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Blackawton bees
P. S. Blackawton, S. Airzee, A. Allen, S. Baker, A. Berrow, C. Blair, M. Churchill, J. Coles, R. F.-J.
Cumming, L. Fraquelli, C. Hackford, A. Hinton Mellor, M. Hutchcroft, B. Ireland, D. Jewsbury, A.
Littlejohns, G. M. Littlejohns, M. Lotto, J. McKeown, A. O'Toole, H. Richards, L. Robbins-Davey, S.
Roblyn, H. Rodwell-Lynn, D. Schenck, J. Springer, A. Wishy, T. Rodwell-Lynn, D. Strudwick and R.
B. Lotto
Biol. Lett. 2011 7, 168-172 first published online 22 December 2010
doi: 10.1098/rsbl.2010.1056


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                                        Biol. Lett. (2011) 7, 168–172         inaccessible to the literate ability of 8- to
                                         doi:10.1098/rsbl.2010.1056           10-year-old children, and second, the true
                                  Published online 22 December 2010           motivation for any scientific study (at least one
    Animal behaviour                                                          of integrity) is one’s own curiousity, which for
                                                                              the children was not inspired by the scientific
                                                                              literature, but their own observations of the
Blackawton bees                                                               world. This lack of historical, scientific context
                                                                              does not diminish the resulting data, scientific
P. S. Blackawton1, S. Airzee1, A. Allen1, S. Baker1,                          methodology or merit of the discovery for the
                                                                              scientific and ‘non-scientific’ audience. On the
A. Berrow1, C. Blair1, M. Churchill1, J. Coles1, R. F.-
                                                                              contrary, it reveals science in its truest (most
J. Cumming1, L. Fraquelli1, C. Hackford1, A. Hinton                           naive) form, and in this way makes explicit the
Mellor1, M. Hutchcroft1, B. Ireland1, D. Jewsbury1,                           commonality between science, art and indeed
A. Littlejohns1, G. M. Littlejohns1, M. Lotto1,                               all creative activities.
J. McKeown1, A. O’Toole1, H. Richards1,                                       Principal finding: ‘We discovered that bumble-
L. Robbins-Davey1, S. Roblyn1, H. Rodwell-Lynn1,                              bees can use a combination of colour and spatial
D. Schenck1, J. Springer1, A. Wishy1,                                         relationships in deciding which colour of flower
                                                                              to forage from. We also discovered that science
T. Rodwell-Lynn1, D. Strudwick1 and R. B. Lotto2,*
1
                                                                              is cool and fun because you get to do stuff that
 Blackawton Primary School, Blackawton, Devon, UK                             no one has ever done before. (Children from
2
 Institute of Ophthalmology, University College London,                       Blackawton)’.
11-43 Bath Street, London EC1V 9EL, UK
*Author for correspondence (lotto@ucl.ac.uk).                                 Keywords: Bombus terrestris; buff-tailed bumble-bee;
Background: Real science has the potential to                                 visual perception; colour vision; behaviour
not only amaze, but also transform the way
one thinks of the world and oneself. This is
because the process of science is little different
from the deeply resonant, natural processes of                                1. INTRODUCTION
play. Play enables humans (and other mam-                                     (a) Once upon a time . . .
mals) to discover (and create) relationships                                  People think that humans are the smartest of animals,
and patterns. When one adds rules to play, a
game is created. This is science: the process of                              and most people do not think about other animals as
playing with rules that enables one to reveal                                 being smart, or at least think that they are not as
previously unseen patterns of relationships                                   smart as humans. Knowing that other animals are as
that extend our collective understanding of                                   smart as us means we can appreciate them more,
nature and human nature. When thought of in                                   which could also help us to help them.
this way, science education becomes a more                                        Scientists do experiments on monkeys, because they
enlightened and intuitive process of asking ques-                             are similar to man, but bees could actually be close to
tions and devising games to address those                                     man too. We see bees in the natural habitat doing what
questions. But, because the outcome of all                                    they do, but you do not really see them doing human
game-playing is unpredictable, supporting this                                things—such as solving human puzzles like Sudoku.
‘messyness’, which is the engine of science, is
                                                                              So it makes you wonder if they could solve a human
critical to good science education (and indeed
creative education generally). Indeed, we have                                puzzle. If they could solve it, it would mean that they
learned that doing ‘real’ science in public                                   are really smart, smarter than we thought before,
spaces can stimulate tremendous interest in                                   which would mean that humans might have some
children and adults in understanding the pro-                                 link with bees. If bees are like us in some way, then
cesses by which we make sense of the world.                                   understanding them could help us understand
The present study (on the vision of bumble-                                   ourselves better.
bees) goes even further, since it was not only                                    To get ready to do the experiments with the bees we
performed outside my laboratory (in a Norman                                  first talked about science being about playing games
church in the southwest of England), but the                                  and making puzzles. We then got into groups and
‘games’ were themselves devised in collabor-                                  made up games to play using random pieces of physical
ation with 25 8- to 10-year-old children. They
asked the questions, hypothesized the answers,                                education equipment. This gave us experience of
designed the games (in other words, the exper-                                thinking of games and puzzles. We then had to explain
iments) to test these hypotheses and analysed                                 our games to other people. After talking about what it
the data. They also drew the figures (in coloured                              is like to create games and how games have rules, we
pencil) and wrote the paper. Their headteacher                                talked about seeing the world in different ways by
(Dave Strudwick) and I devised the educational                                wearing bug eyes, mirrors and rolled-up books. We
programme (we call ‘i,scientist’), and I trained                              then watched the David Letterman videos of ‘Stupid
the bees and transcribed the childrens’ words                                 Dog Tricks’, in which dogs were trained to do funny
into text (which was done with smaller groups                                 things. Next, we too had to learn to solve a puzzle
of children at the school’s local village pub). So                            that Beau (a neuroscientist) and Mr Strudwick (our
what follows is a novel study (scientifically and
                                                                              headteacher) gave us (which took an artificial brain
conceptually) in ‘kids speak’ without references
to past literature, which is a challenge. Although                            10 000 trials to solve, but only four for us). Afterwards,
the historical context of any study is of course                              we started asking questions about bees, and then more
important, including references in this instance                              specific questions about seeing colour using the bee
would be disingenuous for two reasons. First,                                 arena (figure 1).
given the way scientific data are naturally                                        We came up with lots of questions, but the one we
reported, the relevant information is simply                                  decided to look at was whether bees could learn to
Received 8 November 2010
Accepted 30 November 2010                                               168                        This journal is q 2010 The Royal Society
Downloaded from rsbl.royalsocietypublishing.org on December 25, 2012


                                                  Colour and spatial relationships in bees          P. S. Blackawton et al.          169

     (a)                                                          to remember the flowers that were around it, which
                                                                  is like a puzzle.
                                                                      To test this we gave the bees a series of challenges to
                                                                  see if they could complete them or not, and then tested
                                                                  them to see if they solved the puzzle and how they
                                                                  solved it. It was a difficult puzzle, because the bees
                                                                  could not just learn to go to the colour of the flower.
                                                                  Instead, they had to learn to go to one colour (blue)
                                                                  if it was surrounded by the opposite colour (yellow),
                                                                  but also to go to the opposite colour (yellow) if it
                                                                  was surrounded by blue. We also wanted to know if
                                                                  all the bees solved the puzzle in the same way. If not,
                                                                  it would mean that bees have personality (if a bee
                                                                  goes to the blue flower every time, it tells us that it
                                                                  really likes blue).


                                                                  2. MATERIAL AND METHODS
     (b)                                                          (a) The bee arena
                                                                  The bee arena, which was made out of Plexiglas, had six sides. The
                                                                  arena was 1 m high, 1 m wide and 1 m deep, and two of the side
                                                                  panels had three doors each. It had a vertical lightbox at the end
                                                                  opposite the side through which the bees entered by a small hole.
                                                                  The lightbox was made out of aluminium, with a Plexiglas screen
                                                                  in front of the six fluorescent lights. An aluminium cross was
                                                                  placed in front of the Plexiglas screen, and this cross had grooves
                                                                  in its sides so that we could slide four black aluminium panels into
                                                                  the cross. Each panel had 16 cut-out circular holes in four rows of
                                                                  four circles each. Each circle was 8 cm in diameter. The holes were
                                                                  covered by the Plexiglas screen. In the centre of each circle was a
                                                                  Plexiglas rod with a small hole in the middle in which we put
                                                                  sugar water, salt water or nothing. Behind each hole there were
                                                                  slits so that squares of coloured gel filters could be slotted in,
                                                                  making the light shining through each hole coloured. It was like put-
                                                                  ting a piece of coloured see-through paper on a light to let the colour
                                                                  of the paper shine through.

                                                                  (b) The bees
                                                                  The bees had black and yellow stripes with white bottoms. The
                                                                  type of bee was Bombus terrestris. The beehive was delivered from
     (c)                                                          Koppert (UK).

                                                                  (c) Training phase 1
                                                                  To teach the bees to go to the Plexiglas rods as if they were flowers, all
                                                                  the circles in every panel were kept white, and all the rods had sugar
                                                                  water in them. Once the labelled foragers learned that the flowers
                                                                  contained a reward, which took four days, we marked the bees,
                                                                  and then set up the puzzle.

                                                                  (d) Marking bees
                                                                  We let the foragers into the arena and turned the lights off, which
                                                                  made the bees stop flying (because they do not want to fly into any-
                                                                  thing). We picked the bees up with bee tweezers and put them into a
                                                                  pot with a lid. We then put the tube with the bees in it into the
                                                                  school’s fridge (and made bee pie ). The bees fell asleep. Once
                                                                  they fell asleep, we took the bees out, one at a time, and painted
                                                                  little dots on them (yellow, blue, orange, blue-orange, blue-yellow,
Figure 1. Conditions and responses to ‘test 1’ (control).         etc.). We put them into the tube and warmed them up and then
(a) The pattern of colours that the bees were trained to          let them into the arena. No bees were harmed during this procedure.
and tested on in their first test (see text for explanation).
(b) The selections made by all the bees tested (dots show         (e) Training phase 2 (‘the puzzle’ . . .duh duh duuuuhhh)
where each bee landed and tried to get sugar water). (c) A        We set up a puzzle for the bees as in the following. Imagine having a
table showing the preferences of each bee during testing          panel with 16 circles, with a large square of 12 yellow circles on the
                                                                  outside and a small square of four blue circles in the middle. This
(see text for explanation).                                       was the case for two panels, but the other two panels were the oppo-
                                                                  site, and instead of yellow on the outside as the larger square and
                                                                  blue on the inside as the smaller square, we had blue on the outside
use the spatial relationships between colours to figure            and yellow on the inside. The sugar reward (1 : 1 with water) was
out which flowers had sugar water in them and                      only in the middle four flowers inside each panel of 16 flowers.
                                                                  Every 10 –40 min, we swapped the locations of the panels around
which had salt water in them. It is interesting to ask            the different quadrants so that the bees could not learn the locations
this question, because in their habitat there may be              of the rewarding flowers. We also cleaned the Plexiglas stems so that
flowers that are bad for them, or flowers from which                the bees could not use scent to tell the other bees that flower had the
they might already have collected nectar. This would              reward. Instead they had to learn: if there was blue on the outside
                                                                  ring of each panel of 16 circles, then they had to go to the inner
mean that it is important for bees to learn which                 four yellow circles. If, however, there was yellow on the outside
flower to go to or to avoid, which would need them                 ring, then they had to go to the inner four blue circles. During the

Biol. Lett. (2011)
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170 P. S. Blackawton et al. Colour and spatial relationships in bees

first 2 days of training, sugar water was placed only in the four middle       (a)
flowers in each panel and nothing in the outside ring (so that they
would get the hang of it). During the second 2 days we added salt
water to the flowers in the outside rings. We did this so that they
would learn not to go just to the colours, but had to learn the pattern.
Otherwise they might fail the test, and it would be a disaster. After
training, we tested the bees to see if they solved the puzzle.

(f) Testing the bees
We tested the bees using the same pattern of colours, but without
sugar water or salt water, to see which flowers they would go to.
We also moved the locations of the panels so that the layout was
different from when they were just trained. We let the labelled for-
agers into the arena one at a time so that they would not copy
each other (as humans might). We tracked their flower choices
using a sheet of paper with the 64 circles marked into the four quad-
rants. Whenever the bees landed on a flower and stuck their tongue
(proboscis) into the Plexiglas rod, we would mark the matching circle
on the sheet. We marked each circle with a ‘1’, a ‘2’ or a ‘3’ and so
on, to track where they went to see how their behaviour might have
changed with time. After a while, the bees might have got annoyed
because they were not getting a reward, and might have started
making mistakes or searching randomly. So we let each forager
make only around 30 choices before stopping the test. Each bee                (b)
was tested three times (see §3).



3. RESULTS
After training the bees in the arena, we tested them
three times to see if they had learned anything during
training.

(a) Test 1 (the control)
In the first test the bees were given the same pattern we
had trained them with. After training, we moved the
colours of the panels clockwise once, so that the col-
ours of the quadrants would be different for the bees,
and they could not just go to the same place as last
time to get a reward (see figure 1a for a hand drawing                      Figure 2. Conditions and responses to ‘test 2’. (a) The pat-
of the test). If the bees had solved the puzzle, they                      tern of colours that the bees were tested on in their second
should land on the flowers in the middle of each quad-                      test (see text for explanation). (b) A table showing the prefer-
rant and stick their tongues (proboscis) in the flower,                     ences of each bee during test 2 (see text for explanation).
as during training this is how they would have had a
reward (during the test, they did not get a reward).
   Figure 1b shows where four of the bees went during                      went to 31 correct yellow flowers and four incorrect
the test (unfortunately, one of the bees (called ‘yellow’)                 yellow flowers, and never went to blue flowers. The
did not come out of the hive during this test). Each dot                   ‘Blue’ (B) bee went to 33 correct yellow flowers and
in figure 1b is an attempted forage. The figure shows                        only three incorrect yellow flowers, and selected the
that the bees went to the middle flowers 126 times,                         correct blue flowers only once. These results are
and to the outside flowers in the four quadrants a                          shown in figure 1c. We conclude that one bee went
total of 13 times (see ‘total’ in figure 1c). So, out of                    to a mixture of colours in the correct locations, but
139 attempted forages, 90.6 per cent were to correct                       the rest preferred one colour over the other. However,
flowers (correct means flowers that would have had                           although they preferred one colour, they only went to
sugar water during training).                                              the middle of the panel that had that colour (as this
   Figure 1c shows how many times each individual bee                      is the flower that would have had a reward). This test
went to correct and incorrect blue and yellow flowers.                      shows that altogether the bees solved the puzzle very
We did this so that it would be clearer to see where                       well, as their choices collectively were divided between
each bee went during the test. ‘Orange’ (O) bee                            all blue and yellow rewarding flowers. We then pre-
selected seven correct (middle) yellows and only one                       sented the bees with two more tests to see how they
incorrect (outside) yellow. She also went to 29 correct                    solved the puzzle they were trained for.
blue and only one incorrect blue. This bee prefers blue
in the middle, but also prefers yellow in the middle.                      (b) Test 2 (the first experiment)
This bee did extremely well, because it went to                            Test 2 was very similar to test 1, except that the middle
both colours at correct locations in the flowers.                           flowers in each quadrant were green. We did this to see
‘Blue/yellow’ (B/Y) bee went to neither outside                            whether the bees learned to go to the colours or to the
yellow flowers nor middle yellow flowers. Instead it                         location of the rewarding flowers during training. If the
went to 25 correct blue flowers (middle) and only                           bees learned to go to the location of the rewarding
four incorrect blue flowers (outside). So this bee pre-                     flowers, then they should land on the green flowers in
ferred blue to yellow. The ‘Blue/Orange’ (B/O) bee                         test 2. See figure 2a for a hand drawing of this test.
Biol. Lett. (2011)
Downloaded from rsbl.royalsocietypublishing.org on December 25, 2012


                                                     Colour and spatial relationships in bees       P. S. Blackawton et al.   171

   (a)                                                              flowers. If the bees had learned to go to flowers that
                                                                    were fewest in each panel, then they should go to the
                                                                    flowers in the corners.
                                                                       The table in figure 3b shows where all five bees went
                                                                    during the test. You can see that the bees as a group
                                                                    went to the corner flowers 59 times, and to the ‘not-
                                                                    corners’ 86 times (see ‘total’ in figure 3b). So, out of
                                                                    145 attempted forages, 40.1 per cent were to the
                                                                    corners. This is very different from what they did in
                                                                    test 1. When the same flowers were not in the corners
                                                                    but in the middle as in test 1, they selected them 90.6
                                                                    per cent of the time, which is 2.2 times more often. We
                                                                    think that the bees in test 3 selected the flowers randomly,
                                                                    and conclude that the bees did not learn to go to the flow-
                                                                    ers that had the fewest colours in each panel. Also, this
                                                                    time, the B and B/O bees did not prefer the middle flow-
                                                                    ers in each panel. This means that in test 2 they must have
                                                                    used the larger square of blue and yellow flowers to decide
                                                                    to forage from the middle green flowers.
   (b)

                                                                    4. DISCUSSION
                                                                    This experiment is important, because, as far as we
                                                                    know, no one in history (including adults) has done
                                                                    this experiment before. It tells us that bees can learn
                                                                    to solve puzzles (and if we are lucky we will be able
                                                                    to get them to do Sudoku in a couple of years’ time).
                                                                    In this experiment, we trained bees to solve a particular
                                                                    puzzle. The puzzle was go to blue if surrounded by
                                                                    yellow, but yellow if surrounded by blue.
                                                                        Test 1 showed that the bees learned to solve this
                                                                    puzzle. We know this because the test results showed
Figure 3. Conditions and responses to ‘test 3’. (a) The pattern     that they mostly went to the flowers that they were sup-
of colours that the bees were tested on in their third test (see    posed to go to, because those were the ones that had
text for explanation). (b) A table showing the preferences of       contained a sugar reward before. However, we also
each bee during test 3 (see text for explanation).                  noticed that the bees solved the puzzle in different
                                                                    ways, and that some were more clever than others.
                                                                    Two bees preferred yellow and two others preferred
   Figure 2b shows a table of the choices made by the               blue flowers. The B bee was best at understanding
bees during this test. In total, the bees went to the               the pattern in the first test, because it had the most cor-
green middle flowers only 34 times, and to the outside               rect answers compared to incorrect answers. It also
blue and yellow flowers 76 times (see total in                       went both to correct yellow and correct blue flowers,
figure 2b). So, out of 110 attempted forages, 30.9 per               although it preferred the blue flowers.
cent were to the middle flowers. If the bees were gues-                  What is important about this puzzle is that there is
sing, they should have selected the green flowers 25 per             more than one strategy the bees could use to solve it.
cent of the time, which is very close to 30 per cent. So            One strategy would be to use two rules: (i) go to the
we conclude that the bees did not solve test 1 by only              middle four flowers in each panel, and (ii) ignore the
going to the middle flowers of each quadrant (‘dah                   colour. Another strategy would be to go to yellow if
dahhh dahhhhhh’). However, two of the bees (labelled                surrounded by blue or blue if surrounded by yellow.
B/O and B) went most often to the green, middle                     They could also learn to avoid the surrounding flowers,
flowers. So they seemed to have learned a different                  and as a result only go to the middle flowers. Or they
rule to the other three bees.                                       could go to the fewest number of coloured flowers
                                                                    in each panel. Of course they could also have chosen
(c) Test 3 (the second experiment)                                  randomly, and they might get them right or they
In the third test, instead of having large squares of               might get them wrong. Or they could have just gone
yellow and blue around the outside of each panel,                   to a colour, but then they would not have solved the
and a smaller square of yellow and blue on the inside               whole puzzle, only half of it.
of each panel, we took the four inside flowers and                       Test 2 tested whether the bees had learned to go to
put them in the corners of each panel. See figure 3a                 the middle of each panel and ignored the colour. If this
for a hand drawing of what this test looked like. We                was true then they should have gone to the green flow-
did this because we wanted to see if the bees solved                ers. If they had learned to go to only middle blue and
test 1 by learning during training to go to the colours             yellow flowers, then they should have gone either to the
of each panel that were fewest in number. We could                  surrounding blue and yellow flowers or no flowers at
also see if they still preferred to go only to the middle           all. The results tell us that three of the bees preferred
Biol. Lett. (2011)
Downloaded from rsbl.royalsocietypublishing.org on December 25, 2012


172 P. S. Blackawton et al. Colour and spatial relationships in bees

to go to the colours that they had learned before, and              Before doing these experiments we did not really
avoided the middle green flowers. Two of the bees,                think a lot about bees and how they are as smart as
however, mainly went to the middle flowers, including             us. We also did not think about the fact that without
the B bee, which went to both correct yellow and cor-            bees we would not survive, because bees keep the flow-
rect blue flowers during the first (control) test. So they         ers going. So it is important to understand bees. We
had learned to solve the puzzle using different rules.           discovered how fun it was to train bees. This is also
Test 3 also showed that one of the rules was not just            cool because you do not get to train bees everyday. We
to go to any middle flower, as they rarely went to the            like bees. Science is cool and fun because you get to do
middle flowers, or to go to the flowers that had the               stuff that no one has ever done before. (Bees—seem
fewest colours in each panel, because they did not               to—think!)
prefer the corner flowers. Instead, they seemed to
select the flowers at random, but funnily continued               We thank the whole of the Blackawton community, who truly
to go to their ‘favourite’ colour.                               engaged with the science research, including the George
   We conclude that bees can solve puzzles by learning           Inn—where the manuscript was written—for the free Cokes
complex rules, but sometimes they make mistakes.                 for the children (and pints for others). We thank the local
They can also work together (indirectly) to solve a              parish for the use of the Norman church, where the
                                                                 experiments were run, and the parents for letting their
puzzle. Which means that bees have personality and               children ‘work’ outside ‘normal’ school hours. Of course
have their personal ‘likings’. We also learned that the          none of this would have happened without the innovative
bees could use the ‘shape’ of the different patterns of indi-    and enthusiastic support of the teachers of Blackawton. We
vidual flowers to decide which flowers to go to. So they are       are also indebted to Larry Maloney and Natalie Hempel de
quite clever, because they can memorize a pattern. This          Ibarra for their openness to possibility and time, effort and
might help them get more pollen from flowers by learning          detail in writing the commentary, as well as Dale Purves,
which flowers might be best for them without wasting              Lars Chittka, Read Montague, Karl Friston and Geoff
                                                                 North (Current Biology) for their sage advice. Finally, we
energy. In real life this might mean that they collect infor-    thank Chris Frith and Brian Charlesworth for their open-
mation and remember that information when going into             mindedness. The project was funded privately by Lottolab
different fields. So if some plants die out, they can learn to    Studio, as the referees argued that young people cannot do
find nectar in another type of flower.                             real science.




Biol. Lett. (2011)

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2010 - Projeto Abelhas de Blackawton

  • 1. Downloaded from rsbl.royalsocietypublishing.org on December 25, 2012 Blackawton bees P. S. Blackawton, S. Airzee, A. Allen, S. Baker, A. Berrow, C. Blair, M. Churchill, J. Coles, R. F.-J. Cumming, L. Fraquelli, C. Hackford, A. Hinton Mellor, M. Hutchcroft, B. Ireland, D. Jewsbury, A. Littlejohns, G. M. Littlejohns, M. Lotto, J. McKeown, A. O'Toole, H. Richards, L. Robbins-Davey, S. Roblyn, H. Rodwell-Lynn, D. Schenck, J. Springer, A. Wishy, T. Rodwell-Lynn, D. Strudwick and R. B. Lotto Biol. Lett. 2011 7, 168-172 first published online 22 December 2010 doi: 10.1098/rsbl.2010.1056 Supplementary data "Video Podcast" http://rsbl.royalsocietypublishing.org/content/suppl/2010/12/21/rsbl.2010.1056.DC1.ht ml References Article cited in: http://rsbl.royalsocietypublishing.org/content/7/2/168.full.html#related-urls Subject collections Articles on similar topics can be found in the following collections behaviour (567 articles) cognition (116 articles) Email alerting service Receive free email alerts when new articles cite this article - sign up in the box at the top right-hand corner of the article or click here To subscribe to Biol. Lett. go to: http://rsbl.royalsocietypublishing.org/subscriptions
  • 2. Downloaded from rsbl.royalsocietypublishing.org on December 25, 2012 Biol. Lett. (2011) 7, 168–172 inaccessible to the literate ability of 8- to doi:10.1098/rsbl.2010.1056 10-year-old children, and second, the true Published online 22 December 2010 motivation for any scientific study (at least one Animal behaviour of integrity) is one’s own curiousity, which for the children was not inspired by the scientific literature, but their own observations of the Blackawton bees world. This lack of historical, scientific context does not diminish the resulting data, scientific P. S. Blackawton1, S. Airzee1, A. Allen1, S. Baker1, methodology or merit of the discovery for the scientific and ‘non-scientific’ audience. On the A. Berrow1, C. Blair1, M. Churchill1, J. Coles1, R. F.- contrary, it reveals science in its truest (most J. Cumming1, L. Fraquelli1, C. Hackford1, A. Hinton naive) form, and in this way makes explicit the Mellor1, M. Hutchcroft1, B. Ireland1, D. Jewsbury1, commonality between science, art and indeed A. Littlejohns1, G. M. Littlejohns1, M. Lotto1, all creative activities. J. McKeown1, A. O’Toole1, H. Richards1, Principal finding: ‘We discovered that bumble- L. Robbins-Davey1, S. Roblyn1, H. Rodwell-Lynn1, bees can use a combination of colour and spatial D. Schenck1, J. Springer1, A. Wishy1, relationships in deciding which colour of flower to forage from. We also discovered that science T. Rodwell-Lynn1, D. Strudwick1 and R. B. Lotto2,* 1 is cool and fun because you get to do stuff that Blackawton Primary School, Blackawton, Devon, UK no one has ever done before. (Children from 2 Institute of Ophthalmology, University College London, Blackawton)’. 11-43 Bath Street, London EC1V 9EL, UK *Author for correspondence (lotto@ucl.ac.uk). Keywords: Bombus terrestris; buff-tailed bumble-bee; Background: Real science has the potential to visual perception; colour vision; behaviour not only amaze, but also transform the way one thinks of the world and oneself. This is because the process of science is little different from the deeply resonant, natural processes of 1. INTRODUCTION play. Play enables humans (and other mam- (a) Once upon a time . . . mals) to discover (and create) relationships People think that humans are the smartest of animals, and patterns. When one adds rules to play, a game is created. This is science: the process of and most people do not think about other animals as playing with rules that enables one to reveal being smart, or at least think that they are not as previously unseen patterns of relationships smart as humans. Knowing that other animals are as that extend our collective understanding of smart as us means we can appreciate them more, nature and human nature. When thought of in which could also help us to help them. this way, science education becomes a more Scientists do experiments on monkeys, because they enlightened and intuitive process of asking ques- are similar to man, but bees could actually be close to tions and devising games to address those man too. We see bees in the natural habitat doing what questions. But, because the outcome of all they do, but you do not really see them doing human game-playing is unpredictable, supporting this things—such as solving human puzzles like Sudoku. ‘messyness’, which is the engine of science, is So it makes you wonder if they could solve a human critical to good science education (and indeed creative education generally). Indeed, we have puzzle. If they could solve it, it would mean that they learned that doing ‘real’ science in public are really smart, smarter than we thought before, spaces can stimulate tremendous interest in which would mean that humans might have some children and adults in understanding the pro- link with bees. If bees are like us in some way, then cesses by which we make sense of the world. understanding them could help us understand The present study (on the vision of bumble- ourselves better. bees) goes even further, since it was not only To get ready to do the experiments with the bees we performed outside my laboratory (in a Norman first talked about science being about playing games church in the southwest of England), but the and making puzzles. We then got into groups and ‘games’ were themselves devised in collabor- made up games to play using random pieces of physical ation with 25 8- to 10-year-old children. They asked the questions, hypothesized the answers, education equipment. This gave us experience of designed the games (in other words, the exper- thinking of games and puzzles. We then had to explain iments) to test these hypotheses and analysed our games to other people. After talking about what it the data. They also drew the figures (in coloured is like to create games and how games have rules, we pencil) and wrote the paper. Their headteacher talked about seeing the world in different ways by (Dave Strudwick) and I devised the educational wearing bug eyes, mirrors and rolled-up books. We programme (we call ‘i,scientist’), and I trained then watched the David Letterman videos of ‘Stupid the bees and transcribed the childrens’ words Dog Tricks’, in which dogs were trained to do funny into text (which was done with smaller groups things. Next, we too had to learn to solve a puzzle of children at the school’s local village pub). So that Beau (a neuroscientist) and Mr Strudwick (our what follows is a novel study (scientifically and headteacher) gave us (which took an artificial brain conceptually) in ‘kids speak’ without references to past literature, which is a challenge. Although 10 000 trials to solve, but only four for us). Afterwards, the historical context of any study is of course we started asking questions about bees, and then more important, including references in this instance specific questions about seeing colour using the bee would be disingenuous for two reasons. First, arena (figure 1). given the way scientific data are naturally We came up with lots of questions, but the one we reported, the relevant information is simply decided to look at was whether bees could learn to Received 8 November 2010 Accepted 30 November 2010 168 This journal is q 2010 The Royal Society
  • 3. Downloaded from rsbl.royalsocietypublishing.org on December 25, 2012 Colour and spatial relationships in bees P. S. Blackawton et al. 169 (a) to remember the flowers that were around it, which is like a puzzle. To test this we gave the bees a series of challenges to see if they could complete them or not, and then tested them to see if they solved the puzzle and how they solved it. It was a difficult puzzle, because the bees could not just learn to go to the colour of the flower. Instead, they had to learn to go to one colour (blue) if it was surrounded by the opposite colour (yellow), but also to go to the opposite colour (yellow) if it was surrounded by blue. We also wanted to know if all the bees solved the puzzle in the same way. If not, it would mean that bees have personality (if a bee goes to the blue flower every time, it tells us that it really likes blue). 2. MATERIAL AND METHODS (b) (a) The bee arena The bee arena, which was made out of Plexiglas, had six sides. The arena was 1 m high, 1 m wide and 1 m deep, and two of the side panels had three doors each. It had a vertical lightbox at the end opposite the side through which the bees entered by a small hole. The lightbox was made out of aluminium, with a Plexiglas screen in front of the six fluorescent lights. An aluminium cross was placed in front of the Plexiglas screen, and this cross had grooves in its sides so that we could slide four black aluminium panels into the cross. Each panel had 16 cut-out circular holes in four rows of four circles each. Each circle was 8 cm in diameter. The holes were covered by the Plexiglas screen. In the centre of each circle was a Plexiglas rod with a small hole in the middle in which we put sugar water, salt water or nothing. Behind each hole there were slits so that squares of coloured gel filters could be slotted in, making the light shining through each hole coloured. It was like put- ting a piece of coloured see-through paper on a light to let the colour of the paper shine through. (b) The bees The bees had black and yellow stripes with white bottoms. The type of bee was Bombus terrestris. The beehive was delivered from (c) Koppert (UK). (c) Training phase 1 To teach the bees to go to the Plexiglas rods as if they were flowers, all the circles in every panel were kept white, and all the rods had sugar water in them. Once the labelled foragers learned that the flowers contained a reward, which took four days, we marked the bees, and then set up the puzzle. (d) Marking bees We let the foragers into the arena and turned the lights off, which made the bees stop flying (because they do not want to fly into any- thing). We picked the bees up with bee tweezers and put them into a pot with a lid. We then put the tube with the bees in it into the school’s fridge (and made bee pie ). The bees fell asleep. Once they fell asleep, we took the bees out, one at a time, and painted little dots on them (yellow, blue, orange, blue-orange, blue-yellow, Figure 1. Conditions and responses to ‘test 1’ (control). etc.). We put them into the tube and warmed them up and then (a) The pattern of colours that the bees were trained to let them into the arena. No bees were harmed during this procedure. and tested on in their first test (see text for explanation). (b) The selections made by all the bees tested (dots show (e) Training phase 2 (‘the puzzle’ . . .duh duh duuuuhhh) where each bee landed and tried to get sugar water). (c) A We set up a puzzle for the bees as in the following. Imagine having a table showing the preferences of each bee during testing panel with 16 circles, with a large square of 12 yellow circles on the outside and a small square of four blue circles in the middle. This (see text for explanation). was the case for two panels, but the other two panels were the oppo- site, and instead of yellow on the outside as the larger square and blue on the inside as the smaller square, we had blue on the outside use the spatial relationships between colours to figure and yellow on the inside. The sugar reward (1 : 1 with water) was out which flowers had sugar water in them and only in the middle four flowers inside each panel of 16 flowers. Every 10 –40 min, we swapped the locations of the panels around which had salt water in them. It is interesting to ask the different quadrants so that the bees could not learn the locations this question, because in their habitat there may be of the rewarding flowers. We also cleaned the Plexiglas stems so that flowers that are bad for them, or flowers from which the bees could not use scent to tell the other bees that flower had the they might already have collected nectar. This would reward. Instead they had to learn: if there was blue on the outside ring of each panel of 16 circles, then they had to go to the inner mean that it is important for bees to learn which four yellow circles. If, however, there was yellow on the outside flower to go to or to avoid, which would need them ring, then they had to go to the inner four blue circles. During the Biol. Lett. (2011)
  • 4. Downloaded from rsbl.royalsocietypublishing.org on December 25, 2012 170 P. S. Blackawton et al. Colour and spatial relationships in bees first 2 days of training, sugar water was placed only in the four middle (a) flowers in each panel and nothing in the outside ring (so that they would get the hang of it). During the second 2 days we added salt water to the flowers in the outside rings. We did this so that they would learn not to go just to the colours, but had to learn the pattern. Otherwise they might fail the test, and it would be a disaster. After training, we tested the bees to see if they solved the puzzle. (f) Testing the bees We tested the bees using the same pattern of colours, but without sugar water or salt water, to see which flowers they would go to. We also moved the locations of the panels so that the layout was different from when they were just trained. We let the labelled for- agers into the arena one at a time so that they would not copy each other (as humans might). We tracked their flower choices using a sheet of paper with the 64 circles marked into the four quad- rants. Whenever the bees landed on a flower and stuck their tongue (proboscis) into the Plexiglas rod, we would mark the matching circle on the sheet. We marked each circle with a ‘1’, a ‘2’ or a ‘3’ and so on, to track where they went to see how their behaviour might have changed with time. After a while, the bees might have got annoyed because they were not getting a reward, and might have started making mistakes or searching randomly. So we let each forager make only around 30 choices before stopping the test. Each bee (b) was tested three times (see §3). 3. RESULTS After training the bees in the arena, we tested them three times to see if they had learned anything during training. (a) Test 1 (the control) In the first test the bees were given the same pattern we had trained them with. After training, we moved the colours of the panels clockwise once, so that the col- ours of the quadrants would be different for the bees, and they could not just go to the same place as last time to get a reward (see figure 1a for a hand drawing Figure 2. Conditions and responses to ‘test 2’. (a) The pat- of the test). If the bees had solved the puzzle, they tern of colours that the bees were tested on in their second should land on the flowers in the middle of each quad- test (see text for explanation). (b) A table showing the prefer- rant and stick their tongues (proboscis) in the flower, ences of each bee during test 2 (see text for explanation). as during training this is how they would have had a reward (during the test, they did not get a reward). Figure 1b shows where four of the bees went during went to 31 correct yellow flowers and four incorrect the test (unfortunately, one of the bees (called ‘yellow’) yellow flowers, and never went to blue flowers. The did not come out of the hive during this test). Each dot ‘Blue’ (B) bee went to 33 correct yellow flowers and in figure 1b is an attempted forage. The figure shows only three incorrect yellow flowers, and selected the that the bees went to the middle flowers 126 times, correct blue flowers only once. These results are and to the outside flowers in the four quadrants a shown in figure 1c. We conclude that one bee went total of 13 times (see ‘total’ in figure 1c). So, out of to a mixture of colours in the correct locations, but 139 attempted forages, 90.6 per cent were to correct the rest preferred one colour over the other. However, flowers (correct means flowers that would have had although they preferred one colour, they only went to sugar water during training). the middle of the panel that had that colour (as this Figure 1c shows how many times each individual bee is the flower that would have had a reward). This test went to correct and incorrect blue and yellow flowers. shows that altogether the bees solved the puzzle very We did this so that it would be clearer to see where well, as their choices collectively were divided between each bee went during the test. ‘Orange’ (O) bee all blue and yellow rewarding flowers. We then pre- selected seven correct (middle) yellows and only one sented the bees with two more tests to see how they incorrect (outside) yellow. She also went to 29 correct solved the puzzle they were trained for. blue and only one incorrect blue. This bee prefers blue in the middle, but also prefers yellow in the middle. (b) Test 2 (the first experiment) This bee did extremely well, because it went to Test 2 was very similar to test 1, except that the middle both colours at correct locations in the flowers. flowers in each quadrant were green. We did this to see ‘Blue/yellow’ (B/Y) bee went to neither outside whether the bees learned to go to the colours or to the yellow flowers nor middle yellow flowers. Instead it location of the rewarding flowers during training. If the went to 25 correct blue flowers (middle) and only bees learned to go to the location of the rewarding four incorrect blue flowers (outside). So this bee pre- flowers, then they should land on the green flowers in ferred blue to yellow. The ‘Blue/Orange’ (B/O) bee test 2. See figure 2a for a hand drawing of this test. Biol. Lett. (2011)
  • 5. Downloaded from rsbl.royalsocietypublishing.org on December 25, 2012 Colour and spatial relationships in bees P. S. Blackawton et al. 171 (a) flowers. If the bees had learned to go to flowers that were fewest in each panel, then they should go to the flowers in the corners. The table in figure 3b shows where all five bees went during the test. You can see that the bees as a group went to the corner flowers 59 times, and to the ‘not- corners’ 86 times (see ‘total’ in figure 3b). So, out of 145 attempted forages, 40.1 per cent were to the corners. This is very different from what they did in test 1. When the same flowers were not in the corners but in the middle as in test 1, they selected them 90.6 per cent of the time, which is 2.2 times more often. We think that the bees in test 3 selected the flowers randomly, and conclude that the bees did not learn to go to the flow- ers that had the fewest colours in each panel. Also, this time, the B and B/O bees did not prefer the middle flow- ers in each panel. This means that in test 2 they must have used the larger square of blue and yellow flowers to decide to forage from the middle green flowers. (b) 4. DISCUSSION This experiment is important, because, as far as we know, no one in history (including adults) has done this experiment before. It tells us that bees can learn to solve puzzles (and if we are lucky we will be able to get them to do Sudoku in a couple of years’ time). In this experiment, we trained bees to solve a particular puzzle. The puzzle was go to blue if surrounded by yellow, but yellow if surrounded by blue. Test 1 showed that the bees learned to solve this puzzle. We know this because the test results showed Figure 3. Conditions and responses to ‘test 3’. (a) The pattern that they mostly went to the flowers that they were sup- of colours that the bees were tested on in their third test (see posed to go to, because those were the ones that had text for explanation). (b) A table showing the preferences of contained a sugar reward before. However, we also each bee during test 3 (see text for explanation). noticed that the bees solved the puzzle in different ways, and that some were more clever than others. Two bees preferred yellow and two others preferred Figure 2b shows a table of the choices made by the blue flowers. The B bee was best at understanding bees during this test. In total, the bees went to the the pattern in the first test, because it had the most cor- green middle flowers only 34 times, and to the outside rect answers compared to incorrect answers. It also blue and yellow flowers 76 times (see total in went both to correct yellow and correct blue flowers, figure 2b). So, out of 110 attempted forages, 30.9 per although it preferred the blue flowers. cent were to the middle flowers. If the bees were gues- What is important about this puzzle is that there is sing, they should have selected the green flowers 25 per more than one strategy the bees could use to solve it. cent of the time, which is very close to 30 per cent. So One strategy would be to use two rules: (i) go to the we conclude that the bees did not solve test 1 by only middle four flowers in each panel, and (ii) ignore the going to the middle flowers of each quadrant (‘dah colour. Another strategy would be to go to yellow if dahhh dahhhhhh’). However, two of the bees (labelled surrounded by blue or blue if surrounded by yellow. B/O and B) went most often to the green, middle They could also learn to avoid the surrounding flowers, flowers. So they seemed to have learned a different and as a result only go to the middle flowers. Or they rule to the other three bees. could go to the fewest number of coloured flowers in each panel. Of course they could also have chosen (c) Test 3 (the second experiment) randomly, and they might get them right or they In the third test, instead of having large squares of might get them wrong. Or they could have just gone yellow and blue around the outside of each panel, to a colour, but then they would not have solved the and a smaller square of yellow and blue on the inside whole puzzle, only half of it. of each panel, we took the four inside flowers and Test 2 tested whether the bees had learned to go to put them in the corners of each panel. See figure 3a the middle of each panel and ignored the colour. If this for a hand drawing of what this test looked like. We was true then they should have gone to the green flow- did this because we wanted to see if the bees solved ers. If they had learned to go to only middle blue and test 1 by learning during training to go to the colours yellow flowers, then they should have gone either to the of each panel that were fewest in number. We could surrounding blue and yellow flowers or no flowers at also see if they still preferred to go only to the middle all. The results tell us that three of the bees preferred Biol. Lett. (2011)
  • 6. Downloaded from rsbl.royalsocietypublishing.org on December 25, 2012 172 P. S. Blackawton et al. Colour and spatial relationships in bees to go to the colours that they had learned before, and Before doing these experiments we did not really avoided the middle green flowers. Two of the bees, think a lot about bees and how they are as smart as however, mainly went to the middle flowers, including us. We also did not think about the fact that without the B bee, which went to both correct yellow and cor- bees we would not survive, because bees keep the flow- rect blue flowers during the first (control) test. So they ers going. So it is important to understand bees. We had learned to solve the puzzle using different rules. discovered how fun it was to train bees. This is also Test 3 also showed that one of the rules was not just cool because you do not get to train bees everyday. We to go to any middle flower, as they rarely went to the like bees. Science is cool and fun because you get to do middle flowers, or to go to the flowers that had the stuff that no one has ever done before. (Bees—seem fewest colours in each panel, because they did not to—think!) prefer the corner flowers. Instead, they seemed to select the flowers at random, but funnily continued We thank the whole of the Blackawton community, who truly to go to their ‘favourite’ colour. engaged with the science research, including the George We conclude that bees can solve puzzles by learning Inn—where the manuscript was written—for the free Cokes complex rules, but sometimes they make mistakes. for the children (and pints for others). We thank the local They can also work together (indirectly) to solve a parish for the use of the Norman church, where the experiments were run, and the parents for letting their puzzle. Which means that bees have personality and children ‘work’ outside ‘normal’ school hours. Of course have their personal ‘likings’. We also learned that the none of this would have happened without the innovative bees could use the ‘shape’ of the different patterns of indi- and enthusiastic support of the teachers of Blackawton. We vidual flowers to decide which flowers to go to. So they are are also indebted to Larry Maloney and Natalie Hempel de quite clever, because they can memorize a pattern. This Ibarra for their openness to possibility and time, effort and might help them get more pollen from flowers by learning detail in writing the commentary, as well as Dale Purves, which flowers might be best for them without wasting Lars Chittka, Read Montague, Karl Friston and Geoff North (Current Biology) for their sage advice. Finally, we energy. In real life this might mean that they collect infor- thank Chris Frith and Brian Charlesworth for their open- mation and remember that information when going into mindedness. The project was funded privately by Lottolab different fields. So if some plants die out, they can learn to Studio, as the referees argued that young people cannot do find nectar in another type of flower. real science. Biol. Lett. (2011)