were recently adopted to assess risks for bumble bees (Apidae: Bombus terrestris) (OECD, 2017b, 2017c) and in the future for solitary bees (Apidae: Osmia bicornis) (OECD, 2019b).
As discussed above, testing European honey bees as a model organism for bees in general has been the usual way of evaluation, and test methods for honey bees in the laboratory, under semi-field and field conditions have been well-established (Eppo, 2010). They include acute and chronic exposure tests of adult honey bees (OECD, 1998a, 1998b, 2017a) and honey bee larvae (OECD, 2013, 2016), and a test on honey bee development (OECD, 2007). Honey bees are eusocial insects that form perennial colonies with many thousands of individuals. Consequently, they can be repeatedly sampled for individual bees almost year-round, are commercially available, are widely distributed and are therefore ideally suited for experimental usage (Thompson and Pamminger, 2019).
A proper risk assessment of pesticides to bees must integrate two aspects: (a) the toxicity of the pesticide and (b) the probability of exposure (van der Valk et al., 2013). Toxicity of pesticides to non-Apis bees has been suggested to be extrapolatable from data on honey bees (Heard et al., 2017; Lewis and Tzilivakis, 2019; Reid et al., 2020; Thompson and Pamminger, 2019). However, honey bee LD50 values may not always be good predictors across different bee species (Mayack and Boff, 2019), and sensitivity among different taxa can be variable (Arena and Sgolastra, 2014; Lewis and Tzilivakis, 2019) and dependent e.g. on body mass (Thompson, 2016). Even if toxicity data can be extrapolated, there might be still a need for higher tier experiments to account for different exposure probabilities in a realistic setting (Thompson, 2016).
The probability of exposure to PPPs depends not only on the intensity of agricultural practice but also on certain aspects of bee biology including nest location and foraging range as well as time, period of day and number of days when foraging (Brittain and Potts, 2011; van der Valk et al., 2013). Exposure risks to non-Apis bees from PPPs is assumed to be similar or higher than to the European honey bee (Table 1), but in most cases there are still major data gaps that complicate an assessment (Roubik, 2014).
Table 1. Potential exposure routes and their relative importance to European bees (adopted from Fischer and Moriarty, 2011, extended by additional information (Gradish et al., 2019; Sgolastra et al., 2019)); – = no potential exposure; + = low potential exposure; ++ = medium potential exposure; +++ = high potential exposure
European honey bees
+ to +++
+ to +++
++ to +++
+ to +++
+ to +++
+ to +++
+ to +++
Exposure to soil
- to ++
- to +++
Direct spray (at flowering)
To account for some of the described differences in life history traits between bee species, impacts of pesticides on some non-Apis bee species are considered in some cases of the current registration process even though test procedures have not been established and harmonized for every tier and every species. While inclusion of tests on bee species other than honey bees may be desirable in order to be protective of non-Apis bees, it can be challenging to work with them in laboratory or (semi-)field trials. Wild bee species often produce smaller numbers of individuals per population, shorter periods of seasonal activity and restricted food preferences (Table 2, Roubik, 2014).
Table 2. Life history traits of European bee species (based on information from Prŷs-Jones and Corbet, 1991; Winston, 1995; Goulson, 2003; Michener, 2007; Cueva Del Castillo et al., 2015; Westrich, 2018; Sgolastra et al., 2019)
European honey bees
Semi-social, para-social, sub-social, quasi-social or solitary (short-lived)
Queens, drones, worker bees
Queens, males, worker bees
Number of individuals per nest
Up to 50.000
On average 25–150 (species-specific; worldwide mean 20 to 1848)
Single to multiple individuals per nest; in some species aggregations of 10,000 nests and more
Approx. 1,500 eggs per day
Approx. 4 to 16 eggs in batches at a time
Approx. 2 eggs per day (10–40 eggs over entire life span)
Poly- to oligolectic
Poly-, oligo- or monolectic*
Epigaic and/or endogaic
Epigaic or endogaic*
* often with specializations or special requirements
In order to conduct regular trials with a particular species in the framework of the registration process, a species has to be available in large numbers, standardizable and easily measurable in its endpoints* and representative in its life history traits of a larger (sub)group of bee species (Sgolastra et al., 2019). Ideally it should also have a prolonged or relatively flexible foraging season so that it can be used in various settings. So far there have been very few species meeting these requirements.
Bumble bees. Like honey bees, bumble bees are eusocial and form colonies housing defined casts (Table 2). Colonies in the temperate zones are founded by a single queen that forages and raises the first generation of workers (Benton, 2009). Workers then take over brood care and forage while the queen lays eggs. The size of a colony increases until reproductive offspring are produced. While the colony then slowly dies, the reproductive offspring leave the nest and mate, and the gynes hibernate and initiate new colonies in the next season. In a few instances, depending on climate and species, an autumn/winter generation may be established (Stelzer et al., 2010), but data on its reproductive success is lacking.
In contrast to the assessment of honey bee colonies, the production of queens and males is a crucial part in a bumble bee colony cycle and an important endpoint in the assessment of colony performance. However, the number of reproductive offspring is often highly variable even within the same species. Factors influencing this parameter include parasitism, land use context, life span of the founding queen, time of initiation, and growth and size of the colony (Müller and Schmid-Hempel, 1992; Samuelson et al., 2018). This multitude of factors complicates a standardization that has to be ensured for risk assessment trials.
A further essential requirement for conducting standardized risk assessment trials is the availability of colonies. Of the approx. 250 bumble bee species worldwide (Goulson, 2003), there are only a few species that have been successfully established and raised in captivity (Table 3). Although the foundations of bumble bee domestication go back to the 19th century, rearing methods were not fully developed until the late 20th century (Evans, 2017). All (commercially) reared bumble bee species are pollen storers who feed pollen from separate pollen pots to their larvae directly by perforating the cell wall (Sakagami, 1976), in contrast to pocket makers who feed pollen via a pocket at the side of the larval cell (Sladen, 1899). This characteristic is a good example of how life history traits can define exposure probabilities to pesticides (Colla, 2014): pocket makers may feed contaminated pollen to (and only affect) the current cohort of larvae while pollen storers may keep (and mix) it in separate containers and later feed it to all larvae of the colony.
Table 3. Bumble bee species used in ecotoxicological assays (adopted from Arena and Sgolastra, 2014 and references therein; extended by additional references (Way and Synge, 1948; Wu et al., 2010; BioBest, 2020))
Rearing in captivity*
* ca = commercially available
Solitary bees. Of the almost 20.000 known bee species in the world (nearly 2.000 in Europe; Nieto et al., 2014), only a few have been reared in captivity to primarily support the pollination of specific crops in the agricultural landscape (e.g. Bosch and Kemp, 2002). The alfalfa leafcutting bee Megachile rotundata, various mason bees Osmia spp. and the ground-nesting wild bee species Nomia melanderi are some of the few species that have been used in ecotoxicological studies (Table 4, Kopit und Pitts-Singer, 2018). Wild bee species differ in several key traits, including their food and nesting resources (Wcislo und Cane, 1996; Michener, 2007; Roubik, 2014), for which they utilize either one host plant species (monolecty), one host plant family (oligolecty) or more than one host plant family (polylecty) (Cane und Sipes, 2006; Müller und Kuhlmann, 2008).
Table 4. Wild bee species other than Bombus sp. used in ecotoxicological assays (adopted from Arena und Sgolastra, 2014 and references therein; extended by information from additional references (e.g. Way und Synge, 1948; Helson et al., 1994; Bosch und Kemp, 2002; Cauich et al., 2004; Cortopassi-Laurino et al., 2006; Nocelli et al., 2012; Quiroga Murcia et al., 2017; Dharampal et al., 2018; Jütte et al., 2019; Padilha et al., 2020))
Rearing in captivity*
Central and South America
†also native to parts of Asia and North Africa; ††also native to parts of Asia; †††eusocial species * ca = commercially available,
Sociality is another aspect that is highly variable among wild bees, spanning a wide range that includes solitary, semi-social, para-social, sub-social, quasi-social and kleptoparasitic. Sociality can be an important aspect of life history for assessing risks of PPPs to wild bees. Some solitary bee species, e.g. species within the Halictids, perform regurgitation (trophallaxis) like honey bees; this extends exposure from one individual to many (Martins, 2014) and may increase exposure probabilities on a population rather than an individual level. Within the species that are solitary, individual females serve as reproductive units and have to take care of the offspring themselves rather than being replaceable by a group of workers who care for the brood (as in honey bees and bumble bees). Hence, solitary bee females are more comparable to founding bumble bee queens who provide resources to their offspring on their own (Stoner, 2016). PPP exposure of a single female can directly affect reproductive success over the lifespan of this individual (Straub et al., 2015).
Solitary bees usually occur as only one generation per year (univoltine); a few species with higher degrees of sociality have several generations per year (multivoltinism), correlated to environmental factors such as temperature and food resources (Westrich, 1989). Depending on the period of emergence, exposure probabilities may vary greatly, and early-emerging females with one generation face a different risk compared to late-emerging females or species with two generations. Finally, nesting requirements define exposure and can be different between ground-nesting species that dig their own cavities and the species that nest above ground or in existing underground cavities (Sgolastra et al., 2019). Some wild bee species use nesting resources like leaves, soil, resin or fibres to line their brood cells, which may be another source of contaminants (van der Valk et al., 2013).
The high diversity of life-history traits and environmental requirements make solitary bees a group of organisms that are particularly difficult to rear in large numbers. Hence many species are not suitable as model organisms in the risk assessment of registration processes for PPPs. The number of wild bee species used in ecotoxicological tests is therefore limited (Table 4).
Using bee species other than honey bees in the registration process requires not only the knowledge of their characteristics and life history traits but also establishing routines and standards in handling, caring for the bees’ specific requirements and reliably measuring endpoints in 1st tier (laboratory) and higher tier (semi-field and field) trials. There have been numerous studies on various species over the last decades that have collected valuable information on feeding, housing, rearing, overwintering and endpoints in different experimental settings (cf. references in EFSA Panel on Plant Protection Products and their Residues, 2012 and Sgolastra et al., 2019). However, a better understanding of the variability of these traits among bees has only complicated the development of standard procedures.
The Bee Protection Group of the International Commission for Plant Pollinator Relationships (ICPPR) provides a forum, in which these aspects are addressed, and coordinates international research and ring tests**. Its working groups (e.g. Apis, non-Apis) focus on the development of suitable test methods and the evaluation of parameters and endpoints related to bee health and effects of PPPs. Regulatory test guidelines and guidance documents of the Organization for Economic Cooperation and Development (OECD) are often based on data and information collected and collated by the working groups (OECD, 2019a).
As mentioned earlier, laboratory (1st tier) test methods for bumble bees have already been standardized and implemented in guidelines for risk assessment processes (OECD, 2017b, 2017c) using Bombus terrestris (Europe) and Bombus impatiens (North America) as model species. Queenless microcolonies of these two species have been proposed to be a useful tool for evaluating a range of endpoints at colony level (Klinger et al., 2019); however, disadvantages of using only worker bees are likely to outweigh the benefits (cf. Wu-Smart and Spivak, 2018). For example, one limitation of this method is nest initiation by worker bees and subsequent drone production from unfertilized eggs, which is difficult to standardize in the framework of risk assessment.
While laboratory tests have been conducted on more than those two bumble bee species (cf. Table 3), studies on PPPs that include manipulative semi-field and field experiments have so far only utilized the commercially available species Bombus terrestris and Bombus impatiens (Cutler and Scott-Dupree, 2014; Gill and Raine, 2014; Gradish et al., 2016; Woodcock et al., 2017; Siviter et al., 2018; Dietzsch et al., 2019; Rundlöf and Lundin, 2019). These studies used the weight of a colony, the size/volume of the nest and/or the number of workers (colony strength), males and gynes as proxies for a colony’s development and success and thus as endpoints. Rearing colonies from sister queens (queenright) in captivity by commercial suppliers (e.g. Koppert, BioBest) should allow for a way of standardization among colonies that are exposed to the same environmental settings (van der Steen, 2001; Cabrera et al., 2016). While such a restriction of genetic variability in experimental bee colonies neglects a wide range of naturally occurring genetic traits and as a consequence may restrain the generalization of test results (Bakker, 2016), it may not yet have the desired effect of reducing experimental error. Measuring differences in certain endpoints such as gyne production may only be achieved by highly replicating the number of colonies in trials to accomplish an adequate protection goal (e.g. detection of 25% reduction in queen production; cf. Cabrera et al., 2016). Semi-field and field trials have proven different parameters to be significant for colony success, including initial colony strength and its influence on trial duration, colony development and reproductive success in different seasons (Dietzsch et al., 2018). Food availability is another crucial factor for queen production and queen weight (Franke et al., 2018). To further reduce variability in endpoints, colonies should not only contain a similar initial number of workers and brood stages and show an appropriate worker/brood ratio but also develop with a synchronized speed (Klein et al., 2018). This latter criterion is very time-consuming to achieve and requires laboratory space and capacities to conduct assessments for a possibly large number of replicates. While synchronized developmental speed has been shown to work in semi-field trials (Klein et al., 2018) and was included as a criterion in ring tests (Knäbe et al., 2019), it may not be feasible to achieve in field experiments with multiple colonies per site and multiple replicates in each treatment. Other aspects such as colony disturbance during the experimental (semi-) field phase (including removal of wax ceilings for brood nest evaluation) and its influence on endpoints have yet to be experimentally addressed.
Although establishment of – at least 1st tier – guidelines for solitary bees in the risk assessment process has been initiated (OECD, 2019b), so far standardized methods have not been approved. As for bumble bees, laboratory toxicity tests were performed on many different species (Table 4), yet most experiments on effects of PPPs, particularly higher tier tests, have used only commercially available species, e.g. Osmia bicornis, Osmia lignaria and Megachile rotundata (Abbott et al., 2008; Sandrock et al., 2014; Rundlöf et al., 2015; Becker and Keller, 2016; Nicholls et al., 2017; Woodcock et al., 2017; Dietzsch et al., 2019 but Dharampal et al., 2018). This might be problematic since the three species belong to the same family (Megachilidae) and display relatively similar life history traits, hence may only mirror very few aspects of exposure and behavior of solitary bee species. In addition, availability is not always ensured for all areas of a species’ native range in the framework of the registration process. Since imports of such species are restricted, and different regions (e.g. EU authorization zones) within the same registration area may require different native species, the use of a small set of commercially available species can complicate the implementation of adequate tests.
While the difficulty in bumble bee experiments is the handling of high variability within endpoints, problems in experiments with solitary bees occur in relation to standardized feeding of contaminated food under laboratory conditions, general breeding requirements and year-round management/availability of viable individuals. On a laboratory level, methodologies were refined over the last years and standardized ring tests were conducted (Roessink et al., 2018), which led to the above mentioned proposal for a new guideline (OECD, 2019b). Additional 1st tier experiments explored artificial rearing as well as acute and chronic PPP exposure of solitary bee larvae (Sgolastra et al., 2015; Becker and Keller, 2016; Eeraerts et al., 2019). A greater challenge are semi-field and field trials where hatching times and hatching ratios of bee individuals have to be synchronized, and assessment of nest provisioning and mortality rates of adults have to be monitored continuously. Experimental basics such as choice of easily assessable nesting material, hatching times as well as activity patterns and longevity of the solitary bee species over the season were methodologically addressed by some studies (Bosse et al., 2014; Dietzsch et al., 2014; Knäbe et al., 2016; Kondagala et al., 2016). They gave valuable information for semi-field ring tests, which resulted in repeatable and meaningful results of the measured endpoints (Knäbe et al., 2019). Manipulative approaches that combined laboratory methods with field exposure conditions (e.g. experiments on contaminating nesting material; Jütte et al., 2018) highlighted specific exposure routes with little relevance to honey bees and bumble bees. Further experimental aspects such as disturbance during the nesting phase due to assessments (Kunz et al., unpublished data) and establishment of a suitable reference substance for brood studies (Lückmann et al., 2018a) have to be considered in future optimizations of test methodologies.
Besides experiments that only use one species of bee, recent years saw more – primarily laboratory – experiments involving multiple bee species (Arena and Sgolastra, 2014; Uhl et al., 2019). These studies allow direct comparison of sensitivity rather than relying on meta-analyses of data from multiple studies (like discussed in Lewis and Tzilivakis, 2019; Thompson and Pamminger, 2019). Direct comparisons of bees in laboratory and semi-field studies (honey bee vs. bumble bee, honey bee vs. solitary bee; Heard et al., 2017; Sgolastra et al., 2017; Alkassab et al., 2018; Ansell, 2019; Jütte et al., 2019) show clear differences in the sensitivity of bees and in some cases contradict results from the above mentioned meta-analyses. The direct-comparison approach highlights the need for applying the same laboratory and/or environmental conditions on multiple species to better understand and assess effects. Although standardization of test methods for different solitary bee species is still in progress, experimental efforts (Devillers et al., 2003; Arena and Sgolastra, 2014; Uhl et al., 2016; Jütte et al., 2019) have addressed the question of whether and to what extent honey bees are indeed a suitable surrogate for other bee species in the registration process.
By explicitly integrating other bee species into standardized protocols, the current revision of the EFSA Bee Guidance Document (European Food Safety Authority, 2013) emphasizes the need for a broader risk assessment in the PPP registration process. Most of the recently developed test methods for bumble bees (higher tier trials) and solitary bees (all tiers approaches) indicated some shortcomings; they highlight the need for further improvements in standardizing toxicity tests. The (submitted) manuscripts of the ICPPR non-Apis working group on protocols for bumble bees and mason bees under semi-field conditions (Franke et al., 2020; Klein et al., 2020) as well as the results of laboratory ring tests on oral exposure of solitary bees (Roessink et al., 2018) point to model species and test designs for future risk assessment. Further interdisciplinary research can play an integrative role in evaluating and extrapolating these existing data. For example, experiments on the toxicogenomics (Manjon et al., 2018; Beadle et al., 2019; Troczka et al., 2019) and the phylogenetics of bees (Hayward et al., 2019) clarify mechanisms that correlate with the sensitivity of bee species and hence may facilitate finding model species to extrapolate from. Yet, the goal to identify surrogate species among solitary bee species remains extremely difficult to attain due to the huge variability within important life-history traits. The bee species used so far do not adequately cover this variability (e.g. only hole-nesting solitary bee species and bumble bee pollen storers in higher tier studies). Concepts like the “focal species” approach, which is used in higher tier risk assessment of mammals and birds, could give some directions to choosing and testing appropriate bee species (Lückmann et al., 2018b). A ‘focal species’ is a real species that uses the crop of interest when a pesticide is applied. It is considered to be representative of all other species of the same feeding guild that may occur in the particular crop (European Food Safety Authority, 2009).
Future research should also cover aspects essential for everyday agricultural practice such as the impact of tank mixtures and additives on bee health (Robinson et al., 2017; Carnesecchi et al., 2019; Wernecke et al., 2019), which has not yet been systematically tested on honey bees and other bee taxa. By expanding risk assessment to a landscape level and incorporating modelling approaches, exposure routes and landscape-scale/landscape-context effects of PPPs are evaluated for bee populations/communities rather than individual bees (Danner et al., 2014; Rortais et al., 2017; Simon-Delso et al., 2017; Uhl and Brühl, 2019). This allows for factors such as spatiotemporal migratory population dynamics that are difficult to detect with single field experiments due to limitations of experimental duration and of spatial scale (Uhl and Brühl, 2019). By considering a multitude of potential stressors at various spatial and temporal scales we may be able to minimize or even exclude risks for bees in anthropogenic landscapes.
The authors declare that they do not have any conflicts of interest.
Abbott, V.A., J.L. Nadeau, H.A. Higo, M.L. Winston, 2008: Lethal and sublethal effects of imidacloprid on Osmia lignaria and clothianidin on Megachile rotundata (Hymenoptera: Megachilidae). Journal of Economic Entomology 101 (3), 784-796.
Alkassab, A.T., A. Wernecke, T. Jütte, M. Frommberger, J.H. Eckert, J. Pistorius, 2018: PSM-Tankmischungen: Vergleichende Untersuchung der Empfindlichkeit von Honigbienen, Hummeln und Solitärbienen. In: 61. Deutsche Pflanzenschutztagung: Herausforderung Pflanzenschutz - Wege in die Zukunft; 11.–14. September 2018, Universität Hohenheim, Julius-Kühn-Archiv 461, S. 571.
Ansell, G., 2019: Method development for solitary bee pesticide risk assessment using Megachile rotundata as a surrogate species. MSc thesis, University of Guelph.
Arena, M., F. Sgolastra, 2014: A meta-analysis comparing the sensitivity of bees to pesticides. Ecotoxicology 23 (3), 324–334, DOI: 10.1007/s10646-014-1190-1.
Bakker, F., 2016: Design and analysis of field studies with bees: A critical review of the draft EFSA guidance. Integrated Environmental Assessment and Management 12 (3), 422–428, DOI: 10.1002/ieam.1716.
Bartomeus, I., S.G. Potts, I. Steffan-Dewenter, B.E. Vaissière, M. Woyciechowski, K.M. Krewenka, T. Tscheulin, S.P.M. Roberts, H. Szentgyörgyi, C. Westphal, R. Bommarco, 2014: Contribution of insect pollinators to crop yield and quality varies with agricultural intensification. PeerJ 2, e328, DOI: 10.7717/peerj.328.
Beadle, K., K.S. Singh, B.J. Troczka, E. Randall, M. Zaworra, C.T. Zimmer, A. Hayward, R. Reid, L. Kor, M. Kohler, B. Buer, D.R. Nelson, M.S. Williamson, T.G.E. Davies, L.M. Field, R. Nauen, C. Bass, 2019: Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis. PLoS genetics 15 (2), e1007903, DOI: 10.1371/journal.pgen.1007903.
Becker, M.C., A. Keller, 2016: Laboratory rearing of solitary bees and wasps. Insect Science 23 (6), 918–923, DOI: 10.1111/1744-7917.12242.
Benton, T., 2009: Bumblebees, Harper Collins Publishers Limited.
Biesmeijer, J.C., S.P.M. Roberts, M. Reemer, R. Ohlemüller, M. Edwards, T. Peeters, A.P. Schaffers, S.G. Potts, R. Kleukers, C.D. Thomas, J. Settele, W.E. Kunin, 2006: Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313 (5785), 351-354.
BioBest, 2020: Bumblebee species. Zugriff: 27. Februar 2020, URL: https://www.biobestgroup.com/en/biobest/pollination/things-to-know-about-bumblebees-7052/species-6674/.
Bosch, J., W.P. Kemp, 2002: Developing and establishing bee species as crop pollinators: the example of Osmia spp. (Hymenoptera: Megachilidae) and fruit trees. Bulletin of Entomological Research 92 (1), 3–16, DOI: 10.1079/BER2001139.
Bosse, G., T. Jütte, O. Klein, 2014: Experimental designs for field and semi-field studies with solitary wild bees. In: Hazards of Pesticides to Bees - 12th International Symposium of the ICP-PR Bee Protection Group, Ghent (Belgium), September 15-17 2014, Julius-Kühn-Archiv 450, S. 226-229.
Boyle, N.K., T.L. Pitts-Singer, J. Abbott, A. Alix, D.L. Cox-Foster, S. Hinarejos, D.M. Lehmann, L. Morandin, B. O’Neill, N.E. Raine, R. Singh, H.M. Thompson, N.M. Williams, T. Steeger, 2019: Workshop on pesticide exposure assessment paradigm for non-Apis bees: Foundation and summaries. Environmental Entomology 48 (1), 4–11, DOI: 10.1093/ee/nvy103.
Brittain, C.A., S.G. Potts, 2011: The potential impacts of insecticides on the life-history traits of bees and the consequences for pollination. Basic and Applied Ecology 12, 321-331.
Cabrera, A.R., M.T. Almanza, G.C. Cutler, D.L. Fischer, S. Hinarejos, G. Lewis, D. Nigro, A. Olmstead, J. Overmyer, D.A. Potter, N.E. Raine, C. Stanley-Stahr, H. Thompson, J. van der Steen, 2016: Initial recommendations for higher-tier risk assessment protocols for bumble bees, Bombus spp. (Hymenoptera: Apidae). Integrated Environmental Assessment and Management 12 (2), 222–229, DOI: 10.1002/ieam.1675.
Cane, J.H., S.D. Sipes, 2006: Characterizing floral specialization by bees: analytical methods and a revised lexicon for oligolecty. In: Plant-Pollinator Interactions: From Specialization to Generalization. Waser, N.M., J. Ollerton (Eds), Chicago, The University of Chicago Press, S. 99-122.
Carnesecchi, E., C. Svendsen, S. Lasagni, A. Grech, N. Quignot, B. Amzal, C. Toma, S. Tosi, A. Rortais, J. Cortinas-Abrahantes, E. Capri, N. Kramer, E. Benfenati, D. Spurgeon, G. Guillot, J.L.C.M. Dorne, 2019: Investigating combined toxicity of binary mixtures in bees: Meta-analysis of laboratory tests, modelling, mechanistic basis and implications for risk assessment. Environment International 133 (Part B), 105256, DOI: 10.1016/j.envint.2019.105256.
Catarino, R., V. Bretagnolle, T. Perrot, F. Vialloux, S. Gaba, 2019: Bee pollination outperforms pesticides for oilseed crop production and profitability. Proceedings of the Royal Society B-Biological Sciences 286 (1912), 20191550, DOI: 10.1098/rspb.2019.1550.
Cauich, O., J.J.G. Quezada-Euán, J.O. Macias-Macias, V. Reyes-Oregel, S. Medina-Peralta, V. Parra-Tabla, 2004: Behavior and pollination efficiency of Nannotrigona perilampoides (Hymenoptera: Meliponini) on greenhouse tomatoes (Lycopersicon esculentum) in subtropical México. Journal of Economic Entomology 97 (2), 475–481, DOI: 10.1093/jee/97.2.475.
Colla, S., 2014: Bumble bees: Natural history and pesticide exposure routes. In: Pollinator safety in agriculture. Roubik, D.W. (Eds), Rome, Food and Agriculture Organization of the United Nations, S. 49-56.
Cortopassi-Laurino, M., V.L. Imperatriz-Fonseca, D.W. Roubik, A. Dollin, T. Heard, I. Aguilar, G.C. Venturieri, C. Eardley, P. Nogueira-Neto, 2006: Global meliponiculture: Challenges and opportunities. Apidologie 37 (2), 275–292, DOI: 10.1051/apido:2006027.
Cueva Del Castillo, R., S. Sanabria-Urbán, M.A. Serrano-Meneses, 2015: Trade-offs in the evolution of bumblebee colony and body size: a comparative analysis. Ecology and Evolution 5 (18), 3914–3926, DOI: 10.1002/ece3.1659.
Cutler, C.G., C.D. Scott-Dupree, 2014: A field study examining the effects of exposure to neonicotinoid seed-treated corn on commercial bumble bee colonies. Ecotoxicology 23 (9), 1755–1763, DOI: 10.1007/s10646-014-1340-5.
Danner, N., S. Härtel, I. Steffan-Dewenter, 2014: Maize pollen foraging by honey bees in relation to crop area and landscape context. Basic and Applied Ecology 15 (8), 677–684, DOI: 10.1016/j.baae.2014.08.010.
Devillers, J., A. Decourtye, H. Budzinski, M.H. Pham-Delègue, S. Cluzeau, G. Maurin, 2003: Comparative toxicity and hazards of pesticides to Apis and non-Apis bees. A chemometrical study. SAR and QSAR in Environmental Research 14 (5-6), 389-403.
Dharampal, P.S., C.M. Carlson, L. Diaz-Garcia, S.A. Steffan, 2018: In vitro rearing of solitary bees: A tool for assessing larval risk factors. Journal of Visualized Experiments 137, e57876, DOI: 10.3791/57876.
Dietzsch, A.C., M. Frommberger, J. Pistorius, 2018: Developing methods for field experiments using commercially reared bumblebee colonies - initial colony strength and experimental duration as influential factors. In: Hazards of Pesticides to Bees – 13th International Symposium of the ICP-PR Bee Protection Group, October 18 – 20 2017, Valencia (Spain), Julius-Kühn-Archiv 462, S. 176-179.
Dietzsch, A.C., N. Kunz, I.P. Wirtz, M. Frommberger, J. Pistorius, 2014: Evaluating the feasibility of using the red mason bee (Osmia bicornis L.) in different experimental setups. In: Hazards of Pesticides to Bees – 12th International Symposium of the ICP-PR Bee Protection Group, Ghent (Belgium), September 15-17 2014, Julius-Kühn-Archiv 450, S. 174-178.
Dietzsch, A.C., N. Kunz, I.P. Wirtz, M. Stähler, U. Heimbach, J. Pistorius, 2019: Does winter oilseed rape grown from clothianidin-coated seeds affect experimental populations of mason bees and bumblebees? A semi-field and field study. Journal of Consumer Protection and Food Safety 14 (3), 223–238, DOI: 10.1007/s00003-019-01225-5.
Eeraerts, M., M. Pisman, R. Vanderhaegen, I. Meeus, G. Smagghe, 2019: Recommendations for standardized oral toxicity test protocols for larvae of solitary bees, Osmia spp. Apidologie 101 (3), 784, DOI: 10.1007/s13592-019-00704-w.
EFSA Panel on Plant Protection Products and their Residues, 2012: Scientific Opinion on the science behind the development of a risk assessment of Plant Protection Products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA Journal 10 (5), 2668, DOI: 10.2903/j.efsa.2012.2668.
Eppo, 2010: Environmental risk assessment scheme for plant protection products – Chapter 10: honeybees. EPPO Bulletin 40, 1-9.
European Parliament, Council of the European Union, 2009: Regulation (EC) No 1107/2009 of the European Parlament and of the Council of 21 October 2009 concerning the placing of plant protection products on the market and repealing Council Directives 79/117/EEC and 91/414/EEC. Official Journal of the European Union, L 309/1-L 309/50.
Evans, E., 2017: From humble bee to greenhouse pollination workhorse: Can we mitigate risks for bumble bees? Bee World 94 (2), 34–41, DOI: 10.1080/0005772X.2017.1290892.
Fischer, D., T. Moriarty (Eds.), 2011: Pesticide risk assessment for pollinators: Summary of a SETAC Pellston Workshop, Pensacola, FL, USA, Society of Environmental Toxicology and Chemistry.
Franke, L., C. Elston, T. Jütte, O. Klein, S. Knäbe, J. Lückmann, I. Roessink, M. Persigehl, M. Cornement, N. Exeler, H. Giffard, B. Hodapp, S. Kimmel, B. Kullmann, C. Schneider, A. Schnurr, 2020: Results of 2-year ring-testing of a semi-field study design to investigate potential impacts of plant protection products on the solitary bees Osmia bicornis (Linnaeus, 1758) and Osmia cornuta (Latreille, 1805) (Hymenoptera, Megachilidae) and a proposal of a suitable test design. Environmental Toxicology and Chemistry, submitted.
Franke, L., O. Klein, J. Fricke, J. Sorli, S. Knaebe, 2018: 3.11 Bumble bee queen production in semi-field studies: Assessment of endpoints and challenges. In: Hazards of Pesticides to Bees – 13th International Symposium of the ICP-PR Bee Protection Group, October 18 – 20 2017, Valencia (Spain), Julius-Kühn-Archiv 462, S. 134-136.
Garibaldi, L.A., I. Steffan-Dewenter, R. Winfree, M.A. Aizen, R. Bommarco, S.A. Cunningham, C. Kremen, L.G. Carvalheiro, L.D. Harder, O. Afik, I. Bartomeus, F. Benjamin, V. Boreux, D. Cariveau, N.P. Chacoff, J.H. Dudenhöffer, B.M. Freitas, J. Ghazoul, S. Greenleaf, J. Hipólito, A. Holzschuh, B. Howlett, R. Isaacs, K. Javorek, C.M. Kennedy, K. Krewenka, S. Krishnan, Y. Mandelik, M.M. Mayfield, I. Motzke, T. Munyuli, B.A. Nault, M. Otieno, J. Petersen, G. Pisanty, S.G. Potts, R. Rader, T.H. Ricketts, M. Rundlöf, C.L. Seymour, C. Schüepp, H. Szentgyörgyi, T. Hisatomo, T. Tscharntke, C.H. Vergara, B.F. Viana, T.C. Wanger, C. Westphal, N. Williams, A.M. Klein, 2013: Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339 (6127), 1608–1611, DOI: 10.1126/science.1230200.
Gill, R.J., N.E. Raine, 2014: Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure. Functional Ecology 28 (6), 1459–1471, DOI: 10.1111/1365-2435.12292.
Goulson, D., 2003: Bumblebees; their Behaviour and Ecology. Oxford, UK, Oxford University Press.
Goulson, D., E. Nicholls, C. Botías, E.L. Rotheray, 2015: Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347 (6229), 1255957, DOI: 10.1126/science.1255957.
Gradish, A.E., G.C. Cutler, A.J. Frewin, C.D. Scott-Dupree, 2016: Comparison of buckwheat, red clover, and purple tansy as potential surrogate plants for use in semi-field pesticide risk assessments with Bombus impatiens. PeerJ 4, e2228, DOI: 10.7717/peerj.2228.
Gradish, A.E., J. van der Steen, C.D. Scott-Dupree, A.R. Cabrera, G.C. Cutler, D. Goulson, O. Klein, D.M. Lehmann, J. Lückmann, B. O’Neill, N.E. Raine, B. Sharma, H. Thompson, 2019: Comparison of pesticide exposure in honey bees (Hymenoptera: Apidae) and bumble bees (Hymenoptera: Apidae): Implications for risk assessments. Environmental Entomology 48 (1), 12–21, DOI: 10.1093/ee/nvy168.
Hallmann, C.A., M. Sorg, E. Jongejans, H. Siepel, N. Hofland, H. Schwan, W. Stenmans, A. Müller, H. Sumser, T. Hörren, D. Goulson, H. de Kroon, 2017: More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12 (10), e0185809, DOI: 10.1371/journal.pone.0185809.
Handford, C.E., C.T. Elliott, K. Campbell, 2015: A review of the global pesticide legislation and the scale of challenge in reaching the global harmonization of food safety standards. Integrated Environmental Assessment and Management 11 (4), 525-536.
Hayward, A., K. Beadle, K.S. Singh, N. Exeler, M. Zaworra, M.-T. Almanza, A. Nikolakis, C. Garside, J. Glaubitz, C. Bass, R. Nauen, 2019: The leafcutter bee, Megachile rotundata, is more sensitive to N-cyanoamidine neonicotinoid and butenolide insecticides than other managed bees. Nature Ecology & Evolution 3 (11), 1521–1524, DOI: 10.1038/s41559-019-1011-2.
Heard, M.S., J. Baas, J.-L. Dorne, E. Lahive, A.G. Robinson, A. Rortais, D.J. Spurgeon, C. Svendsen, H. Hesketh, 2017: Comparative toxicity of pesticides and environmental contaminants in bees: Are honey bees a useful proxy for wild bee species? Science of the Total Environment 578, 357–365, DOI: 10.1016/j.scitotenv.2016.10.180.
Helson, B.V., K.N. Barber, P.D. Kingsbury, 1994: Laboratory toxicology of six forestry insecticides to four species of bee (Hymenoptera: Apoidea). Archives of Environmental Contamination and Toxicology 27, 107-114.
Jütte, T., C. Steinigeweg, J. Pistorius, 2018: Exposure by nesting material? – Investigation of potentially suitable methods for higher tier studies with solitary bees. In: Hazards of Pesticides to Bees - 13th International Symposium of the ICP-PR Bee Protection Group, October 18 – 20 2017, Valencia (Spain), Julius-Kühn-Archiv 462, S. 164-169.
Jütte, T., A. Wernecke, G. Bischoff, A. Krahner, A. Dietzsch, J. Pistorius, 2019: Sensitivity of the honey bee and different wild bee species to plant protection products – two years of comparative laboratory studies: Book of Abstracts. Bern.
Klein, A.M., B. Vaissière, J.H. Cane, I. Steffan-Dewenter, S.A. Cunningham, C. Kremen, T. Tscharntke, 2007: Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences 274, 303-313.
Klein, O., C. Elston, L. Franke, T. Jütte, S. Knäbe, J. Lückmann, J. van der Steen, M.J. Allan, A. Alscher, K. Amsel, M. Cornement, N. Exeler, J. Sorli Guerola, B. Hodapp, C. Jenkins, S. Kimmel, V. Tänzler, 2020: Results of 2-year ring-testing of a semi-field study design to investigate potential impacts of plant protection products on bumble bees (Hymenoptera, Apidae) and a proposal of a suitable test design. Environmental Toxicology and Chemistry, submitted.
Klein, O., L. Franke, J. Fricke, J. Sorli, S. Knaebe, 2018: 3.10 Bumble bee semi-field studies: Choice and management of colonies to reduce variability in assessment endpoints. In: Hazards of Pesticides to Bees - 13th International Symposium of the ICP-PR Bee Protection Group, October 18 – 20 2017, Valencia (Spain), Julius-Kühn-Archiv 462, S. 132-134.
Klinger, E.G., A.A. Camp, J.P. Strange, D. Cox-Foster, D.M. Lehmann, 2019: Bombus (Hymenoptera: Apidae) microcolonies as a tool for biological understanding and pesticide risk assessment. Environmental Entomology 48 (6), 1249–1259, DOI: 10.1093/ee/nvz117.
Knäbe, S., M. Allan, A. Alscher, K. Amseld, C. Classen, M. Cornement, C. Elston, N. Exeler, L. Franke, J. Fricke, M. Frommberger, H. Giffard, J. Sorli Guerola, S. Hecht-Rost, B. Hodapp, I. Hotopp, C. Jenkins, T. Jütte, S. Kimmel, O. Klein, B. Kullmann, J. Lückmann, M. Persigehl, I. Roessink, C. Schneider, A. Schnurr, V. Tänzler, S. Van der Steen, 2019: 2.1. Summary of an ICPPR Non-Apis workshop – Subgroup higher tier (bumble bees and solitary bees) with recommendations for a semi-field experimental design: Book of Abstracts. Bern.
Knäbe, S., M.M. Candolfi, L. Franke, J. Fricke, T. Jütte, O. Klein, A. Schuster, T. Vollmer, 2016: Experimental design for semi-field trials to test brood affecting plant protection products with solitary bees. In: 26th Annual Meeting SETAC Europe, Nantes, France.
Kondagala, V., M. Candolfi, T. Jütte, O. Klein, S. Knäbe, T. Vollmer, 2016: Development of suitable experimental designs for semi-field trials with solitary bees. In: 26th Annual Meeting SETAC Europe, Nantes, France.
Kopit, A.M., T.L. Pitts-Singer, 2018: Routes of pesticide exposure in solitary, cavity-nesting bees. Environmental Entomology 47 (3), 499–510, DOI: 10.1093/ee/nvy034.
Lewis, K.A., J. Tzilivakis, 2019: Wild bee toxicity data for pesticide risk assessments. Data 4 (3), 98, DOI: 10.3390/data4030098.
Lückmann, J., C. Claßen, O. Mayer, O. Jakoby, 2018a: 3.9 Semi-field testing of the solitary bee Osmia bicornis (L., 1758) (Hymenoptera, Megachilidae) in flowering Phacelia tanacetifolia – Chances, improvements and limitations. In: Hazards of Pesticides to Bees – 13th International Symposium of the ICP-PR Bee Protection Group, October 18 – 20 2017, Valencia (Spain), Julius-Kühn-Archiv 462, S. 126-131.
Lückmann, J., M. Faupel, J.-D. Ludwigs, 2018b: 3.8 ‘Focal species’ – can this well-known concept in higher-tier risk assessments be an appropriate approach for solitary bees? In: Hazards of Pesticides to Bees - 13th International Symposium of the ICP-PR Bee Protection Group, October 18 – 20 2017, Valencia (Spain), Julius-Kühn-Archiv 462, S. 122-125.
Manjon, C., B.J. Troczka, M. Zaworra, K. Beadle, E. Randall, G. Hertlein, K.S. Singh, C.T. Zimmer, R.A. Homem, B. Lueke, R. Reid, L. Kor, M. Kohler, J. Benting, M.S. Williamson, T.G.E. Davies, L.M. Field, C. Bass, R. Nauen, 2018: Unravelling the molecular determinants of bee sensitivity to neonicotinoid insecticides. Current Biology 28 (7), 1137-1143.e5, DOI: 10.1016/j.cub.2018.02.045.
Martins, D.J., 2014: Sweat bees (Halictidae): Natural history and pesticide exposure. In: Pollinator safety in agriculture. Roubik, D.W. (Eds), Rome, Food and Agriculture Organization of the United Nations, S. 75-89.
Mayack, C., S. Boff, 2019: LD50 values may be misleading predictors of neonicotinoid toxicity across different bee species. Uludağ Arıcılık Dergisi 19 (1), 19–33, DOI: 10.31467/uluaricilik.568251.
Michener, C.D., 2007: The Bees of the World. Baltimore, Johns Hopkins University Press.
Morse, R., N.W. Calderone, 2000: The value of honey bees as pollinators of U.S. crops in 2000. Bee Culture 128, 1-15.
Müller, A., M. Kuhlmann, 2008: Pollen hosts of western palaearctic bees of the genus Colletes (Hymenoptera: Colletidae): the Asteraceae paradox. Biological Journal of the Linnean Society 95 (4), 719–733, DOI: 10.1111/j.1095-8312.2008.01113.x.
Müller, C.B., P. Schmid-Hempel, 1992: Correlates of reproductive success among field colonies of Bombus lucorum: The importance of growth and parasites. Ecological Entomology 17 (4), 343–353, DOI: 10.1111/j.1365-2311.1992.tb01068.x.
Mwebaze, P., G. Marris, G. Budge, M. Brown, S.G. Potts, T.D. Breese, A. MacLeod, 2010: Quantifying the Value of Ecosystem Services: A Case Study of Honeybee Pollination in the UK. From the Wealth of Nations to the Wealth of Nature: Rethinking Economic Growth, Venice, Italy.
Nicholls, E., R. Fowler, J.E. Niven, J.D. Gilbert, D. Goulson, 2017: Larval exposure to field-realistic concentrations of clothianidin has no effect on development rate, over-winter survival or adult metabolic rate in a solitary bee, Osmia bicornis. PeerJ 5, e3417, DOI: 10.7717/peerj.3417.
Nieto, A., S.P.M. Roberts, J. Kemp, P. Rasmont, M. Kuhlmann, García Criado, M., J.C. Biesmeijer, P. Bogusch, H.H. Dathe, P. de La Rúa, T. de Meulemeester, M. Dehon, A. Dewulf, F.J. Ortiz-Sánchez, P. Lhomme, A. Pauly, S.G. Potts, C. Praz, M. Quaranta, V.G. Radchenko, E. Scheuchl, J. Smit, J. Straka, M. Terzo, B. Tomozii, J. Window, D. Michez, 2014: European Red List of Bees. Luxembourg, Publication Office of the European Union.
Nocelli, R.C.F., T.C. Roat, Zacarin, Elaine Cristina Mathias da Silva, O. Malapisina, 2012: Riscos de pesticidas sobre as abelhas. In: Semana dos Polinizadores, Petrolina, Embrapa Semiárido, S. 196-212.
OECD, 1998a: Test No. 213: Honeybees, acute oral toxicity test. OECD Guidelines for the Testing of Chemicals, Organisation for Economic Co-operation and Development.
OECD, 1998b: Test No. 214: Honeybees, acute contact toxicity test. OECD Guidelines for the Testing of Chemicals, Organisation for Economic Co-operation and Development.
OECD, 2007: No. 75: Guidance document on the honey bee (Apis mellifera L.) brood test under semi-field conditions, Series on Testing and Assessment, Organisation for Economic Co-operation and Development.
OECD, 2013: Test No. 237: Honey bee (Apis mellifera) larval toxicity test, single exposure. OECD Guidelines for the Testing of Chemicals, Organisation for Economic Co-operation and Development.
OECD, 2016: No. 239: Guidance document on honeybee larval toxicity test following repeated exposure, Series on Testing and Assessment, Organisation for Economic Co-operation and Development.
OECD, 2017a: Test No. 245: Honey bee (Apis mellifera L.), chronic oral toxicity test (10-day feeding). OECD Guidelines for the Testing of Chemicals, Organisation for Economic Co-operation and Development, DOI: 10.1787/9789264284081-en.
OECD, 2017b: Test No. 246: Bumblebee, acute contact toxicity test. OECD Guidelines for the Testing of Chemicals, Organisation for Economic Co-operation and Development, DOI: 10.1787/9789264284104-en.
OECD, 2017c: Test No. 247: Bumblebee, acute oral toxicity test. OECD Guidelines for the Testing of Chemicals, Organisation for Economic Co-operation and Development, DOI: 10.1787/9789264284128-en.
OECD, 2019a: OECD Work Related to Bees/Pollinators. Zugriff: 28. Februar 2020, URL:https://www.oecd.org/chemicalsafety/pesticides-biocides/work-related-beespollinators.htm.
OECD, 2019b: Project 2.65: New TG on Acute Contact Toxicity Test for the solitary living Mason Bee (Osmia spp.).
Oré Barrios, C., E. Mäurer, C. Lippert, S. Dabbert, 2017: Eine ökonomische Analyse des Imkerei-Sektors in Deutschland.
Padilha, A.C., B. Piovesan, M.C. Morais, J. de BPazini, M.J. Zotti, M. Botton, A.D. Grützmacher, 2020: Toxicity of insecticides on Neotropical stingless bees Plebeia emerina (Friese) and Tetragonisca fiebrigi (Schwarz) (Hymenoptera: Apidae: Meliponini). Ecotoxicology 29 (1), 119–128, DOI: 10.1007/s10646-019-02150-x.
Potts, S.G., J.C. Biesmeijer, C. Kremen, P. Neumann, O. Schweiger, W.E. Kunin, 2010: Global pollinator declines: trends, impacts and drivers. Trends in Ecology and Evolution 25 (6), 345–353, DOI: 10.1016/j.tree.2010.01.007.
Prŷs-Jones, O., S. Corbet, 1991: Bumblebees. Slough, The Richmond Publishing.
Quiroga Murcia, D.E., M.J. Zotti, I. Zenner de polania, E.E. Pech-Pech, 2017: Toxicity evaluation of two insecticides on Tetragonisca angustula and Scaptotrigona xanthotricha (Hymenoptera: Apidae). Agronomía Colombiana 35 (3), 340–349, DOI: 10.15446/agron.colomb.v35n3.65447.
Reid, R.J., B.J. Troczka, L. Kor, E. Randall, M.S. Williamson, L.M. Field, R. Nauen, C. Bass, T.E. Davies, 2020: Assessing the acute toxicity of insecticides to the buff-tailed bumblebee (Bombus terrestris audax). Pesticide Biochemistry and Physiology, 104562, DOI: 10.1016/j.pestbp.2020.104562.
Robinson, A., H. Hesketh, E. Lahive, A.A. Horton, C. Svendsen, A. Rortais, J.L. Dorne, J. Baas, M.S. Heard, D.J. Spurgeon, 2017: Comparing bee species responses to chemical mixtures: Common response patterns? PLoS ONE 12 (6), e0176289, DOI: 10.1371/journal.pone.0176289.
Roessink, I., N. Hanewald, C. Schneider, N. Exeler, A. Schnurr, A.-M. Molitor, E. Soler, S. Kimmel, C. Molitor, G. Smagghe, S. Van der Steen, 2018: 4.6 A method for a solitary bee (Osmia sp.) first tier acute contact and oral laboratory test: an update. In: Hazards of Pesticides to Bees - 13th International Symposium of the ICP-PR Bee Protection Group, October 18 – 20 2017, Valencia (Spain), Julius-Kühn-Archiv 462, S. 158.
Rortais, A., G. Arnold, J.-L. Dorne, S.J. More, G. Sperandio, F. Streissl, C. Szentes, F. Verdonck, 2017: Risk assessment of pesticides and other stressors in bees: Principles, data gaps and perspectives from the European Food Safety Authority. Science of the Total Environment 587-588, 524–537, DOI: 10.1016/j.scitotenv.2016.09.127.
Roubik, D.W. (Eds.), 2014: Pollinator safety in agriculture, Rome, Food and Agriculture Organization of the United Nations.
Rundlöf, M., G.K.S. Andersson, R. Bommarco, I. Fries, V. Hederstrom, L. Herbertsson, O. Jonsson, B.K. Klatt, T.R. Pedersen, J. Yourstone, H.G. Smith, 2015: Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521 (7550), 77-80, DOI: 10.1038/nature14420.
Rundlöf, M., O. Lundin, 2019: Can costs of pesticide exposure for bumblebees be balanced by benefits from a mass-flowering crop? Environmental Science & Technology 53 (24), 14144–14151, DOI: 10.1021/acs.est.9b02789.
Sakagami, S.F., 1976: Specific differences in the bionomic characters of bumblebees. A comparative review. Journal of the Faculty of Science, Hokkaido University. Series 6, Zoology 20 (3), 390-447.
Samuelson, A.E., R.J. Gill, M.J.F. Brown, E. Leadbeater, 2018: Lower bumblebee colony reproductive success in agricultural compared with urban environments. Proceedings of the Royal Society B-Biological Sciences 285 (1881), 20180807, DOI: 10.1098/rspb.2018.0807.
Sánchez-Bayo, F., K.A.G. Wyckhuys, 2019: Worldwide decline of the entomofauna: A review of its drivers. Biological Conservation 232, 8–27, DOI: 10.1016/j.biocon.2019.01.020.
Sandrock, C., L.G. Tanadini, J.S. Pettis, J.C. Blessmeijer, S.G. Potts, P. Neumann, 2014: Sublethal neonicotinoid insecticide exposure reduces solitary bee reproductive success. Agricultural and Forest Entomology 16, 119–128, DOI: 10.1111/afe.12041.
Seibold, S., M.M. Gossner, N.K. Simons, N. Blüthgen, J. Müller, D. Ambarlı, C. Ammer, J. Bauhus, M. Fischer, J.C. Habel, K.E. Linsenmair, T. Nauss, C. Penone, D. Prati, P. Schall, E.-D. Schulze, J. Vogt, S. Wöllauer, W.W. Weisser, 2019: Arthropod decline in grasslands and forests is associated with landscape-level drivers. Nature 574 (7780), 671–674, DOI: 10.1038/s41586-019-1684-3.
Sgolastra, F., S. Hinarejos, T.L. Pitts-Singer, N.K. Boyle, T. Joseph, J. Luckmann, N.E. Raine, R. Singh, N.M. Williams, J. Bosch, 2019: Pesticide exposure assessment paradigm for solitary bees. Environmental Entomology 48 (1), 22–35, DOI: 10.1093/ee/nvy105.
Sgolastra, F., P. Medrzycki, L. Bortolotti, M.T. Renzi, S. Tosi, G. Bogo, D. Teper, C. Porrini, R. Molowny-Horas, J. Bosch, 2017: Synergistic mortality between a neonicotinoid insecticide and an ergosterol-biosynthesis-inhibiting fungicide in three bee species. Pest Management Science 73 (6), 1236–1243, DOI: 10.1002/ps.4449.
Sgolastra, F., S. Tosi, P. Medrzycki, C. Porrini, G. Burgio, 2015: Toxicity of spirotetramat on solitary bee larvae, Osmia cornuta (Hymenoptera: Megachilidae), in laboratory conditions. Journal of Apicultural Science 59 (2), 73–83, DOI: 10.1515/JAS-2015-0024.
Simon-Delso, N., G. San Martin, E. Bruneau, C. Delcourt, L. Hautier, 2017: The challenges of predicting pesticide exposure of honey bees at landscape level. Scientific Reports 7 (1), 3801, DOI: 10.1038/s41598-017-03467-5.
Siviter, H., M.J.F. Brown, E. Leadbeater, 2018: Sulfoxaflor exposure reduces bumblebee reproductive success. Nature, DOI: 10.1038/s41586-018-0430-6.
Sladen, F.W.L., 1899: Bombi in captivity, and habits of Psithyrus. Entomologist’s Monthly Magazine 35, 230-234.
Stelzer, R.J., L. Chittka, M. Carlton, T.C. Ings, 2010: Winter active bumblebees (Bombus terrestris) achieve high foraging rates in urban Britain. PLoS ONE 5 (3), e9559, DOI: 10.1371/journal.pone.0009559.
Stoner, K.A., 2016: Current pesticide risk assessment protocols do not adequately address differences between honey bees (Apis mellifera) and bumble bees (Bombus spp.). Frontiers in Environmental Science 4, 813, DOI: 10.3389/fenvs.2016.00079.
Straub, L., G.R. Williams, J. Pettis, I. Fries, P. Neumann, 2015: Superorganism resilience: eusociality and susceptibility of ecosystem service providing insects to stressors. Current Opinion in Insect Science 12, 109–112, DOI: 10.1016/j.cois.2015.10.010.
Thompson, H., 2016: Extrapolation of acute toxicity across bee species. Integrated Environmental Assessment and Management 12 (4), 622–626, DOI: 10.1002/ieam.1737.
Thompson, H.M., T. Pamminger, 2019: Are honeybees suitable surrogates for use in pesticide risk assessment for non-Apis bees? Pest Management Science 75 (10), 2549–2557, DOI: 10.1002/ps.5494.
Troczka, B.J., R.A. Homem, R. Reid, K. Beadle, M. Kohler, M. Zaworra, L.M. Field, M.S. Williamson, R. Nauen, C. Bass, T.G.E. Davies, 2019: Identification and functional characterisation of a novel N-cyanoamidine neonicotinoid metabolising cytochrome P450, CYP9Q6, from the buff-tailed bumblebee Bombus terrestris. Insect Biochemistry and Molecular Biology 111, 103171, DOI: 10.1016/j.ibmb.2019.05.006.
Uhl, P., O. Awanbor, R.S. Schulz, C.A. Brühl, 2019: Is Osmia bicornis an adequate regulatory surrogate? Comparing its acute contact sensitivity to Apis mellifera. PLoS ONE 14 (8), e0201081, DOI: 10.1371/journal.pone.0201081.
Uhl, P., C.A. Brühl, 2019: The impact of pesticides on flower-visiting insects: A review with regard to European risk assessment. Environmental Toxicology and Chemistry 38 (11), 2355–2370, DOI: 10.1002/etc.4572.
Uhl, P., L.A. Franke, C. Rehberg, C. Wollmann, P. Stahlschmidt, L. Jeker, C.A. Brühl, 2016: Interspecific sensitivity of bees towards dimethoate and implications for environmental risk assessment. Scientific Reports 6, 34439, DOI: 10.1038/srep34439.
van der Steen, J.J.M., 2001: Review of the methods to determine the hazard and toxicity of pesticides to bumblebees. Apidologie 32 (5), 399-406.
van der Valk, H., I. Koomen, R.C.F. Nocelli, M. d. F. Ribeiro, B.M. Freitas, S.M. Carvalho, J.M. Kasina, D.J. Martins, G. Maina, P. Ngaruiya, M. Gikungu, M. Mutiso, C. Odhiambo, W. Kinuthia, P. Kipyab, T. Blacquière, J. van der Steen, I. Roessink and J. Wassenberg, B. Gemmill-Herren, 2013: Aspects determining the risk of pesticides to wild bees: Risk profiles for focal crops on three continents. Rome, Food and Agriculture Organization of the United Nations.
Venturini, E.M., F.A. Drummond, A.K. Hoshide, A.C. Dibble, L.B. Stack, 2017: Pollination reservoirs for wild bee habitat enhancement in cropping systems: A review. Agroecology and Sustainable Food Systems 41 (2), 101–142, DOI: 10.1080/21683565.2016.1258377.
Way, M.J., A.D. Synge, 1948: The effects of D.D.T. and of benzene hexachloride on bees. Annals of Applied Biology 35 (1), 94–109, DOI: 10.1111/j.1744-7348.1948.tb07353.x.
Wcislo, W.T., J.H. Cane, 1996: Floral resource utilization by solitary bees (Hymenoptera: Apoidea) and exploitation of their stored foods by natural enemies. Annual Review of Entomology 41, 257–286, DOI: 10.1146/annurev.en.41.010196.001353.
Wernecke, A., M. Frommberger, R. Forster, J. Pistorius, 2019: Lethal effects of various tank mixtures including insecticides, fungicides and fertilizers on honey bees under laboratory, semi-field and field conditions. Journal of Consumer Protection and Food Safety 14 (3), 239–249, DOI: 10.1007/s00003-019-01233-5.
Westrich, P., 1989: Die Wildbienen Baden-Württembergs. Stuttgart, Verlag Eugen Ulmer.
Westrich, P., 2018: Die Wildbienen Deutschlands. Stuttgart, Ulmer.
Westrich, P., U. Frommer, K. Mandery, H. Riemann, H. Ruhnke, C. Saure, J. Voith, 2011: Rote Liste und Gesamtartenliste der Bienen (Hymenoptera, Apidae) Deutschlands. In: Rote Liste gefährdeter Tiere, Pflanzen und Pilze Deutschlands: Band 3: Wirbellose Tiere (Teil 1). Bundesamt für Naturschutz (Eds), Bonn-Bad Godesberg, S. 373-416.
Winston, M.L., 1995: The Biology of the Honey Bee. Cambridge, Harvard University Press.
Woodcock, B.A., J.M. Bullock, R.F. Shore, M.S. Heard, M.G. Pereira, J. Redhead, L. Ridding, H. Dean, D. Sleep, P. Henrys, J. Peyton, S. Hulmes, L. Hulmes, M. Sárospataki, C. Saure, M. Edwards, E. Genersch, S. Knäbe, R.F. Pywell, 2017: Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science 356 (6345), 1393–1395, DOI: 10.1126/science.aaa1190.
Wu, J., J.-L. Li, W.-J. Peng, F.-L. Hu, 2010: Sensitivities of three bumblebee species to four pesticides applied commonly in greenhouses in China. Insect Science 17 (1), 67–72, DOI: 10.1111/j.1744-7917.2009.01286.x.
Wu-Smart, J., M. Spivak, 2018: Effects of neonicotinoid imidacloprid exposure on bumble bee (Hymenoptera: Apidae) queen survival and nest initiation. Environmental Entomology 47 (1), 55-62, DOI: 10.1093/ee/nvx175.
Measurement Endpoint: a measurable ecological characteristic that is related to the valued characteristic chosen as the assessment endpoint and is a measure of biological effects (e.g. death, reproduction, growth) of particular species, and can include measures of exposure as well as measures of effects; Assessment Endpoint: a qualitative/quantitative expression of a specific factor with which a risk may be associated as determined through an appropriate risk assessment; an explicit expression of the environmental value that is to be protected
Ring test: an inter-laboratory test that allows to evaluate the performance of testing laboratories, and is based on analysis of similar homogeneous samples