Supplementary Material...Supplementary Material Characterizing honey bee exposure and effects from...

Supplementary Material

Characterizing honey bee exposure and effects from pesticides for chemical

prioritization and life cycle assessment

Eleonora Crennaa1, Olivier Jollietb, Elena Collinaa, Serenella Salac, Peter Fantked*

a Department of Earth and Environmental Sciences, University of Milano-Bicocca, Piazza della Scienza 1, 20126

Milan, Italy

b Environmental Health Sciences, School of Public Health, University of Michigan, Ann Arbor, USA

c European Commission, Joint Research Centre, Via Enrico Fermi 2749, 21027 Ispra (VA), Italy

d Quantitative Sustainability Assessment, Department of Technology, Management and Economics, Technical

University of Denmark, Produktionstorvet 424, 2800 Kgs. Lyngby, Denmark

* Corresponding author: Peter Fantke, phone: +45 45254452, Email: [email protected]

27 pages, 19 tables, 4 figures

Table of contents

S-1. Keywords for understanding the model ...................................................................................... 2

S-2. Honey bee ecology behind exposure to pesticide residues .......................................................... 3

S-3. Impact characterization framework: full model description ........................................................ 4

S-3.1 Calculating parameter Nforager i ............................................................................................. 6

S-3.2 Calculating parameter dermal Qforager i, j ............................................................................... 7

Calculating parameter Mforager i, j ...................................................................................................... 7

Calculating parameter frforager i ......................................................................................................... 7

S-3.3 Calculating parameter frA .................................................................................................. 11

S-3.4 Calculating parameter oral Qforager i, nectar ............................................................................ 11

S-3.5 Parameter C and mappl for the pesticides selected in the case study ................................... 12

S-3.6 Additional analysis on pesticide residues .......................................................................... 15

S-3.7 Parameter LD50 for the pesticides selected in the case study ............................................ 19

S-4. Results of the illustrative case study ......................................................................................... 20

S-5. Monte Carlo uncertainty analysis .............................................................................................. 22

References ............................................................................................................................................. 25

1 Present address: Technology and Society Laboratory, Empa, Lerchenfeldstrasse 5, CH-9014, St. Gallen,

Switzerland

S2

S-1. Keywords for understanding the model

Table S1 summarizes the keywords used to describe the main elements of the impact characterization

framework for insect pollinators’ exposure to pesticides.

Table S1. Relevant keywords.

Keywords Definition

Pollen Protein rich food, collected from flowers

Nectar Sugar rich food, collected from flowers

Pollen forager Honey bee forager type that collects actively pollen and delivers it to the

hive

Nectar forager

Honey bee forager type that collects actively nectar, either with or

without getting in contact with pollen, and delivers it to the hive. In case

of pollen contact, the fraction of nectar foragers collecting pollen

delivers also pollen to the hive

Pollen load

Amount of fresh pollen, in shape of balls formed by honey bees, stored

on both the hind legs in the pollen baskets and carried to the hive as a

source of food for the colony, especially for the larvae

Nectar load

Amount of fresh nectar stored by a honey bee in the so-called honey

stomach (or secondary stomach) and carried to the hive as a source of

food for the colony, especially for the larvae

Nectar consumption Amount of fresh nectar taken in by all the honey bees forager types as a

source of immediate energy for supporting foraging and flying activities.

Exposure time

fraction

Fraction of time over 24 hours, during which individual honey bee

forager types are exposed to agricultural pesticides, via dermal contact of

either pollen or nectar.

sFforager i

Dermal contact fraction, i.e. the amount of a certain pesticide

transferred via contact exposure from pollen or nectar load to the surface

(i.e. either skin or honey stomach) of the specific honey bees forager

type, per unit of the same pesticide applied in the crop field, over a

certain exposure time. It is measured as kgdermal contact/kgapplied

iFforager i

Oral intake fraction, i.e. the amount of pesticide taken in via

consumption of nectar by all types of forager honey bees per unit of the

same pesticide applied to the crop field. It is measured as

kg oral intake/kgapplied

S3

S-2. Honey bee ecology behind exposure to pesticide residues

There are different ways through which pollinating insects can be exposed to pesticides, whose

relevance generally depends on the life stage of the organisms.1 For honey bees foraging in field, the

most relevant exposure pathway is via oral ingestion of contaminated pollen, nectar and water.

Additionally forager bees can get in contact with pesticide residues dermal contact, e.g. when insects

fly in the field while spraying, although the use of some pesticide during the flying hours of pollinators

is normally forbidden by the regulations2,3. Also through contact with treated surfaces (e.g. contaminated

pollen, nectar, water and guttation fluids, which are collected both in- and off-field by insect pollinators

4,5) or through dust dispersed after seed treatments. Dermal contact can be external (e.g. via external

body surface contact) or internal (via contact with a secondary stomach, called “honey stomach”).

Pollen foragers and nectar foragers have different behaviors in-field and inside the hive, which causes

them to be exposed in different ways to pesticide residues.

Pollen foragers actively collect pollen. They use their mandibles or legs to move the anthers of the

flowers, allowing the pollen to stick to the hair that covers their body. Then, the bees clean themselves,

packing the pollen grains in form of balls, together with some nectar used as glue. The pollen balls,

called pollen load, are stored in the baskets made of specialized hairs on the hind legs. When the full

load is reached, the bees return to the hive, where the pollen is unloaded in cells.6 While, nectar foragers

use their tongues to suck the nectar out of the flowers, found in the nectarines which usually are at the

base of the flower, and store it in a secondary stomach, called “honey stomach”, which is separated from

the digestive stomach.7 As soon as the honey stomach is full, nectar foragers return to the hive and

transfer the nectar to the other non-foraging workers. Depending on the shape of the flower and on the

foragers’ attitude, nectar foragers may also get in contact with the anthers and pollen grains can stick to

their body hair. For example, honey bees that forage on oilseed rape plants can either push their tongues

between the petals “thieving” nectar from the side without contacting the anthers or enter directly the

front of the flowers getting in contact with pollen.8 Then, as pollen foragers do, nectar foragers pack

pollen in balls on the hint legs, to be then brought to the hive.9 Generally, nectar foragers return to the

hive due to a full nectar load before the pollen baskets are full.7

Notwithstanding honey bees’ efficiency in cleaning their body hair, some pollen grains can remain on

the bees’ bodies during foraging, enhancing crop pollination.9 For the sake of model simplicity, the

exposure of honey bees via these residues is considered negligible, as well as the exposure to the nectar

used for sticking pollen grains into the baskets.

Additionally, all forager honey bees collect nectar for self-consumption, since foraging and flying

activities are energy demanding tasks.

Both pollen and nectar foragers make the same number of trips to the flowers over a day (10 trip per

day on average)10, but pollen foragers spend less time in the field for getting a full pollen load. In fact,

pollen foragers make shorter trips (10 minutes per trip on average)11 since they travel shorter distances

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compared to nectar foragers (55 minutes per trip on average)10. Nectar foragers are in charge of more

energy- and time-demanding tasks, spending more time in the field for foraging.

Figure S1 describes what happens when forager bees come back to the hive.

Figure S1. Reception and arrangement of the food and energy supplies carried in the hive by the foragers bees,

adapted from (Seeley, 1995).

Generally, pollen foragers spend more time in the hive after unloading compared with nectar foragers,

which in turn spend more time in the hive from the arrival until the end of the unloading process. This

is mainly due to the fact that pollen foragers need less time to end the unloading because they do not

need to wait for a store bee, namely they go directly to the combs and unload the pollen in the empty

cells. However, it takes more time to them for preparing leaving the hive since they communicate with

other bees in order to receive information on the needs of the hive for pollen (trophallactic interactions).6

S-3. Impact characterization framework: full model description

As explained in the paper, the impact characterization framework has been developed to quantify the

in-field exposure of forager honey bees to pesticides and the related potential toxicological effects.

Additional preliminary CFs are calculated for in-hive bees exposure.

The framework provides characterization factors (CFs) for dermal and oral exposure, that summed up

together give the overall CF for a selected pesticide:

CF = sFforager 𝑖 × EFdermal + iFforager 𝑖 × EForal + iFhive × EForal Eq. S1

We calculated the CFs for three specific types of forager honey bees, namely pollen foragers (i=p),

nectar foragers (i=n) and nectar-pollen foragers (i=np), and the CF for hive bees as follows:

S5

Pollen foragers (p)

𝐂𝐅𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝐩 = (𝐍𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝒑×𝐐𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝐩,𝐩𝐨𝐥𝐥𝐞𝐧

𝐝𝐞𝐫𝐦𝐚𝐥 ×𝐟𝐫𝐀×∫ 𝐂𝐩𝐨𝐥𝐥𝐞𝐧,𝒙,𝒚 𝐝𝐭𝐭𝟏

𝐭𝟎

𝒎𝐚𝐩𝐩𝐥,𝒙,𝒚 ×

𝟎.𝟓

𝐋𝐃𝟓𝟎𝐝𝐞𝐫𝐦𝐚𝐥) +

(𝐍𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝒑×𝐐𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝐩,𝐧𝐞𝐜𝐭𝐚𝐫

𝐨𝐫𝐚𝐥 ×∫ 𝐂𝐧𝐞𝐜𝐭𝐚𝐫,𝒙,𝒚 𝐝𝐭𝐭𝟏

𝐭𝟎

𝒎𝐚𝐩𝐩𝐥,𝒙,𝒚×

𝟎.𝟓

𝐋𝐃𝟓𝟎𝐨𝐫𝐚𝐥) Eq.S2

with Qforager p,pollendermal = Mforager p,pollen × frforager p

Nectar foragers (n)

𝐂𝐅𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝐧 = (𝐍𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝐧×𝐐𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝐧,𝐧𝐞𝐜𝐭𝐚𝐫

𝐝𝐞𝐫𝐦𝐚𝐥 ×∫ 𝐂𝐧𝐞𝐜𝐭𝐚𝐫,𝒙,𝒚 𝐝𝐭𝐭𝟏

𝐭𝟎


𝟎.𝟓


(𝐍𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝐧×𝐐𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝐧,𝐧𝐞𝐜𝐭𝐚𝐫


𝐭𝟎


𝟎.𝟓


with Qforager n,nectardermal = Mforager n,nectar × frn

Nectar-pollen foragers (np, which represent a subset of nectar foragers)

𝐂𝐅𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝐧𝐩 = (𝐍𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝐧𝐩×𝐐𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝐧𝐩,𝐩𝐨𝐥𝐥𝐞𝐧

𝐝𝐞𝐫𝐦𝐚𝐥 ×𝐟𝐫𝐀×∫ 𝐂𝐩𝐨𝐥𝐥𝐞𝐧,𝒙,𝒚 𝐝𝐭𝐭𝟏

𝐭𝟎


𝟎.𝟓


(𝐍𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝐧𝐩×𝐐𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝐧𝐩,𝐧𝐞𝐜𝐭𝐚𝐫

𝐝𝐞𝐫𝐦𝐚𝐥 ×∫ 𝐂𝐧𝐞𝐜𝐭𝐚𝐫,𝒙,𝒚 𝐝𝐭𝐭𝟏

𝐭𝟎


𝟎.𝟓

𝐋𝐃𝟓𝟎𝐝𝐞𝐫𝐦𝐚𝐥) + (𝐍𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝐧𝐩×𝐐𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝐧,𝐧𝐞𝐜𝐭𝐚𝐫


𝐭𝟎


𝟎.𝟓


with Qforager np,pollendermal = Mforager np,pollen × frforager n

and Qforager np,nectardermal = Mforager np,nectar × frforager n

Hive bees

𝐢𝐅𝐡𝐢𝐯𝐞 =∑ 𝐍𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝒊×𝑴𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝒊,𝐧𝐞𝐜𝐭𝐚𝐫×∫ 𝐂𝐧𝐞𝐜𝐭𝐚𝐫,𝒙,𝒚𝐝𝐭

𝒕𝟏𝒕𝟎

𝒊=𝐧,𝐧𝐩

𝒎𝐚𝐩𝐩𝐥,𝒙,𝒚+

∑ 𝐍𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝒊×𝑴𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝒊,𝐩𝐨𝐥𝐥𝐞𝐧×∫ 𝐂𝐩𝐨𝐥𝐥𝐞𝐧,𝒙,𝒚𝐝𝐭𝒕𝟏

𝒕𝟎𝒊=𝐩,𝐧𝐩

𝒎𝐚𝐩𝐩𝐥,𝒙,𝒚

Eq.S5

where:

− Nforager 𝑖 [bees/ha] is the average density of the specific type of honey bee forager (i = p, n, np)

on field;

− Mforager 𝑖,j [kgcontact/bee – d] is the daily load of pollen or nectar (j) carried by each specific type

of honey bee forager (i);

− frforager 𝑖 [d/d] represents the fraction of time over a day during which a specific type of forager

honey bee i is exposed to pesticide residues;

S6

− frA [-] is the fraction of forager bees' external body surface area exposed to pesticide residues in

pollen;

− Qforager 𝑖,nectaroral [kg/bee – d] is the daily nectar consumption rate of each specific type of forager

honey bee (i);

− ∫ C dt𝑡1

𝑡0[kg – d/kg pollen or nectar] is the residual concentration of pesticide x in nectar or pollen of

crop species y within the flowering period, integrated over the entire exposure and flowering

period, t0 being either the start of the flowering period or the time of application if the flowering

period has already started, and t1 the end of the flowering period;

− mappl,x,y [kgapplied/ha] is the applied mass of pesticide x to crop species y;

− LD50 [kg/bee] is the amount of a certain pesticide taken up (via dermal exposure) or in (via oral

exposure) by an exposed honey bee population, that affects 50% of the exposed bee population

over background terms of lethal effects.

S-3.1 Calculating parameter Nforager i

The average density of bees per each forager type is derived as the product of the fraction of the hive

density in the field, the average hive population, the fraction of foragers out of a colony and the fraction

of the specific honey bee forager type (namely i = p, n, np, as explained above).

Table S2. Numerical values used for building the model with regard to the main scenario-independent, constant

parameter Nforager i. When available in literature, the range of variation is reported.

Parameter description and related sources Unit Value Range of variation

Number of hives per hectare recommended for

oilseed rape crop fields 8,12 * hives/ha 3 2 to 4

Number of bees per hive during the spring/summer

period 13 bees/hive 18,500 7,000 to 30,000*

Fraction of forager honey bees, out of the total

population of honey bees in an average hive 14 - 0.26 -

Fraction of honey bee pollen foragers (p), out of the

total forager population in an average hive 15 - 0.25 -

Fraction of honey bee nectar foragers without pollen

contact (n), out of the total forager population in an

average hive 15

- 0.58 -

Fraction of honey bee nectar foragers potentially in

contact with pollen (np), out of the total forager

population in an average hive 15

- 0.12 -

Fraction of other honey bee foragers (e.g. water

collectors), out of the total forager population in an

average hive 15

- 0.05 -

* This parameters may depend on the specific case study, namely on the geographical location of the hive (e.g.

Northern or Southern Europe), on the crop species and, for managed honey bees, on recommended beekeepers’

practice. The value herein reported is referred to oilseed rape (Brassica napus) in central/northern Europe.

S7

S-3.2 Calculating parameter dermal Qforager i, j

The quantity of pollen or nectar per day that is in dermal contact with the skin or honey sack of forager

bees (i = p, n, np) is obtained as the product of the daily load of pollen or nectar of each specific honey

bee forager (i.e. Mi) by the daily exposure time fractions for pollen and nectar foragers (i.e. frforager i).

Calculating parameter Mforager i, j

The daily load of pollen or nectar carried by each specific type of honey bee forager (i = p, n, np) is

obtained as the product of the load of pollen or nectar load carried during each trip to the hive and the

average number of trips per day done by the forager bees.


parameter Mforager i,i. When available in literature, the range of variation is reported

Parameter description and related sources Unit Value Range of variation

Average pollen load per trip carried by an

individual pollen forager (p) 13,16

kgdermal

contact/(bee×trip) 2.00×10-5 1×10-5 to 3×10-5

Average pollen load per trip carried by an

individual nectar forager in contact with

pollen (np) 13,16

kgdermal

contact/(bee×trip) 1.00×10-5 (minimum value)

Average nectar load per trip carried by an

individual nectar forager without pollen

contact (n) 13,16

kgdermal

contact/(bee×trip) 3.25×10-5 2.5×10-5 to 4×10-5

Average number of trips per day for both

honey bee pollen and nectar foragers 10,17 trips/d 10 5-15

Calculating parameter frforager i

The daily exposure time fractions for pollen foragers and nectar foragers are calculated as fraction of

time over a day that an individual honey bee spends (a) collecting, actively or not, pollen and nectar in

the crop field, (b) flying back into the nest and (c) unloading:

Generally, pollen foragers spend more time in the hive after unloading compared with nectar foragers,

which in turn spend more time in the hive from the arrival until the end of the unloading process. This

is mainly due to the fact, that pollen foragers need less time to end the unloading because they do not

need to wait for a store bee, namely they go directly to the combs and unload the pollen in the empty

cells. However, it takes more time to them for preparing leaving the hive since they communicate with

other bees in order to receive information on the needs of the hive for pollen (trophallactic interactions).6

Additionally, both nectar and pollen foragers make the same number of trips to the flowers over a day,

but pollen foragers spend less time in the field for getting a full pollen load. In fact, pollen foragers make

shorter trips since they travel shorter distances compared to nectar foragers.10 Nectar foragers are in

charge of more energy- and time-demanding tasks, spending more time in the field for foraging. The

S8

estimate of the fractions of time spent inside versus outside the hive are based on the study of Seeley.18

According to this, we assume that nectar foragers behave as the foragers, which fly long distances from

the hive, i.e. to a far feeder; while pollen foragers behave as the foragers flying shorter distances, i.e. to

a near feeder. The fraction of time spent flying back to the nest is principally based on the speed that a

honey bee can reach while it is loaded with food,19 whereas the fraction of unloading time is calculated

according to in-field data from several ecological studies.6,20,21


parameter frforager i for pollen foragers (i=p). When available in literature, the range of variation is reported.

Parameter description and related sources Unit Value Range of

variation*

Average time per round trip 11 min/d 20 10 to 30

Fraction of time outside the hive, out of the total

round trip time 18 % 59(a) 58 to 60%

Fraction of time spent flying, out of the time spent

outside the hive 18 % 35(b) 34 to 36%

Fraction of time flying out (i.e. from the hive to the

food source), out of the total time spent flying while

outside the hive 19

% 13.5(c) 12.8 to 13.8%

Fraction of time flying in (i.e. from the food source

back to the hive), out of the total time spent flying

while outside the hive 19

% 21.5(d) 21.2 to 22.2%

Fraction of time spent foraging at the food source, out

of the time spent outside the hive 18 % 24.1(e) 23.8 to 24.8%

Fraction of time spent inside the hive, out of the total

round trip time 18 % 41(f) 40 to 42%

Fraction of time exposed in the hive (i.e. from the

arrival to the end of the unloading process), out of the

total time spent in the hive 20

% 13(g) 11 to 16%

Fraction of time spent in other activities after the end

on the unloading process, out of the total time spent

in the hive 20

% 28(h) 26 to 29%

fr𝑖=p d/d 0.08(i) 0.03 to 0.09

S9

* calculated by considering the minimum and maximum value or fraction for each parameter.

(a) Calculated as average of the ratios between the time spent outside the hive and the time of a round

trip for near-feeder cases, as (143s/246s + 133s/223s)/2

(b) Calculated as average of the ratios between the total time spent flying and the time spent outside the

hive for near-feeder cases, multiplied by the percentage obtained from (a), as (82s/143s +

80s/133s)×59%

(c) According to Kacelnik et al.,19 the speed of a unloaded honey bee is 8 m/s, while the flying speed

linearly decreases at 5 m/s when the honey bee is loaded with 36 mg of sugar solution. We assume that

a honey bee carrying a full load of pollen has the same speed, as confirmed by a beekeepers’

association.22 Assuming a unit distance food-hive (1 m/trip), we calculate the time per trip that takes a

honey bee when unloaded (0.13 s/trip, i.e. 38% out of the total time spent flying) and loaded (0.20 s/trip,

i.e. 62% out of the total time spent flying). Therefore, the fraction of time flying out with respect to the

time spent outside the hive is derived as 38% multiplied by 35% (i.e. the fraction obtained from (b))

(d) According to (c), the fraction of time flying in is derived as 62% multiplied by 35% (i.e. the fraction

obtained from (b))

(e) Calculated as (a) – (b), i.e. 59%-35%

(f) Calculated as difference between 100% (i.e. fraction of a total round trip) and 59% (i.e. fraction

obtained from (a), referred to the fraction of time spent outside the hive out of a total round trip)

(g) Calculated as average of the ratios between the time spent from the arrival at the hive up to the end

of the unloading process and the total time spent in the hive for each case reported, as (80s/290.9s +

109.7s/316.2s + 89.9s/247.3s + 139.6s/375.5s + 100.6s/362.6s + 86.3s/278.3s)/6=32%. This fraction is

confirmed also in the study by Seeley.6 Then, the fraction of exposure time in the hive out of the total

time spent in the hive is derived as 32% multiplied by 41% (i.e. the fraction obtained from (f), which is

the fraction of time spent inside the hive, out of the total round trip time).

(h) According to (g), the fraction of time spent in other activities after the end on the unloading process

is derived as (1-32%) multiplied by 41% (i.e. the fraction obtained from (f), which is the fraction of time

spent inside the hive, out of the total round trip time)

(i) Calculated as [20 min/trip × 10 trip/d × (21% + 24% + 13%)]/1440 min/d


parameter frforager i for nectar foragers, both with and without pollen contact (i = n, np). When available in

literature, the range of variation is reported.


variation*

Average time per round trip 10 min×d-1 55 30 to 80

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variation*

Fraction of time outside the hive, out of the total

round trip time 18 % 66(a) 65 to 67%

Fraction of time spent flying, out of the time spent

outside the hive 18 % 41(b) 39 to 42%

Fraction of time flying out (i.e. from the hive to the

food source), out of the total time spent flying while

outside the hive 19

% 15.9(c) 15.8 to 16%

Fraction of time flying in (i.e. from the food source

back to the hive), out of the total time spent flying

while outside the hive 19

% 25.1(d) 23.2 to 26

Fraction of time spent foraging at the food source, out

of the time spent outside the hive 18 % 25(e) 25 to 26%

Fraction of time spent inside the hive, out of the total

round trip time 18 % 34(f) 33 to 35%

Fraction of time exposed in the hive (i.e. from the

arrival to the end of the unloading process), out of the

total time spent in the hive 21

% 22(g) 19 to 25%

Fraction of time spent in other activities after the end

on the unload process, out of the total time spent in

the hive 21

% 12(h) 9 to 15%

fr𝑖=n,np d/d 0.28(i) 0.15-0.39

* calculated by considering the minimum and maximum value or fraction for each parameter.

(a) Calculated as average of the ratios between the time spent outside the hive and the time of a round

trip for far-feeder cases, as (294s/440s + 233s/359s)/2

(b) Calculated as average of the ratios between the total time spent flying and the time spent outside the

hive for far-feeder cases, multiplied by the percentage obtained from (a), as (184s/294s +

140s/233s)×66%

(c) According to Kacelnik et al.,19 the speed of a unloaded honey bee is 8 m/s, while the flying speed

linearly decreases at 5 m/s when the honey bee is loaded with 36 mg of sugar solution. We assume that

a honey bee carrying a full load of nectar has the same speed, as confirmed by a beekeepers’

association.22 Assuming a unit distance food-hive (1 m/trip), we calculate the time per trip that takes a

S11

honey bee when unloaded (0.13 s/trip; 38% out of the total time spent flying) and loaded (0.20 s/trip,

i.e. 62% out of the total time spent flying). Therefore, the fraction of time flying out with respect to the

time spent outside the hive is derived as 38% multiplied by 41% (i.e. the fraction obtained from (b))

(d) According to (c), the fraction of time flying in is derived as 62% multiplied by 41% (i.e. the fraction

obtained from (b))

(e) Calculated as (a) – (b), i.e. 66%-41%

(f) Calculated as difference between 100% (i.e. fraction of a total round trip) and 66% (i.e. fraction

obtained from (a), referred to the fraction of time spent outside the hive out of a total round trip)

(g) Calculated as average of the ratios between the time spent from the arrival at the hive up to the end

of the unloading process and the total time spent in the hive for each case reported, as (68s/91s + 50s/70s

+ 46s/68s + 64s/115s)/4=66%. Then, the fraction of exposure time in the hive out of the total time spent

in the hive is derived as 66% multiplied by 34% (i.e. the fraction obtained from (f), which is the fraction

of time spent inside the hive, out of the total round trip time)

(h) According to (g), the fraction of time spent in other activities after the end on the unloading process

is derived as (1-66%) multiplied by 34% (i.e. the fraction obtained from (f), which is the fraction of time

spent inside the hive, out of the total round trip time)

(i) Calculated as [55 min/trip × 10 trip/d × (25% + 25% + 22%)]/1440 min/d

S-3.3 Calculating parameter frA

The parameter fr𝐴 defines the body surface area of a forager honey bee that is exposed to pesticide

residues in pollen. It applies to pollen and nectar-pollen foragers. The parameter fr𝐴 derives from the

ratio between the mean apparent exposure surface area and the mean total physical surface area, as

defined by Poquet et al. (2014).23

Parameter description Unit Value Range of variation*

Mean apparent exposure surface area cm2/beee 1.056 0.726 to 1.386

Mean total physical surface area cm2/bee 3.276 3.046 to 3.506

S-3.4 Calculating parameter oral Qforager i, nectar

The daily nectar consumption rate for both pollen and nectar foragers (i=p, n, np) is directly derived

from USEPA Guidance for Assessing Pesticide Risks to Bees. 24

Table S6. Numerical values for scenario-independent, constant parameter 𝐐𝐟𝐨𝐫𝐚𝐠𝐞𝐫 𝒊,𝐧𝐞𝐜𝐭𝐚𝐫𝐨𝐫𝐚𝐥 used in the model,

referred to nectar consumption.

Parameter description

and related sources Unit Value Range of variation

Daily nectar consumption rate of pollen

foragers (i=p)24 kg intake/(bee×d) 4.35×10-5 3.5×10-5 to 5.2×10-5

S12

Parameter description

and related sources Unit Value Range of variation

Daily nectar consumption rate of nectar

foragers (both with and without pollen

contact) (i=n, np)10,24,25

kg intake/(bee×d) 2.92×10-4 2.13×10-4 to 4.28×10-4 *

* Nectar foragers consume 32–128.4 mg of sugar per day. Depending on its floral origin, nectar may

contain between 5–80% of sugar. Assuming 30% content of sugar in oilseed rape flower (30g of sugar

into 100ml of nectar, according to Pierre et al. (1999)26), we calculated the maximum daily nectar

consumption rate of nectar foragers as ratio between the maximum amount of sugar consumed per day

(128 mg) and the fraction of sugar in oilseed rape nectar.

S-3.5 Parameter C and mappl for the pesticides selected in the case study

The final concentration of pesticides in pollen and nectar mainly depends on the duration of the

flowering period of the crop species on which the pesticide is applied (

In fact, under the assumption of first-order kinetics, the dissipation of the pesticide is expressed as:

𝐂𝒋,𝒙,𝒚(𝐭) = 𝐂𝒋,𝒙,𝒚(𝐭𝟎) × 𝒆(−𝐤𝒋,𝒙,𝒚×𝐭) Eq.S8

where Cj,𝑥,𝑦(t0) [kg/kg] is the initial concentration of pesticide x in pollen or nectar (j) of crop y, and

kj,x,y [d-1] represents the first-order rate constant for the exponential dissipation of the pesticide in pollen

and nectar over time. The initial concentration of pesticide in pollen and nectar is based on empirically

measured data. To calculate kj,x,y, we retrieved information from studies reporting measurements of the

residual concentration (kg/kg) in pollen and nectar at different times after pesticide application, which

is the mass of a residual pesticide per mass of a collected pollen or nectar sample measured. We

estimated kj,x,y in pollen and nectar separately, by the linear least-square regression of Eq.S8:

ln[C𝑗,𝑥,𝑦(t)] = ln[C𝑗,𝑥,𝑦(t0)] − k𝑗,𝑥,𝑦 ×t Eq.S9

thus, k𝑗,𝑥,𝑦 [d-1] graphically represents the slope of the line fitting the experimental residual pesticide

data in pollen/nectar. Finally, solving the integral, we obtain:

∫ C𝑗,𝑥,𝑦t1

t0dt =

Cj,𝑥,𝑦(t0)

k𝑗,𝑥,𝑦× e−k𝑗,𝑥,𝑦×t0 − e − k𝑗,𝑥,𝑦×t1 Eq.S10

Table S7) and the intrinsic physic-chemical properties of the pesticide, which determine the persistence

of the pesticide residue in the environmental compartments (Table S8).

In general, the integral mean values of the residual concentration of a certain pesticide x in nectar and

in pollen of a certain crop species y within the flowering period are calculated respectively as:

S13

∫ 𝐂𝐩𝐨𝐥𝐥𝐞𝐧,𝒙,𝒚 𝐝𝐭𝐭𝟏

𝐭𝟎=

𝐂𝐩𝐨𝐥𝐥𝐞𝐧,𝒙,𝒚(𝐭𝟎)

𝐤× [𝐞−𝐤𝐩𝐨𝐥𝐥𝐞𝐧,𝒙,𝒚×𝐭𝟎 − 𝐞−𝐤𝐩𝐨𝐥𝐥𝐞𝐧,𝒙,𝒚×𝐭𝟏] Eq.S6

∫ 𝐂𝐧𝐞𝐜𝐭𝐚𝐫,𝒙,𝒚 𝐝𝐭𝐭𝟏

𝐭𝟎=

𝐂𝐧𝐞𝐜𝐭𝐚𝐫,𝒙,𝒚(𝐭𝟎)

𝐤× [𝐞−𝐤𝐧𝐞𝐜𝐭𝐚𝐫,𝒙,𝒚×𝐭𝟎 − 𝐞−𝐤𝐧𝐞𝐜𝐭𝐚𝐫,𝒙,𝒚×𝐭𝟏] Eq.S7

In fact, under the assumption of first-order kinetics, the dissipation of the pesticide is expressed as:

𝐂𝒋,𝒙,𝒚(𝐭) = 𝐂𝒋,𝒙,𝒚(𝐭𝟎) × 𝒆(−𝐤𝒋,𝒙,𝒚×𝐭) Eq.S8

where Cj,𝑥,𝑦(t0) [kg/kg] is the initial concentration of pesticide x in pollen or nectar (j) of crop y, and

kj,x,y [d-1] represents the first-order rate constant for the exponential dissipation of the pesticide in pollen

and nectar over time. The initial concentration of pesticide in pollen and nectar is based on empirically

measured data. To calculate kj,x,y, we retrieved information from studies reporting measurements of the

residual concentration (kg/kg) in pollen and nectar at different times after pesticide application, which

is the mass of a residual pesticide per mass of a collected pollen or nectar sample measured. We

estimated kj,x,y in pollen and nectar separately, by the linear least-square regression of Eq.S8:

ln[C𝑗,𝑥,𝑦(t)] = ln[C𝑗,𝑥,𝑦(t0)] − k𝑗,𝑥,𝑦 × t Eq.S9

thus, k𝑗,𝑥,𝑦 [d-1] graphically represents the slope of the line fitting the experimental residual pesticide

data in pollen/nectar. Finally, solving the integral, we obtain:

∫ C𝑗,𝑥,𝑦t1

t0dt =

Cj,𝑥,𝑦(t0)

k𝑗,𝑥,𝑦× [e−k𝑗,𝑥,𝑦×t0 − e−k𝑗,𝑥,𝑦×t1] Eq.S10

Table S7. Average duration of the flowering period for oilseed rape (Brassica napus) in Europe, based on Klein

et al.27

Crop Location Average start

flowering period

(Julian day)

Average end

flowering period

(Julian day)

Average

duration

flowering period

Duration

uncertainty

range

oilseed rape Europe 134 (t0) 159 (t1) 24 days 8 to 32 days

Table S8. Numerical values used for quantifying the concentration of pesticides in either pollen or nectar over

the flowering period, based on empirical residual data. Variability is reported in brackets. Data come from the

references reported close to the name of each pesticide, unless otherwise specified.

Parameter descriptions Boscalid28 Lambda-cyhalothrin29

CAS number 188425-85-6 91465-08-6

S14

Parameter descriptions Boscalid28 Lambda-cyhalothrin29

Pesticide class Fungicide/Carboxamide Insecticide/Pyrethroid

Mass of pesticide applied [kg applied/ha] 0.250 * 0.0075 **

kpollen, i.e. the dissipation rate in pollen [d-1] 0.25 (a)

(0.21 to 0.30) (b) 1.33 (a)

(1.13 to 1.58) (b)

Cpollen(𝑡0), i.e. the initial concentration in

pollen [kg in pollen /kg pollen]

1.39×10-5

(3×10-6 to 2.62×10-5)

1.59×10-6 (c)

(1.54×10-6 to 1.64×10-6)(d)

knectar, i.e. the dissipation rate in nectar [d-1] 0.43 (a)

(0.36 to 0.51) (b) 1.33 (a)

(1.13 to 1.58) (b)

Cnectar(𝑡0), i.e. the initial concentration in

nectar [kg in nectar /kg nectar]

1.43×10-6

(2.50×10-8 to 1.60×10-6) 7.93×10-7 (e)

(7.67×10-7 to 8.73×10-7) (f)

* 50 g a.i./100 g product × 500 g product/ha =250 g a.i./ha = 0.250 kg/ha

**100 g a.i./L product × 0.075 L product /ha = 7.5 g/ha = 0.0075 kg/ha

(a) Dissipation rate of the selected pesticide in pollen or nectar, calculated as ratio between ln(2) and

the residues half-life in pollen or nectar of mustard (Brassica juncea), used as proxy for oilseed rape

(Brassica napus).

(b) Choudhary and Sharma (2008)29 report for different pesticide half-life in nectar and pollen between

a factor of 1.1 and 1.4 variability for the same pesticide. We derived minimum and maximum values

of the dissipation rate of the selected pesticide in pollen or nectar by applying a factor 1.4 to the

residues half-life in pollen or nectar of mustard (Brassica juncea), used as proxy for oilseed rape

(Brassica napus).

(c) Initial concentration in pollen of mustard (Brassica juncea), used as proxy for oilseed rape

(Brassica napus), measured at the application day. This value is calculated as average between the

average residual concentrations in pollen measured at the application day during the following seasons

2003-2004 (1.577×10-6 kgin pollen/kgpollen) and 2004-2005 (1.607×10-6 kgin pollen/kgpollen).29

(d) Minimum and maximum initial concentrations in pollen are calculated as average between the

residual concentration in pollen measured at the application day by respectively bioassay and chemical

assay methods, during the following seasons 2003-2004 (bioassay: 1.542×10-6 kgin pollen/kgpollen;

chemical assay: 1.672×10-6 kgin pollen/kgpollen) and 2004-2005 (bioassay: 1.542×10-6 kgin pollen/kgpollen;

chemical assay: 1.612×10-6 kgin pollen/kgpollen).29

(e) Initial concentration in nectar of mustard (Brassica juncea), used as proxy for oilseed rape

(Brassica napus), measured at the application day. This value is calculated as average between the

average residual concentrations in nectar measured at the application day during the following seasons

2003-2004 (8.58×10-7 kgin nectar/kgnectar) and 2004-2005 (7.28×10-7 kgin nectar/kgnectar).29

S15

(f) Minimum and maximum initial concentrations in nectar are calculated as average between the

residual concentration in nectar measured at the application day by respectively bioassay and chemical

assay methods, during the following seasons 2003-2004 (bioassay: 8.06×10-7 kgin nectar/kgnectar; chemical

assay: 9.09×10-7 kgin nectar/kgnectar) and 2004-2005 (bioassay: 7.27×10-7 kgin nectar/kgnectar; chemical assay:

8.06×10-7 kgin nectar/kgnectar).29

S-3.6 Additional analysis on pesticide residues

Before selecting specific pesticides for the case study, we performed additional analysis on pesticide

residues data to better understand how pesticides accumulate in pollen and nectar, and to find a possible

relation between these two environmental compartments.

Firstly, we studied the possible interdependence between pesticide residues in pollen and in nectar, to

verify if one of these environmental compartments could be used as a proxy for the other, thus

addressing only one exposure compartment. We retrieved data (both average value or temporal series)

of residues in both pollen and nectar of 12 pesticides applied on four different crop species relevant

for honey bees (Table S9). We observed a good correlation (R2=0.6875, see Figure S2). However,

considering the different crops species and pesticides separately (Figure S3.), the correlation values

significantly change from R2=0.0006 in imidacloprid residues found in squash (Cucurbita pepo) to

R2=1 in e.g., thiacloprid residues found in oilseed rape (Brassica napus). This very wide variation does

not make it possible to use one compartment as a proxy for the other.

Table S9. Pesticide residues, measured in log scale, in pollen and nectar of four crop species relevant for honey

bees.

Crop species

relevant for bees

(common name)

Crop species

relevant for bees

(scientific name)

Pesticide

residues

in pollen

[log ppb]

residues

in nectar

[log ppb]

Ref.

oilseed rape Brassica napus imidacloprid 0.88 -0.09 30

oilseed rape Brassica napus imidacloprid 0.64 -0.22 30

squash Cucurbita pepo imidacloprid 1.17 1.01 31



sunflower Helianthus annuus imidacloprid 0.59 0.28 33

mustard Brassica juncea lambda-cyhalothrin 3.22 2.96 29













S16

Crop species

relevant for bees

(common name)

Crop species

relevant for bees

(scientific name)

Pesticide

residues

in pollen

[log ppb]

residues

in nectar

[log ppb]

Ref.


oilseed rape Brassica napus clothianidin 0.30 0.00 34,35

oilseed rape Brassica napus clothianidin 0.40 0.73 34



oilseed rape Brassica napus clothianidin -0.22 0.41 36




oilseed rape Brassica napus clothianidin -0.30 -0.17 39

oilseed rape Brassica napus clothianidin -0.01 -0.11 39



oilseed rape Brassica napus thiamethoxam 0.60 0.15 34



oilseed rape Brassica napus thiamethoxam -0.22 0.43 36


squash Cucurbita pepo thiamethoxam 1.11 1.06 31



oilseed rape Brassica napus acetamiprid 1.02 0.88 36

oilseed rape Brassica napus deltamethrin 1.67 1.08 42

oilseed rape Brassica napus deltamethrin 2.78 1.28 42

oilseed rape Brassica napus boscalid 4.14 3.16 28




oilseed rape Brassica napus thiacloprid 1.91 -0.05 36

oilseed rape Brassica napus thiacloprid 0.49 1.82 36

alfalfa Medicago sativa oxydemeton-methyl 3.13 4.34 43



mustard Brassica juncea spiromesifen 3.32 3.16 29














mustard Brassica juncea endosulfan I (alpha) 3.14 3.04 29



S17

Crop species

relevant for bees

(common name)

Crop species

relevant for bees

(scientific name)

Pesticide

residues

in pollen

[log ppb]

residues

in nectar

[log ppb]

Ref.












mustard Brassica juncea endosulfan II (beta) 2.92 2.86 29














Figure S2. Correlation between residues of 12 pesticides in pollen and nectar of four relevant crops for honey

bees.

S18

Figure S3. Correlation between residues of 12 pesticides in pollen and nectar of four relevant crops for honey

bees, aggregated by crop species and pesticide.

In the specific case of neonicotinoid insecticides, we also investigated the potential interdependence

between pesticide residues in pollen and nectar with residues in leaves to see if leaves could be used as

a proxy for either pollen or nectar (Table S10). In fact, neonicotinoids have systemic properties, namely

they are taken up through roots and leaves and translocated into other crop components.

Table S10. Residues, in log scale, of some neonicotinoids in leaves, pollen and nectar of three crop species relevant

for honey bees.

Crop species

relevant for bees

(common name)

Crop species

relevant for bees

(scientific name)

Pesticide

residues

in leaves

[log ppb]

residues

in pollen

[log ppb]

residues

in nectar

[log ppb]

Ref.

squash Cucurbita pepo imidacloprid 1.36 1.26 0.79 32

squash Cucurbita pepo imidacloprid 1.60 1.50 0.96 32

sunflower Helianthus annuus imidacloprid 0.66 0.48 n.a. 30

oilseed rape Brassica napus clothianidin 0.46 0.28 n.a. 44

oilseed rape Brassica napus thiamethoxam 0.02 0.50 n.a. 44

squash Cucurbita pepo thiamethoxam 2.24 1.39 1.03 32

squash Cucurbita pepo thiamethoxam 2.15 1.40 0.63 32

S19

Figure S4. Correlation between residues of neonicotinoids in leaves and in pollen and nectar of three relevant

crops for honey bees.

We observed a high correlation between residues in leaves and pollen (R2 close to 1), while the

correlation between residues in leaves and nectar is very low (R2 close to 0). However, neonicotinoids

represent a specific group of insecticides with intrinsic properties, which cannot be used as a proxy for

other pesticides.

S-3.7 Parameter LD50 for the pesticides selected in the case study

The ecotoxicological endpoints used to derive the effect factors (EF), associated with both dermal and

oral exposure, were retrieved from the Pesticide Properties DataBase45 and from the publication by

Simon-Delco and colleagues. Figures are reported in Table S11, with related ranges of variability.

For lambda cyhalothrin, the same ecotoxicological endpoint values are used for forager and hive bees,

due to the lack of detailed and specific data for larvae, queen and other in-hive bees.

Table S11. Ecotoxicological endpoint for the selected pesticides.

Parameter descriptions and related source Boscalid Lambda-cyhalothrin

LD50 contact for worker bees [μg/bee] 200 45,46 *

(63 to 632) (a) 0.038 45,47 *

(0.0013 to 0.051) (b)

LD50 oral for worker bees [μg/bee] 760 48 **

(166 to 1660) (c) 0.91 45,47 *

(0.16 to 1.6) (d)

LD50 oral for hive bees [μg/larva] 75.19 49 §

(55.99 to 102.82) 49

0.91 45,47 §§

(0.16 to 1.6) (d)

* Acute value, obtained over 48h experimental test on adult worker honey bees, used as a proxy

** Chronic value, obtained over 25 days experimental test on adult worker honey bees § Chronic value, obtained over 22 days experimental test on honey bee larvae.

§§ Acute LD50 oral for worker bees has been used as a proxy for hive bees

S20

(a) According to Uhl et al. (2016)50, the sensitivity of different bee species toward a specific pesticide

vary around 1 order or magnitude, consistently with other studies for other species. Therefore, we

assumed a factor 10 variation around the mean value.

(b) The minimum value is taken from Johnson et al. (2006),51 as worst case LD50 value for worker

bees. The maximum value is from the National Pesticide Information Centre (2001).52

(c) The minimum value is taken from the Pesticide Properties Database45. The maximum value is

calculated by assuming a factor 10 variation around the mean value, as for (a).

(d) The minimum value is from the National Pesticide Information Centre (2001).52 The maximum

value is calculated by assuming a factor 10 variation around the mean value, as for (a).

S-4. Results of the illustrative case study

Table S12 reports the main results of the impact characterization framework for the specific types of

forager honey bees and hive bees, namely the dermal contact fractions, the oral intake fractions, the

effect factors associated with both dermal and oral exposure, and the characterization factors.

Table S12. Main results of the impact characterization framework

Parameter description Boscalid Lambda-

cyhalothrin

sFforager p , i.e. dermal contact (with pollen) for all pollen foragers

[kg dermal contact/kg applied] 4.07×10-6 2.95×10-6

sF forager n , i.e. dermal contact (with nectar) for all nectar foragers

[kg dermal contact/kg applied] 9.94×10-6 5.89×10-5

sFforager np , i.e. dermal contact (with pollen) for the fraction of

nectar foragers potentially in contact with pollen

[kg dermal contact/kg applied]

5.39×10-6 1.46×10-5

iFforager p , i.e. oral intake for all pollen foragers

[kg oral intake/kg applied] 2.06×10-6 1.22×10-5

iFforager n+np, i.e. oral intake for all nectar foragers


iFhive , i.e. oral intake for hive bees


EF dermal for all foragers [bee/kg dermal contact] 2.50×106 1.32×1010

EF oral for all foragers [bee/kg intake] 6.58×105 5.49×108

S21

Parameter description Boscalid Lambda-

cyhalothrin

EF oral for hive bees [bee/kg intake] 5.00×106 5.49×108

CF for pollen foragers (p) [bees affected/kg applied ] 11.5 4.55×104

CF for all nectar foragers (n + np) [bees affected/kg applied] 63.8 1.09×106

Overall CF for forager bees [bees affected/kg applied] 75.3 1.14×106

CF for hive bees [bees affected/kg applied] 1.18×103 2.17×105

Table S13 reports the impact scores (IS) that we estimated to better compare the impacts on forager

honey bees due to the application of the selected pesticides. IS, which quantify the fraction of bees

affected per application, are reported for both the pesticide selected in the case study.

Table S13. Impact scores (IS) associated with the selected pesticides and contribution of each impact pathway.

IS [beesaffected/ha] Boscalid Lambda-

cyhalothrin

Contribution from:

Dermal exposure of pollen foragers

sFp × EFdermal × mappl 3 (14%) 291 (3%)

Dermal exposure of nectar foragers

sFn × EFdermal × mappl 6 (33%) 5,816 (68%)

Dermal exposure of nectar-pollen foragers

sFnp × EFdermal × mappl 3 (18%) 1,441 (17%)

Oral exposure of pollen foragers

iFp × EForal × mappl <1 (2%) 50 (1%)

Oral exposure of nectar foragers without pollen

contact

iFn × EForal × mappl

5 (28%) 783 (9%)

Oral exposure of nectar foragers potentially in

contact with pollen

iFnp × EForal × mappl

1 (6%) 162 (2%)

Overall IS for foragers * 19 8,544

Oral exposure of hive bees

iFhive × EForal × mappl 39 1,628

S22

* Out of a population of 55000 honey bees in a bee hive, of which 13445 forager bees potentially exposed to

pesticide residues in pollen and nectar via dermal or ingestion exposure. Specifically, forager bees are 3538 pollen

foragers and 9907 nectar foragers, of which 1698 potentially in contact with pollen.

Table S14 reports the Potentially Affected Fractions (PAF) of forager honey bees following the

application of selected pesticide.

Table S14. Potentially affected fractions (PAF) of forager honey bees due to the application of the selected

pesticides and the contribution of each impact pathway referred to the related exposure type.

PAF [% bees affected,

out of related forager type] Boscalid Lambda-cyhalothrin

Dermal exposure of pollen foragers

(sFforager p × EFdermal × mappl) / Nforager p

0.07% 8.22%

Dermal exposure of nectar foragers

(sFforager n × EFdermal × mappl) / Nforager n 0.08% 70.86%

Dermal exposure of nectar-pollen foragers

(sFforager np × EFdermal × mappl) / Nforager np 0.20% 84.87%

Oral exposure of pollen foragers

(iFforager p × EForal × mappl) / Nforager p 0.01% 1.42%

Oral exposure of nectar foragers without

pollen contact

(iFforager n × EForal × mappl) / Nforager n

0.06% 9.54%

Oral exposure of nectar foragers with pollen

contact

(iFforager np × EForal × mappl) / Nforager np

0.06% 9.54%

Oral exposure of hive bees

(iFhive × EForal × mappl) / Nhive 0.09% 3.87%

S-5. Monte Carlo uncertainty analysis

As input data for our model vary within specific ranges, we conduct a Monte Carlo uncertainty

analysis, where we randomly varied model inputs in 100,000 realizations. We assumed uniform

distribution for each variable within a fixed range, defined by minimum and maximum values. Tables

S15 to S19 reports the average values calculated over the 100,000 realizations of the Monte Carlo

analysis, and minimum and maximum variability.

Table S15. Outputs of the Monte Carlo analysis for both dermal and oral exposure fractions for each honey bee

forager type: p = pollen foragers, n = nectar foragers without pollen contact, np = nectar foragers with pollen

contact; hive = in-hive bees.

S23

Pesticide Exposure fraction Model

output Average Min Max

Boscalid

sFp [kg dermal contact/kg applied] 4.07×10-6 4.73×10-6 3.14×10-8 8.41×10-5

sFn [kg dermal contact/kg applied] 9.94×10-6 6.11×10-6 1.43×10-8 7.52×10-5

sFnp [kg dermal contact/kg applied] 5.39×10-6 5.00×10-6 5.68×10-8 5.07×10-5

iFp [kg oral intake/kg applied] 2.06×10-6 1.18×10-6 9.76×10-9 5.98×10-6

iFn [kg oral intake/kg applied] 3.21×10-5 2.03×10-5 1.34×10-7 1.18×10-4

iFnp [kg oral intake/kg applied] 6.64×10-6 4.19×10-6 2.77×10-8 2.44×10-5

iFhive [kg oral intake/kg applied] 2.36×10-4 2.26×10-4 8.20×10-6 1.60×10-3

Lambda

cyhalothrin

sFp [kg dermal contact/kg applied] 2.95×10-6 3.35×10-6 6.40×10-8 3.59×10-5

sFn [kg dermal contact/kg applied] 5.89×10-5 6.60×10-5 2.07×10-6 5.04×10-4

sFnp [kg dermal contact/kg applied] 1.46×10-5 1.63×10-5 5.09×10-7 1.17×10-4

iFp [kg oral intake/kg applied] 1.22×10-5 1.28×10-5 2.50×10-6 3.75×10-5

iFn [kg oral intake/kg applied] 1.90×10-4 2.19×10-4 3.09×10-5 7.06×10-4

iFnp [kg oral intake/kg applied] 3.93×10-5 4.53×10-5 6.39×10-6 1.46×10-4

iFhive kg oral intake/kg applied] 3.95×10-4 4.10×10-4 4.24×10-5 1.66×10-3

Table S16. Outputs of the Monte Carlo analysis for both dermal and oral effect factors (EF).

Pesticide Effect factor

[bee/kg]

Model


Boscalid

EF dermal for foragers 2.50×106 2.02×106 7.91×105 7.91×106

EF oral for foragers 6.58×105 7.71×105 3.01×105 3.01×106

EF oral for hive bees 5.00×106 6.50×106 4.86×106 8.92×106

Lambda

cyhalothrin

EF dermal for foragers 1.32×1010 3.70×1010 9.80×109 3.91×1011

EF oral for foragers 5.49×108 7.99×108 3.13×108 3.13×109

EF oral for hive bees 5.49×108 7.99×108 3.13×108 3.13×109

Table S17. Outputs of the Monte Carlo analysis for characterization factors (CF), for both dermal and oral

exposure pathways for each honey bee forager type: p = pollen foragers, n = nectar foragers without pollen

contact, np = nectar foragers with pollen contact; hive = in-hive bees

Pesticide CF

[bees affected/kg applied ]

Model


Boscalid

CF p (dermal) 10.2 9.54 3.64×10-2 3.14×102

CF n (dermal) 24.9 12.32 1.16×10-2 3.48×102

CF np (dermal) 13.5 10.09 6.48×10-2 2.76×102

CF p (oral) 1.35 0.92 3.75×10-3 1.59×101

CF n (oral) 21.1 15.69 6.20×10-2 2.82×102

CF np (oral) 4.37 3.25 1.28×10-2 5.82×101

S24

Pesticide CF

[bees affected/kg applied ]

Model


CF hive (oral) 1.18×103 1.47×103 44.9 1.27×104

Lambda

cyhalothrin

CF p (dermal) 3.88×104 1.24×105 9.42×102 9.23×106

CF n (dermal) 7.76×105 2.44×106 2.75×104 1.07×108

CF np (dermal) 1.92×105 6.03×1015 6.82×103 2.62×107

CF p (oral) 6.71×103 1.03×104 8.48×102 1.03×105

CF n (oral) 1.04×105 1.75×105 1.25×104 1.82×106

CF np (oral) 2.16×104 3.62×104 2.60×103 3.77×105

CF hive (oral) 2.17×105 3.28×105 1.42×104 3.88×106

T

able S18. Outputs of the Monte Carlo analysis for impact scores (IS), for both dermal and oral exposure

pathways for each honey bee forager type: p = pollen foragers, n = nectar foragers without pollen contact, np =

nectar foragers with pollen contact; hive = in-hive bees

Pesticide IS

[beesaffected/ha]

Model


Boscalid

IS p (dermal) 2.55 2.39 3.64×10-3 78.51

IS n (dermal) 6.21 3.08 1.16×10-3 86.88

IS np (dermal) 3.37 2.52 6.48×10-2 69.05

IS p (oral) 0.34 0.23 3.75×10-4 3.98

IS n (oral) 5.27 3.92 6.20×10-2 70.38

IS np (oral) 1.09 0.81 1.28×10-3 14.56

IS hive (oral) 2.95×102 3.66×102 11.2 3.17×103

Lambda

cyhalothrin

IS p (dermal) 2.91×102 9.30×102 7.06 6.92×104

IS n (dermal) 5.82×103 1.83×104 2.07×102 8.00×105

IS np (dermal) 1.44×103 4.52×103 51.15 1.96×105

IS p (oral) 50.3 76.88 6.36 7.69×102

IS n (oral) 7.83×102 1.31×103 94.08 1.37×104

IS np (oral) 1.62×102 2.71×102 19.46 2.82×103

IS hive (oral) 1.63×103 2.46×103 1.07×102 2.91×104

Table S19. Outputs of the Monte Carlo analysis for impact scores (IS), for both dermal and oral exposure

pathways for each honey bee forager type: p = pollen foragers, n = nectar foragers without pollen contact, np =

nectar foragers with pollen contact; hive = in-hive bees

Pesticide IS

[beesaffected/ha]

Model


Boscalid PAF p (dermal) 7.19×10-4 6.77×10-4 5.42×10-6 1.58×10-2

S25

Pesticide IS

[beesaffected/ha]

Model


PAF n (dermal) 7.57×10-4 3.76×10-4 8.24×10-7 7.32×10-3

PAF np (dermal) 1.98×10-3 1.49×10-3 1.84×10-5 2.72×10-2

PAF p (oral) 9.57×10-5 6.46×10-5 6.80×10-7 6.29×10-4

PAF n (oral) 6.43×10-4 4.77×10-4 4.25×10-6 5.05×10-3

PAF np (oral) 6.43×10-4 4.77×10-4 4.25×10-6 5.05×10-3

PAF hive (oral) 7.02×10-3 4.60×10-4 8.72×10-3 4.19×10-2

Lambda

cyhalothrin

PAF p (dermal) 0.082 0.262 0.004 13.177

PAF n (dermal) 0.709 2.231 0.061 90.720

PAF np (dermal) 0.849 2.662 0.077 107.297

PAF p (oral) 0.014 0.022 0.005 0.121

PAF n (oral) 0.095 0.159 0.034 0.986

PAF np (oral) 0.095 0.159 0.034 0.986

PAF hive (oral) 0.039 0.058 0.008 0.408

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