0:02 i just want to say that i'm really excited about this lecture i know i say that at every lecture but you know like every parent or all parents have a favorite um and i'm really looking forward to this i want welcome to professor chipka and dr natasha graver we are all in different places lars is in mexico city and natasha is in copenhagen and i am in london um but it's great that we can all get together okay so this is being recorded and it will be uploaded to our youtube channel later on in about 10 days or so if you have questions please don't put them in the chat box please put them in the q a box where natasha can find them at the end of the presentation and also for everyone here there is a discount
0:50 code for lars book which i will be putting in the chat box so look out for that and now over to natasha who will be introducing the lecture and professor chipka thank you hello thank you thank you so much uh padma so first of all to everybody welcome to the linnaean society nature reader events um many of you will be joining us as fellows of the society but for those who are not please do consider joining us uh the mission of the lennaian society is a vision where nature is understood valued and protected the society encourages the debate and discussion of natural history bringing
1:35 together diverse communities and engaging with scientists historians artists and all those interested in nature so our nature reader events are a core part of our work so i am very excited to introduce to you professor lars chikka lars is a professor at queen mary university of london where he founded a new research center for psychology in 2008 and was its scientific director until 2012. lars is a world authority on the behavior cognition and ecology of bumblebees and honeybees and their interactions with flowers he discovered that bees can count they could learn by observing each other
2:22 and have a rich inner world of sensations and memories and in this lecture this evening he will explore the bee's remarkable cognitive abilities and share some of the stories that we can learn some more about in his new book the mind of the bee so i'm really looking forward to this talk this evening so away with way with your talk class thank you so much natasha for this um very kind introduction and to padma for for the invitation so i'm super excited to talk about this book it is actually a real thing it exists out there um and i'm excited because this has been my work for the last 30 years and it's
3:08 my first book and it contains most of the things i did over 30 years so let me see if i can infuse you a little bit about the excitement of the research stories that are inside it so what do i mean by a mind in the case of an animal and specifically in the case of an animal such as a bee so there are many ways to look at animal minds and i'll focus only on on some of them because obviously there's limited time so the things i'll be talking about today that are related to an animal's mind are the question of whether they have mental representations of things and of
3:55 space and of things in space um i want to explore if they can flexibly access autobiographical memories i want to ask if they can look into the future if they have a form of an appreciation of the outcomes of their own actions and i want to ask perhaps the most contentious question in the course of this talk is whether they have emotions and these for me are key ingredients of a mind i hope i'll convince you that there is something like a mind residing in the tiny head of a bee but if not then at least i hope i'll convince you that they are um
4:40 very intelligent creatures in a manner that you might not have thought about insects before so there is an appreciation i think in general that insects can do very complex things but that they do so by means that are wholly different from the way how humans achieve complex things so if you look at these two structures here they look remotely single similar one of them is the la in barcelona and the other is a termite hill and the the exterior structure if you strip away the size is perhaps remotely similar in these two structures but the general thinking is that
5:28 in humans but not insects or other animals these kinds of architectural accomplishments come about by a top-down process where an architect dreams up the whole structure in advance and then hands down clear instructions to his his teams of constructors and electricians and what have you and uh and then to build the structure according to a plan where is so the current thinking in social insects there's no plan whatsoever there's only interactions between individuals that function entirely by innate routines and as a result of all of these local interactions between tiny robots so to speak you get
6:14 complexity but without any kind of outcome awareness and this is what i this view i want to deconstruct a little bit today discussion is not old and not not new it's actually quite old and one of the things that i think the book does that i hope to achieve is take a historical perspective into the history of many of the questions that still keep scientists busy today it's often very humbling to see just how long ago scientists have expressed certain very modern ideas so charles bonaire swiss naturalist was one of many historic scholars to think about the remarkable regularity of the
7:00 honeybee comb it's a highly regular hexagonal structure highly symmetrical it's also close to mathematically optimal in terms of how much material is used in a trade-off for storage space for honey and larvae and so on and he thought charbonnet thought the following about how this structure might come about placed together in the same room 10 000 automatons animated with a living force and induced through the perfect resemblance of their outer and inner being if we admit the least degree of feeling in these automatons even only so much as necessary for them to be conscious of their own existence seek their own conservation avoid
7:45 noxious things prepare useful things etc their work will not only be regular well proportioned similar equal but it will also have symmetry strength and convenience to the highest point of perfection so it's curious that bonaire thinks that consciousness and feelings are at the root of these kinds of constructions and then these highly regular architectures arise as a byproduct of things like consciousness and this is somewhat counter to present day views that consciousness is somehow has only arisen near the end of the phylogenetic tree and
8:31 early on people have explored these questions but we know from today's vantage point often humans of course are very cruel in sticking 10 000 individuals into a common room and we know that something like the complex structures of honeycomb does not just naturally pop out of that so it takes a little more than putting sentient individuals into crowded conditions and one of the earliest scholars to explore experimentally the question of honeycomb how honeycomb is constructed was from soybear another swiss naturalist who was interested in studying the inner workings of honeybee colonies and
9:18 therefore experimented with glass walls and ceilings to observe how this construction process works and you can see here the typical construction a typical construction in progress they invariably in natural hives start at the top to build with the wax construction and then work their way down along gravity producing typically multiple separate tongues of honeycomb that that are later emerged and so the first thing that uber did was to introduce a glass ceiling to observe this process in detail and what he found very quickly was that the bees did not like very much to
10:04 attach their comb to glass because obviously it's a slippery surface it's not um not as convenient to attach your construction to as wood but what his bees did in that case was they simply inverted the whole construction in their alignment to gravity and started at the bottom built the honeycomb from the bottom up essentially now as a tower construction so entirely reversed in its alignment to gravity now you might think well that's still a highly repetitive process that lends itself to robotic routines but if you had built a robot to just mimic the natural process start at the top work down along the direction of gravity
10:50 that robot would already have fallen flat on its face with this simple challenge this is a challenge that nobody has ever been encountering in its evolutionary history there's never been a glass ceiling in um in in a honey um in a beehive or in the cavity where bees naturally nest so uber thought okay let's make this even a little more complicated so he introduced in addition to a glass ceiling a glass floor so that both the floor and the ceiling were now sub-optimal surfaces to attach wax construction tool and what the bees did was simply start at one of the side walls and build the construction laterally through the cavity of the hive box
11:38 and again there is another degree of freedom there in the building process that had you simply build robots to face with the challenges of coming from the top to the bottom or bottom up again you'd have to reprogram your robot to achieve that routine as well but after they discovered this uber and his team in this case his uh his wife and servant um placed yet another challenge into the bee's construction that is after the lateral construction through the cavity had already begun the team put a glass surface into the path of the growing comb construction so this is what you can see in panel b
12:24 at the bottom of these two images so there was now in the path of the ongoing construction there was another glass surface that was later introduced after the bees had started building and what the bees did in that case is that before they had actually reached the glass surface before that reached the sub-optimal outcome of um that might have materialized had they just continued in the same direction was the bees several days before they would have reached that sub-optimal result turned the entire construction 90 degrees and attached the comb to the nearest wood wall and the remarkable thing there is that rather than continuing the construction along innate routines that would have
13:10 been dictated by just building a two-dimensional sheet of two-sided honeycomb is before reaching any kind of sub optimal outcome the beast seemed to anticipate what would happen if they extrapolated the comb in the same direction avoided the outcome and turned the construction 90 degrees and what yubel exclaimed over 200 years ago after these experiments was that he acknowledged that i could not suppress a sentiment of admiration for an action in which the brightest foresight was displayed now these experiments await replication one of my team members is interested in exploring this further we of course we need
13:56 um modern sample sizes and so on explains that he did this experiment multiple times and always with the same results but of course we'd like to um see the actual sample sizes and so on nonetheless there was over 200 years ago an indication that these complex structures are not just achieved by repetitive robotic routines but that there was a kind of planning involved in achieving outcomes that are functional and stable in this case now much of bee's learning behavior today is studied outside the hive and that's regrettable because i think there might be all kinds of intelligent things going
14:44 on inside the hive so i think we should return to uber's early approaches but much of the learning behavior we study is an exploitation of what bees naturally do at flowers and there are a few things that every bee must do by every bee i mean not just the familiar honey bees and bumble bees but also solitary bees in that all of these species in addition to these social species there are actually many thousand species of solitary species all of them have a home they have a home base to which they must return after visiting flowers and which therefore they must remember and this is not a trivial process if you imagine that bees often fly several kilometers in honeybees in the place of
15:31 honeybee over 10 kilometers away from their hive sometimes and these excursions last hours often and they have to reliably find their way back to this home and that distinguishes them from other insects flies butterflies that might more or less aimlessly drift across the landscape that do not have a home to return to the selection pressure for precise spatial memory is is very tough because if you fail if you don't remember where your home is then in a case of a solitary bee that's that means your offspring will die in the case of a social bee of course your your own existence might be less important for a colony
16:19 with thousands of individuals but nonetheless of course you might be lost as an individual and your efforts in terms of collecting nectar for uh offspring inside the quality are also lost so you need a very precise spatial memory in addition you need to be a careful shopper in what i call the flower supermarket that is you need to be able to identify those flower species or patches of flowers that deliver the best rewards in terms of nectar and pollen and you need to remember very much like a human shopper in a supermarket remember the advertisement that defines the package that you're buying so you might discover as an individual that the blue
17:06 flowers are the most rewarding and then of course you can save yourself the effort of sampling other species and focus your foraging efforts on those uh flower species that deliver the best cost-benefit ratio and this learning process of flower signals including their colors their shapes their scents is something that we capitalize on in our experiments so here's a typical example of such an experiment where on the left side we're rewarding a honey bee that is approaching an image of a human face and this these were experiments by adrian dyer who trained bees to associate a little nectar droplet
17:52 that you can see on a little landing platform in front of this face and if you do that a few times and then remove the rewards and just give the bees a choice between different faces in this case you can then test if she remembers what previously was associated with a nectar droplet and indeed bees recognize such images of human faces in this case but the b does not necessarily this does not mean that the b recognizes the face as a face it just means it's a pattern that the b associates with a reward so in a sense what the b is doing here is judging the face as a kind of strange flower that predicts for it the existence of a nectar droplet
18:38 to return to this question of spatial navigation we can perhaps appreciate how difficult it is to navigate unfamiliar environments if we've ever traveled to a city where we don't speak the local languages or can't read the signs so this i think is shanghai and we might our phone might have run out of batteries so we have to use landmarks to navigate now in the case of man-made environments and cities are manmade environments of course that's actually a relatively easy challenge because the landmarks the buildings are often built to be memorable they're meant to be unique and to stand out from other buildings and so therefore even in an unfamiliar
19:25 environment that you're navigating for the first time it's typically easy to find or facilitated to find your way by there being unique landmarks now a bee's natural landscape and many animals natural landscape is a bit more like this okay and i've deliberately chosen a foggy image here of a landscape in central mexico because that is often a kind of environment that bees have to navigate and so in this particular case that a bee's nest might be under this under the tree indicated by the central arrow here and there will be thousands of trees that are very close very similar in shape to that one yet you have to remember that one tree
20:10 and in this landscape there are for us us orbeez there are no um no paths there are no indicators i don't know if any of you do sort of wild hiking without any kind of satnav equipment but it is a tough challenge in such environments and if you're a bee then you might find a good nectar patch perhaps a kilometer behind the hill on the right and another pollen patch that's over here on the left and you have to keep all of these locations and the way between them in mind reliably and without fail um and find your your way back and forth between them and that is not a trivial challenge if you have a brain the size of a
20:56 pinhead now the way we nowadays study navigation of bees is with equipment called harmonic raider this is a an equipment that as you can see rotating on the right has two dishes one of them emits a raiders signal which is picked up by a transponder which is glued to a b's back here on the left bounced back by it and transported to a different frequency that's why it's called transponder which in turn is picked up by the top dish and you can then um from that signal extrapolate where the b is currently foraging or flying and
21:42 so this transponder of course looks uh humongous compared to the size of a b but it's actually very lightweight it's about a tenth of what a b can naturally carry uh when she uh loads up with nectar under or pollen and the idea behind us using such equipment ultimately and that's a long distance vision is that we want to be able to take the view from the cockpit of a bee while she's navigating her natural environment so here is a track of a 3d track of a um of a bee that is is flying around an uh environment near rothmuster research north of london and these two boomerang shaped structures are the bee's two eyes
22:28 and you can see through these eyes how it views the landscape while she's flying you can see that the pixel that the image is very coarse pixelated so the the vision of a bee has fewer pixels than than we humans do but bees compensate for that to some extent by by being able to process more information per unit time than for example humans can do and here's the kind of challenge that we're setting bees when we're studying their navigation with harmonic radar so here's a simple version of a so-called travelling salesman problem which as the name suggests is exactly the same kind of problem as that faced
23:14 in the human domain by traveling salesmen that have to visit perhaps a number of cities in the course of a day and while they're doing that they have to make sure that they minimize travel distance and time expenditure and and finding an optimal route between multiple locations and this is a problem that for a substantial number of sites at least can keep supercomputers busy for extended period so here's a simple version of that problem we have a hive at the bottom and five foraging locations five feeding stations that in volume that that can be collected there are adjusted so that the bee has to visit all five stations to um to
24:01 fill up her tummy ones and you can see here a root green is early in the root orange in the middle red is later that is clearly not yet optimal so the bee needs to find the optimum root over time and this is work by joseph woodgate and others that you can see how the bee with time and experience optimizes her route on the right side so she's the bee has now discovered the bottom two feeding stations and she's still exploring she's now found the second two and finally the fifth uh station on the top but you can see that there's still a great deal of exploration of the bee in the environment vicinity of these feeding stations she's still trying to find better ones and also a better route
24:47 between these stations we're counting the numbers on the top left um so we're known to 35 parts and at the end of that the b has actually found the optimum route to connect all of these five feeding stations so bees are good at these multi um station [Music] travelling salesman type of problems but we're also interested in how bees naturally navigate when we do not actually set them any challenges but we just want to ask how a bee organizes its own orientation and its own foraging life um when left to its own devices and that's what we're doing here we're following a single bee
25:32 for um several days or weeks uh in its entire foraging career from her maiden flight so what we're seeing now is the bee's very first flight sped up by more than a hundred times as she's exploring her environment around the nest for the first time this is a bumblebee and she is looping in various directions from her hive coming always back to the vicinity of the hive but not entering it the entire flight takes over two hours of bee exploring in different directions always returning to the vicinity of her hive and then exploring in a different direction and you can see in the course of this flight the bee is exploring one forest edge on
26:20 the top there which will become of interest later in her life now we're on day two and the b does one more green again is early in the process yellow later red at the end you can see that the bee makes one more exploratory flight in a south easterly southwesterly direction that's the green loop here and then she's found something she's now found a foraging location at a forest edge on the top left here in the north westerly direction from the hive and then she does nothing but visit that location she just exploits a single location for multiple days and always
27:06 shuttles back and forth between her hive and that particular patch then there were a few days of implement whether the bee stayed at home and after that this is what happened um so we're now on day 11 of that bee's life life at least as an adult after she she started her foraging process and she's now visiting a few more times that forest edge that she had visited in the early stage of her life and then halfway along an outbound flight to that patch she appears to change her mind and then shows up at this forest edge a location that she had only visited a single time 10 days earlier
27:52 on the very first excursion from her hive without retracing her steps back to near the hive but flying straight over to um this new forest edge as if she recovered uh a memory from in a beast case early in her life ten days earlier and then um exploits a patch there for the rest of her days until at some point she just vanished during a regular foraging bot um presumably being eaten by an insectivorous bird or a crab spider or something of sort so that's a single bees cv if you wish it's all of its special foraging activities in a few figures and that's all that bee ever did now other bees are very different in
28:37 how they organize exploitation and exploration across their careers there are some bees that almost never stop exploring and and never really seem to switch to rigorous exploitation there are other bees that interface the two activities um several times so that they might find that in a previously familiar patch is no longer profitable then they explore a bit more and then concentrate on a new patch so all of these kinds of learning abilities are spatial learning and flower color learning and so on are of course fairly close to what a bee naturally does
29:23 in in its own natural life and when i've discussed this kind of work with colleagues who work with primates and corvette birds conventional models of animal intelligence they've always looked down on this a little bit and said well yes they can learn things about flowers because that's what they need to do all the time in a that's what a bee normally has to do and they were not impressed by that and they they said that um one of their strategies and testing the intelligence of their intelligent animals is to to set them challenges that they never encounter in their usual environment and one common such task is a string pulling task that's often been tested with with
30:09 primates and parrots and so on and the string pulling task that you see here is basically reminiscent of these these tasks just adapted for a b's scale you see three artificial flowers on the left they're presented under plexiglas screen so to get to the reward that's contained in the center of these flowers in a little well you have to pull a string and so here's the first bee that ever managed this task in our lab this is work by savannah lim and other team members and you can see that while that bee is still a little clumsy and pulling the strings she clearly knows what she's doing and now she's got her reward that she's now happily imbibing and we can present bees with amazingly
30:57 complex versions of this challenge this now is worked by chow wen who presented the flowers with the kind of trick presentation where the shorter string is actually interrupted and the longer string is what need what leads the b to a reward the remarkable thing is these bees have previously learned to string pull but they have not been previously faced with interrupted strings so the b needs to recognize spontaneously without further training that um that she can get the reward only by pulling on the long side of the string and on the left is a different kind of version of the same task where the long string is diagonal and then there's a shorter string that again is interrupted
31:45 and if the b just pulled on the string that's perpendicular and shortest to the to lead to the flower then she would be tricked into pulling the interrupted string now this b is a little flaky she gives up several times but you can see that she never attempts to pull the short and interrupted string now she's finally properly pulled out a flower and imbibes the nectar solution the list of animals that can do this spontaneously is very very short it's humans and some other primates end of list dogs fail it cats fail it dolphins fail it and so on other animals can solve this kind of task after training that pulling on interrupted strings does not
32:31 lead to a reward orbeez do it spontaneously so this is really very surprising and uh indicates some form of means and comprehension in this particular task now what we can also do is let the bees train each other in such tasks so what you see here is an experience b marked with a red dot that knows how to string pull and she is paired up with a naive individual that has never done this task before and you can clearly see that without there was only one bee doing any work and the other one is now simply scrounging on the efforts of the experienced demonstrator as we call it and now they're happily sucking the
33:17 nectar together and you can see now they're getting a little bit antsy because the nectar droplet is actually been emptied out and the red marked individual is now running over to the next flower and pulling the string there the other naive individual clearly doesn't know what she's doing yet so she's still trying there must be something here but um doesn't find anything then again she runs over to join the experienced individual to capitalize on that bee's work but if you do that a good number of times then the previously naive individual will start to string paul by herself and and in this way the technique can spread through entire
34:02 populations you can see now again the repetition of the process the experience b pulse the next string and so on and what you're seeing here is how the string pulling technique spreads through an entire colony of of bees we have all individuals one dot on this circle is an individual we have all of them arranged in a big circle and what you can see the yellow marked individual at the top is our first generation demonstrator so to speak that was the first individual that solved the technique and wherever there's a line form that's an interaction between two individuals that have joined the in the arena and one of them pulls
34:49 the string now when one of these dots turns colored so you now have several orange dots that means that the target individual has now managed to string pull by herself so all the orange beans are so are our second generation learners that that have picked up the technique from the yellow individual so very much like you can monitor a meme spreading through social media in in a social network you can see how this technique spreads through a population of bumblebees and you can now see at the bottom a few purple dots and these are individuals of the yet of the third generation these are not proper biological generations just
35:36 generations of learners these are individuals that have no longer picked up the technique from the individual that was originally mastering the technique but from second generation learners and indeed in this particular case the technique continued to spread through the colony even after the original knowledgeable individual had passed away bees only live for a few weeks but in that short life they learn an amazing number of things and can even of course spread these things on from one individual to another and after you've trained multiple individuals in that kind of manner you can actually see them working together in this case at pulling out the
36:22 multiple strings so you can see there's a clear attraction of bees to join others and pulling strings and here they're pulling out a whole number of different flowers from from underneath a plexiglass table so for the next um experiment um i'll let uh damn jane goodall do the introduction i hope you can all hear this it's a little quiet so you might you have to pick up your ears the most recent uh example which blows people's minds is the bumblebee and
37:08 the bumblebee has been torn to roll a little ball he rolls it backwards rows the little ball until he can push it down or maybe she i don't know into a a hole like a goal and as soon as this little ball gets into the goal the bumble bee is given a little drop of nectar as a reward so we learned to do this but the mind-blowing thing is other bumblebees who've merely watched a taught bumblebee can do the same without being taught just by watching and that is supposed to be a mark of very superior intelligence so this is something we're learning all the time we have been far too arrogant the
37:56 animal kingdom of which we are apart is filled with secrets and gosh i'd love to be young and learning about these things now because all the doors are wide open and you never know what you're going to find yeah so that was very moving for us often the primate scientists are a little bit dismissive of um of uh b's intelligence but but clearly john godel was excited by our work and that was exciting for us in turn so let me explain this um experiment in a little bit more detail so as um jane just just explained the
38:41 task here is in its elementary form is to roll this ball into a goal area in this case the yellow circle at the center and then she gets a little nectar reward as uh is usually the case if the bees get something right in their experiments but the twist in this particular experiment and the question again of the social learning abilities of the bee is the following we were interested in a sense whether bees understand the desirable outcome of this task and again what we've done here is we've paired a knowledgeable individual bottom center one that's already learned how to roll a ball with a completely naive bee
39:27 that has never rolled balls for rewards before and you can see there's again a central goal area this year yellow circle and there are three balls and obviously the best way in theory of solving this task is to pick the closest ball is to pick the one that has the shortest distance to the destination and move that to get to the target but that's not what will happen now and that's because this experience be at the bottom knows that the two closest balls are actually glued to the surface she can't move so she's learned i can only move the most distance ball piston ball and that is also what the naive individual gets to see as shown here so we can see the experience be
40:13 swiftly rolling the ball to the center and then both individuals get to consume the reward by the way you can see here how we identify the bees they have little number tags glued to their backs so we can identify which individual has had which experience in the past so point here is that the naive individual gets shown to row that leading the furthest ball to this to the target destination leads to reward and we then ask that b after she's been observing that experienced individual three times how would you solve this task so here's here's our b our observer b alone now and so she has no experience yet with
40:59 ball rolling and we're asking will she simply ape the demonstrator will she stupidly copy the actions that she has seen the demonstrator perform or will she use spontaneously a better solution to the same task that is to put to roll the closest ball and this is what the b does she picks the ball that's closest to the target she does not copy the actions of the demonstrator but spontaneously improves you can see she's very clumsy but she gets the the um the task right and spontaneously uses an improved version of the demonstrator's accent with actions which indicates to us a kind of outcome awareness a kind of
41:46 awareness of the desirable end result of of the bees actions now we know from other authors work that bees are very good at recognizing patterns but it turns out that many of these flower pattern recognition tasks can at least in theory be solved with very simple neurobiological processes such as edge detectors so these are called simple feature detectors they're either detecting edges or edge orientations or just certain colors and so on without there necessarily being a need for a kind of virtual image that's that's floating around in a bee's head
42:33 so can bees picture things do they have a mental representation of object qualities and this is what we're exploring now in a an experiment that uses cross-model shape recognition where we're asking if there is a representation of shape properties in a bee's head then it should be accessible from multiple different sensory modalities in this case vision and touch and the experiment is in a sense quite simple we're training the bee for the example uh in this case here to associate ball-shaped things with rewards and cubes with not rewards and so that's
43:19 what the b has to learn a ball is good a cube is bad um but you can see in this image that these um shapes are actually presented under plexiglas screen in a screen in a petri dish where she can see that we can see the the objects but not touch them and we then ask after the bees have only seen these shapes will they recognize them when they can only feel them so the experiment then is after they've learned the to solve the task using vision can they now solve it using touch in complete darkness this is not a cruel experiment for bees because naturally in bumblebee's cases in many species they nest underground
44:04 where it is completely dark and it turns out that without further training these bees then spontaneously recognize the sphere only by touch without being able to solve the terms so this is perhaps a little reminiscent of the sort of child birthday parties game where you have to reach um with your hand into a bag where you can't look but you have to identify certain things by touch even if you've previously only seen them and you can also do the reverse that is we're training the bees to recognize well one group is gets trained on balls and another one on one spheres to recognize shapes only by touch and then confront them with the same shapes
44:50 using vision in the light again where in the test situation the bee can now not touch she's not allowed to feel the objects only to see them that indicates to us that indeed the bees have a kind of mental representation of these object properties that are accessible from multiple different sensory modalities now perhaps to the most controversial question do bees have emotions do insects have emotions and um this is of course but it's been asked before a long time
45:36 ago um including by charles turner and uh so turner is a was an american scientist who is in multis so because of his ethnicity he found it impossible to gain a major research university and did much of his work while being a high school teacher at a special school for african-american children and while doing that he published over 70 articles some of them in the most prestigious science journals and um articles that were highly visionary in my opinion in terms of their outlook on animal intelligence
46:23 animal cognition but he also thought creatively about the possibility of insect emotion so this figure and text is from one of his articles where this is about um a coiled antenna the protruding mouthparts and the general attitude indicate intense excitement one who believes that insects have emotion have emotions will find much in the attitude of these two homophilus to support his view so in general um i encourage you strongly to read um this scientists works they're extremely visionary i think and uh and very much in contrast to
47:09 the views that prevailed at the time about much of animal learning being associative and later in nature as advocated by pavlov and thorndike and so on charles turner thought that that animals could solve problems by insight and and so on so highly recommended now the way we can nowadays study emotion um is using various experimental paradigms in the laboratory and here's one of them that got me thinking um about the possibility of emotion-like states in bees so we were interested in whether bees can learn about predation threat and what you see here are crab spiders lurking on
47:55 flowers these are spiders that basically chameleon style can adopt the color of the flower on which they forage or hunt and um and so we took this station and built what we call a robotic crab spiders as you can see on the right side here we either had cryptic yellow spiders on a yellow background or white ones that were highly detectable and there are two sponge pads driven by a solenoid that could briefly capture a b so they're very soft nothing bad happens to the b physically um and briefly captures it then releases so this is the equivalent of a of um a spider briefly capturing onto a b but then not
48:41 being able to subdue it and i'm going to show you a little video of this sort of capture attempt so here's our bee first landing on a safe flower there's no spider there and now she just makes a mistake and lands on a flower with a spider on it so again there's no um injury here because these pads are very soft but clearly the bee is not very happy and so we were interested in do the bees and the question do bees learn to avoid flowers with these spiders on them and they do but um but there was something
49:26 else that caught our attention so first of all bees do indeed learn to avoid the flowers or the flower species artificial flowers be pieces that harbor such spiders but also their entire demeanor so the bees now scanned every single flower often extensively before landing on the flowers now that is still that is an adaptive behavior although one that extends beyond a mere reflexive behavior of trying to escape the predation threat so the bees typically scanned the flowers for more for landing but the most remarkable thing in the sense [Music] the um the bees not only showed improved
50:12 predator avoidance but actually displayed false alarm behavior that is they scanned the flower extensively and often a perfectly safe flower and then rejected it even though there was no spider on it so they behaved as if they were seeing ghosts as if there was a threat that they detected and flew away from it even though there was none there which very much looked like a kind of post-traumatic stress disorder if you wish i wouldn't probably do such experiments now again but at the time 15 years ago we hadn't anticipated this sort of result but it indicated to us that there is indeed a kind of uh almost anxiety um type response to a
51:00 threat that in many cases actually had ceased to exist and nonetheless the bees seemed to perceive a threat where there was none and more recently a more conventional paradigm to study emotion like states is basically to ask if how an animal responds to ambiguous stimuli and that's essentially the same as asking a human being whether their glasses are full or half empty so we have here a glass that's 50 filled with water and an optimist would judge that as well it's basically almost full looking good to me whereas a pessimist judges exactly the same stimulus as uh it's already close to empathy
51:48 and this kind of paradigm is used for example in domestic animals to tell if goats sheep cows and so on are kept under conditions that induces them to have a positive outlook on their life or whether they're there the conditions under which they're kept are actually unfavorable and we adapted this paradigm again to the world of bees and flowers so you can see on the top left in panel a is a small flight arena where the bee enters into it from the left and on the right side there are five little tunnels that can be marked with a color and also where there can be a reward and we train the bees at least of one group the one that's shown here that when there was a
52:35 blue stimulus on the left there was always a reward when there was a green stimulus on the right there was never a reward okay and that's what the bees learned at any time there was only one stimulus available whenever the bee entered this this arena and she learned that blue is good and green is not good and then as shown in panel c um we give the bee after she's learned this various ambiguous stimuli in between what she previously learned as good and as bad that's our glass 50 filled and we're asking well how do you judge this and so what we see after training is is shown here we see that the bees that have learned blue on the left is good
53:21 will will fly straight to that target whereas bees that have learned that and the same bees have learned that green on the right is no good they will eventually accept it but only after a great deal of perhaps a minute or two of faffing about and say all right well if nothing else is being shown to me here i might as well try it anyway and see if there isn't a reward after all but only after a great deal of hesitation and then we give the bees the ambiguous option the option in between turquoise or um some of the the options in between we did one additional thing and that is that some of the bees that have previously been trained as shown on top
54:07 some of these bees were given a little surprise reward before entering the flight arena they were given a 5 microliter droplet of sucrose solution whereas our control group of bees didn't get such a reward and it turns out that the judgment of the ambiguous stimuli depends on what happened to the beast before we tested them to the extent that if they had been given a surprise reward they would judge the ambiguous stimulus as more likely being rewarding than not and that's shown here on the bottom right this is the only data slide so by and large this has been a very video based and data avoid data shy
54:55 presentation but here's one data slide but i'll make it simple on the bottom left marked p that's the positive stimulus and you can see that no matter what if we show them blue rewarding the bees respond fast after less than 10 seconds they've made their choice and flown to the target if on the other hand we present them with the negative stimulus green on the right it takes them about over 100 seconds nearly two minutes on average to accept that stimulus and all the other responses are in between but crucially and that's the red curve here if the bees have been given a surprise reward before entering the arena before even being tested their response times are shorter
55:41 for all the ambiguous options for turquoise and the options in between so the red curve shows how these uh response times are shorter compared to the black curve where the bees are more hesitant to accept these ambiguous stimuli so bees that have been given a reward where they've not expected it judge the ambiguous stimulus that they've never seen before as more likely being rewarding so that's our glass 50 filled where the bees now when they've had a surprise reward judge it as more likely being a rewarding option so by the same criteria as we're judging domestic animals as being more optimistic in this conditions the bees also qualify
56:28 um and um and and seem to judge the stimulus optimistically a few brief words about bees brains aren't bee's brains just too tiny to contain anything such as a mind and all of these problem-solving capacities that have shown here so the number of neurons in a b's brain is indeed small compared to ours so there are about 850 000 neurons in a honeybee's brain um here's a portrait of such a brain so the um optical eval neural evaluation centers are on the left shown in in blue and this some sort of old-fashioned telephone dial
57:14 arrangements marked a l here is um is is the so-called internal lobe that evaluates all factory information and all of these peripheral neural evaluation centers send their information to the mushroom bodies shown at the top which function as centers of multi-sensory integration and associative learning now while there are only 850 000 neurons in a bee's brain the wiring diagram is very very far from simple so here's a single one of these neurons this one was discovered by martin hummer in randolph mensah's lab in the 1990s and you can see its um cell body is this
58:00 little blob above the letters sog and it has branching structures throughout the entire brain almost throughout the internal lobes and the mushroom bodies this single cell has perhaps the complexity of a fully grown tree and each individual nerve cell in a bee's brain might make connections with up to 10 000 other neurons now imagine that all of these connection points the synapses are at least potentially plastic and can respond to to experience then we have an amazingly complex system that even though perhaps in insects we're closer to understand brain
58:46 functionality in anything close to being comprehensive we're closer than people who are exploring the human brain perhaps but we're still a long long way from actually understanding it we're still looking at um at um small parts of the the entire um connection diagram now i wanted to quote here from um from one of the pioneers of um neuroscience santiago ramuni cacao who was interested of course in general in how nervous system works but the complexity of insect nervous systems uh did not escape him and he compared um the the brains of
59:33 uh bees and dragonflies with those of um fish and um and amphibians and uh and found or stated the following about these different types of brains so he says that the excellence of the psychic machine does not increase with zoological hierarchy instead one realizes that in facial amphibians the nervous centers have undergone an unexpected simplification of course the mass of gray matter has cons the gray matter has can increase considerably in mass but when the structure of their brains is compared with that of bees are dragonflies they're excessively plain coarse and rudimentary it is as if one were to pretend to hold
1:00:20 as equals the merits of a rough grandfather clock with the quality of a fine pocket watch a marvel of fineness delicacy and precision as always in building her marvelous works nature distinguishes herself much more in her tiny creations than in the large and we see on the bottom here a drawing from uh ramonica khale and his colleague diego sanchez that is actually remarkably detailed in the the wiring diagram diagram of the bee's visual system i should say that in a bee's visual system or in the fly we now know that there are about 150 neuron types just in the visual optic ganglia which by far exceeds the number of types that
1:01:05 exist in the human retina which is about 80. so there is amazing complexity in a bee's brain and i think not too much too little complexity to conjecture that it might contain a mind so some conclusions i think i have shown that bees have representations of space of things in space that they can learn by observation and display simple to use in a manner that indicates a form of outcome awareness or intentionality they have flexible access to a memory library an idea of what they want and explore mentally explore solutions to get there using an awareness of the possible outcomes of their own actions and they appear to be indeed a motion-like
1:01:51 states attached to rewards and also punishments and all of these i think are key ingredients of a mind and i think that we need to therefore recognize that we as humans are thinking suffering and enjoying beings in a world that contains other thinking and suffering and enjoying beings with different minds and perceptions and i think this commands some respect for the environment that these animal minds have evolved in and a responsibility to preserve these environments okay thank you very much i'll stop now and i'll be happy to hear your questions hello
1:02:37 thank you so much for that talk that was absolutely fabulous um i have really really enjoyed um finding out so much about what visa are doing and i love the intricacy of how you have over those years gradually teased apart these mechanisms and how they do that and the beautiful experiments of how they they go about and understand their world um lars we have many questions um so i'm gonna it's gonna be almost a selection of questions um so i'm going to pick them as we go through so they'll be kind of in the order of your presentation
1:03:23 um and we'll see how many we can get through in the next 15 minutes or so so a question that has come up from a couple of people is is about how bees navigate and whether they um use celestial objects such as the sort of sun moon or stars in order to assist with that do and indeed again this is not a trivial undertaking they use the sun as a compass cube and the sun unlike a magnetic compass of course has the added complication that it's in different locations at different times of day so unlike a magnetic compass where the needle always points north the sun is not always in the south or
1:04:09 north but it changes its angular position um above the horizon with time of day so you need to have an an inner clock a circadian clock you need to know what time it is to read correctly how the sun indicates the direction where you want to fly but moreover the sun has another disadvantage and that it's sometimes disappeared behind clouds or behind trees are indeed behind the horizon and you still want to find the direction correctly and bees can do that too and they can do that by analyzing the direction of polarized light in the sky
1:04:54 so you might recall from physics lessons that um that light has wave kind of property so you can imagine it in the same way as when you tie a rope to a wall and then you shake the other end up and down then it spreads in then you have waves um along along europe and in the same ways the ropes swings in a certain direction within a plane um light swings in a particular direction and the pattern in which the light swings so to speak um indicates if you have the equipment to analyze that pattern indicates where the sun is even if the sun is hidden so by analyzing the pattern of polarized light in the sky
1:05:41 you can reconstruct the position of the sun even if the sun itself is not visible and that in turn means you can then again only if you need the if you know the time of day um use it as a compass queue fabulous so and again the complexity of of their ability to do that is fabulous really interesting now i have a question here which um very simple question you you always are mentioning the the bees that you're talking about as females is it just females and being worked with here and why is that it's a very good question um in the bees world um it's typically only the females that work
1:06:29 or at least that work for um the the communal country that is in social bees it's only the female worker bees that actually bring back nectar and pollen to the hive um they're the only ones that that engage in construction of the nestrahive that defend the colony and so on the males in honeybees are good only for one thing you can imagine what that is but they don't ever deliver anything for for the colony indeed they need to be fed by the workers because they can't even feed themselves in bumblebees the workers the males at least can feed themselves they visit florists by
1:07:15 themselves and contribute to pollination so they're not quite as helpless as honeybee males now the reason we typically work with the female worker bees is that as opposed to many other experimental animals they never satiate that is once the tummies are full with nectar if we've rewarded them enough they fly straight home to the the hive unload what they've gathered and come straight back to collect more rewards so they're highly motivated to um to engage with our experiments because there's always a little reward at the end whereas male bees even if they're bumble bees that can
1:08:00 feed themselves once their tummies fall they'll basically sit in the corner and burp and say thank you very much but i'm now done with your experiment you can nonetheless train them they are able to learn colors of flowers for example and in fact there are no worse at it than um than worker bees of the same species um but it takes a lot of effort to give them very very tiny rewards so they don't satiate very quickly but they can learn and and honeybees can also honeybee males can certainly locate learn to locate the location of their hive to which they reliably return also from their excursions when they're trying to met with queens so males are pretty useless except for sex but
1:08:47 but when you put them on the spot they can actually learn some things at least fantastic thank you um now a slightly sort of difficult question here amelia lewis um can we say anything given that individuals have variation in in foraging behavior do they have personalities or do you see a lot of variation in what they're doing indeed we do and this is um again there's an interesting historical perspective because when when i started as a young scientist such variation was largely ignored um and people thought that they just have to um average all the individual responses to get a meaningful species picture people
1:09:34 thought that individual variation is noise and when we later explored this a bit more in more detail more rigorously we found that when all psychological traits that we can measure for bees whether this is learning speed or neophobia neophilia the extent to which they are more exploratory and so on for all of these traits we found very strong individual variation and such variation is also heritable so there are whole colonies of faster learners and slower learners and so on so for all of these psychological traits we find individual variation and some of at least some of it is is heritable so in the same
1:10:21 by the same criteria that a vertebrate biologist would diagnose their dog or cat as having personality i think the bees also qualify it turns out again that if you take a deeper historical perspective charles turner the scientist whom i mentioned earlier was very aware of such inter-individual variation in insects he didn't call it by the flashy word of personality but it was a common thread through throughout his work that he from his very early publications when he was a 25 year old man in this case studying spiders diagnosed individual variation in the the um the intelligence of um of
1:11:06 weaving spiders for example so people have observed this a long time before us but we're now gradually rediscovering these entire individual psychological trait variations and bees as well brilliant thank you thank you the question from george yang here so um sometimes or um for a lot of the social learning you're using bumblebees some of the earlier work was using honeybees how are you deciding which species of bee to use and do you see big variations within those so some of the the choice is mere convenience um the the reasons why we're working mostly
1:11:51 working at least with social bees is that it's easier because there's often a long history of how to best keep them and we can obtain responses from large number of individuals and so on um there is i think an urgent need to study more species and specifically more solitary species um i mentioned earlier that actually the vast majority of bee species are solitary and they they differ hugely in their biology and it's therefore to be expected that they also will differ in their levels of intelligence if you wish and specifically the the kinds of tasks that they are or
1:12:38 are not able to solve so with some things such as color learning abilities we've tested a few species of solitary bees and found that there wasn't actually much difference in these abilities between social and solitary species more recently oli lucola and my team has tested some interesting aspects of social learning learning from others in nesting solitary bees where these bees inspect nests in existing nests in the vicinity of where they're considering nesting themselves and specifically their um evaluating the nest existing nests for signs of parasitism and if they find sites of parasitism
1:13:24 they not only learn they not only avoid the sight but they also are able to learn to associate symbols associated with that site so if there are parasitized sites marked with triangles and you then give these solitary bees between sites marked with triangles and squares they'll pick the one with squares instead so there is a kind of unique learning ability that is linked to these bees decisions of where to nest and to avoid sites that dangerous because of parasites found in these solitary species and i imagine that if we cast the net more widely and study bees with more differences in biology then we'll also find more
1:14:09 variation in which kinds of tasks they're able to solve intelligently oh thank you um and then actually continuing with the line of question of of the the sort of different sort of species and and how the learning takes place there's a few questions here which i'll try and sort of summarize into one question which is um within the colony particularly for the bumblebees and the honeybees um will the bees all learn from each other equally or could uh say different origins of honeybees or bumblebees um make a difference to to who who is learning from whom kind of thing that makes sense yeah so i mean first of all there is an
1:14:57 amazing flexibility in terms of from whom bees can learn we've actually asked the question can bumblebees learn flower color preferences from honeybees and vice versa and in this case this was not a difficult task such as object manipulation or anything like that but simply which colors of flowers to choose and in that case not only will bumblebees learn from other bumblebees but they can also learn from honeybees foraging activities and vice versa um and then of course i guess a next question is canopy figure out who is a most more reliable demonstrator of high quality information
1:15:45 in the same sense as you might require might recognize a good teacher from from someone who is not a suitable role model and that's difficult to answer in natural bee populations because there's very little variation in terms of how bees look they're not easily recognizable as as individuals but one of my former phd students eric romero he actually marked bees with little color dots and then showed their behavior to naive observers and in this case when they were actually made individually when the demonstrators were made individually
1:16:31 recognizable so that the observer could learn how that be with a blue dot is a really not a knowledgeable teacher whereas the one with the yellow [Music] then when so when you artificially emphasize the variation the visible variation then other bees also recognize a good role model from a bad role model and focus their following activities on those bees that are particularly knowledgeable fascinating thank you thank you um a couple couple more questions if that's if that's okay we're rattling through these um so the many of the experiments for example with the the bumblebees um we're looking
1:17:17 at social learning where the the bees are next to each other and they're teaching tool use or how to do a particular task how does that relate to the kind of real life at the flower front when the bumblebees are often foraging individually they are often foraging individually but often the densities of individuals on flower patches can be quite high and so there is certainly if you specifically seek out patches with more pollinator activity there is ample opportunity for observing which other which flowers are visited by other bees and moreover how they're visited
1:18:04 so charles darwin for example thought that bees could learn by observing each other the technique of nectar rubbing and this is where flowers that have very long tubes and their whose nectar is therefore difficult to access if you as a bee have a relatively short tongue some bees will actually bite holes into the spurs of the flowers and in that way extract nectar without necessarily touching the reproductive parts of the flower and darwin thought that not only could these bumblebees learn this technique from each other but honeybees could learn by observing observing the bumblebees activities
1:18:51 and there are a variety of ways in which that could manifest one is that you actually see um while you're hovering around a flower that's being exploited in that way you're seeing what a knowledgeable individual is doing
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