science.sciencemag.org/content/368/6493/881/suppl/DC1

Supplementary Materials for

Bumble bees damage plant leaves and accelerate flower production

when pollen is scarce

Foteini G. Pashalidou*, Harriet Lambert*, Thomas Peybernes,

Mark C. Mescher†, Consuelo M. De Moraes†

*These authors contributed equally to this work.

†Corresponding author. Email: consuelo.demoraes@usys.ethz.ch (C.M.D.M.);

mescher@usys.ethz.ch (M.C.M.)

Published 22 May 2020, Science 368, 881 (2020)

DOI: 10.1126/science.aay0496

This PDF file includes:

Materials and Methods

Figs. S1 to S5

Tables S1 to S3

Caption for Movie S1

References

Other Supplementary Material for this manuscript includes the following:

(available at science.sciencemag.org/content/368/6493/881/suppl/DC1)

Movie S1 (.mp4)

1

Materials and Methods

Plants and insects: Bombus terrestris colonies were obtained commercially from the Biobest

group (Belgium). These included queenless microcolonies and founding queenright hives. Each

queenless “mini-hive” box contained approximately 30 workers. Founding queenright hives (two

weeks younger than usually distributed) contained a queen and approximately 20 workers. Both

queenless and queenright hives were equipped with tanks of Biogluc sugar solution (1.5kg and

2.1kg, respectively). Upon arrival, all hives were weighed, checked for queen presence and had

their nest examined.

Brassica nigra, B. oleracea, Solanum elaeagnifolium, S. melongena and S. lycopersicum

plants were grown from seed in a climate chamber (Kälte 3000, RH 60–80%, LD 16:8). Brassica

nigra seeds for this study were provided by the Centre of Genetic Resources in Wageningen, the

Netherlands (accession number: CGN06619). These seeds were used to grow plants at field sites

around Wageningen, which were exposed to wild pollinators; ripe fruits and seeds were then

collected from these plants and used in our experiments. Brassica oleracea var. capitata (white

cabbage) seeds from the commercial variety “ESCAZU” (seed lot 2875500), were provided by

Syngenta Crop Protection AG (Basel, Switzerland). S. melongena var. black beauty

0041(eggplant) and lycopersicum var. Siberian 34500 (tomato) seeds were provided by Zollinger

bio (Port-Valais, Switzerland). Other plants used in our rooftop studies were obtained from a

local nursery (Hauenstein, Zurich, Switzerland), depending on availability: Alliaria petiolata (ca.

2 months old), Antirrhinum yellow and orange (ca. 3 months old), Armoracia rusticana (ca.1

year old), Aurinia saxatilis Compacta (ca. 3 months old), Fragaria vesca (ca. 3 months old),

Isatis tinctoria (ca. 1 year old). None of these plants were treated with chemicals by the supplier.

A pre-existing rooftop garden present in our (2019) rooftop study was planted with various

wildflower species (including, Trifolium spp., Ranunculus spp., Alyssum spp., and wild herbs).

Flowering time studies: Plants in each flowering-time experiment were assigned to one of three

treatment groups: control (undamaged), bee-damaged, and mechanically damaged (S.

lycopersicum, n=20 per treatment; B. nigra, n=10 per treatment). At the start of the experiment

plants were of uniform age (S. lycopersicum, 6 weeks old; B. nigra, 9 weeks old). Plants in the

bee damaged treatments were placed together with a pollen-deprived B. terrestris colony inside a

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mesh enclosure (W250 x D75 x H220cm for B. nigra; W75 x D75 x H115cm for S.

lycopersicum) within a climate chamber (Kälte 3000, RH 60–80%, LD 16:8). To standardize

damage, plants were removed when bees had made 5–10 leaf holes (5 for S. lycopersicum; 5–10

for B. nigra), a number reflecting preliminary observations of daily damage inflicted by an

individual colony; damage treatments took between 2 minutes and 3 hours, depending on the

activity level of the colony. Each plant in the mechanical damage treatments was then paired

with a plant in the corresponding bee-damage treatment, and we used a metal forceps and razor

to replicate the damage pattern observed in the bee-damaged plant as closely as possible. Plants

from both damage treatments, as well as undamaged controls, were then placed at randomly

selected positions within a climate chamber (Kälte 3000, 60–80% RH, LD 16: 8) and moved to

new random positions every two days. Plants were monitored daily, and flowering time was

reported as days elapsed since treatment (i.e., bee-damage, mechanical damage, no-damage). For

S. lycopersicum, flowering was assessed by monitoring the number of nodes formed on the initial

apical meristem, and then recording the appearance of the first inflorescence. The S.

lycopersicum experiment was terminated when all plants had begun to flower (day 78 after

damage). For B. nigra, flowering was assessed as the first appearance of flower buds at the top of

the main shoot. The B. nigra experiment was terminated on day 40 due to logistical constraints.

Laboratory pollen deprivation study: We assessed damage behavior by Bombus

terrestris microcolonies that were either given abundant pollen resources within the hive (pollen-

satiated) or deprived of pollen (pollen-deprived). These microcolonies were queenless, but

contained psuedoqueens that produced haploid larvae. Queenless microcolonies are commonly

used for behavioral experiments with B. terrestris and have been shown to serve as good models

for investigating a variety of behavioral, developmental, and ecological questions (32). Two

colonies from each treatment were placed in mesh cages (250 x 220 x 75 cm), within a large

growth chamber (Kälte 3000, RH 60–80%, LD 16:8) on day 1 of the experiment. For the pollen-

satiated treatment, a paste of 5g dried pollen granules and 30% sugar solution was placed directly

inside the hive daily, ensuring that pollen was always available in excess; no pollen was provided

for colonies in the pollen-deprived treatment. All colonies had access to external feeders

containing Biogluc sugar solution throughout the experiment (to encourage foraging). Colonies

were given three days (days 2–4) to adjust to the treatments prior to being exposed to plants. On

3

day 5, two flowerless B. nigra plants (5-7 weeks old) were placed into each cage. Plants were

replaced daily over three days (days 5–7) and we recorded the proportion of leaves damaged for

each plant. On day 8, all plants were removed and the treatment (pollen satiated vs pollen

deprived) for each colony was reversed. Colonies were then given three days (days 9–11) to

adjust to the new treatments before again being exposed to plants on days 12–14 (with daily

replacement and damage assessment as above). Hives were weighed on days when the treatments

were implemented or reversed (days 1 and 8) and monitored during the subsequent adjustment

periods. At the end of the experiment (Day 15), final measurements were taken and hives were

frozen and kept for dissection (Fig. S4).

Roof study 2018:

Phase one (March 26th – May 25th): Bombus terrestris microcolonies were placed on a rooftop

(on the Zentrum campus of ETH Zurich; Zurich, Switzerland) near a focal patch of 36 flowerless

(i.e., not currently in flower) plants of 6 different plant species (initially, Alliaria petiolata,

Alyssum montanum, Aurinia saxatilis, Brassica nigra, Brassica oleracea, and Isatis tinctoria)

(Fig. S5a). A. montanum was replaced by Fragaria vesca early in the experiment (13th April

2018) because bee-inflicted damage was not visible on the very small leaves of A. montanum.

Bumblebee colonies were deprived of pollen for 3 days prior to the experiments, and received no

supplemental pollen during the experiment, but had access to the Biogluc sugar solution within

the hive throughout the study. Colonies were replaced approximately every 3 weeks, in

accordance with the timeframe for effective pollination estimated by the commercial distributor.

Plants were replaced at the same time. A total of three colonies were used during phase one.

Damage was scored as the number of new leaf-holes produced each day (to facilitate tracking,

damaged leaves, having known numbers of pre-existing holes, were individually marked with

small green metal rings). On sampling days (all weekdays except when it rained) we also

recorded the number of bumblebees entering and exiting the hive and the number of returning

foragers with and without pollen during three 60-minute periods per day (beginning at ~09:00,

~13:00, and ~16:00).

Phase two (June 4th- July 20th): Starting on June 4, we repeated the experimental design of

phase one, except that we additionally placed a patch of 100 plants in flower, comprising four

species (Brassica nigra, Fragaria vesca, Isatis tinctoria, Alliaria petiolata), separated by ~1 m

4

from the focal patch of 36 flowerless plants (Fig.S5a). Additionally, on sampling days we

recorded the number and species identity of any bees visiting our flowering patch, as well as

those visiting the flowerless patch, during three 60-minute periods per day (beginning at ~09:00,

~13:00, and ~16:00), along with the other observations described for phase one. Plants in the

flowering patch that started fruiting were replaced. As in phase one, bee colonies (and plants in

the flowerless patch) were replaced every three weeks; two colonies were employed during this

phase.

2019 Rooftop experiment (May 29th – July 13th):

Sixteen founding queenright Bombus terrestris colonies were equally divided between two

treatments (flowerless and flowering) and placed on separate rooftops, including the rooftop used

during the 2018 study (Roof 1) and another nearby (Roof 2; ~200m from Roof 1). Colonies on

both Rooftops (n = 8 per roof) were placed near focal patches of 300 flowerless plants

comprising 7 different species (Armoracia rusticana, Aurinia saxatilis, Brassica nigra, Fragaria

vesca, Isatis tinctorial, Solanum lycopersicum and Solanum melongena). No plants in flower

were present on Roof 1, but Roof 2 had a rooftop garden sown with wildflowers (4.5 x 7m;

~20m from the focal patch); in addition, we placed 30 additional flowering (i.e, currently in

flower) border plants (Antirrhinum ca. 3 months old) near the focal patch on Roof 2 (Fig. S5b).

All colonies on both rooftops were oriented in the same direction, with nest entrances facing

West, and were sheltered from direct sunlight. Colonies were not given access to any

supplemental pollen or nectar resources, except on June 17th and 27th, when all colonies on both

rooftops were provided with Biogluc sugar solution within the hive for 24h to mitigate the

effects of heavy rain and hot weather (respectively). Additionally, colonies were provided with

external water feeders to provide relief to the hive during hot weather. Colonies were weighed

and measured twice a week (after sunset) to monitor queen presence and hive development. The

rooftop garden (on Roof 2) was mowed on June 29, and we also removed the other flowering

plants on Roof 2 on this date, after which point no plants in flower were present on either roof.

Colonies and focal (flowerless) plant patches were kept in place until the onset of the

reproductive switch point (measured as the appearance of the first drone). All hives were

removed for continued monitoring in climate chambers on experimental day 45. Damage was

monitored, as in the 2018 experiment, for 150 randomly selected flowerless plants in each focal

5

patch. Plants in the focal patches were replaced after three weeks to ensure they remained in a

flowerless state. Concurrently, we conducted a transect study between 11th March- 26th July to

roughly estimate surrounding floral resources. Plants in flower were identified along two 1 km

long transects (with North-South and East-West axes) originating at Roof 1. Surveys were

conducted every two weeks, during which we identified all flowering plants visible within 5m of

the transect (using the iNaturalist app). Because many plants were not accessible for close

examination in in this urban environment, we did not count individual flowers, but instead used

species richness as a metric for changes in resource availability over time (Fig. S2).

Statistical analyses: All statistical analyses were carried out using R: A language and

Environment for Statistical Computing version 2.15.3 (R Core Team 2013).

To test for effects of the three damage treatments on flowering time, we used generalized

additive models (GAMs) using the “gam” function in the R package mgvc. To account for the

fact that six plants in the B. nigra experiment (4 in the undamaged control treatment and 2 in the

mechanically damaged treatment) did not flower by day 40 (termination of experiment), we

converted flowering data into a binary response variable, with each plant classified as

“flowering” or “not-flowering” on each experimental day. After initial data exploration, we

decided to model flowering time as a function of treatment, time itself, and plant ID, with an

interaction between time and plant. Treatment and time were entered as parametrically estimated

explanatory variables, with the smoothed term including time by plant (Table. S3). We set the

data family to binomial and the basic dimension of the smoothing function to ‘re’ in order to

account for random factors. Additionally, we used the package itsadug to handle the

autocorrelation within the time series. Models were validated by plotting Pearson versus Fitted

residuals for response variables and covariates, to ensure that homoscedasticity and normality

assumptions were met. Model selection was made using the ANOVA function and AIC to get the

best fit. This approach allowed us to explore the simultaneous effects of treatment and time and

thereby explain a high proportion of deviance within the model. Following this analysis, we used

a generalized linear model (GLM) with a binomial error distribution and logistic-link function to

calculate the least square means comparisons between the treatments (33). Additionally, we used

the mean least squares coefficients to estimate the estimated time to reach 50% of flowering

plants for each treatment.

6

To test for effects of pollen availability on damaging behavior, we used a generalized linear

model with discrete error distribution (Poisson), with diet as a fixed effect and colony as a

random effect. We used backwards stepwise model simplification based on likelihood ratio tests

to reduce model complexity as far as possible (33).

To test for differences among damage treatments over the course of our rooftop studies, we

used a series of generalized linear mixed effect models (GLMMs). For the 2018 rooftop study,

we used a GLMM with Poisson error fitted by maximum likelihood, in order to look at

differences between the phases. Date was included to account for temporal non‐independence of

data. We used backwards stepwise model simplification based on likelihood ratio tests to reduce

model complexity as far as possible (33). We also calculated a rolling 7-day average for plant

damage, using weekday data to estimate the weekends, using the “zoo” package. In 2019, we

also used a GLMM to look at the effect of roof treatment, in addition to using a general linear

model to test for differences before and after the roof treatment was cut. These models were also

validated using backwards stepwise model simplification.

7

Fig. S1.

Estimate of time required for S. lycopsicum and B. nigra subjected to three damage

treatments (bee damage [yellow], mechanical damage [blue], no damage [green]) to flower

based on GLM with a binomial error distribution and logistic-link function. The least

square means comparisons between the treatments were calculated from this model in order to

test the effects of damage treatments on flowering time. Additionally, an estimate of the time

required for 50% of the plants in each treatment was calculated using the mean least squares

coefficients. (a) S. lycopersicum: The bee damage treatment was significantly different from the

mechanical damage and control treatments (Bee damage Vs Control; estimate=0.5681, P

<0.001), (Bee damage vs Mechanical; estimate=-0.5004, P < 0.001); however, the mechanical

treatment was not significantly different from the control (Mechanical Vs Control;

estimate=0.0677, P =0.192). Bee damaged tomato plants were predicted to reach 50% flowering

8

at 35 days (estimate=1.436, t=31.05), mechanically damaged plants at 62 days (estimate=0.705,

11.93) and control plants at 73 days (estimate=0.548, t=9.12). Bee damaged plants were

predicted to flower 38 days earlier than undamaged control plants and 27 days earlier than

mechanically-damaged plants. (b) B. nigra: All treatments were significantly different from one

another (Bee damage Vs Control; estimate=0.658, P =<0.001), (Bee damage Vs Mechanical;

estimate=-0.388, P =< 0.001), (Mechanical Vs Control; estimate=0.270, P =0.0034). Bee

damaged B. nigra plants were predicted to reach 50% flowering at 17 days (estimate=2.783,

t=43.11), mechanically damaged plants at 26 days (estimate=1.925, t=47.53) and control plants

at 35 days (estimate=0.388, t=14.35). Bee damaged B. nigra plants were thus predicted to flower

18 days earlier than undamaged control plants and 8 days earlier than mechanically-damaged

plants.

Fig. S2.

2019 flower transect study measuring species richness in a 500m radius around rooftop 1.

Transect was conducted along two axes (North-South and East-West) for 1km; and marked out

using satellite images from Google earth.

9

Fig. S3.

Counts of the different bee species that visited flowering edge plants during Phase 2 of the 2018

rooftop experiment. Data were collected for 1 hour, 3 times per day (beginning at ~ 09:00; 13:00;

16:00). While only bumblebee species were observed visiting the focal patch of flowerless

plants, other pollinators were observed in the flowering plant patch throughout Phase 2.

10

Fig. S4.

Post-experiment dissection of B. terrestris microcolony that had been subject to pollen

deprivation. Drone brood cells, nectar pots, and one pollen pot are visible. Drone cells (circled in

blue) are large, uniform in color, round and capped. Nectar pots (circled in red) tend to be

smaller than egg cells, uncapped and filled with nectar. Pollen pots (circled in green) are similar

in size to nectar pots and containing pollen. Hive structures were inspected before experimental

onset for storage capacity and queen presence.

11

Fig. S5.

Experimental setup for semi-natural outdoor experiments. (a) In 2018, individual queenless

microcolonies were consecutively placed on a rooftop on the ETH Zentrum campus. During

phase 1 (March 26th – May 25th), hives 1-3 were placed under a sheltered overhang on a

westward facing wall near a focal patch of 36 flowerless plants. No floral resources were

provided during this period. During phase 2 (June 4th – July 20th) hives 4-5 were similarly

placed, and a patch of 100 plants in flower were placed along the border of the roof. Hives had

open foraging access during the day and access to water feeders on the roof. (b) In 2019,

queenright founding colonies were divided into two roof treatments in early summer (June–

July). On Roof 1, eight hives were placed along a sheltered western wall; on Roof 2, another

eight hives were placed in the same orientation and sheltered by large insulating boxes. Three

focal plant patches comprising 300 flowerless plants each were placed on each roof. In addition,

hives on Roof 2 had continuous access to a rooftop garden sown with wildflowers (4.5 x 7m;

A

B

Hive location

Phase 1 Phase 2

Roof 1

Roof 2

Water feeder

Non-flowering plants

Flowering plants

2018

2019

12

sown during weeks 1-4), along with 30 additional plants in flower placed along the border of the

roof. Hives on both rooftops had access to water feeders.

Table S1.

Generalized additive models analyzing the binary response variable ‘flowering’ against a

selection of covariates.

Model Parametric terms d.f Chi.sq p

S. lycopersicum Treatment 2 54.27 <0.001

S. lycopersicum Time 1 180.39 <0.001

S. lycopersicum Treatment: Time 2 15.07 <0.001

B. nigra Treatment 2 17.752 <0.001

B. nigra Time 1 120.071 <0.001

B. nigra Treatment: Time 2 8.363 0.01528

Smoothing terms e.d.f Chi.sq p

S. lycopersicum Time: Plant ID 0.9741 39.46 <0.001

B. nigra Time: Plant ID 0.9941 181.9 <0.001

Interaction effects are indicated by a colon. Overall r2 (adjusted) = 0.794 (n= 4800

observations) for S. lycopersicum and 0.532 (n=1200 observations) for B. nigra respectively.

E.D.F., estimated degrees of freedom for the model terms; d.f., degrees of freedom for

reference distributions.

13

Table S2.

Damage inflicted by 10 additional pollen-satiated B. terrestris microcolonies during several

different experiments. All colonies were caged and given access to external nectar feeders to

encourage foraging. When presented with plants, the proportion of leaves damaged by these

microcolonies was consistently similar to that of pollen satiated hives in our pollen deprivation

experiment (Figure 2).

Dates Experiment Hive ID Number of Plants Total leaves % Damage

09.10.18-

20.10.18 1 1 8 85 5%

09.10.18-

20.10.18 1 2 8 62 18%

28.10.18-

03.11.18 2 3 4 71 6%

28.10.18-

03.11.18 2 4 4 34 18%

03.05-19-

14.05.19 3 5 4 65 0%

03.05-19-

14.05.19 3 6 4 52 2%

15.05.19-

26.05.19 4 7 4 50 6%

15.05.19-

26.05.19 4 8 4 65 3%

29.05.19-

09.06.19 5 9 4 69 0%

29.05.19-

09.06.19 5 10 4 73 3%

14

Table S3.

Numbers of bumblebee workers (from three species) directly observed damaging experimental

plants during the 2018 Rooftop experiment (both phases).

Bombus species Phase Months observed Number of individuals

damaging

Bombus terrestris 1-2 April-June 28

Bombus lucorum 2 June 3

Bombus lapidarius 2 June-July 4

Movie S1.

Movie showing workers from a pollen-deprived colony damaging B. nigra plants.

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