Content uploaded by Silvia Hinarejos
Author content
All content in this area was uploaded by Silvia Hinarejos on Dec 10, 2018
Content may be subject to copyright.
1
Published by Oxford University Press on behalf of Entomological Society of America 2018.
This work is written by (a) US Government employee(s) and is in the public domain in the US.
Pollinator Ecology and Management
Pesticide Exposure Assessment Paradigm for Solitary
Bees
FabioSgolastra,1,10 SilviaHinarejos,2 Theresa L.Pitts-Singer,3 Natalie K.Boyle,3
TimothyJoseph,4 JohannesLūckmann,5 Nigel E.Raine,6 RajwinderSingh,7
Neal M.Williams,8 and JordiBosch9
1Dipartimento di Scienze e Tecnologie Agro-Alimentari, Università di Bologna, viale Fanin 42, 40127 Bologna, Italy, 2Valent U.S.A.
LLC, 6560 Trinity Court, Dublin, CA 94568, 3USDA ARS Pollinating Insects Research Unit, Logan, UT 84322, 4Landis on behalf Mitsui,
6 Wetherburn Way, Greensboro, NC 27410, 5RIFCON GmbH, 69493 Hirschberg, Germany, 6School of Environmental Sciences,
University of Guelph, Guelph, Ontario N1G 2W1, Canada, 7BASF, 26 Davis Drive, Research Triangle Park, NC 27502, 8Department
of Entomology and Nematology, University California Davis, Davis, CA, 9Centre for Ecological Research and Forestry Applications,
CREAF, Edifici C, Campus UAB, Bellaterra 08193, Spain, and 10Corresponding author, e-mail: fabio.sgolastra2@unibo.it
Subject Editor: Gloria DeGrandi-Hoffman
Received 19 March 2018; Editorial decision 25 June 2018
Abstract
Current pesticide risk assessment for bees relies on a single (social) species, the western honey bee, Apis mellifera
L. (Hymenoptera: Apidae).However, most of the >20,000 bee species worldwide are solitary. Differences in life
history traits between solitary bees (SB) and honey bees (HB) are likely to determine differences in routes and
levels of pesticide exposure. The objectives of this review are to: 1)compare SB and HB life history traits relevant
for risk assessment; 2)summarize current knowledge about levels of pesticide exposure for SB and HB; 3)identify
knowledge gaps and research needs; 4)evaluate whether current HB risk assessment schemes cover routes and
levels of exposure of SB; and 5)identify potential SB model species for risk assessment. Most SB exposure routes
seem well covered by current HB risk assessment schemes. Exceptions to this are exposure routes related to nesting
substrates and nesting materials used by SB. Exposure via soil is of particular concern because most SB species
nest underground. Six SB species (Hymenoptera: Megachilidae - Osmia bicornis L., O. cornifrons Radoszkowski,
O. cornuta Latreille, O. lignaria Say, Megachile rotundata F., and Halictidae - Nomia melanderi Cockerell) are
commercially available and could be used in risk assessment. Of these, only N.melanderi nests underground, and
the rest are cavity-nesters. However, the three Osmia species collect soil to build their nests. Life history traits of
cavity-nesting species make them particularly suitable for semifield and, to a lesser extent, field tests. Future studies
should address basic biology, rearing methods and levels of exposure of ground-nesting SB species.
Key words: risk assessment, pollinator, Osmia, Megachile, Nomia, ecotoxicology
Bees (Hymenoptera: Apoidea, Anthophila) are an extraordinarily
speciose group, with more than 20,000 species worldwide (Michener
2007, Ascher and Pickering 2017) and comprising a wide range of
biological traits and life histories. Although social species (such as
honey bees, bumblebees, and stingless bees) are most known and
recognized by the general public, most bees (ca. 70% in temper-
ate ecosystems) are solitary. Solitary life implies that each female
builds and provisions her nest and raises her offspring alone, with
no cooperation from other individuals. Another substantial portion
of bee species (ca. 20% in temperate ecosystems) are cleptoparasitic.
These species lay their eggs in the nests of other (mostly solitary)
bee species and feed on their hosts’ provisions. The remaining bee
species are social, i.e., they live in colonies with one reproductive
female and a number of nonreproductive workers (from tens to tens
of thousands, depending on the species).
Bees provide pollination services to 87% of wild owering
plants (Ollerton et al. 2011) and 75% of cultivated crops (Klein
et al. 2007). Although most agricultural pollination tradition-
ally has been attributed to the western honey bee, Apis mellifera
L.(Hymenoptera: Apidae) (Carreck and Williams 1998), other bee
species also contribute decisively to crop pollination. This contri-
bution comes not only from wild bee populations (Garibaldi etal.
2013), but also from a handful of managed species used as com-
mercial pollinators (Johansen etal. 1978, van Heemert etal. 1990,
Bosch and Kemp 2002, Pitts-Singer and Cane 2011, Peterson and
Artz 2014, Isaacs etal. 2017).
In recent decades, declines in bee diversity have been documented
in various parts of the world (Biesmeijer etal. 2006, Potts etal. 2010,
Cameron etal. 2011, Bartomeus etal. 2013, Burkle etal. 2013). The
drivers of these declines are at least partially known and include
Environmental Entomology, XX(X), 2018, 1–14
doi: 10.1093/ee/nvy105
Review
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvy105/5216970 by guest on 07 December 2018
habitat destruction and fragmentation, insufcient oral resources,
and pesticide use (Kluser and Peduzzi 2007, NRC 2007, Vanbergen
et al. 2013, Potts et al. 2016). For this reason, bee conservation
has become a priority in many countries, and several initiatives
have been undertaken at global and regional scales to reverse bee
declines and secure pollination services (Dias etal. 1999, Byrne and
Fitzpatrick 2009, Potts etal. 2016). One of these initiatives involves
the review of environmental risk assessment schemes required for
the registration and re-evaluation of plant protection products.
Regulatory agencies in the European Union and the United States
have already started this process with the publication of scientic
opinion and guidance documents (EFSA 2012, EFSA 2013, USEPA
etal. 2014). Until now, pesticide risk assessment for bees has relied
on a single species, the western honey bee, Apis mellifera L.(EPPO/
OEPP 2010). This approach assumes that the worst-case scenarios
used in honey bee risk assessment schemes are sufciently conser-
vative to protect other bee species, or that predictions for other bee
species can be extrapolated from honey bee results. However, details
of the interspecic differences in exposure and potential impacts
of pesticides are lacking. In fact, an increasing body of knowledge
shows that the impact of pesticides on bees strongly depends on spe-
cic life history traits, that ultimately determine routes and levels
of exposure, as well as on differences in sensitivity among different
taxa (Brittain and Potts 2011, Arena and Sgolastra 2014, Thompson
2016, Stoner 2016, Kopit and Pitts-Singer 2018). Consequently, the
aforementioned EFSA and USEPA documents on bees and pesticides
highlight knowledge gaps that may impede efforts to develop risk
assessment schemes that are more inclusive of the variation in life
histories found among such a diverse group of organisms. The EFSA
document (EFSA 2013), in particular, considers separate risk assess-
ment schemes for honey bees, bumblebees, and solitarybees.
This paper focuses on solitary bees and is one in a series of docu-
ments generated at the Workshop on ‘Pesticide Exposure Assessment
Paradigm for non-Apis bees’ held in 10–12 January 2017, at the
United States Environmental Protection Agency (USEPA) in
Arlington, Virginia (USA). The aim of the workshop was to focus on
routes of pesticide exposure and to understand whether the western
honey bee sufciently serves as a surrogate for pesticide risk assess-
ment for all bee species. This paper summarizes the results of the
workshop and reviews relevant facts and data with the following
objectives: 1)to provide a comparison of solitary bee and honey bee
life history traits relevant for risk assessment; 2)to summarize cur-
rent knowledge about comparative levels of pesticide exposure for
solitary bees and honey bees; 3)to identify gaps in our knowledge of
exposure and research needs; 4)to ask if the current honey bee risk
assessment paradigm provides coverage of all the routes and levels
of exposure of solitary bees; and 5)to identify potential solitary bee
model species for pesticide risk assessment.
Life History Differences Between Honey
Bees and Solitary Bees and Implications for
Pesticide Risk Assessment
As mentioned, the vast majority of bees in temperate ecosystems
are either solitary or cleptoparasites of solitary species. Like social
bees (Human etal. 2007), adult solitary bees feed mostly on nectar,
but they also ingest small amounts of pollen (especially females that
require protein to mature their eggs) (Cane 2016). Female solitary
bees build nests composed of multiple cells. In each cell, the nesting
female forms a pollen-nectar provision upon which an egg is laid.
The provision mass serves as food for the developing larva. Solitary
bees, therefore, are mass-provisioners, in contrast to social bees
whose workers typically feed larvae progressively.
Most solitary bees (ca. 65%) excavate their nests under-
ground. Underground nesting is typical of species in the families
Andrenidae, Halictidae, Melittidae, Stenotritidae, and some Apidae
and Colletidae. Most ground-nesting solitary bees line their nest cells
with glandular secretions. The rest of the species (most Megachilidae,
some Colletidae and some Apidae) nest above-ground. Most above-
ground nesters use existing cavities, such as hollow stems and aban-
doned beetle burrows in dead wood, but some excavate their nests
in dead wood or in soft-pith stems. Many of these species collect one
or more natural materials to build their nest cells (soil, leaves, resin,
plant pubescence, oral oils, etc.), and some line their cells with
glandular secretions. In contrast to social species, most solitary bees
are short-lived. Individual females live about 20–30 d, and the ight
season of a population at a given site may span 2–3 mo. In contrast
to the reproductive members of social bee colonies, fecundity is low
in solitary bees (10–40 eggs per female). In temperate climates, most
solitary bee species are univoltine (have a single generation per year),
but some may complete two or more generations per year (multivol-
tinism) under conducive environmental conditions.
The life history traits of solitary bees and honey bees that are
relevant to pesticide exposure are outlined in Table 1. Differences
between these two groups of bees in body size, foraging range, level
of pollen and nectar consumption, and exposure to various envir-
onmental materials (soil, leaves, plant pubescence, etc.) may result
in different routes and levels of exposure. Social versus solitary life
history traits may also entail different ecological consequences. For
example, in solitary bees, the death of a nesting female results in a
complete cessation of its reproductive output, whereas in social bees,
the deaths of nonreproductive individuals can be buffered by the sur-
vival of other colony members and the production of new members
(i.e., superorganism resilience) (Straub etal. 2015).
Potential Surrogate Species to Estimate
Exposure for SolitaryBees
It is obviously not feasible to examine every bee species. The use of
surrogates is a common procedure in risk assessment, and a good
surrogate species should: 1) be commercially reared so that suf-
ciently large managed populations are available; 2)be easily handled
in laboratory, semield and eld conditions; and 3)show behavioral
and life history traits representative of other species of the same tax-
onomic or ecological group. In addition, surrogate species would
ideally be natively distributed over a large geographicarea.
In spite of their diversity and importance as crop pollinators,
only a few solitary bee species are commercially reared or propa-
gated (Johansen etal. 1978, Richards 1984, Bosch and Kemp 2001,
2002, Pitts-Singer and Cane 2011, Peterson and Artz 2014). These
include: Osmia cornifrons Radoszkowski (the hornfaced bee) in
eastern Asia, Osmia cornuta Latreille (the horned mason bee) and
Osmia bicornis (= rufa) L.(the red mason bee) in Europe, Osmia lig-
naria Say (the blue orchard bee), Megachile rotundata F.(the alfalfa
leafcutting bee), and Nomia melanderi Cockerell) (the alkali bee) in
North America (Fig.1).
N.melanderi (Hymenoptera: Halictidae) is the only ground-nest-
ing species propagated for large-scale pollination (of alfalfa) (Pitts-
Singer 2008). Although it is representative of the nesting behavior
found most commonly in solitary bees, nesting aggregations only
occur in very restricted regions of the western United States. Due to its
ground-nesting behavior, N.melanderi is difcult to rear and manip-
ulate in laboratory or semield conditions, and limited attempts to
2 Environmental Entomology, 2018, Vol. XX, No. X
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvy105/5216970 by guest on 07 December 2018
Table1. Life history traits of honey bees compared with solitary bees and implications for risk assessment
Traits Honey bees Solitary bees Implications for risk assessment
Level of sociality Eusocial Solitary Due to colony resilience in social bees, extrapolation of tness
effects from the individual to the population level is easier in
solitary bees. Nesting activity and reproductive output of in-
dividual females can be measured in solitary bees, thus facili-
tating the detection of certain sublethal effects. Reproductive
output of a honey bee colony is much more difcult to
measure.
Fecundity Circa 1,500 eggs per day Usually no more than 2 eggs per
day (10–40 eggs over entire life
span)
Supply of bees for toxicological assays is much higher for
honey bees.
Trophallaxis Present Absent In solitary bees, only individual feeding is feasible in labora-
tory tests. Individual feeding is more labor intense, but the
amount of solution ingested by each individual can be accur-
ately controlled.
Nesting substrate Large cavities; hives Most species nest underground.
Others nest in small cavities
above ground.
Pesticide exposure via excavation and dwelling in soil is an im-
portant route of exposure in ground nesting solitary species.
Natural cavities used by honey bees and above-ground soli-
tary bees are unlikely exposure routes.
Nesting material Wax and propolis Mud, soil, leaves, resin, oral
oil, etc.
Several environmental matrices may be highly relevant to soli-
tary bees but less so to honey bees.
Foraging range Mean: 1.5 km
Maximum: 16 km
Mean: 100 m; Maximum: 2 kmaThe typical size of test elds (1 ha) is much more representative
of the foraging area of solitary bees than honey bees. For full
eld testing in honey bees, distance between test hives needs
to be very large to avoid overlap of control and treatment
colony foraging areas (exposure uncertainty).
Amenability to
nest in conned
conditions
Low High The behavior of solitary bees is much less affected by conne-
ment (greenhouses, screened cages). Due to their reduced
foraging range and short life span, the entire nesting period
of single nesting females can be monitored in semi-eld
conditions.
Nesting period All or most of the year Usually 2–3 mo in spring or
summer
Adult solitary bees are only available for some months (3–4
with appropriate temperature management) in spring or
summer.
Pollen transport On hind legs (in cor-
biculae); pollen wetted
with nectar and glan-
dular secretions
Most species carry dry pollen on
hind legs or ventral abdomen
(in scopae). Some species carry
pollen mixed with nectar inside
crop.
Risk of exposure via pollen is probably greatest in bees that
carry pollen inside their crop.
Body size ~100mg (workers) 2–400mgbBecause exposure level and sensitivity are body-size dependent,
a possible extrapolation factor from honey bees to solitary
bees should consider the large body size variability. Solitary
bees also show greater intraspecic variability.
Adult food Nectar + small amounts
of pollen
Nectar + small amounts of pollen The amounts and identity of nectar and pollen consumed
may vary widely depending on body size, natural history
and physiological traits (known for very few species).
Honey bees prefer to visit owers with high sugar con-
centration. Pollen ingestion in foraging honey bees is not
relevant. Nurse honey bees ingest pollen in the form of
beebread (stored pollen mixed with nectar/honey). Solitary
bee females ingest freshly-collected pollen, not mixed with
nectar.
Flower preferences Broad generalists.
Colonies typically col-
lect pollen and nectar
from many sources.
Most are generalists, but many
show a marked preference for
certain plants. Some are oligo-
lectic (collect pollen from only
one plant family)
In open eld tests, honey bees are expected to collect pollen
from the eld test and from other sources within their
foraging range. In semi-eld test, solitary species will for-
age and develop normally on non-preferred host plants.
However, in eld tests they may ignore the test eld if other
preferred pollen sources are available within their foraging
range.
Larval food Royal jelly, bee bread,
and honey
All use pollen mixed with nectar;
some species also consume
oral oil.
In honey bees, larval exposure is ‘ltered’ by nurse bees (raw
food is processed and larvae are fed glandular secretions
by workers). Solitary bee larvae consume unprocessed
food.
Environmental Entomology, 2018, Vol. XX, No. X 3
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvy105/5216970 by guest on 07 December 2018
create articial rearing protocols have failed. Consequently, informa-
tion on its biology is scarce.
Commercially available M. rotundata, O.lignaria, O.corni-
frons, O.cornuta, and O. bicornis are cavity-nesting species in
the family Megachilidae. Unlike ground-nesting species, they do
not excavate their nests, and readily accept a variety of articial
nesting sites. They are fairly easy to rear and manipulate. Large
M. rotundata and O. cornifrons populations are commercially
available in North America and eastern Asia (Japan, China, South
Korea), respectively. Supplies of O.lignaria are becoming more
widely available in the western United States, and O.cornifrons,
which was introduced to the United States from Japan in the
1980s (Batra 1998), can be purchased from a few vendors in the
Eastern United States where those bees have become established
and wild populations occur. Osmia cornuta and O.bicornis are
increasingly becoming available for commercial use in various
countries in Europe. The biology of both Megachile and Osmia
is wellknown.
Studies on the effects of pesticides on N.melanderi are sparse
(Torchio 1973, Johansen et al. 1984). Better studied is the eco-
toxicology of M.rotundata (Torchio 1973 1983; Johansen et al.
1984; Abbott etal. 2008; Huntzinger etal. 2008a,b; Scott-Dupree
etal. 2009; Hodgson etal. 2011; Artz and Pitts-Singer 2015) and
especially Osmia spp. (Ladurner etal. 2003, Tesoriero etal. 2003,
Ladurner etal. 2005, Abott etal. 2008, Ladurner etal. 2008, Scott-
Dupree etal. 2009, Biddinger et al. 2013, Hinarejos etal. 2015,
Sandrock et al. 2014, Artz and Pitts-Singer 2015, Jin etal. 2015,
Roessink etal. 2015, Ründlof etal. 2015, Sgolastra etal. 2015,
Heard etal. 2017, Peters et al. 2016, Spurgeon at al., 2016, Uhl
etal. 2016, Sgolastra etal. 2017). O.cornuta and O.bicornis are
the two risk assessment model species proposed by EFSA (European
Food Safety Authority) in Europe (EFSA 2013). Standard protocols
Fig.1. Solitary bee species commercially available in different parts of the world. Photo credits: Osmia lignaria (Derek Artz), Megachile rotundata (Theresa Pitts-
Singer), Nomia melanderi (James Cane), Osmia cornuta (Fabrizio Santi), Osmia bicornis (Laura Bortolotti), Osmia cornifrons (Suzanne Batra).
Traits Honey bees Solitary bees Implications for risk assessment
Larval food
provisioning
Progressive feeding Mass-provisioning In honey bees, the food consumed by an individual larva may
have been collected over a long period of time, and the time
between provisioning and feeding may be long. In solitary
bees, the larval food is collected over a short period of time
(1–2 d), and the larva starts feeding within a few days (e.g., 7
in Osmia, 3 in Megachile) after egg is laid.
Larval feeding period 5 d Highly variable: from a few days
to 1 mo, depending on the
species
Solitary bee larvae may feed for considerably longer periods
than honey bees.
aData from agricultural elds.
bData for European species.
Table1. Continued
4 Environmental Entomology, 2018, Vol. XX, No. X
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvy105/5216970 by guest on 07 December 2018
for laboratory and semield tests are currently being ring-tested
in Europe by the non-Apis working group of the International
Commission for Plant-Pollinator Relationships (ICPPR) (Roessink
etal. 2015).
Life History of N.melanderi
N.melanderi is native to the Western United States (Fig.1). It is a
gregarious species that excavates nests in alkaline soils. Each cell
is provisioned with nectar and pollen and sealed with a polished
soil cap. This bee is active from late June to late August. The larval
period lasts ca. 15 d, and the fth instar overwinters as a prepupa.
Development is completed in the summer, and the pupal period
lasts 10–15 d. Most populations are univoltine, but in southern
California they may produce a second generation (or more) whose
adults nest in the same summer as their mother and, thus, have
an extended ight period (Fig. 2). N. melanderi are propagated
for alfalfa pollination in certain locations of Washington State and
Oregon where natural bee beds are protected and articial beds are
created for new establishments near alfalfa elds. Aggregations are
occasionally found in other states (e.g., California, Utah, Wyoming,
and Colorado) where they were once more abundant thannow.
Life History of Osmia Species
The four aforementioned Osmia species (O. lignaria in North
America, O.cornifrons in Asia and North America, O.cornuta and
O. bicornis in Europe) (Fig. 1), often referred to as mason bees,
belong to the same subgenus Osmia (Osmia) and have very simi-
lar natural histories. As mentioned, O. cornifrons was introduced
into the United States in the 1980s and has become feral in some
states, especially in the higher latitudes of the eastern part of the
country. These Osmia spp. overwinter as cocooned adults, emerge
in early spring, and produce only one generation per year (i.e., are
univoltine). Adult females are active for ca. 2 mo between February
and May, depending on the species and the geographic area. They
use mud to build cell partitions and to seal the nest entrance. The
larval feeding period lasts ca. 1 mo. The prepupal period lasts 1–2
mo, and the pupal period ca. 1 mo. Adults eclose in late summer, but
do not emerge from cocoons until the following spring (Fig.3). All
four species have been developed as orchard pollinators in different
parts of theworld.
Life History of M.rotundata
M.rotundata is native to Europe and southwestern Asia. The spe-
cies was unintentionally introduced into North America around the
early 1940s and currently occurs across most of the United States
and southern Canada (Pitts-Singer and Cane 2011). Adults are
active for ca. 3 mo starting in June-July depending on the latitude.
They usually produce a partial second generation (and sometimes a
third and fourth generation), especially in southern latitudes. Adult
females use cut-leaf pieces to line each brood cell and to cap the nest
entrance. The larval period last ca. 20 d, and the pupal period 15
d.They overwinter as prepupae (Fig. 4). M. rotundata is the most
important alfalfa pollinator for seed production in central Canada
and the western United States. Management protocols for M.rotun-
data are well developed.
Routes of Pesticide Exposure
The relative importance of different exposure routes to adult and
larval honey bees and solitary bees of the three potential surrogate
taxa is summarized in Table2. Exposure via air particles (dust and
spray) and nectar consumption are important routes of exposure in
both honey bee and solitary bee adults (EFSA 2013, USEPA et al.
2014) (Table2). Adult honey bee workers consume bee bread (aged
Fig.2. Life cycle of Nomia melanderi. Photo credits: egg (James Cane), prepupa (James Cane), pupa (Bill Nye), adult (James Cane).
Environmental Entomology, 2018, Vol. XX, No. X 5
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvy105/5216970 by guest on 07 December 2018
pollen mixed with nectar) during the rst 2wk of their life while
they are nurse bees. In contrast, female solitary bees consume fresh
pollen throughout their entire life span (Cane 2016). In contrast to
honey bees, there are no reports that solitary bees consume honey-
dew or guttation water in natural conditions (Table2).
Soil is not likely to be an important route of exposure for honey
bees, but it is very relevant for species like N.melanderi that nest
underground (Table2). Osmia females collect soil to build nest cell
partitions, and, therefore, are also directly exposed to residues in
this material. M.rotundata females cut pieces of leaves to line and
cap their nests, and, therefore, are likely to be exposed to residues in
plant tissues and on their surfaces.
In larvae, exposure via nectar and pollen is highly relevant in
all bee species (Table2). However, honey bee larvae consume food
that may have been collected from various sources over a longer
expanse of time and stored for an extended period in the form of
bee bread (pollen with some nectar) and honey (nectar). Bee bread
and honey are ingested and processed by nurse bees before being
regurgitated into larval cells. Thus, the pollen and nectar eaten by
larvae have undergone complex aging and enzymatic transforma-
tion. In contrast, solitary bees consume recently-collected provisions
of unprocessed (often single-sourced) pollen mixed with nectar. On
the other hand, solitary bee larvae may take much longer than honey
bee larvae to consume the entire food provision. These differences
Fig.4. Life cycle of Megachile rotundata. Photo credits: egg (Bill Nye), prepupa (Alan Anderson), pupa (Alan Anderson), adult (Theresa Pitts-Singer).
Fig.3. Life cycle of Osmia spp. Photo credits: egg (USDA), prepupa (USDA), pupa (USDA), cocooned adult (USDA), emerged adult (Serena Magagnoli).
6 Environmental Entomology, 2018, Vol. XX, No. X
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvy105/5216970 by guest on 07 December 2018
in feeding strategies between honey bees and solitary bees may have
consequences on the degradation and dilution of chemical residues
found in pollen and nectar that are eventually consumed by the lar-
vae (Table1).
N. melanderi and Osmia larvae may be orally and topically
exposed to residues from soil, whereas, Megachile larvae, as well as
larvae of other solitary bees using plant materials in their nests, may
be exposed to residues from leaf surfaces that wick into the provi-
sion (Table2). Larvae of ground-nesting bees such as N.melanderi
may additionally be exposed to residues in water that are incorpo-
rated into the cell through the soil matrix.
To further understand how differences in the natural history of
honey bees and solitary bees may have consequences for pesticide
exposure, we scored the relative importance of different pesticide
exposure routes within each bee group (Table3). For adults, expos-
ure via air particles (by contact) and via pollen and nectar (oral)
are the most important exposure routes (score=4) in both honey
bees and solitary bees. However, other routes of exposure are more
important for certain solitary bees than for honey bees. Evaluation
of exposure routes indicate that the worst-case exposure scenario for
honey bee adults used in current risk assessment schemes may be suf-
cient to evaluate the potential effects on other bees, except in three
cases: 1)the likelihood of exposure via contact with pollen is sub-
stantially greater for solitary bees because they collect large amounts
of pollen throughout their activity period; honey bees collect pol-
len only for a limited period of time, and they mix it with nectar
and glandular secretions for transportation to the nest; 2)pesticide
exposure via soil is more biologically relevant in ground-nesting spe-
cies such as N.melanderi and in species that collect mud such as
Osmia spp.; and 3)all bee species are susceptible to exposure to pes-
ticides through contact with plant surfaces, but M.rotundata adults
are also orally exposed because they may ingest small amounts of
plant material while cutting leaf pieces.
As for larvae, the exposure routes that are insufciently covered
by the current honey bee risk assessment are: 1)exposure via soil,
which is highly relevant in N.melanderi and Osmia spp., but not in
honey bee larvae, which are never exposed to soil; 2)oral and con-
tact exposure via water, which is relevant in N.melanderi, because
both larvae and their pollen/nectar provision are in direct contact
with the cell soil and, therefore, may absorb contaminated water;
and 3)exposure via plant surfaces in M.rotundata larvae, because
their cells are lined with leaf cuttings.
Levels of Pesticide Exposure
Even when different species share similar exposure routes, the lev-
els of exposure may be highly species-dependent. Table4 provides
estimates of nectar and pollen intake for adult honey bees, Osmia
spp., M.rotundata and N. melanderi, as well as estimates of the
amounts of water, soil and leaves collected by these bees. Of all
the nectar collected by adult bees (both honey bees and solitary
species), some is regurgitated into the nest, and some is consumed
by the foraging bee. For this reason, direct measures of the level of
exposure via nectar in adult bees are difcult to obtain. Current
approaches rely on estimates of ight duration, energy requirements
for sustained ight, amounts of nectar collected, and nectar sugar
concentration. Using this approach, EFSA (2012) estimated nectar
consumption per foraging trip and day for honey bees (Table4).
These estimates are based on the following information: sugar
consumption per unit time during ight (8–12mg/h) (Balderrama
etal. 1992), foraging trip duration (30–80min in nectar foragers,
10min in pollen foragers) (Winston 1987), proportion of this time
Table2. Relative importance (based on expert knowledge) of pesticide exposure routes to honey bees, Osmia spp., Megachile rotundata
and Nomia melanderi
Exposure route Life stage A.mellifera Osmia spp. M.rotundata N.melanderi
Air Particles (Contact) Adults 4/0/1 4 4 4
Larvae 0 0 0 0
Nectar (Oral) Adults 4/3/2 4 4 4
Larvaea4 4 4 4
Pollen (Oral) Adults 1/3/1 4 4 4
Larvaeb4 4 4 4
Mud/Soil (Contact) Adultsc0/0/0 2 0 4
Larvae 0 1 0 4
Wax (Contact) Adults 1/3/3 0 0 0
Larvae 4 0 0 0
Water (Oral) Adults 4/1/1 1 1 1
Larvae 1 0 0 2
Plant Surfaces (Contact) Adults 3/0/0 3 4d3
Larvae 0 0 4 0
Propolis/Resin (Contact) Adults 3/1/1 0 0 0
Larvae 0 0 0 0
Honeydew (Oral) Adults 4/2/0 0 0 0
- - - -
Gutattion Water (Oral) Adults 1/1/1 0 0 0
- - - -
Values are intended for comparisons across taxa (rows), not for within-taxon comparisons (columns).
Designated values rank from 0 (marginal or no likelihood of exposure) to 4 (high likelihood of exposure), for both adults and larval bees. Under each exposure
route identied, the primary category of exposure (contact or oral) is specied. For honey bees, relative values are provided for foragers, in-hive bees and over-
wintering bees, respectively.
aAll larvae are also subject to contact exposure through nectar.
bAll larvae are also subject to contact exposure through pollen.
cAdult Osmia spp. and N.melanderi are also subject to oral exposure through mud/soil.
dAdult M. rotundata are also subject to oral exposure via plant surfaces.
Environmental Entomology, 2018, Vol. XX, No. X 7
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvy105/5216970 by guest on 07 December 2018
spent ying (80%) (Rortais etal. 2005), and 10 foraging trips per
day (Winston 1987). In these estimates, sugar content in nectar
was assumed to be 15% (w:w). The sugar concentration of nectar
loads brought into a honey bee hive ranges from 15 to 65% (Seeley
1985). Therefore, 15% can be considered a realistic worst-case sce-
nario (at higher sugar concentrations bees would require less nec-
tar and consequently would be exposed to lower pesticide levels).
There are two problems with these kinds of estimates of nectar
consumption per bee. First, each of the ve parameters involved in
the calculations (i.e., quantity of sugar required for ight, number
of foraging trips per day, duration of a foraging trip, fraction of the
foraging trip spent ying, and nectar sugar concentration) is highly
variable. For example, metabolic rates of honey bees in ight are
highly dependent on a number of factors such as ambient tem-
perature, ight speed, load carriage, and bee ontogeny and genetic
makeup (Harrison and Fewell 2002). Yet, available measures are
usually limited to a small number of individuals and environmental
conditions (often from a single study). Second, information on the
distribution of values across the observed ranges is often missing.
To avoid over-estimates that would result from using the upper
ranges of the various parameters, results in Table 4 (nectar for-
agers: 213mg/day; pollen foragers: 70mg/day) are based on the
lower estimates of each parameter, and, therefore, should be con-
sidered a conservative estimate.
Independent estimates of nectar consumption were calculated by
USEPA etal. (2012). USEPA assigned a distribution (either lognor-
mal or uniform) to each of the ve parameters involved and then
used Monte Carlo simulations to randomly select values from each
distribution. The USEPA etal. (2012) analysis also accounted for
the energy requirements of bees while at rest and assumed mean
sugar content in the nectar to be 30% based on measurements on
various plants. Using this approach, median nectar ingestion by nec-
tar foragers was estimated at 292mg/day (95th percentile: 499mg/
day) (Table4). For in-hive honey bees (brood-attending nurse bees),
nectar consumption was estimated to be at least 113mg/day (USEPA
etal. 2012). This result is based on Rortais etal. (2005) and assumes
a nectar sugar concentration of 30%. In another study (Decourtye
et al. 2005), consumption values for newly emerged bees were
22–45mg/day with a nectar sugar concentration of 500g/liter. The
lower values in the Decourtye etal. (2005) study are probably a con-
sequence of holding bees in laboratory cages at 33°C and without
brood. Under these (resting) conditions bees are expected to show
lower metabolic consumption rates than bees inside a hive. Estimates
of sugar (nectar) and protein (pollen) ingestion rates for solitary bees
are currently not available. Information on the number of foraging
trips per day and number of owers visited per trip is available for
Osmia (Bosch 1994, Bosch and Kemp 2001), but information on
energy budgets during ight that might be used to calculate sugar
consumption are lacking. However, consumption of sugar solution
(330g/liter) in newly emerged O.bicornis females maintained under
laboratory conditions averaged 59.8 (range: 31.7–104.2) µl/day
(Sgolastra etal., unpublisheddata).
The quantity of pollen consumed per day by honey bees has
been estimated at 6.5–12mg for in-hive worker bees and 0.04mg
for foraging worker bees (Table 4). Solitary bees (especially
females) are known to ingest pollen throughout their adult life, but
consumption estimates are lacking (Cane 2016; Cane etal. 2017) .
For example, a N.melanderi female rells its crop with pollen two
to three times per day, and each pollen rell contains ca. 34,000
alfalfa pollen grains (Cane et al. 2017). Thus, the amount of pol-
len consumed by N. melanderi could be estimated by obtaining
weight measurements of fresh alfalfa pollen. Apollen load and a
Table3. Relative importance (based on expert knowledge) of pesticide exposure routes to honey bees, Osmia spp., Megachile rotundata and Nomia melanderi
Exposure
route
Air particles Nectar Pollen Mud/Soil Wa x Water Plant Surfaces Propolis/Resin Honeydew Guttation
Water
Bee group Life stage Contact Oral Contact Oral Contact Oral Contact Oral Contact Oral Contact Oral Contact Oral Contact Oral Contact Oral Contact Oral
Apis mellifera Larvae00444400300100000101
Adults40141400200230110101
Osmia spp.Larvae00444420000000000000
Adults40042421000030000000
M.rotundata Larvae00444400000020000000
Adults40042400000032000000
N.melanderi Larvae00444440002200000000
Adults40040441000030000000
Values are intended for comparison across exposure routes within each taxon (rows), not for comparisons across taxa (columns).
Designated values rank from 0 (marginal or no likelihood of exposure) to 4 (high likelihood of exposure), for both adults and larval bees. Under each exposure route identied, separate rankings are provided for contact or
oral exposure.
8 Environmental Entomology, 2018, Vol. XX, No. X
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvy105/5216970 by guest on 07 December 2018
nest provision are ca. 200,000 and ca. 4.25 million alfalfa grains,
respectively (Cane etal. 2017).
Daily rates of water collection were estimated by EFSA (2012)
for honey bees by assuming that individuals conduct an average of
46 water trips per day with a crop capacity of 30–58µl. Comparable
data are not currently available for solitary bees, but water ingestion
has rarely been observed in this group of bees. There is a critical need
for research to understand if water is directly taken in by solitary
bees (adults and larvae), and if this activity is ubiquitous among all
solitary bees or restricted to certain life histories or environmental
conditions.
Body surface area of a bee is a useful measure for estimating top-
ical exposure. Using X-ray computed tomography, and the residues
found on the body surface after a spray application with a Potter
tower, Poquet etal. (2014) estimated the body surface area of honey
bee workers (Table4). To our knowledge, this kind of information
represents another knowledge gap for solitarybees.
Amounts of mud collected throughout the nesting period in
O.cornuta are 2.2–4.4 g (dry weight), corresponding to 1.1g per
nest (Bosch and Vicens 2005). In M.rotundata, a female can collect
up to 4.9g of leaves throughout her nesting period (Klostermeyer
etal. 1973). Apossible calculation for chronic pesticide exposure (µg
of active ingredient/day) via plant surface for the adults of M.rotun-
data is estimated with the formula:
ExposureARFTC ET=** *
Where:
AR=pesticide application rate (µg a.i./cm2);
F=% fraction of application rate available for transfer to bees
(USEPA 1996);
TC=transfer coefcient (cm2/unittime);
ET=exposure time to foliage (unit time/day).
Estimates of nectar and pollen intake for the larvae of honey bees
and non-Apis bees are summarized in Table5. Total nectar consump-
tion by a honey bee worker larva has been estimated by USEPA etal.
(2012) based on total food consumed (120mg) during days 4 and 5
(only royal jelly is consumed in the rst 3 d), minus the amount of
pollen (5.4mg), and corrected by the percentage of sugar in honey
(45%) and nectar (30%). Daily nectar consumption has been esti-
mated based on rates of food consumption and exponential growth
during the last 2 d of larval development (USEPA et al. 2012).
Overall pollen consumption of honey bee larvae has been estimated
Table4. Available estimates of food (nectar and pollen) and water intake and other parameters relevant to pesticide exposure levels in
honey bees, Osmia spp., Megachile rotundata and Nomia melanderi adults
Exposure route Apis mellifera (by task) Osmia spp. Megachile
rotundata
Nomia
melanderi
Nectar consumption/foraging trip Nectar foragera: ≥21.3mg; ? ? ?
Pollen foragera: ≥7 mg
Nectar consumption/day Nectar foragera,b: ≥213mg; 292 mg ? ? ?
Pollen foragera: ≥70 mg
In-hive beeb,i: ≥113mg; 140 mg
Pollen consumption/day Nectar foragerc: 0.041mg; ? ? ?
Pollen foragerc: 0.041 mg*
In-hive beed: 6.5–12 mg
Body surface area Workere: 1.05cm2? ? ?
Amount of soil/leaves collected during life span NR 2.2–4.4gg≥ 4.9gh?
Water collected/day Water foragerf: 1.4–2.7 ml NR NR NR
Values presented herein are supported by the following references: aEFSA (2012); bUSEPA (2012); cCrailsheim etal. (1992, 1993); dRortais etal. (2005); ePoquet
etal. (2014); fEFSA (2012); gBosch and Vicens (2005); hKlostermeyer etal. (1973); iUSEPA (2014).
*Forager pollen exposure is predominantly through contact.
NR: Not relevant.?: Unknown.
Table5. Available estimates of food intake and other parameters relevant to pesticide exposure levels in honey bee, Osmia spp., Megachile
rotundata and Nomia melanderi larvae
Route of exposure Apis mellifera Osmia spp. Megachile
rotundata
Nomia
melanderi
Life span nectar consumption 172mga; 59.4mg (sugar)b87mgd31mge?
Daily nectar consumption Day 4: 56mgc-60mgf2.9mgd3.1mg ?
Day 5: 117c-120mgf
Life span pollen consumption 1.5–5.4mgb455mgd62mge?
Daily pollen consumption 2.7mgc15.2mgd6.2mg ?
Day 4: 1.8mgf
Day 5: 3.6mgf
Wax contact ? NR NR ?
Soil contact NR ? NR ?
Leaf contact NR NR ? NR
Values presented herein are supported by the following references: aUSEPA (2012); bEFSA (2013); cRortais etal. (2005); dIndependent EFSA (2013) estimates
of sugar and pollen consumption in Osmia larvae are 54 and 387mg, respectively; eEFSA (2012); fUSEPA (2014).
NR: Not relevant.?: Unknown.
Environmental Entomology, 2018, Vol. XX, No. X 9
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvy105/5216970 by guest on 07 December 2018
from 1.5 (maize pollen) to 5.4 (red clover pollen) mg, (Rortais etal.
2005), which corresponds to 0.75–2.7mg of pollen perday.
The ratio of nectar to pollen in the provision of solitary bees var-
ies widely across species. For example, provisions have a higher nec-
tar content in M.rotundata (nectar/pollen weight ratio: 2:1 (Cane
et al. 2011) than in O. cornuta (nectar/pollen weight ratio: 1:3,
Ladurner etal. 1999). Even after accounting for this degree of varia-
bility, pollen consumption appears to be higher in solitary bees than
in honey bees. In O.cornuta, nectar and pollen consumption was
estimated by EFSA (2013) based on mean female provision weight
(542mg) (Bosch and Vicens 2002) and the nectar/pollen weight ratio
(Ladurner etal. 1999). Daily rates of food consumption were calcu-
lated assuming a feeding period of 30 d under eld conditions (Bosch
etal. 2008). Nectar and pollen consumption of M.rotundata was
estimated by EFSA (2012) based on provision weight (90–94mg),
percentage of pollen and nectar weight in the provision (33–36 and
64–67, respectively) (Cane etal. 2011), and larval feeding period (10
d) (Kemp and Bosch 2000). Comparable information is not available
for N.melanderi.
Information needed to estimate the levels of exposure via wax
in honey bees, and via soil in Osmia spp. and N.melanderi is insuf-
cient. However, combined contact and oral exposure via leaves in
M.rotundata can be possiblyestimated again with the formula:
ExposureARFTC ET=** *
Which can be simpliedto
Exposure**=
AR FSAi
Where:
SAi=internal surface area of nest cell (cm2)
assuming a worst-case scenario under which pesticide residues of
the leaf surface in contact with the pollen-nectar provision are com-
pletely transferred (TC=1) and incorporated by the bee throughout
its larval life span.
Discussion
The aim of this paper is to examine differences between life his-
tory traits between honey bees and solitary bees that reveal to what
extent the current honey bee risk assessment is sufcient for evaluat-
ing pesticide exposure in solitary bee species.
Exposure routes adequately addressed by current honey bee-
based risk assessment schemes include routes that are more relevant
for honey bees than for solitary bees (e.g., honeydew, wax, guttation
uid and water in adults), as well as those that are shared by both
bee groups (air particles, nectar in adults). Other routes of exposure
show important differences between honey bees and solitary bees, but
might be well covered by current honey bee risk assessment schemes,
which rely on conservative worst-case scenario assumptions (e.g.,
that the entire food provision consumed by a larva is contaminated,
and that no pesticide degradation occurs over time). However, larval
exposure to pollen and nectar is very different between honey bees
and solitary bees. First, overall pollen consumption per larva is much
greater in solitary bees. Second, in honey bees, pollen and nectar
larval exposure is ‘ltered’ by nurse bees, whereas larvae of solitary
bees consume unprocessed food and are, therefore, more directly
exposed. Third, honey bee larvae consume food that may have been
collected and stored over a longer period of time and, thus, may have
been exposed to a long aging period, potentially allowing for greater
degradation and dilution of chemicals. Lastly, some solitary bees
have longer feeding periods than honey bees. The expected effects of
a pesticide (and its degradation products) will vary due to the afore-
mentioned differences in food provisioning and feeding behavior, as
well as the chemical properties of the compound.
Some exposure routes relevant for solitary bees are not relevant
for honey bees, or represent higher levels of exposure for solitary
bees than honey bees, and therefore are not sufcientlyaddressed
by the current honey bee risk assessment paradigm. One particularly
important route for solitary bees is exposure via soil, including con-
tact with the soil itself, as well as contact and ingestion of water
from the soil. This route of exposure is obviously very important for
both adults and larvae of species nesting underground. N.melanderi
would be a good surrogate solitary bee to study this exposure route,
but this species is only available in limited numbers in small areas
of the Western United States. The three Osmia species considered
in this review use mud to build their nest cells and, therefore, are
also exposed to soil contaminants, although to a lesser extent than
ground nesting species. These Osmia species could be used as sur-
rogates for ground-nesting bees until a better alternative becomes
available. Plant surfaces are an exposure route relevant to both leaf-
cutting bees and other solitary species that use plant material to build
their nests (e.g., masticated leaf pulp in many Osmia species; plant
pubescence in Anthidium species (Hymenoptera: Megachilidae)). As
such, M.rotundata would be a good species for studies that quantify
this route of exposure. Importantly, soil and mud are only two of the
various natural products used by solitary bees to construct and line
their nests. Some species use resin (e.g., Heriades, some Megachile
and some Anthidiini; Hymenoptera: Megachilidae), and some use
oral oils (e.g., some Centris; Hymenoptera: Apidae). To our knowl-
edge, potential levels of contamination in these matrices have not
been investigated.
There is currently insufcient information on adult exposure via
pollen in solitary bees compared to honey bees. However, it is known
that solitary bee females transport and manipulate large amounts
of unprocessed pollen during foraging, ying to the nest, and pro-
visioning throughout their life time. Honey bees, on the other hand,
only collect pollen towards the end of their life span, and they mix
it with nectar and glandular secretions for transportation. The three
solitary bee taxa considered, Osmia spp., M.rotundata and N.mel-
anderi, would be good representatives of most solitary bees to cover
this exposure route. In addition to pollen and nectar, an estimated
1.4% of solitary bee species consume oral oils (as adults and/or as
larvae) (Buchmann 1987). This route of exposure is not experienced
by honey bees or any of the three solitary bee taxa proposed here as
surrogate species.
Our review identies some important gaps in knowledge relat-
ing to pesticide exposure levels for solitary bees. Estimates of nec-
tar and pollen consumption in adult Osmia spp., M. rotundata
and N. melanderi, in particular, should become a research priority.
These estimates could be obtained following the same approach used
with honey bees. At least for Osmia spp. and M.rotundata, most of
the parameters needed to calculate pollen and nectar consumption
are available, but measures of energetic expenditure during ight
are lacking. Importantly, these calculations should account for the
high level of variability associated with these measures (Harrison
and Fewell 2002). Quantication of the levels of exposure via soil
and plant surfaces are also lacking in solitary bees. We provide
an approach for the estimation of these levels in Osmia spp. and
M.rotundata, respectively, but further studies are needed to measure
some of the parameters involved.
Table6 shows a comparison of the three solitary bee taxa pro-
posed as model species for risk assessments. N.melanderi is the only
representative species of the most common nesting behavior found
10 Environmental Entomology, 2018, Vol. XX, No. X
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvy105/5216970 by guest on 07 December 2018
in solitary bees. However, its use as a surrogate species is hindered
by its limited availability, its restricted geographical range and the
very particular type of soil required for its nesting. For these reasons,
we see the study of the basic biology and the establishment of rear-
ing methods for ground-nesting species with more generalist nesting
habits as a research priority. The highly speciose and widely distrib-
uted genus Andrena (Hymenoptera: Andrenidae) could be a good
alternative. Although not commercially available, the hoary squash
bee (Peponapis pruinosa (Say), Hymenoptera: Apidae) is a ground
nesting species that is geographically widespread in North America
(López-Uribe etal. 2016). The ecology and behavior of this special-
ist pollinator of cucurbit crops (e.g., pumpkin, squash, and water-
melon) is comparatively well studied (Hurd et al. 1974, Willis and
Kevan 1995, Julier and Roulston 2009), with an increasing focus on
the potential impacts of pesticide exposure (e.g., Stoner and Eitzner
2012, Health Canada 2014). Recent success establishing popula-
tions of nesting females in enclosures (DSW Chan and NE Raine,
personal communication) increases the potential of this species for
ecotoxicological tests under semield and eld conditions, although
utility for laboratory studies remains unknown.
As for cavity-nesters, both Osmia spp. and M. rotundata are
good surrogate species. M.rotundata is commercially available in
large numbers, but only in North America. Osmia spp. are avail-
able in smaller numbers, but are more widely spread, and their use
as commercial pollinators is increasing. Osmia spp. have been sug-
gested as model solitary bees for risk assessment in Europe (EFSA
2013), where test protocols are under development (Roessink etal.
2015), and information on their ecotoxicology is accumulating.
Our review of the life history traits of solitary bees reveals that
both Osmia spp. and M.rotundata meet criteria for being practical
surrogates for semield and full-eld toxicity tests. Semield tests are
typically conducted with small honey bee colonies in screen cages
or plastic tunnels planted with a pollinator-attractive crop such as
oilseed rape (Brassica napus, Brassicaceae) or lacy phacelia (Phacelia
tanacetifolia, Boraginaceae). However, even for a small colony, it is
challenging to provide sufcient oral resources in an enclosure, and
honey bees tend to become stressed in these conditions. By contrast,
the behavior of solitary bees is much less affected by connement.
Due to their more localized foraging range, lower food requirements
and shorter life span, it is relatively easy to provide sufcient o-
ral resources. Nesting activities of individually-marked females can
be monitored, and several variables related to individual reproduc-
tive success can be measured (Tepedino and Torchio 1982, Sugiura
and Maeta 1989, Peach etal. 1995, Ladurner etal. 2008, Sandrock
etal. 2014, Artz and Pitts-Singer 2015, Sgolastra etal. 2016). The
possibility to monitor individual females throughout their activity
period also facilitates the observation of behavioral responses, and,
therefore, the detection of sublethal effects. Although both Osmia
spp. and M.rotundata females show preferences for certain pollen
types, under conned conditions, they readily collect a variety of
pollen/nectar sources (including lacy phacelia and/or oilseed rape in
Osmia spp.) on which progeny successfully develop. The short for-
aging ranges and the possibility to measure a number of endpoints
related to reproductive success at the individual level (Bosch and
Vicens 2006), make these species also appropriate for eld tests.
However, in this case, the pollen preferences of each species (fruit
trees (Rosaceae) for O.cornuta, O.lignaria and O.cornifrons, oak
(Fagaceae) for O. bicornis, and legumes (Fabaceae) for M.rotun-
data), should be taken into account to ensure that females do most
of their foraging in the testeld.
In addition to exposure routes and levels of exposure, other
factors differ between honey bees and solitary bees in response to
pesticides. These factors include the differential sensitivity to pes-
ticide exposure among different bee species (Arena and Sgolastra
2014, Uhl etal. 2016, Sgolastra etal. 2017). These differences may
be due to variability in specic detoxication capacities, and also to
differences in body size. Mass-specic metabolic rates increase with
decreasing body size. Thus, for a given pesticide concentration in
nectar or pollen, smaller bees are expected to ingest larger amounts
of pesticides per body mass unit. Similarly, the ratio of body surface
area to body volume increases with decreasing body size. Therefore,
smaller bees are also likely to be subjected to higher levels of con-
tact exposure per unit of body mass. Future research is needed to
address differences in sensitivity to pesticides among bee species,
including honey bees, bumblebees, and solitary bees. These studies
will be essential not only to detect differences in sensitivity among
species but also to establish factors that can be used to extrapolate
pesticide toxicity from honey bees to other bee species (Arena and
Sgolastra 2014, Thompson 2016). Ultimately, exposure cannot be
disassociated from effects (toxicity) in risk assessment, and integra-
tion of these two areas of knowledge is imperative to assure bee
safety in managed environments.
Acknowledgments
The authors acknowledge the input received by all participants of the
Workshop on ‘Pesticide Exposure Assessment Paradigm for non-Apis bees’.
We also appreciate the helpful comments of Christoph Sandrock and an
anonymous reviewer.
ReferencesCited
Abbott, V. A., J.L. Nadeau, H. A. Higo, and M. L.Winston. 2008. Lethal
and sublethal effects of imidacloprid on Osmia lignaria and clothianidin
on Megachile rotundata (Hymenoptera: Megachilidae). J. Econ. Entomol.
101: 784–796.
Arena, M., and F.Sgolastra. 2014. A meta-analysis comparing the sensitivity
of bees to pesticides. Ecotoxicology. 23: 324–334.
Artz, D. R., and T. L. Pitts-Singer. 2015. Effects of fungicide and adjuvant
sprays on nesting behavior in two managed solitary bees, Osmia lignaria
and Megachile rotundata. Plos One. 10: e0135688.
Table6. Features of potential solitary bee surrogate taxa for pesticide risk assessment
Management consideration Osmia spp. Megachile rotundata Nomia melanderi
Availability (commercial populations) + ++ -
Availability (geographical distribution) North America, Europe, Eastern Asia North America Small area in North America
Availability (seasonality) 3–4 mo (spring) 4–5 mo (summer) 4–5 mo (summer)
Rearing and management + + -
Representative of other bees species -/+ - ++
(above-ground-nesting, soil) (above-ground-nesting, leaves) (ground-nesting)
General background information +++ +++ +
Ecotoxicological information ++ + -
Environmental Entomology, 2018, Vol. XX, No. X 11
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvy105/5216970 by guest on 07 December 2018
Ascher, J. S., and J.Pickering. 2017. Discover Life bee species guide and world
checklist (Hymenoptera: Apoidea: Anthophila). http://www.discoverlife.
org/mp/20q?search=Apoidea
Balderrama, N. M., L.O. Almeida, and J. A.Núñez. 1992. Metabolic rate dur-
ing foraging in the honeybee. J. Comp. Physiol. B. 162: 440–447.
Bartomeus, I., J.S. Ascher, J. Gibbs, B. N. Danforth, D. L. Wagner, S. M.
Hedtke, and R.Winfree. 2013. Historical changes in northeastern US bee
pollinators related to shared ecological traits. Proc. Natl. Acad. Sci. USA.
110: 4656–4660.
Batra, S. W.T. 1998. Hornfaced bees for apple pollination. Am. Bee J. 138:
364–365.
Biddinger, D. J., J. L. Robertson, C. Mullin, J. Frazier, S. A. Ashcraft, E. G.
Rajotte, N. K. Joshi, and M.Vaughn. 2013. Comparative toxicities and
synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia
cornifrons (Radoszkowski). Plos One. 8: e72587.
Biesmeijer, J. C., S.P. Roberts, M. Reemer, R. Ohlemüller, M. Edwards, T.
Peeters, A. P. Schaffers, S. G. Potts, R. Kleukers, C. D. Thomas, etal. 2006.
Parallel declines in pollinators and insect-pollinated plants in Britain and
the Netherlands. Science. 313: 351–354.
Bosch, J. 1994. The nesting behaviour of the mason bee, Osmia cornuta
(Latr) with special reference to its pollinating potential (Hymenoptera,
Megachilidae). Apidologie. 25: 84–93.
Bosch, J., and W. P.Kemp. 2001. How to Manage the Blue Orchard Bee as
an Orchard Pollinator. Sustainable Agriculture Network, Beltsville, MA.
Bosch, J., and N.Vicens. 2002. Body size as an estimator of production costs
in a solitary bee. Ecol. Entomol. 27: 129–137.
Bosch, J., and N.Vicens. 2005. Sex allocation in the solitary bee Osmia cor-
nuta: do females behave in agreement with Fisher ́ s theory? Behav. Ecol.
Sociobiol. 59: 124–132.
Bosch, J. and N. Vicens. 2006. Relationship between body size, provision-
ing rate, longevity and reproductive success in females of the solitary bee
Osmia cornuta. Behav. Ecol. Sociobiol. 60: 26–33.
Bosch, J., J. Bosch, and W. P.Kemp. 2002. Developing and establishing bee
species as crop pollinators: the example of Osmia spp. (Hymenoptera:
Megachilidae) and fruit trees. Bull. Entomol. Res. 92: 3–16.
Bosch, J., F.Sgolastra, and W. P. Kemp. 2008. Life cycle ecophysiology of
Osmia mason bees used as crop pollinators, pp. 83–104. In R. R. James,
and T. L. Pitts- Singer (eds.), Bee pollination in agricultural ecosystems.
Oxford University Press, Oxford, UK.
Brittain, C., and S. G.Potts. 2011. The potential impacts of insecticides on the
life-history traits of bees and the consequences for pollination. Basic Appl.
Ecol. 12: 321–331.
Buchmann, S. L. 1987. The ecology of oil owers and their bees. Annu. Rev.
Ecol. Syst. 18: 343–369.
Burkle, L. A., J.C. Marlin, and T. M.Knight. 2013. Plant-pollinator interac-
tions over 120years: loss of species, co-occurrence, and function. Science.
339: 1611–1615.
Byrne, A., and F.Fitzpatrick. 2009. Bee conservation policy at the global,
regional and national levels. Apidologie. 40: 194–210.
Cameron, S. A., J. D.Lozier, J. P.Strange, J. B.Koch, N.Cordes, L. F.Solter, and
T. L.Griswold. 2011. Patterns of widespread decline in North American
bumble bees. Proc. Natl. Acad. Sci. 108: 662–667.
Cane, J. H. 2016. Adult pollen diet essential for egg maturation by a solitary
Osmia bee. J. Insect Physiol. 95: 105–109.
Cane, J. H., D. R.Gardner, and P. A.Harrison. 2011. Nectar and pollen sug-
ars constituting larval provisions of the alfalfa leaf-cutting bee (Megachile
rotundata) (Hymenoptera: Apiformes: Megachilidae). Apidologie. 42:
401–408.
Cane, J. H., H. E.M.Dobson, and B.Boyer. 2017. Timing and size of daily
pollen meals eaten by adult females of a solitary bee (Nomia melanderi)
(Apiformes: Halictidae). Apidologie. 48: 17–30.
Carreck, N., and I.Williams. 1998. The economic value of bees in the UK. Bee
World. 97: 115–123.
Crailsheim, K., L. H.W.Schneider, N.Hrassnigg, G.Bühlmann, U.Brosch,
R.Gmeinbauer, and B.Schöffmann. 1992. Pollen consumption and utili-
zation in worker honeybees (Apis mellifera carnica): dependence on indi-
vidual age and function. J. Insect Physiol. 38: 409–419.
Crailsheim, K., N. Hrassnigg, R. Gmeinbauer, M J. Szolderits,
L. H.W.Schneider, and U.Brosch. 1993. Pollen utilization in non‐breed-
ing honeybees in winter. J. Insect Physiol. 39: 369–373.
Decourtye, A., J. Devillers, E. Genecque, K. Le Menach, H. Budzinski,
S. Cluzeau, and M. H.Pham-Delègue. 2005. Comparative sublethal toxic-
ity of nine pesticides on olfactory learning performances of the honeybee
Apis mellifera. Arch. Environ. Contam. Toxicol. 48: 242–250.
Dias, B. S. F., A. Raw, and V. L. Imperatriz-Fonseca. 1999. International
Pollinators Initiative: The Sao Paulo declaration on pollinators, report on
the recommendations of the workshop on the conservation and sustaina-
ble use of pollinators in agriculture with emphasis on bees. [online] www.
biodiv.org/doc/case-studies/agr/cs-agr-pollinator-rpt.pdf
European and Mediterranean Plant Protection Organization (EPPO/OEPP).
2010. Environmental risk assessment scheme for plant protection prod-
ucts, Chapter10: honeybees. EPPO Bull. 40: 323–331.
European Food Safety Authority (EFSA). 2012. Scientic 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 J.
10: 1–275. doi:10.2903/j.efsa.2012.2668
European Food Safety Authority (EFSA). 2013. Guidance document on
the risk assessment of plant protection products on bees (Apis mellif-
era, Bombus spp. and solitary bees). EFSA J. 11: 1–266. doi:10.2903/j.
efsa.2013.3295
Garibaldi, L. A., I.Steffan-Dewenter, R.Winfree, M. A.Aizen, R.Bommarco,
S. A.Cunningham, and A. M.Klein. 2013. Wild pollinators enhance fruit
set of crops regardless of honey bee abundance. Science 339: 1608–1611.
Harrison, J. F., and J. H.Fewell. 2002. Environmental and genetic inuences
on ight metabolic rate in the honey bee, Apis mellifera. Comp. Biochem.
Physiol. A.Mol. Integr. Physiol. 133: 323–333.
Health Canada. 2014. Initiation of Special Reviews: Potential environmen-
tal risk related to Peponapis pruinosa exposure to clothianidin, imida-
cloprid and thiamethoxam used on cucurbits. https://www.canada.ca/
en/health-canada/services/consumer-product-safety/reports-publications/
pesticides-pest-management/decisions-updates/reevaluation-note/2014/
peponapis-pruinosa-exposure-clothianidin-imidacloprid-thiamethox-
am-rev2014-06.html
Heard, M. S., J. Baas, J. L. Dorne, E. Lahive, A. G. Robinson, A. Rortais, D.
J. Spurgeon, C. Svendsen, and H.Hesketh. 2017. Comparative toxicity of
pesticides and environmental contaminants in bees: are honey bees a use-
ful proxy for wild bee species? Sci. Total Environ. 578: 357–365.
van Heemert, C., A.de Ruijter, J.van den Eijnde, and J.van der Steen. 1990.
Year-round production of bumblebee colonies for crop pollination. Bee
World. 71: 54–56.
Hinarejos S., X.Domene, and J.Bosch. 2015. Oral toxicity of dimethoate to
adult Osmia cornuta using an improved laboratory feeding method for
solitary bees. 12th Int Symp of ICP-PR. Hazards of Pesticides to Bees,
Ghent, Belgium, 15–17 September 2014. Julius-Kuhn-Arch 450: 192.
Hodgson, E. W., T.L. Pitts-Singer, and J. D. Barbour. 2011. Effects of the
insect growth regulator, novaluron on immature alfalfa leafcutting bees,
Megachile rotundata. J. Insect Sci. 11: 43.
Human, H., S.W. Nicolson, K. Strauss, C. W. Pirk, and V.Dietemann. 2007.
Inuence of pollen quality on ovarian development in honeybee workers
(Apis mellifera scutellata). J. Insect Physiol. 53: 649–655.
Huntzinger, C. I., R.R. James, J. Bosch, and W. P.Kemp. 2008a. Laboratory
bioassays to evaluate fungicides for chalkbrood control in larvae of the
alfalfa leafcutting bee (Hymenoptera: Megachilidae). J. Econ. Entomol.
101: 660–667.
Huntzinger, C. I., R.R. James, J. Bosch, and W. P.Kemp. 2008b. Fungicide
tests on adult alfalfa leafcutting bees (Hymenoptera: Megachilidae). J.
Econ. Entomol. 101: 1088–1094.
Hurd P. D., E. G.Linsley, and A. E.Michelbacher. 1974. Ecology of the squash
and gourd bee, Peponapis pruinosa, on cultivated cucurbits in California
(Hymenoptera: Apoidea). Smithsonian Institution Press, Washington, DC.
Isaacs, R., N. Williams, J. Ellis, T. L. Pitts-Singer, R. Bommarco, and
M.Vaughan. 2017. Integrated Crop Pollination: combining strategies to
ensure stable and sustainable yields of pollination-dependent crops. Basic
Appl. Ecol. 22: 44–60.
12 Environmental Entomology, 2018, Vol. XX, No. X
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvy105/5216970 by guest on 07 December 2018
Jin, N., S. Klein, F. Leimig, G. Bischoff, and R. Menzel. 2015. The neonico-
tinoid clothianidin interferes with navigation of the solitary bee Osmia
cornuta in a laboratory test. J. Exp. Biol. 218: 2821–2825.
Johansen, C. A., D. F.Mayer, and J. D.Eves. 1978. Biology and management
of the alkali bee, Nomia melanderi Cockerell (Hymenoptera: Halictidae).
Melanderia. 28: 25–46.
Johansen, C. A., C. M.Rincker, D. A.George, D. F.Mayer, and C. W.Kious.
1984. Effects of aldicarb and its biologically-active metabolites on bees.
Environ. Entomol. 13: 1386–1398.
Julier, H. E., and T. H.Roulston. 2009. Wild bee abundance and pollination
service in cultivated pumpkins: farm management, nesting behavior and
landscape effects. j. Econ. Entomol. 102: 563–573.
Kemp, W. P., and J.Bosch. 2000. Development and emergence of the alfalfa
pollinator Megachile rotundata (Hymenoptera : Megachilidae). Ann.
Entomol. Soc. Am. 93: 904–911.
Klein, A. M., B.E. Vaissière, J. H. Cane, I. Steffan-Dewenter, S. A. Cunningham,
C. Kremen, and T.Tscharntke. 2007. Importance of pollinators in chan-
ging landscapes for world crops. Proc. Biol. Sci. 274: 303–313.
Klostermeyer, E. C., S. J.Mech Jr., and W. B.Rasmussen. 1973. Sex and weight
of Megachile rotundata (Hymenoptera: Megachilidae) progeny associated
with provision weights. J Kans. Entomol. Soc. 46: 536–548.
Kluser, S., and P.Peduzzi. 2007. Global pollinator decline: a literature review,
UNEP/GRID-Europe, Geneva. pp. 10.
Kopit, A. M., and T. L.Pitts-Singer. 2018. Routes of pesticide exposure in
solitary, cavity-nesting bees. Environ. Entomol. 47: 499–510.
Ladurner, E., B. Maccagnani, D. Tesoriero, M. Nepi, and A. Felicioli.
1999. Laboratory rearing of Osmia cornuta Latreille (Hymenoptera
Megachilidae) on articial diet. Boll. Ist. Entomol. “G. Grandi” Univ.
Bologna. 53: 133–146.
Ladurner, E., J.Bosch, S.Maini, and W. P. Kemp. 2003. A method to feed
individual bees (Hymenoptera: Apiformes) known amounts of pesticides.
Apidologie. 34: 597–602.
Ladurner, E., J.Bosch, S.Maini, and W. P.Kemp. 2005. Assessing delayed and
acute toxicity of ve formulated fungicides to Osmia lignaria Say and Apis
mellifera. Apidologie. 36: 449–460.
Ladurner, E., J. Bosch, W. P. Kemp, and S.Maini. 2008. Foraging and nesting
behavior of Osmia lignaria (Hymenoptera: Megachilidae) in the presence
of fungicides: cage studies. J. Econ. Entomol. 101: 647–653.
López-Uribe, M. M., R. L.Minckley, J.Cane, and B. N.Danforth. 2016. Crop
domestication facilitated rapid geographical expansion of a specialist pol-
linator, the squash bee Peponapis pruinosa. Proc. Roy. Soc. Lond. B Bio.
283: 20160443.
Michener, C. D. 2007. The bees of the world, 2nd ed. John Hopkins University
Press, Baltimore, MA.
National Research Council (NRC). 2007. Status of pollinators in North
America. Committee on the Status of Pollinators in North America; Board
on Life Sciences; Board on Agriculture and Natural Resources; Division on
Earth and Life Studies. National Academy Press, Washington, DC.
Ollerton, J., R.Winfree, and S.Tarrant. 2011. How many owering plants are
pollinated by animals? Oikos. 120: 321–326.
Peach, M. L., A. G.Alston, and V. J. Tepedino. 1995. Sublethal effects of
carbaryl bran bait on nesting performance, parental investment, and
offspring size and sex ratio of the alfalfa leafcutting bee (Hymenoptera:
Megachilidae). Environ. Entomol. 24: 34–39.
Peters, B., Z.Gao, and U.Zumkier. 2016. Large-scale monitoring of effects of
clothianidin dressed oilseed rape seeds on pollinating insects in Northern
Germany: effects on red mason bees (Osmia bicornis). Ecotoxicology. 25:
1679–1690. doi:10.1007/s10646-016-1729-4
Peterson, S. S., and D. R.Artz. 2014. Production of solitary bees for polli-
nation in the United States, pp. 653–681. In J. A. Morales-Ramos, M.
Guadalupe Rojas, and D. I. Shapiro-Ilan (eds.), Mass production of bene-
cial organisms. Academic Press, Cambridge, MA.
Pitts-Singer, T. L. 2008. Past and present management of alfalfa bees, pp.
105–123. In R. R. James, and T. L. Pitts-Singer (eds.), Bee pollination in
agricultural ecosystems. Oxford University Press, Oxford, UK.
Pitts-Singer, T. L., and J. H.Cane. 2011. The alfalfa leafcutting bee, Megachile
rotundata: the world’s most intensively managed solitary bee. Annu. Rev.
Entomol. 56: 221–237.
Poquet, Y., L. Bodin, M. Tchamitchian, M. Fusellier, B. Giroud, F. Lafay, A.
Buleté, S. Tchamitchian, M. Cousin, M. Pélissier, etal. 2014. A pragmatic
approach to assess the exposure of the honey bee (Apis mellifera) when
subjected to pesticide spray. Plos One. 9: e113728.
Potts, S., S.Roberts, R.Dean, G.Marris, M.Brown, R.Jones, P.Neumman,
and J.Settele. 2010. Declines of managed honey bees and beekeepers in
Europe. J. Apicult. Res. 49: 15–22.
Potts, S. G., V. L. Imperatriz-Fonseca, and H. T. Ngo, (eds). 2016. The
assessment report of the Intergovernmental Science-Policy Platform on
Biodiversity and Ecosystem Services (IPBES) on pollinators, pollination
and food production. In Secretariat of the Intergovernmental Science-
Policy Platform on Biodiversity and Ecosystem Services. Bonn, Germany.
552 pp.
Richards, K. W. 1984. Alfalfa leafcutter bee management in Western Canada.
Agriculture Canada Publication 1495/E, Agriculture Canada, Ottawa,
Canada.
Roessink, I., N.Hanewald, C.Schneider, P.Medrzycki, J.Bosch, S.Hinarejos,
D.Gladbach, L.Stanisavljević, S.Krnjajić, A.Schnurr, etal. 2015. First
results of a method proposal for a solitary bee (Osmia spp.) rst tier
acute contact laboratory test. Presentation at 25th Annual Meeting of the
Society of Environmental Toxicology and Chemistry (SETAC). Barcelona,
Spain, May 2015.
Rortais, A., G. Arnold, M. P.Halm, and F.Touffet-Briens. 2005. Modes of
honeybees exposure to systemic insecticides: estimated amounts of con-
taminated pollen and nectar consumed by different categories of bees.
Apidologie. 36: 71–83.
Rundlöf, M., G. K. Andersson, R. Bommarco, I. Fries, V. Hederström,
L. Herbertsson, O. Jonsson, B. K. Klatt, T. R. Pedersen, J. Yourstone, etal.
2015. Seed coating with a neonicotinoid insecticide negatively affects wild
bees. Nature. 521: 77–80.
Sandrock, C., L. G.Tanadini, J. S. Pettis, J. C.Biesmeijer, S. G.Potts,
and P.Neumann. 2014. Sublethal neonicotinoid insecticide exposure
reduces solitary bee reproductive success. Agr. Forest Entomol. 16:
119–128.
Scott-Dupree, C. D., L. Conroy, and C. R.Harris. 2009. Impact of currently used
or potentially useful insecticides for canola agroecosystems on Bombus
impatiens (Hymenoptera: Apidae), Megachile rotundata (Hymentoptera:
Megachilidae), and Osmia lignaria (Hymenoptera: Megachilidae). J. Econ.
Entomol. 102: 177–182.
Seeley, T. D. 1985. Honeybee ecology: a study of adaptation in social life.
Princeton University Press, Princeton, NJ.
Sgolastra F., S.Tosi, P. Medrzycki, C.Porrini, and G.Burgio. 2015. Toxicity
of spirotetramat on solitary bee larvae, Osmia cornuta (Hymenoptera:
Megachilidae), in laboratory conditions. J. Apic. Sci. 59: 73–83.
Sgolastra, F., X.Arnan, T. L.Pitts-Singer, S.Maini, W. P. Kemp, and J.Bosch.
2016. Pre-wintering conditions and post-winter performance in a solitary
bee: does diapause impose an energetic cost on reproductive success? Ecol.
Entomol. 41: 201–210.
Sgolastra, F., P. Medrzycki, L. Bortolotti, M. T. Renzi, S. Tosi, G. Bogo, D.
Teper, C. Porrini, R. Molowny-Horas, and J. Bosch. 2017. Synergistic
mortality between a neonicotinoid insecticide and an ergosterol-bio-
synthesis-inhibiting fungicide in three bee species. Pest Manag. Sci. 73:
1236–1243.
Spurgeon, D., H.Hesketh, E. Lahive, C. Svendsen, J. Baas, A. Robinson,
A.Horton, and M.Heard. 2016. Chronic oral lethal and sub-lethal tox-
icities of different binary mixtures of pesticides and contaminants in bees
(Apis mellifera, Osmia bicornis and Bombus terrestris). EFSA supporting
publication. 13: EN-1076.
Stoner, K. A. 2016. Current pesticide risk assessment protocols do not
adequately address differences between honey bees (Apis mellifera) and
bumble bees (Bombus spp.). Front. Environ. Sci. 4: 79.
Stoner, K. A., and B. D.Eitzer. 2012. Movement of soil-applied imidacloprid
and thiamethoxam into nectar and pollen of squash (Cucurbita pepo).
Plos One. 7: e39114.
Straub, L., G. R. Williams, J. Pettis, I. Fries, and P. Neumann. 2015.
Superorganism resilience: eusociality and susceptibility of ecosys-
tem service providing insects to stressors. Curr. Opin. Insect Sci. 12:
109–112.
Environmental Entomology, 2018, Vol. XX, No. X 13
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvy105/5216970 by guest on 07 December 2018
Sugiura, N., and Y.Maeta. 1989. Parental investment and offspring sex ratio
in a solitary mason bee, Osmia cornifrons (Radoszkowski) (Hymenoptera,
Megachilidae). Jpn J.Entomol. 57: 861–875.
Tepedino, V. J., and P. F. Torchio. 1982. Phenotypic variability in the
nesting success among Osmia lignaria propinqua females in a glass-
house environment (Hymenoptera: Megachilidae). Ecol. Entomol. 7:
453–462.
Tesoriero, D., B.Maccagnani, F.Santi, and G.Celli. 2003. Toxicity of three
pesticides on larval instars of Osmia cornuta: preliminary results. B.
Insectology. 56: 169–171.
Thompson, H. 2016. Extrapolation of acute toxicity across bee species. Integr.
Environ. Assess. Manag. 12: 622–626.
Torchio, P. F. 1973. Relative toxicity of insecticides to the honey bee, alkali
bee, and alfalfa leafcutting bee (Hymenoptera: Apidae, Halictidae,
Megachilidae). J. Kans. Entomol. Soc. 46: 446–453.
Torchio, P. F. 1983. The effects of eld applications of naled and trichlorfon
on the alfalfa leafcutting bee, Megachile rotundata (Fabricius). J. Kans.
Entomol. Soc. 56: 62–68.
Uhl, P., L. A.Franke, C.Rehberg, C. Wollmann, P.Stahlschmidt, L.Jeker,
and C. A.Brühl. 2016. Interspecic sensitivity of bees towards dimetho-
ate and implications for environmental risk assessment. Sci. Rep. 6:
34439.
U.S. Environmental Protection Agency (USEPA). 1996. Occupational
and Residential Exposure Test Guidelines. OPPTS 875.2100 Foliar
Dislodgeable Residue Dissipation, 1–5. https://nepis.epa.gov/Exe/ZyPDF.
cgi/P100HZDR.PDF?Dockey=P100HZDR.PDF
U.S. Environmental Protection Agency (USEPA), Health Canada Pest
Management Regulatory Agency (PMRA), and California Department of
Pesticide Regulation. 2012. White paper in support of the proposed risk
assessment process for bees Submitted to the FIFRA Scientic Advisory
Panel for Review and Comment Ofce of Chemical Safety and Pollution
Prevention Ofce of Pesticide Programs Environmental Fate and Effects,
1–275. https://www.epa.gov/sites/production/les/2014-06/documents/
pollinator_risk_assessment_guidance_06_19_14.pdf
U.S. Environmental Protection Agency (USEPA), Health Canada Pest
Management Regulatory Agency (PMRA), and California Department of
Pesticide Regulation. 2014. Guidance for Assessing Pesticide Risks to Bees.
Ofce of Pesticide Programs USEPA, Health Canada PMRA, CDPR. June
19, 2014 https://www.epa.gov/sites/production/les/2014-06/documents/
pollinator_risk_assessment_guidance_06_19_14.pdf
Vanbergen, A. J., M.Baude, J. C.Biesmeijer, N. F.Britton, M. J.F.Brown, M.Brown,
J.Bryden, G. E.Budge, J. C.Bull, C.Carvell, etal. 2013. Threats to an ecosys-
tem service: pressures on pollinators. Front. Ecol. Environ. 11: 251–259.
Willis, D. S., and P. G.Kevan. 1995. Foraging dynamics of Peponapis pru-
inosa (Hymenoptera: Anthophoridae) on pumpkin (Cucurbita pepo) in
Southern Ontario. Can. Entomol. 127: 167–175.
Winston, M. 1987. The biology of the honey bee. Harvard University Press,
Cambridge, MA.
14 Environmental Entomology, 2018, Vol. XX, No. X
Downloaded from https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvy105/5216970 by guest on 07 December 2018
