ArticlePDF Available

Detection and Learning of Floral Electric Fields by Bumblebees

Abstract and Figures

Insects use several senses to forage, detecting floral cues such as color, shape, pattern, and volatiles. We report a formerly unappreciated sensory modality in bumblebees (Bombus terrestris), detection of floral electric fields. These fields act as floral cues, which are affected by the visit of naturally charged bees. Like visual cues, floral electric fields exhibit variations in pattern and structure, which can be discriminated by bumblebees. We also show that such electric field information contributes to the complex array of floral cues that together improve a pollinator's memory of floral rewards. Because floral electric fields can change within seconds, this sensory modality may facilitate rapid and dynamic communication between flowers and their pollinators.
Content may be subject to copyright.
mortality or b reeding phenology, including fre-
quency of winter reproduction, should be part of
futu re research, as should quantifying vegetation
quality that could reflect, for example, continent-
scale long-term variation in climate or nutrient
Irrespective of the proximate process (or pro-
cesses) affecting winter population growth rate, the
coherence of the changes coinciding with a period
of ongoing global environmenta l change suggests
increasingly frequent prolonged periods of low
am plitude, although high-amplitude vole peaks
as seen in 201 1 in northern Fennoscandiamay
occasionally reappear. The loss of years of super-
abundant vol es could reduce zoonotic disease risk
and crop damage (27). Continent-scale collapses
in population cycles are likely to be deleterious
for vole predators because for most, reproduc-
tion is modulated by vole density in spring, which
is when the strongest and most consistent dam-
pening occurs. Large impacts on vegetation (6)
and predator populations (1, 28) could see cas-
cading effects on other compartments of the food
webs (3, 29) in ecosystems as diverse as farm-
land, forest, and arctic tundra.
References and Notes
1. B. rnfeldt, T. Hipkiss, U. Eklund, Proc. Biol. Sci. 272,
2045 (2005).
2. K. B. Strann, N. G. Yoccoz, R. A. Ims, Ecography 25,
81 (2002).
3. R. A. Ims, E. V. A. Fuglei, Bioscience 55, 311 (2005).
4. R. A. Ims, J.-A. Henden, S. T. Killengreen, Trends Ecol. Evol.
23, 79 (2008).
5. J. ty, G. Gauthier, E. Korpimäki, J.-F. Giroux, J. Anim.
Ecol. 71 , 88 (2002).
6. J. Olofsson, H. Tommervik, T. V. Callaghan, Nat. Clim.
Change, published online 22 May 2012 (10.1038/
7. F. Ecke, P. Christensen, P. Sandström, B. rnfeldt,
Landscape Ecol. 21 , 485 (2006).
8. T. Saitoh, B. Cazelles, J. O. Vik, H. Viljugrein, N. C. Stenseth,
Clim. Res. 32, 109 (2006).
9. S. M. Bierman et al., Am. Nat. 167, 583 (2006).
10. J. E. Brommer et al., Glob. Change Biol. 16, 577 (2010).
11. N. C. Stenseth, Oikos 87 , 427 (1999).
12. K. L. Kausrud et al., Nature 456, 93 (2008).
13. T. F. Hansen, N. C. Stenseth, H. Henttonen, Am. Nat.
154, 129 (1999).
14. Materials and methods are available as supplementary
materials on Science Online.
15. R. A. Fleming, H. J. Barclay, J.-N. Candau, Ecol. Modell.
149, 127 (2002).
16. T. F. Hansen, N. C. Stenseth, H. Henttonen, J. Tast,
Proc. Natl. Acad. Sci. U.S.A. 96, 986 (1999).
17. L. Hansson, Oikos 40, 258 (1983).
18. I. Hanski, H. Henttonen, J. Anim. Ecol. 65, 220 (1996).
19. R. A. Ims, N. G. Yoccoz, S. T. Killengreen, Proc. Natl.
Acad. Sci. U.S.A. 108, 1970 (2011).
20. P. Turchin, L. Oksanen, P. Ekerholm, T. Oksanen,
H. Henttonen, Nature 405, 562 (2000).
21. B. rnfeldt, Oikos 107, 376 (2004).
22. D. M. Johnson et al., Proc. Natl. Acad. Sci. U.S.A. 107,
20576 (2010).
23. J. R. Bell et al., Ecol. Lett. 15, 310 (2012).
24. L. Korslund, H. Steen, J. Anim. Ecol. 75, 156 (2006).
25. N. C. Stenseth et al., Proc. Natl. Acad. Sci. U.S.A. 100,
11478 (2003).
26. M. J. Smith, A. White, X. Lambin, J. A. Sherratt, M. Begon,
Am. Nat. 167, 695 (2006).
27. N. C. Stenseth et al., Front. Ecol. Environ 1, 367
28. N. M. Schmidt et al ., Proc. R Soc. B 279, 4417
29. R. W. Summers, L. G. Underhill, E. E. Syroechkovski,
Ecography 21, 573 (1998).
30. T. Royama, Analytical Population Dynamics, M. B. Usher,
Ed. (Chapman & Hall, London, 1992), pp. 5560.
Acknowledgments: This research was funded by the national
funders Natural Environment Research Council, Research
Council of Norway, and Agence Nationale de la Recherche,
part of the 2008 ERA-Net BiodivERsA call for research
proposals. D.A.E. was funded by the Scottish Government.
We thank R. B. OHara and F. Barraquand for useful
methodological inputs and all the contributors to vole
sampling over decades. General correspondence should be
addressed to X.L. and specific requests to T.C. (cornulier@ Raw data are available in supplementary text
section IX). Authors declare no conflicts of interest. A.B., B.H.,
B.J., C.I., E.F., E.T., F.E., H.H., H.P., J.E.B., J.J., K.Z., O.H., S.J.P.,
V.B., and X.L. led the data collection; T.C., N.G.Y., R.A.I.,
A.M., and X.L. conceived the ideas for the paper and its
structure; T.C., N.G.Y., D.A.E., and X.L. designed the analyses;
T.C. and X.L. wrote the manuscript; and all authors discussed
the results and commented on the manuscript.
Supplementary Materials
Materials and Methods
Supplementary Text
Figs. S1 to S6
References (3147)
17 August 2012; accepted 12 February 2013
Detection and Learning of Floral
Electric Fields by Bumblebees
Dominic Clarke,* Heather Whitney,* Gregory Sutton, Daniel Robert
Insects use several senses to forage, detecting floral cues such as color, shape, pattern, and
volatiles. We report a formerly unappreciated sensory modality in bumblebees (Bombus terrestris),
detection of floral electric fields. These fields act as floral cues, which are affected by the visit of
naturally charged bees. Like visual cues, floral electric fields exhibit variations in pattern and
structure, which can be discriminated by bumblebees. We also show that such electric field
information contributes to the complex array of floral cues that together improve a pollinators
memory of floral rewards. Because floral electric fields can change within seconds, this sensory
modality may facilitate rapid and dynamic communication between flowers and their pollinators.
lowers produce a diverse range of cues
and attractants to pollinators and in doing
so act as sensory billboards (1). The di-
versity of floral cues encompasses intricate color
hues and patterns, petal texture, fragrant volatiles,
local air humidity , and echolocation fingerprints
(14). The impact of floral cues on pollinator be-
havior has been observed since Aristotle (5), yet
new floral cues are still being discovered (3, 4).
Multimodal floral cues have been found to en-
hance both pollinator foraging efficiency and
pollination (6), and thus facilitate increased seed
and fruit set.
Flying insects, including pollinators like honey-
bees, usually possess a positive electric poten-
tial (710). Conversely , flowers often exhibit a
negative potential (7, 11). Electric fields arising
as a result of this potential difference between
flowers and insects promote pollen transfer and
adhesion over short distances (7, 8, 12, 13). Fur-
thermore, these fields differ according to the
pollination status of the flower, as the deposi-
tion of pollen and resulting pollination changes
flower electric potential (14, 15). However, the
use of electric fields by pollinators as informa-
tive cues has not been investigated. In the com-
plex world of plant-pollinator interactions, any
cue that increases pollination and foraging effi-
ciency should be mutually beneficial. Here, we
report that bumblebees can detect and learn to
use floral electric fields, and their structural var-
iation, to assess floral reward and discriminate
among flowers.
The electrical interactions between the bee
and the flower arise from the charge carried by
the bee and the potential of the flower in rela-
tion to the atmospheric electric field. To quan-
tify bee charge, individual B. terres tris workers
were trained to fly into a Faraday pail that con-
tained a sucrose reward. The net charge q car-
ried by the bee was measured from the induced
voltage on a calibrated capacitor (methodology
described in supplementary materials). Measured
on 51 individuals, 94% of bees were positively
charged and 6% negatively charged (q
5 pC, SD = 35pC) (Fig. 1A). These results cor-
roborate previous measurements on the honeybee
Apis melifera (9) and establish that the majority
of bees flying in the arena carry a positive charge
susceptible to transfer .
Electrical interaction between bee and flower
was further explored by placing Petunia integrifolia
flowers in an arena with free-flying foraging
bees. The electric potential in Petunia stems was
recorded to assess the electrical signature produced
by the approach and landing of an individual
charged bee. Charge transfer to the flower re-
sulted in a positive change in electric potential
recorded in the stem. The landing of 50 indi-
School of Biological Sciences, University of Bristol, Woodland
Road, Bristol BS8 1UG, UK.
*These authors contributed equally to this work.
Corresponding author. E-mail:
5 APRIL 2013 VOL 340 SCIENCE www.sciencemag.org66
viduals resulted in a mean potential change last-
ing ~100 s, which peaked at ~25 T 3mV(SD=
24, n = 50) (Fig. 1B). Such change exceeds
natural fluctuations in the absence of bees (Fig.
1B) and outlasts the presence of the bee on the
flower. This change in potential is often initiated
before contact with the bee (movie S1), sug-
gesting that this is not simply a hydraulic wound-
response variation potential as in (16) but involves
direct electrostatic induction between the charged
bee and the grounded flower as hypothesized
in (7, 8).
Because the floral electric potential is di-
rectly affected by pollination (14, 15)andbee
visitation (Fig. 1B), it potentially carries infor-
mation for other visiting pollinators regarding
floral resources. V isiting pollinators affect floral
cues directly , by leaving scent marks on the pe-
tal surface, or by initiating changes in floral cues,
such as color, shape, and humidity (4, 1719).
Such changes typically occur in the time frame
of minutes to hours. The variation potential pro-
duced by bee visitation occurs within a time
frame of seconds (Fig. 1B).
For a floral electric field to act as a cue, it
must be possible for pollinators to detect and
discriminate it from the background. We used
differential conditioning (3) to test the ability
of bumblebees to discriminate between artifi-
cial flowers (E-flowers) with differing electric
fields. E-flowers consisted of a 35-mm-diameter
by 1.5-mm-thick steel base disk decorated with
a purple epoxy top disk. Half the E-flowers
were held at a biologically relevant 30-V dc bias
voltage. This voltage was chosen as a proxy for
the electric field of an isolated flower standing
30-cm tall in a typical 100 V m
electric field (20). Charged E-flowers of f e r e d a
sucrose reward, while identical E-flowers were
held at ground (0 V) and provided a bitter qui-
nine hemisulfate solution (3). E-flowers were
indistinguishable in every other respect. During
the course of 50 bee visits, there was an increase
in the relative number of visits to rewarding
charged flowers (Fig. 2A). To measure bee learn-
ing, we compared the mean accuracy of the final
10 visits (visit 41 to 50) to a random choice
model. In their final 10 visits to 30-V charged
E-flowers, bees (n = 11) achieved 81 T 3%
accuracy (T
= 10.8, P =7.4×10
). Both
flower types were then grounded and the choice
test continued. Without the electric cue, the same
set of trained bees could no longer discriminate
between the rewarding and unrewarding E-flowers,
also demonstrating the absence of systematic
experimental bias. Accuracy after the electric cue
is removed was 54 T 4%, which does not differ
significantly from random choice (T
P = 0.35) (Fig. 1B). Using a 10-V bias failed to
elicit significant learning (n = 10, mean accu-
racy = 56 T 4%, T
=1.4,P = 0.19) (Fig.
2, A and B).
Floral cues are diverse and address the mul-
timodal perception of pollinators. Working in
concert, floral cues enhance foraging efficien-
cy (6) and constitute a complex informational
ecology of competing flower advertisement. Col-
or cues rely both on hue and on contrast between
hues and their geometrical patterns. Nectar
guides constitute such patterns, providing infor-
mation attractive to pollinators and facilitating
foraging efforts (21, 22). By analogy , the geom-
etry of floral electric fields may carry additional
information important for pollinators. The diver-
sity of floral electric field geometry can be ex-
perimentally visualized by coating flowers with
positively charged colored particles released as
an aerosol close to the corolla. The heterogeneous
Fig. 1. Electric charge carried
by bumblebees and its trans-
fer to flowers. (A)Histogramof
electric charge of flying bumble-
bees. Boxplot shows median, SD,
interquartile range, and outliers.
(B) Mean variation potential in
the Petunia stem resulting from
bee landings (red, n =51),shown
with T1 SEM (gray). Distribution
of the natural variation of stem
potential (measured along 35 sam-
ples of 30 s) in absence of bees,
truncated at 2 SD (blue).
Charge (pC)
Stem Potential (mV)
Time (s)
Mean = 32pC
Median = 29pC
SD = 35pC
SEM = 5pC
10 50
Visit Number
30V (n=11)
10V (n=10)
30V E-Flower 10V E-Flower
% Correct Choices
% Correct Choices
30 402010
Fig. 2. Bumblebees learn the presence of an electric field. (A) Learning curves of foraging bees, trained to 30-V (red diamonds) or 10-V (blue circles)
E-flowers. Dashed line shows switching off electric field. (B) Mean correct choices to 30-V (left) and 10-V (right) E-flowers over visits 41 to 50 in (A) during
training (voltage on) and control (voltage off). Error bars show SEM. SCIENCE VOL 340 5 APRIL 2013
pattern of color deposition reveals the struc-
ture of the electric field at the flowers surface
(Fig. 3A).
Electric field structure was also visualized
using finite element (FE) modeling of an ide-
alized 30-cm-tall flower in a physically realis-
tic, 100 V m
atmospheric electric field (20)
(Fig. 3B, left). Plants are conductively linked
to ground via their stems and roots, a connec-
tion that maintains them close to ground poten-
tial (7). Hence, a grounded 30-cm-tall plant in
such an atmospheric electric field exhibits a
30-V potential difference between its inflores-
cent structures and the surrounding air, exhib-
iting a patterned electric field (Fig. 3B). This
experimental and modeling evidence reveals
that flower morphology determines electric field
T o test the bees ability to discriminate E-field
geometries, differential conditioning was used
with two types of E-flowers, providing similar
voltage but different local patterns (Fig. 3C). Re-
warding E-flowers presented a bulls eye pat-
tern, with the outer ring held at +20 V and the
center ring at 10 V. A versive E-flowers presented
a homogeneous voltage at +20 V (Fig. 3C). Bees
(n = 10) learned to discriminate between these two
patterns, reaching 70 T 3% accuracy over their
final 10 visits, performing significantly better than
random choice (T
=6.7,P =8×10
(Fig. 3E). After this task, a subset of the bees
(n = 4) was allowed to complete 50 additional
visits to rewarding and aversive E-flowers with
identical homogeneous +20 V fields. These bees
failed to discriminate between E-flowers (Fig.
3E). Altogether , these tests show that bumble -
bees can discriminate charged from uncharged
flowers and can distinguish between flowers that
differ in the geometry of their electric field. As
such, E-fields could be used by flowers to pro-
vide information to their pollinators.
Floral cues can work individually or com-
plementarily (1, 6). When presented together,
multimodal cues enhance the certainty of sen-
sory information used by honeybees. Specifical-
ly, the association of color with olfactory floral
cues reduces the bees perceptual uncertainty
their ability to distinguish between rewarded
Fig. 4. Multimodal fa-
cilitation. Colors (A)and
voltage configurations (B)
associated with rewarding
and aversive E-flowers. (C)
Mean number of visits taken
by bees in each group to
reach 80% correct choices.
Hue + E-Field
Hue Only
Mean # of visits
Hue Stimuli
E-Field Stimuli
Fig. 3. Geometry of floral
electric field and discrim-
ination task. (A)Flowers
before (left half) and after
(right) spraying with electro-
static colored powder; (a)
Gerbera hybrida,(b)Digital-
is p urpurea,(c)Geranium
hybrida,(e)Petunia hybrida,
(f) Clematis armandii.Den-
sity of powder deposition
reflects the variation in elec-
tric field strength at the flow-
ers surface. (B) FE model of
an idealized 30-cm-tall flow-
er, equipotential with ground,
in an atmospheric field of
100 V/m. Left: scalar electric
potential. Right: electric field
magnitude. (C)FEmodels
of electric field produced by
E-flowers. (D) Color scale for
(B ) an d (C). (E) Pattern dis-
crimination as mean per-
centage of correct choices
over the last 10 visits for
patterns on and off. Error
bars show SEM.
and aversive stimuli (23). The hypothesis can
be formulated that the floral electric field re-
inforces the effectiveness of other floral cues.
If true, an electric cue paired with a color cue
should produce an enhanced learning outcome
equivalent to that obtained with the test using
color and scent. Differential conditioning was
used to test this hypothesis. The same two green
target hues were used as in (23), but olfactory
cues were replaced with a patterned electric field
(Fig. 3C). Bees were trained to discriminate be-
tween E-flowers of hue 120° HSB (hue, satura-
tion, brightness) which offered a sucrose reward,
and E-flowers of hue 140° HSB, which provided
an aversive quinine solution (Fig. 4A). Bees
learned to discriminate between the rewarding
and aversive chargeless E-flowers either using
color information alone (n = 16) or in combi-
nation with the patterned E-field (n = 18) (Fig.
4A). When learning color on its own, discrim-
ination to 80% success (i.e., 8 out of the last 10
choices correct) took 35 T 3 visits. When com-
bined with the E-field pattern, the number of
visits required was significantly reduced to 24 T
2-sample; unequal
= 2.86, P = 0.008) (Fig. 4A).
Th is de m on s t r a te s th at th e com bination of two
cues, E-field and hue, enhances the bees ability
to discriminate.
Our results show that electric field consti-
tutes a floral cue. Contributing to a varied floral
display aimed at pollinator senses, electric fields
act to improve both speed and accuracy with
which bees learn and discriminate rewarding re-
sources. As such, electric field sensing consti-
tutes a potentially important sensory modality,
which should be considered alongside vision
and olfaction. The ubiquity of electric fields in
nature and their integration into the bees sen-
sory ecology suggest that E-fields play a thus
far unappreciated role in plant-insect interac-
tions. The present study raises the possibility of
reciprocal information transfer between plants
and pollinators at time scales of milliseconds
to seconds, much faster than previously de-
scribed alterations in floral scent, color, or hu-
midity (4, 18, 19). The remarkably accurate
discrimination and learning of color patterns
by bees was revealed by both laboratory and
field training experiments (19, 2123). Sim-
ilarly, the present laboratory study reveals that
floral electric fields occur in patterns and that
they can be perceived. Hence, our study pro-
vides a framework for exploring the function
and adaptive value of the perception of weak
electric fields by bees in nature.
References and Notes
1. R. A. Raguso, Curr. Opin. Plant Biol. 7, 434 (2004).
2. R. Simon, M. W. Holderied, C. U. Koch, O. von Helversen,
Science 333, 631 (2011).
3. H. M. Whitney et al., Science 323, 130 (2009).
4. M. von Arx, J. Goyret, G. Davidowitz, R. A. Raguso,
Proc. Natl. Acad. Sci. U.S.A. 109, 9471 (2012).
5. Aristotle, Historia Animalium (Harvard Univ. Press,
Cambridge, MA, 1970).
6. A. S. Leonard, A. Dornhaus, D. R. Papaj, Curr. Zoology
57, 215 (2011).
7. S. A. Corbet, J. Beament, D. Eisikowitch, Plant Cell
Environ. 5, 125 (1982).
8. Y.Vaknin,S.Gan-Mor,A.Bechar,B.Ronen,D.Eisikowitch,
Plant Syst. Evol. 222, 133 (2000).
9. M. E. Colin, D. Richard, S. Chauzy, J. Bioelectric. 10,17
10. Y. K. Yeskov, A. M. Sapozhnikov, Biophysics (Oxf.) 21,
1124 (1976).
11. G. E. Bowker, H. C. Crenshaw, Atmos. Environ. 41,
1587 (2007).
12. E. H. Erikson, S. L. Buchmann, in Handbook of
Pollination Biology, C. E. Jones, R. J. Little, Eds.
(Van Nostrand Reinhold, New York, 1983).
13. S. Gan-Mor, Y. Schwartz, A. Bechar, D. Eisikowitch,
G. Manor, Can. Agric. Eng. 37, 189 (1995).
14. W. N. We¸dzony, M. Filek, Acta Physiol. Plant. 20, 291
15. J. Fromm, M. Hajirezaei, I. Wilke, Plant Physiol. 109,
375 (1995 ).
16. B. Stanković, T. Zawadzki, E. Davies, Plant Physiol. 115 ,
1083 (1997).
17. J. C. Stout, D. Goulson, Anim. Behav. 62, 183 (2001).
18. M. R. Weiss, Am. J. Bot. 82, 167 (1995).
19. P. Willmer, D. A. Stanley, K. Steijven, I. M. Matthews,
C. V. Nuttman, Curr. Biol. 19, 919 (2009).
20. M. J. Rycroft, S. Israelsson, C. Price, J. Atmos. Sol. Terr. Phys.
62, 1563 (2000).
21. N. M. Waser, M. V. Price, Nature 302, 422 (1983).
22. A. S. Leonard, D. R. Papaj, Funct. Ecol. 25, 1293 (2011).
23. A. S. Leonard, A. Dornhaus, D. R. Papaj, J. Exp. Biol. 214,
113 (2011 ).
Acknowledgments: This work was sponsored by a grant from
the Leverhulme Trust (RPG 173). H.W. is supported by the
European Research Council and Association for the Study of
Animal Behaviour. D.R. is supported by the Royal Society of
London. The authors declare no conflict of interest. All data
are available in the supplementary materials. We thank
K. Strickland for help with data collection and C. Evans for
illustrative work. We thank A. Radford, J. Matthews, and
S. Rands for reading the manuscript and helpful feedback.
Supplementary Materials
Materials and Methods
References (2426)
Movie S1
Data File S1
1 October 2012; accepted 5 February 2013
Published online 21 February 2013;
Recovery of an Isolated Coral Reef
System Following Severe Disturbance
James P. Gilmour,
* Luke D. Smith,
Andrew J. Heyward,
Andrew H. Baird,
Morgan S. Pratchett
Coral reef recovery from major disturbance is hypothesized to depend on the arrival of propagules
from nearby undisturbed reefs. Therefore, reefs isolated by distance or current patterns are
thought to be highly vulnerable to catastrophic disturbance. We found that on an isolated reef
system in north Western Australia, coral cover increased from 9% to 44% within 12 years of a
coral bleaching event, despite a 94% reduction in larval supply for 6 years after the bleaching.
The initial increase in coral cover was the result of high rates of growth and survival of remnant
colonies, followed by a rapid increase in juvenile recruitment as colonies matured. We
show that isolated reefs can recover from major disturbance, and that the benefits of their isolation
from chronic anthropogenic pressures can outweigh the costs of limited connectivity.
oral reefs are dynamic ecosystems pe-
riodically subjected to severe disturbances,
such as cyclones, from which they typ-
ically recover at scales of one to two decades
(1, 2). Today, this recovery is undermined by
increasing anthropogenic pressures leading to
global declines in coral cover (3, 4) and diver-
sity (5, 6). Understanding the global degradation
of coral reef ecosystems requires long-term data
on population and community dynamics, espe-
cially demographic processes (79). However,
the rarity of such data has precluded a thorough
assessment of the future of coral reef ecosystems
in the IPCC report on climate change (10, 11),
and current knowledge is mostly derived from
studies of reef degradation (9, 12)ratherthanreef
recovery . Here, we document the recovery of coral
assemblages at Australias largest oceanic reef
system, where changes in assemblage structure
and key demographic parameters were quantified
for 16 years, through a regime of disturbances
beginning with a catastrophic mass bleaching
event in 1998.
The Scott system of reefs is surrounded by
oceanic waters on the edge of W estern Australias
continental shelf. It is more than 250 km from
the mainland and other reefs in the region, and
more than 1000 km from a major center of ur-
banization (fig. S1). There is little fishing pres-
sure at the reefs, apart from the harvesting of
sea cucumber, trochus, and shark fin by In-
donesian islanders using traditional fishing meth-
ods for more than 300 years (13, 14). Such oceanic
reef systems may provide a critical refuge for
coral reef assemblages because they are far re-
moved from most direct anthropogenic pres-
sures. Conversely, isolation and a consequent
lack of connectivity may make such systems
Australian Institute of Marine Science (AIMS), University of
Western Australia Oceans Institute, Perth, WA 6009, Australia.
ARC Centre of Excellence for Coral Reef Studies, James Cook
University, Townsville, QLD 4811, Australia.
*Corresponding author. E-mail:
Present address: Woodside Energy Limited, Perth, WA 6000,
Australia. SCIENCE VOL 340 5 APRIL 2013 69
... They are able to forage up to 1-2 km from their colony with a ground speed of 54km/h (Osborne et al., 1999;Walther-Hellwig and Frankl, 2000;Dramstad et al., 2003) [41,59,15] . Bumblebees have tendency of flower constancy and able to identify the flower recently visited by other bees through detection of electric field (Clarke et al., 2013) [11] and identify flowers through temperature of flowers (Harrap et al., 2017) [25] . Sapir et al. (2017) [46] most interestingly, the bumblebees also changed the behavior of the honeybees, thereby increasing their pollination efficiency. ...
... They are able to forage up to 1-2 km from their colony with a ground speed of 54km/h (Osborne et al., 1999;Walther-Hellwig and Frankl, 2000;Dramstad et al., 2003) [41,59,15] . Bumblebees have tendency of flower constancy and able to identify the flower recently visited by other bees through detection of electric field (Clarke et al., 2013) [11] and identify flowers through temperature of flowers (Harrap et al., 2017) [25] . Sapir et al. (2017) [46] most interestingly, the bumblebees also changed the behavior of the honeybees, thereby increasing their pollination efficiency. ...
Full-text available
Bumblebees are efficient pollinator of various fruit and vegetable crops as compare to honeybees under protected condition as well as open conditions. The cross pollination carried out by bumblebees known as myophilly. Bumblebees have tend to forage faster than honeybees, pollinate more flowers per bee, long tongue prefers flower with long corolla tube. At low temperature and low light intensities, the foraging activities of bumblebees are more efficient and cost-effective alternate to hand/manual pollination even. They are perfect pollinator of flowers of family Solanaceae because sonication is required for pollination. Now a days, the population of bumblebees is decreasing at global level due to indiscriminate use of pesticides, loss of natural habitats, mechanization in agriculture and climate changes. The conservation techniques like modification of landscape such as promoting wild flowers and creation of niches for their hibernation, survival and reproduction etc. which provide favorable conditions to increase the bumblebees abundance, foraging behavior and their efficiency. The scientists should attempts for evaluating the pollination efficiency of bumblebees to boost the production of vegetable and fruit crops.
... In addition to visual cues, flowers provide mechanosensory (Goyret 2006), gustatory (Ruedenauer et al. 2015), electrostatic (Clarke et al. 2013), and olfactory information (Lawson et al. 2018;Odell et al. 1999;Reinhard et al. 2010;Schaeffer et al. 2019;Schiestl 2015;Srinivasan and Reinhard 2009). As with color, there is evidence that bumble bees have innate odor preferences (Renner and Nieh 2008;Suchet et al. 2010). ...
... These scent marks appear to be passive footprint odors that are left behind when bumble bees forage (Saleh et al. 2007;Wilms and Eltz 2007) and are variable between individuals and colonies (Pearce et al. 2017). Electrostatic cues may also signal recent visitation by another individual via detection of a weakened floral-electric field (Clarke et al. 2013;Eskov 2018;Kaplan 2013;Koh et al. 2019;Koh and Robert 2020;Montgomery et al. 2019;Sutton et al. 2016). Avoidance of recently visited flowers should increase foraging efficiency. ...
Bumble bee foragers provide essential pollination services in both natural and agricultural ecosystems. However, foraging is not monolithic; rather, it is a complex behavior encompassing multiple phases that utilize different sensory cues and decision-making processes. Understanding how the interplay of spatial scale and forager experience interact with behavioral state to modulate what sensory information is necessary across foraging phases is a critical component of understanding how anthropogenic modifications to the environment impact bumble bee ecology and conservation. The lack of a comprehensive framework and common vocabulary characterizing foraging behaviors can result in difficulty interpreting and applying experimental findings in the literature. This manuscript proposes a scaffolding framework for foraging behaviors organized by behavioral states and state-transitions, spatial scale, and experience to facilitate more clarity in interpretation and design of future foraging studies. Given the similarities between bumble bees and other central place foragers, this framework has broad applicability.
... Previous studies have suggested biological effects of EMR on insects. The EMR can affect morphology and biological processes, such as reproduction by insects (Cammaerts et al. 2012;Clarke et al. 2013). Exposing fruit flies, Drosophila melanogaster (Meigen, 1830) to ionizing radiation can increase their protein stress levels and reduce their viability (Moskalev et al. 2015). ...
... Failure to resolve the threats of EMR has potential to create 'ecological traps' for species (Hale and Swearer 2016), leading to their extirpation, and reduced ecological services. For instance, impairing the cognitive and motor abilities of honey bees by EMR would lead to reduced crop pollination (Shepherd et al. 2018), and decline in bumble bees, Macronomia rufipes (Smith, 1875) has potential to reduce crop pollination and production (Clarke et al. 2013). Furthermore, EMR may lead to changes in foraging behavior and distribution in fauna, such as honey bees (Taye et al. 2017). ...
Inappropriate deployment of linear physical infrastructures, such as game fences, roads, electric power-lines, buildings, and phone masts can be detrimental to wild fauna. Fatalities arising from wildlife collisions with such infrastructure have been widely documented. However, there are non-physical and less studied effects, such as the ‘hidden’ negative ecological effects of electromagnetic radiation (EMR) on terrestrial fauna. In this study, the effects of phone mast-generated EMR on abundance, richness and distribution of terrestrial birds and insects in the Kafue National Park were studied. Ten (10) sample plots of 100 m x 100 m each were set at three (3) radial locations, based on the phone mast generated EMR strengths. For birds, point counts, while hand collection, cryptic searching, vegetation beating, sweep netting, pitfall trapping, sorting and identification for insects were employed for data collection. Data were analysed using biological indices (i.e., Shannon-Wiener and Simpson’s) and Analysis of Variance (ANOVA). The wildlife diversity significantly reduced with increasing EMR strengths, especially in areas (<12 km from phone mast) with greater than 250±20 µA/m EMR levels. We suggest that deployment of wireless telecommunication infrastructure should take into account EMR levels, safe zones and avoid or minimize biological loss in hotspots.
... They are able to detect magnetic field and EMR of same magnitude for orientation, navigation and foraging (Venbergen et al., 2019). Sometimes for intraspecific and interspecific (plant-pollinator) communication, they also utilize EMR (Clarke et al., 2013;Greggers et al., 2013). But ultimately it could disturb the physiological functions even more in some cases affects its survival. ...
... Bumble bees have been known for their flower constancy and are able to forage up to 1-2 km from their colony with a ground speed of 54 km/h Walther-Hellwig and Frankl, 2000;Dramstad et al., 2003). Bumble bees are able to recognize the flowers recently visited by other bees through detection of electric field (Clarke et al., 2013) and identify flowers through temperature of flowers (Harrap et al., 2017). After recognition of flowers, the long tongue species inserted lapping tongue for collection of 1 2 nectar, whereas short tongue robbed nectar by biting corolla which does not help in pollination (Maloof, 2001). ...
... Bumble bees have been known for their flower constancy and are able to forage up to 1-2 km from their colony with a ground speed of 54 km/h Walther-Hellwig and Frankl, 2000;Dramstad et al., 2003). Bumble bees are able to recognize the flowers recently visited by other bees through detection of electric field (Clarke et al., 2013) and identify flowers through temperature of flowers (Harrap et al., 2017). After recognition of flowers, the long tongue species inserted lapping tongue for collection of 1 2 nectar, whereas short tongue robbed nectar by biting corolla which does not help in pollination (Maloof, 2001). ...
... The communication mechanisms within the system are still poorly understood, but the possibility of having electrical currents as a means of fast information transfer would provide a system akin to a central neuronal system that could result in a coordinated behaviour required in such a complex system as a soil. Electrical currents have been shown not only to be important for the coordination of cell behaviour at all biological levels, i.e. from bacteria to humans (Piccolino 1997;Brenner et al. 2006;Prindle et al. 2015;Canales, Henriquez-Valencia and Brauchi 2018), but also for intracolony or interspecies communication (Clarke et al. 2013;Beagle and Lockless 2015;Prindle et al. 2015). The cell morphology and growth mode of filamentous fungi provides, in theory, an ideal system for electrical signalling, but the use of traditional electrophysiological methods for measuring these signals is extremely challenging (Adamatzky 2022). ...
Full-text available
Fungi, with their enormous diversity, bear essential roles both in nature and our everyday lives. They inhabit a range of ecosystems, such as soil, where they are involved in organic matter degradation and bioremediation processes. More recently, fungi have been recognised as key components of the microbiome in other eukaryotes, such as humans, where they play a fundamental role not only in human pathogenesis, but also likely as commensals. In the food sector, fungi are used either directly or as fermenting agents and are often key players in the biotechnological industry, where they are responsible for the production of both bulk chemicals and antibiotics. Although the macroscopic fruiting bodies are immediately recognisable by most observers, the structure, function and interactions of fungi with other microbes at the microscopic scale still remain largely hidden. Herein, we shed light on new advances in the emerging field of Fungi-on-a-Chip microfluidic technologies for single-cell studies on fungi. We discuss the development and application of microfluidic tools in the fields of medicine and biotechnology, as well as in-depth biological studies having significance for ecology and general natural processes. Finally, a future perspective is provided, highlighting new frontiers in which microfluidic technology can benefit this field.
... Most plant-pollinator interactions involve the plant producing signals that manipulate the pollinator to bring it to the plant. These signals can work across many different sensory modalities, and may include color (Gumbert et al. 1999, Glover and Whitney 2010, Dyer et al. 2012, shape and pattern Papaj 2011, Lawson et al. 2017a), symmetry (Rodríguez et al. 2004, Krishna andKeasar 2018), scent (Miyake et al. 1998, Theis 2006, Raguso 2008, Lawson et al. 2018, temperature (Dyer et al. 2006, Whitney et al. 2008, Harrap et al. 2017, texture (Kevan and Lane 1985, Goyret and Raguso 2006, Whitney et al. 2009, Goyret 2010, electrostatic charge (Clarke et al. 2013(Clarke et al. , 2017. Recently, humidity has been suggested to be another sensory modality which could be used for signaling to pollinators. ...
Full-text available
Flowers produce local humidity that is often greater than that of the surrounding environment, and studies have shown that insect pollinators may be able to use this humidity difference to locate and identify suitable flowers. However, environmental humidity is highly heterogeneous, and is likely to affect the detectability of floral humidity, potentially constraining the contexts in which it can be used as a salient communication pathway between plants and their pollinators. In this study, we use differential conditioning techniques on bumblebees Bombus terrestris audax (Harris) to explore the detectability of an elevated floral humidity signal when presented against different levels of environmental noise. Artificial flowers were constructed that could be either dry or humid, and individual bumblebees were presented with consistent rewards in either the humid or dry flowers presented in an environment with four levels of constant humidity, ranging from low (~20% RH) to highly saturated (~95% RH). Ability to learn was dependent upon both the rewarding flower type and the environment: the bumblebees were able to learn rewarding dry flowers in all environments, but their ability to learn humid rewarding flowers was dependent on the environmental humidity, and they were unable to learn humid rewarding flowers when the environment was highly saturated. This suggests that floral humidity might be masked from bumblebees in humid environments, suggesting that it may be a more useful signal to insect pollinators in arid environments.
... Flowers send signals to particular type of pollinators that are facilitated by floral characteristics or traits known as "pollination syndrome" [37,38]. Flower traits such as shape, size, colour, scent production, electric fields and movement have been measured and recognized to play roles in the recognition and attraction of pollinators to flowers [39][40][41][42][43]. Pollinator especially bees and other insects are impressively influenced by shape, outline form, length of flowers, odour, colour, pollen, nectar and other flower rewards of flowers. ...
Plants are the basis of nearly all food chains. The evolutionary response to inevitable predatory and other contingent hazards has provided plants with remarkable regenerative and plastic capabilities. Teleonomy has been characterized as purposive, adaptive and goal-directed behaviour. The evidence that plants are agents, that they act purposefully, is indicated by numerous behaviours, most notably plasticity. Through recurrent information exchange, growing roots construct a dynamic niche with bacterial and fungal symbionts. Purposeful shoot plasticity enables adaptive responses to abiotic and biotic hazards, with the goal of survival. Transgenerational inheritance furthers that goal for sibling survival. Teleonomic goals in shoot growth use proprioception to ensure successful tropic responses. Unlike animals that acquire energy biotically, nearly all plants are dependent solely on the physical environment. Convergent evolution is common and may result from the constraints of unchanging physical laws. Phenotypic plasticity initially provides a direction for evolutionary change. Our article indicates that there are features to evolutionary change in plants additional to those indicated by the modern synthesis and thus supports the extended evolutionary hypothesis.
Full-text available
Flowers are multisensory displays used by plants to influence the behavior of pollinators. Although we know a great deal about how individual signal components are produced by plants and detected or learned by pollinators, very few experiments directly address the function of floral signal complexity, i.e. how the multicomponent nature of these signals benefits plant or pollinator. Yet, experimental psychology suggests that increasing complexity can enhance subjects' ability to detect, learn and remember stimuli, and the plant's reproductive success depends upon ensuring that pollinators learn their signals and so transport pollen to other similar (conspecific) flowers. Here we explore functional hypotheses for why plants invest in complex floral displays, focusing on hypotheses in which floral signals interact to promote pollinator learning and memory. Specifically, we discuss how an attention-altering or context-providing function of one signal may promote acquisition or recall of a second signal. Although we focus on communication between plants and pollinators, these process-based hypotheses should apply to any situation where a sender benefits from enhancing a receiver's acquisition or recall of information.
Full-text available
The measurements of Yes'kov & Sapozhnikov (1976) suggest that electrostatic potentials on foraging honeybees can reach hundreds of volts. Pollen grains of oilseed rape, Brassica napus L., subjected experimentally to potentials of this order, jumped a distance that increased approximately as the square of the voltage, between two pin electrodes on which, in some experiments, were impaled an anther or stigma of oilseed rape or a freshly-killed honeybee. Most floral surfaces were insulated, but there was a low-impedance path to earth via the stigma, and the electrostatic field due to an approaching charged bee must therefore concentrate there. Thus, if electrostatic potentials of this magnitude occur in nature they may increase the chance that pollen from bees will reach the stigma rather than other floral surfaces, as well as enabling pollen to jump from anther to bee and from bee to stigma across an air gap of the order of 0.5 mm.
Full-text available
We wished to understand the effects on pollinator behaviour of single mutations in plant genes controlling flower appearance. To this end, we analysed snapdragon flowers (Antirrhinum majus), including the mixta and nivea mutants, in controlled laboratory conditions using psychophysical tests with bumblebees. The MIXTA locus controls petal epidermal cell shape, and thus the path that incident light takes within the pigment-containing cells. The effect is that mixta mutant flowers are pink in comparison to the wild type purple flowers, and mutants lack the sparkling sheen of wild type flowers that is clearly visible to human observers. Despite their fundamentally different appearance to humans, and even though bees could discriminate the flowers, inexperienced bees exhibited no preference for either type, and the flowers did not differ in their detectability in a Y-maze—either when the flowers appeared in front of a homogeneous or a dappled background. Equally counterintuitive effects were found for the non-pigmented, UV reflecting nivea mutant: even though the overall reflectance intensity and UV signal of nivea flowers is several times that of wild type flowers, their detectability was significantly reduced relative to wild type flowers. In addition, naïve foragers preferred wild type flowers over nivea mutants, even though these generated a stronger signal in all receptor types. Our results show that single mutations affecting flower signal can have profound effects on pollinator behaviour—but not in ways predictable by crude assessments via human perception, nor simple quantification of UV signals. However, current models of bee visual perception predict the observed effects very well.
Full-text available
This paper reviews research on the role of electrostatic forces in pollination, both in natural and in agricultural systems. Researchers from various fields of biological studies have reported phenomena which they related to electrostatic forces. The theory of electrostatically mediated pollen transfer between insect pollinators and the flowers they visit is described, including recent studies which confirmed that the accumulated charges on airborne honey bees are sufficient for non-contact pollen detachment by electrostatic forces (i.e., electrostatic pollination). The most important morphological features in flower adaptiveness to electrostatic pollination were determined by means of two theoretical models of a flower exposed to an approaching charged cloud of pollen; they are style length and flower opening. Supplementary pollination by using electrostatic techniques is reported, and its possible importance in modern agriculture is discussed.
When Keith (1963) published his ‘Wildlife’s 10-year cycle’, available information on the theme was minimal. Many theories were no more than conjectures. In 1961, realizing that further theorizing would get him nowhere, Keith and a team of researchers from the Wisconsin school of wildlife ecology, launched a long-term field study on snowshoe hare (Lepus americanus) populations near Rochester, Alberta. A number of important papers from this study have appeared since then, including the monograph (Keith and Windberg, 1978) that provides a nearly complete 15-year set of demographic data. I shall call this work ‘the Rochester study’.
1. Many floral displays are visually complex, transmitting multi-coloured patterns that are thought to direct pollinators to nectar rewards. These ' nectar guides' may be mutually beneficial, if they reduce pollinators' handling time, leading to an increased visitation rate and promoting pollen transfer. Yet, many details regarding how floral patterns influence foraging efficiency are unknown, as is the potential for pollinator learning to alter this relationship. 2. We compared the responses of bumblebee (Bombus impatiens Cresson) foragers to artificial flowers that either possessed or lacked star-like patterns. By presenting each bee with two different foraging scenarios (patterned flowers rewarding/plain flowers unrewarding, plain flowers rewarding/patterned flowers unrewarding) on different days, we were able to assess both short-and long-term effects of patterns on bee foraging behaviour. 3. Bees discovered rewards more quickly on patterned flowers and were less likely to miss the reward, regardless of whether corollas were circular or had petals. Nectar guides' effect on nectar discovery was immediate (innate) and persisted even after experience, although nectar discovery itself also had a learned component. We also found that bees departed patterned flowers sooner after feeding. Finally, when conditions changed such that flowers no longer provided a reward, bees visited the now-unrewarding flowers more persistently when they were patterned. 4. On the time-scale of a single foraging bout, our results provide some of the first data on how pollinators learn to forage efficiently using this common floral trait. Our bees' persistent response to patterned flowers even after rewards ceased suggests that, rather than being consistently mutually beneficial to plant and pollinator, nectar guide patterns can at times promote pollen transfer for the plant at the expense of a bee's foraging success.
Bumblebees (Bombus spp.) and honeybees, Apis mellifera, both use odour cues deposited on flowers by previous visitors to improve their foraging efficiency. Short-lived repellent scents are used to avoid probing flowers that have recently been depleted of nectar and/or pollen, and longer-term attractant scents to indicate particularly rewarding flowers. Previous research has indicated that bumblebees avoid flowers recently visited by themselves, conspecifics and congeners, while honeybees avoid flowers visited by themselves or conspecifics only. We found that both bumblebees and honeybees also avoided flowers previously visited by each other when foraging on Melilotus officinalis, that is, bumblebees avoided flowers recently visited by honeybees and vice versa. Twenty-four hours after a visit, this effect had worn off. Honeybees visited flowers that had been visited 24h previously more often than flowers that had never been visited. The same was not true for bumblebees, suggesting that foraging honeybees were also using long-term attractant scent marks, whilst bumblebees were not. Flowers previously visited by conspecifics were repellent to bumblebees and honeybees for ca.40min. During this time, nectar replenished in flowers. Honeybees were previously thought to use a volatile chemical (2-heptanone) as a repellent forage-marking scent. We suggest that they may be using a less volatile chemical odour to detect whether flowers have recently been visited, possibly in addition to 2-heptanone.
Ontogenetic color changes in fully turgid flowers are widespread throughout the angiosperms, and in many cases are known to provide signals for pollinators. A broad survey of flowering plants demonstrates that such color changes appear in at least 77 diverse families. Color-changing taxa occur commonly within what are considered derived lineages, and only rarely in early or primitive groups. The pattern of distribution of floral color change across orders, families, genera, and species demonstrates that the occurrence of the phenomenon within a group is not simply a result of phylogenetic history. Color changes can affect the whole flower or they can be localized, affecting at least nine floral parts or regions. The scale of color change (localized or whole-flower) is broadly correlated with the type of pollinator that characteristically visits the plant. Color changes can come about through seven distinct physiological mechanisms, involving anthocyanins, carotenoids, and betalains. Color changes due to appearance of anthocyanin are the most common, occurring in 68 families. Floral color change has clearly evolved independently many times, most likely in response to selection by visually oriented pollinators, and reflects a widespread functional convergence within the angiosperms.
Various insects, especially social insects, possess electric charges. Erickson (1982, 1983) shows their involvement in the odor receptor efficiency of honey bee antenna. Also, the author suggests the importance of charges in the transfer of pollen grains from flowers to pollinator insects. To measure directly electric charges, we fit a sensor used to determine the charges of raindrops. Strongly clustered wintering bees and foraging bees were measured. The individual values range between −400pC to +600pC (m = 153 +/105pC) during winter time. The foraging bees possess variable charges, generally smaller than wintering bees (m = 29 +/− 40pC). 7.0% of measured bees whole are charged negatively and less than 1% of these have no charges. The presence of electric charges throughout bees yearly cycle is significant for the insect society. Moreover electric forces contribute to explain some aspects of bee-parasite relationships.