text: For years, cognitive scientist Lars Chittka felt a bit eclipsed by his colleagues at Queen Mary University of London. Their studies of apes, crows, and parrots were constantly revealing how smart these animals were. He worked on bees, and at the time, almost everyone assumed that the insects acted on instinct, not intelligence. "So there was a challenge for me: Could we get our small-brained bees to solve tasks that would impress a bird cognition researcher?" he recalls. Now, it seems he has succeeded at last. 
   
   Chittka’s team has shown that bumble bees can not only learn to pull a string to retrieve a reward, but they can also learn this trick from other bees, even though they have no experience with such a task in nature. The study “successfully challenges the notion that 'big brains' are necessary" for new skills to spread, says Christian Rutz, an evolutionary ecologist who studies bird cognition at the University of St. Andrews in the United Kingdom. 
   
   Many researchers have used string pulling to assess the smarts of animals, particularly birds and apes. So Chittka and his colleagues set up a low clear plastic table barely tall enough to lay three flat artificial blue flowers underneath. Each flower contained a well of sugar water in the center and had a string attached that extended beyond the table's boundaries. The only way the bumble bee could get the sugar water was to pull the flower out from under the table by tugging on the string. 
   
   Video of Hints of tool use, culture seen in bumblebees 
   
   The team put 110 bumble bees, one at a time, next to the table to see what they would do. Some tugged at the strings and gave up, but two actually kept at it until they retrieved the sugar water. In another series of experiments, the researchers trained the bees by first placing the flower next to the bee and then moving it ever farther under the table. More than half of the 40 bees tested learned what to do, Chittka and his colleagues report this week in PLOS Biology . 
   
   Next, the researchers placed untrained bees behind a clear plastic wall so they could see the other bees retrieving the sugar water. More than 60% of the insects that watched knew to pull the string when it was their turn. In another experiment, scientists put bees that knew how to pull the string back into their colony and a majority of the colony's workers picked up string pulling by watching one trained bee do it when it left the colony in search of food. The bees usually learned this trick after watching the trained bee five times, and sometimes even after one observation. Even after the trained bee died, string pulling continued to spread among the colony’s younger workers. 
   
   But pulling a string does not quite qualify as tool use, because it would have to be an independent object that wasn’t attached to the flower in the first place. And other invertebrates have shown they can use tools: Digger wasps pick up small stones and use them to pack down their burrow entrances, for example. But that two bees figured out how to pull the string with no help and further, that other bees could pick up on that ability was “most impressive,” says Ivo Jacobs, a cognitive zoologist at Lund University in Sweden who was not involved with the work. “The fact that bumble bees could learn to do so shows their unexpected behavioral flexibility.” 
   
   The findings could also hint at a rudimentary form of culture in bees, Jacobs says. With their ability to learn where others are, find out what they are doing, and experimenting on their own, the insects demonstrated that they can pass on knowledge—a key requirement of culture, normally considered to be a more complex phenomena, he explains. “It's interesting to see that the bees have this capacity." 
   
   Rutz is impressed, too, because the work involved almost 300 bees and clearly documented how string pulling spread from bee to bee in multiple colonies. Cognitive studies of vertebrates like birds and monkeys typically involve about an order of magnitude fewer individuals, he notes. 
   
   With additional experiments, Chittka hopes to figure out the neural basis of these “smarts” in the bumble bees. He cautions that the insects might not be all that intelligent, but that instead, “these results may mean that culturelike phenomena might actually be based on relatively simple mechanisms.” ||||| Conversely, after 48 h of extensive training (20 instances of string pulling), 11 of the 15 foragers solved the task without feedback from the moving blue flower ( S5 Video ). Latency to obtaining the reward (147 ± 23.44 s) was much higher than for normal blue flower training (22.1 ± 1.5 s; t test: t25 = 6.25, p < 0.0001). The subjects’ success differs significantly from their performance when they were relatively inexperienced (McNemar Test, χ 2 1 = 7.111, p = 0.008), thus indicating that the majority of highly experienced individuals may no longer require visual feedback to perform the necessary sequence of motor actions. In fact, experienced bees may not need the blue flower at all and perhaps have associated the string with the reward. 
   
   The success of bees learning such a behavior raises the question about the mechanisms by which the demonstrators learned to pull the string. One possibility is that demonstrators are stimulated to repeat the specific sequence of actions (moving the string with their legs) that induces the conditioned stimulus (i.e., the blue flower positioned under the table) to move a little closer. If so, we would expect bees not to move the string with their legs and fail at the task if the colored target stimulus is not present. To test this prediction, we challenged bees (Colony 2) to access the reward when a string was attached to only a colorless inverted Eppendorf cap containing sucrose solution (Materials and Methods) immediately after their initial stepwise training and then again after extensive experience with blue flowers and strings. Without a colored stimulus, only 2 of 15 bees tested obtained the reward after their initial training. We thus hypothesized that relatively inexperienced bees rely on visual feedback of the colored target moving closer while the string is being pulled. To explore this further, we examined the video material for the unsuccessful bees to see if they would attempt to pull the strings and then abort this action when visual feedback was not forthcoming. However, none of the unsuccessful bees demonstrated even an aborted pulling action on the colorless flower’s string. This suggests that most relatively inexperienced bees require the presence of the blue flower to even begin attempting to string pull. (However, there is also evidence for the importance of visual feedback during pulling from an experiment with coiled strings; see section The Mechanisms of Observational Learning in String Pulling.) 
   
   In comparison, we were able to train 23 of 40 individuals (Colony 1) through a stepwise training procedure to successfully pull a string to obtain reward ( Fig 1B horizontal black bar in column 4, S1 – S4 Videos). The stepwise training consisted of four steps of incremental difficulty within which flowers with strings were placed at progressively more distant positions under the transparent table (Steps 1–4, Fig 1A and 1B ). On average, successful training for an individual bee took 309 ± 18 min. Gaining access to the reward in the final step required grasping the string with the forelegs and/or mandibles and pulling it closer ( S4 Video ). The mean time required (latency) to obtain sucrose decreased significantly as a function of experience within each of the four successive training phases (Friedman test, Step 1: χ 2 4 = 59.1, p = <0.001; Step 2: χ 2 4 = 53.1, p = <0.001; Step 3: χ 2 4 = 52.1, p = <0.001; Step 4: χ 2 10 = 92.3, p < 0.001; Fig 1C and 1D ). Eight, three, one, and five individuals gave up at Steps 1, 2, 3, and 4, respectively, either because they ceased foraging activity or had irregular foraging activity (n = 11), or because they failed to obtain the reward (n = 6). Three of these successfully trained bees were later used as demonstrators in the social learning experiment. 
   
   (A) Arena set up for the observation of string pulling. (B) The various testing procedures. Tests 1 and 2 were identical and consisted of giving 5 min to individual bees to solve the string pulling task. After having been trained to forage from blue artificial flowers, bees were tested a first time (Test 1). Then, demonstrators were trained (see Fig 1 ) and used to display string pulling (two instances, straight strings) during each of five foraging bouts to individual observers (n = 52) placed in a transparent Plexiglas cage. After the observation phase, 25 observers were tested again with the straight-string task (Test 2) and 27 with the coiled-string task. Fifteen different bees observed the flower moving without visible actor so that a forager could then obtain the sucrose solution (“Ghost control”) and, where tested, with the straight-string task subsequently. Untrained bees (n = 25) were also tested a second time with string pulling. (C) Percentage of successful untrained, social, and nonsocial observer bees in Tests 1 and 2. Asterisk: Fisher’s exact test, p ≤ 0.0001. Double S: McNemar test, χ 2 1 = 13.067, p < 0.001. (D) Mean ± s.e. (s) latency in accessing the reward in untrained and observer bees. Observers’ latency was not different from that of the two “innovators” (Mann–Whitney U test, U 15 = 6, p = 0.205), (see S1 Data ). 
   
   (A) Stepwise string pulling training protocol. Successive steps: Step 0, pretraining on blue artificial flowers (note that all bees were trained on this step); Step 1, 50% of the flower covered by the transparent table; Step 2, 75% of the flower covered; Steps 3 and 4, 100% of the flower covered. The flower was positioned at the edge in Step 3 and 2 cm under the table in Step 4. (B) Percentage of successful bees in Steps 1 to 4 (n = 40, 32, 29, and 28, respectively). Black horizontal lines within bars indicate the percentage of bees of the original 40. (C) and (D), mean ± standard error (s.e.) (line and shaded area, s) latency to obtain the reward in Steps 1–3 and 4. (C) Mean latency for the five foraging bouts of Steps 1–3. Data points, from left to right, in (D) indicate the latency to reward in Step 4 for the bout with first occurrence of string pulling and the ten foraging bouts that followed. Bees needed 6.17 ± 1.2 foraging bouts before displaying string pulling in Step 4 (see S1 Data ). 
   
   To test bees’ capacity to learn the technique of string pulling, we first challenged untrained individuals with a stepwise training procedure (Materials and Methods; S1 – S4 Videos). We presented individual bees with three blue artificial flowers with a string attached to each flower and placed under a small transparent Plexiglas table (Materials and Methods). After learning to associate the reward with artificial flowers in a flight arena (Step 0, Fig 1A ), but prior to string pulling training, none of the bees from the eight colonies in which individuals were tested singly (n = 291) could solve the string pulling task on their first 5-min attempt (Test 1, Fig 2B ). Naïve to the string task but attracted to the artificial flowers, these bees tried to reach the reward from the top of the table through the Plexiglas. 
   
   We gave 50 individuals (Colony 1) the opportunity to solve the string pulling task spontaneously after having learnt that blue flowers are rewarding when they were openly accessible during pretraining (for a 5-min observation period). None of these individuals solved the task. When given a second 5-min opportunity, two of 25 untrained bees succeeded in obtaining the reward ( S6 Video ). However, they were more than ten times slower at obtaining the reward than experienced string pullers (22.1 ± 1.5 s, mean ± standard error [s.e.], Mann–Whitney U test, U 23 < 0.001, p = 0.024), requiring a relatively long latency of 245 ± 3.53 s. These two bees were exceptionally explorative, trying a wide variety of methods, and solved the task in several attempts by moving the string accidently while trying to reach the flower under the table (see S6 Video and legend for more information). This shows clearly that string pulling can be learned individually by some bumblebees, but this may be an exceptionally rare ability. Across experiments (see below), 291 naïve individuals were tested once, and a total 110 were tested twice, but no further “innovators” were found. In one experiment (the transmission chain experiment below, in which control colonies were not seeded with a skilled demonstrator), bees were given extensive opportunities. After 5 d of foraging, with a maximum number of 18 foraging bouts per individual, no single bee learned to pull the string. Of the 165 bees tested in this experiment in total, nine individuals were tested more than 10 times, and 26 more than 5 times, but all were invariably unsuccessful. Thus, solving a string pulling task spontaneously is a relatively rare occurrence in bumblebees and might either reflect an unusually explorative “personality” in these individuals or simple “luck” in the process of random exploration. 
   
   Finally, because smaller bees might be able to reach further under the table than larger bees, we examined whether body size influenced success in solving the task (Colony 1). Thorax width (as a proxy for body size) was not different between demonstrators (n = 40), observers (n = 25), and untrained bees (n = 25) (ANOVA, F 69 = 0.728, p = 0.486). Thorax width affected neither demonstrators’ (Student’s t test, t 26 = 0.659, p = 0.516) nor observers’ success rate (Mann–Whitney U test, U 23 = 79, p = 0.846). Similarly, the latency to obtain the reward was not affected by thorax width of demonstrators (Pearson correlation, r 23 = -0.086, p = 0.696) or observers (Pearson correlation, r 15 = 0.375, p = 0.169). 
   
   We also wished to disentangle the effects of demonstrator copying and object movement copying in how string pulling was learnt by observation. To this end, we used an experimental “ghost control” ([ 40 ], S8 Video ). We trained 15 nonsocial observers (Colony 3) in exactly the same manner as above with the modification that the flowers were moved without a visible actor: an experimenter pulled the flowers with thin nylon threads attached to the strings while the observers were locked inside the observation chamber (Materials and Methods). Once the string had been pulled, an untrained forager was released into the arena to feed from the now accessible flower. Without direct demonstration of string pulling by a bumblebee forager, none of the observers managed to solve the string pulling task. Nonsocial observers mostly tried to obtain the reward from the top of the table, indicating that the bees need to observe string pulling actions demonstrated by conspecifics to learn the technique. However, because no video material is available to show that observer bees directed their gaze towards the moving flower, it is also possible that in the absence of a conspecific demonstrator, observers simply failed to attend to the movement of the flower. 
   
   We explored whether uninformed bees (Colony 1) could learn this novel foraging technique via observation. After pretraining on blue flowers and Test 1 (Materials and Methods), an uninformed observer bee was placed in a transparent chamber ( Fig 2A ) where it could observe a demonstrator solve the string pulling task ten times. These observers (n = 25) were subsequently tested on the string pulling task alone (Test 2, Fig 2B ). In this experiment, observers never interacted directly with demonstrators in the flight arena and had access only to visual social information ( S7 Video ). Sixty percent of the individuals (15 of 25) that had the opportunity to observe a skilled demonstrator managed to pull the string and obtained the reward on the first trial after having observed the demonstration (Test 2, Fig 2C , S6 Video ). These bees, however, were initially almost as slow as the two individuals that solved the tasks without demonstration (181 ± 19 s; Fig 2D ). We speculate that the observers picked up the correct location to access the reward from observing skilled demonstrators but did not learn from them the actual technique of string pulling (further explored in the section beneath about the mechanisms of social learning). 
   
   Finally, trial-and-error learning was also evident in the learning process. Because individuals might only learn where to obtain the reward and then learn the string pulling by trial-and-error, observer bees (n = 27, Colony 5) were tested with a coiled-string paradigm where trial-and-error learning of actions causing the rewarding object moving closer is ineffective. After a standard demonstration of string pulling (Materials and Methods), a 14 cm string was attached to the flower and coiled under the table so that initial tugs on the string would provide no visual feedback of the flower moving closer to the bee. Such coiled-string tests have in the past been used to test whether animals can solve a string pulling puzzle by means-end comprehension, without the perceptual feedback of the reward coming closer [ 44 , 45 ]. Long-tailed macaques (Macaca fascicularis) [ 47 ] and wolves (Canis lupus) [ 48 ] have indeed been shown to solve the task even if the string is coiled. However, none of these observer bees were able to solve this task (n = 27, Fig 2B , S10 Video ), indicating that observers did not glean information about the string pulling technique itself by observing a demonstrator but instead were merely guided to the demonstrator’s previous location (by local enhancement) and the position of the string (stimulus enhancement). The actual act of string pulling relied on individual trial-and-error learning, which in turn necessitates the sensory feedback of tugging on the string, resulting in the target moving closer. We also tested eight experienced individuals (with an experience of more than 20 instances of string pulling) with the coiled-string test; three of these bees succeeded in pulling the coiled string to obtain the reward ( S11 Video ), indicating that highly experienced individuals do not necessarily require the feedback from seeing the flower move closer while they pull the string. In summary, these results suggest that observational learning of the string pulling task does not involve the “understanding” of the task (“insight”) but the combined use of several simple associative mechanisms and trial-and-error learning. 
   
   (A) Regions of interest used for the video analysis of bee behaviors (not true to scale): the original region (where the demonstrator pulled a string, solid dark grey), top region (on the table, solid light grey), the two regions where the string could be presented when it was at variance with the location during the observation phase in the stimulus enhancement tests (thin grey stripes on black) and the adjacent regions where no string was presented (thin black stripes on grey). When testing stimulus enhancement, bees were challenged with a string protruding on the opposite side of one of Plexiglas tables or at 90° compared to the location where it was seen during observational conditioning (dotted lines). Regions were all 16 cm 2 (adjacent areas: 8 x 2 cm; top region 4 x 4 cm). (B) Mean ± s.e. (s) time spent by unsuccessful observer (n = 10) and unsuccessful untrained bees in two of the four regions of interest in their first attempt to retrieve the reward (Test 1) the second attempt (Test 2). Light grey: top of table; dark grey: region where string protruded during observation. Asterisk: Friedman test, p < 0.01; letters and figures: post-hoc Tukey test. (C) Percentage of time spent by observer bees in the four regions of interest when the string was protruding in the region where bees had observed demonstrators (left bar, unsuccessful observers, n = 10) or the region of the table where the string protruded when it was incongruent with that seen from the observation chamber (right bar, bees tested for stimulus enhancement, n = 14). The shades in the various regions of the stacked bars correspond to the shades in Fig 3A (see S1 Data ). 
   
   To examine the local and stimulus enhancement possibilities, we analyzed the video footage to determine the time bees spent in four different regions of the arena (see Fig 3A , Materials and Methods). In Test 2, unsuccessful observers (n = 10, Colony 1) spent more time in the region where the demonstrator was observed (Friedman test, χ 2 3 = 14.160, p = 0.003, Fig 3B ), and untrained bees (n = 23, Colony 1) spent more time on top of the table closest to the flower (Friedman test, χ 2 3 = 35.162, p < 0.001, Fig 3B ) than in Test 1, indicating that local enhancement played a part in learning. None of the bees managed to obtain the reward when the string protruded in an area incongruent with that seen during demonstration. However, the string itself also played a role. If the string protruded from a different side of the table compared to the location during the observation period, observer bees (Test 2, n = 14, Colony 4; S9 Video ) spent more time exploring the region with the string than the region where the demonstrator had been observed (Mann–Whitney U test, U 22 = 105, p = 0.038, Fig 3C ), indicating that observers had noticed the string during the observation period and were thus attracted to it. In theory, however, these longer dwelling times in the string region might be explained by bees randomly exploring the edges of the table and simply stopping at a region that contains any protruding object. To explore this possibility, we also evaluated bees’ first approach flights after being released from the observation chamber before they had a chance of interacting with the string. If the string was in the same location as during observation, 92% of observers flew straight to the side of the string. When the location of the string was incongruent with demonstrator location, only 28.5% of observers first visited the region where the demonstrator had been observed (where chance expectation is 25%). The choice frequencies for the four sides of the table are significantly different depending on whether the string was in the correct location (Chi-square of fit, χ 2 4 = 206.857, p < 0.0001), indicating that bees were able to see the string from the observation chamber and responded differently when it was presented in an unexpected location. However, there was no appreciable attraction to the string when its location was at variance with that seen from the observation chamber (28.5%). Taken together, these results indicate a strong role for local enhancement (bees were attracted to the location where they had observed a demonstrator) and a subordinate role for stimulus enhancement (bees were attracted to the string when its location was concordant with that during prior observation) [ 25 , 46 ]. 
   
   What mechanisms were the observers using to copy the behavior? To answer this question, we explored several associative mechanisms: local enhancement [ 30 , 41 , 42 ], whereby observers are attracted to the location of their conspecific; stimulus enhancement [ 30 , 43 ], an attraction to the item handled by the demonstrator; and perceptual feedback [ 44 , 45 ], a form of trial-and-error learning in which action causing movement of the rewarding object towards the animal produces positive feedback for continuing that action. We found that all three associative mechanisms were involved in the learning of the string pulling process. 
   
   The Spread of String Pulling in a Transmission Chain Experiment 
   
   Can the combination of multiple simple social learning mechanisms mediate the establishment of a culture-like phenomenon (e.g. group-specific behaviors, such as foraging techniques, that are transmitted via social learning and retained in the group over long periods)? We tracked the diffusion of an experimentally introduced string pulling behavior among foragers of test colonies (Colonies 6, 7, 8) to explore the speed of diffusion and also the retention of the technique in the group beyond the demonstration provided by the first knowledgeable individual. To seed the technique, we trained a single demonstrator per colony to pull the string. Subsequently, we allowed pairs of bees to engage with the string pulling task and tracked the diffusion of the technique among the foraging population (Materials and Methods, Fig 4). Pairs of bees were tested in the order in which they arrived in the corridor connecting the hive to the arena; pairs could be any combination of bees regardless of whether they were naïve, the seeded demonstrator, or a successful learner (S12 Video). As a control, foragers of three separate colonies were tested in the same manner without a seeded demonstrator (Colonies 9, 10, 11). 
   
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   larger image TIFF original image Download: Fig 4. Cultural diffusion paradigm. Bees were group-trained to feed from blue flowers in the foraging arena. Three bees were trained to pull a string to obtain an artificial flower from under a table where they would get reward (sucrose solution; see Fig 1A). These three demonstrators were placed in colonies 6, 7, and 8 (one each; seeded colonies), and bees that came out of the colony were paired up in order of exit from the hive to forage within the arena and tested with the string pulling task. Each bout was capped at 5 min, and we recorded 150 foraging bouts (150 bee pairs). In colonies 9, 10, and 11 (control colonies), no trained demonstrator was present. 150 foraging bouts were recorded (150 bee pairs) (see S2 Data). https://doi.org/10.1371/journal.pbio.1002564.g004 
   
   After only 150 paired foraging bouts, a large proportion of each of the test colonies’ forager population (Colony 6: n = 25/47, Colony 7: n = 17/29, Colony 8: n = 12/28) learnt to string pull, whereas none of the control colony foragers (Colony 9, 10, 11: n = 51, 58, 57) learnt to pull the string (Fig 5, Materials and Methods, S13–S18 Videos). We conducted additional foraging bouts in two of the tested colonies and found that the technique continued to spread among the foragers for as long as we allowed the spread to progress (Colony 6: 34/47, Colony 8: 18/28, Fig 5, S13 and S15 Videos). 
   
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   larger image TIFF original image Download: Fig 5. Diffusion of string pulling in bumblebee colonies. (A–F) Nodes represent individual bees. Lines indicate that two bees interacted at least once. Thickness of lines represent total number of interactions between two individuals—one interaction equals one point line thickness and each interaction increases the line thickness by one point. See top insert for indication of line thickness and number of interactions. Size of nodes indicates number of interactions of that individual bee with any other bee—each interaction increases the size of a node by 15% of the original size (3% of the plot width). See middle insert for indication of node size and interactions. Color represents experience (learning “generation”) of that bee: prior to any experience, nodes are grey. After a bee interacts for the first time in the foraging arena, its node turns white. The “seeded” demonstrator (D1), pretrained to pull a string, is marked yellow and at the twelve o’clock position. Once a bee learns to string pull, its node turns from white to another color: orange for a first-order learner (D2, interacting with the seeded demonstrator and lower-order bees); pink for a second-order learner (D3, interacting with first-order and lower-order bees); blue for a third-order learner (D4, interacting with second-order and lower-order bees). See bottom insert for indication of node color and learning generation. Networks for the experiments (A–C) only show interactions within bouts where at least one bee pulled the string at least once. (A) Network for test colony 6 (bout n = 189). (B) Network for test colony 7 (bout n = 114). (C) Network for test colony 8 (bout n = 249). (D) Network for control colony 9 (bout n = 149). (E) Network for control colony 10 (bout n = 150). (F) Network for control colony 11 (bout n = 150) (see S2 Data). https://doi.org/10.1371/journal.pbio.1002564.g005 
   
   We quantified the behavioral changes in learner bees over the time of the diffusion experiments. We first screened 81 of the total 419 available videos (~20%) of the paired bouts between demonstrators and learners and inventoried the repertoire of behavioral interactions. We listed 11 types of interactions (Table 1), the frequency of which changed with increasing experience of the learners (Fig 6). Behaviors went through a series of steps with increasing competence, which typically followed the following sequence. During an observer bee’s first few bouts, she would spend most of her time flying around the arena, occasionally landing on top of the table (NI, No Interaction) and spend little or no time near the table, strings, or the other bee. She would gradually start to land beside a bee who had already pulled a string for reward, thereby gaining reward without pulling a string (Sc, scrounging). The observer thus learns to associate the other bee with reward and typically begins following her around the table, keeping in close contact as they both walk (Fo, following). After one or more occurrences of scrounging, the observer bee would begin to reach under the table, sometimes extending her proboscis towards the flower, seemingly in an attempt to gain access to the flower without manipulating the string. While moving around the edge of the table and trying to reach under it, the observer bee might accidentally move a string, but make no subsequent effort to continue moving it (AMS, Accidentally Moving String). Often the observer bee would then position herself next to the bee already pulling a string. She would be in direct contact with the string pulling bee throughout the pull, usually not touching the string (A, Attending), although in some instances ineffectively manipulating the string (STA, String Touching while Attending), and ultimately gaining reward through the other bee’s efforts. Eventually, while in direct contact with a more knowledgeable bee, the observer bee would pull the string, but not enough to move the flower close enough to the edge of the table, extract it, and obtain the reward (PA, Pulling Action with demonstrator). In this phase, she would still rely on the efforts by the more experienced bee to obtain the reward (RP, Rewarded Pull). After more experience, the observer bee would attempt to pull the string on her own without interacting with the other bee, for example, while the demonstrator was flying around the arena. On the first few attempts to string pull on their own, the observer bees did not move the flower enough to be able to obtain the reward (PAa, Pulling Action alone). Finally, after few unrewarded attempts, and typically when paired with a less knowledgeable bee, the observer bee would learn to pull the string on her own to the point of extracting the flower from underneath the table and gaining reward (RPa, Rewarded Pulling alone) and become a trained observer. 
   
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   larger image TIFF original image Download: Fig 6. Change in learners’ behavioral interactions. Stacked bars represent the proportion of interactions observed as a function of experience (number of paired foraging bouts). Colors indicate behavioral interactions (abbreviations, see Table 1). We evaluated the behavior of 15 randomly selected individuals (5 from each test colony that had been seeded with a trained demonstrator) for these interactions, scrutinizing 174 5-min videos totaling 14.5 h of footage (see S2 Data). https://doi.org/10.1371/journal.pbio.1002564.g006 
   
   These changes in behavior are reflected in the relative frequencies of behavior classes as a function of experience (Fig 6). Whilst nonsocial interactions such as NI and Sc represented more than 55% of the interactions at the onset of the diffusion experiment, they decreased rapidly to 0% over time (Fig 6). In comparison, the percentage of pulling actions displayed by the learners continuously increased with experience from 15% of the interactions at the onset to 60% after 11 bouts. Overall, no major change was observed for the other behavior classes. These results show that learners progressively changed their foraging behaviors from scroungers to competent string pullers. 
   
   In test colonies, on average 2 ± 0.06 string pulls were performed per foraging bout and 20 ± 3.9 pulls were displayed per individual over the whole diffusion experiment. Bees needed to be shown 5 ± 0.45 instances of string pulling by an experienced demonstrator before being able to pull the string themselves without demonstration and subsequently demonstrate the technique. Notably, 15 of 104 foragers (Colony 6, 7, 8: n = 10, 3, 2, respectively) picked up the technique very rapidly after only one or two observations. There was a significant variation between tested colonies in the average number of string pulls displayed per bee (Colony 6, 7, 8: n = 13 ± 4.7, 15.4 ± 9.2, 34.5 ± 7.6, respectively; Kruskal–Wallis test, H 2 = 8.790, p = 0.012) and the number of observations necessary for a bee to learn the technique (Colony 6, 7, 8: n = 4.1 ± 0.4, 7.6 ± 1.1, 5.9 ± 0.9, respectively; Kruskal–Wallis test, H 2 = 17.179, p ≤ 0.001). In addition, some bees did not manage to acquire the technique despite having been shown the same number of string pulling by other bees (5.6 ± 0.7; Mann–Whitney test, U 93 = 1075.5, p = 0.261). These results suggest colony and individual variation in social learning ability. 
   
   To determine whether experience of the second bee influenced the observer bee’s choice of string to pull, we analyzed the pulling behavior of 25 randomly selected observer bees over the complete sequence of their foraging career during the diffusion experiment (282 paired foraging bouts). We found that observer bees more often pulled the same string as the other bee when paired with a more experienced observer bee or the seeded demonstrator (42 RP instances) than when paired with a less experienced bee (9 RP instances). In contrast, observer bees more often pulled a string alone when paired with a less experienced bee (72 RPa instances) than when paired with a more experienced observer bee or a seeded demonstrator (27 RPa instances). 
   
   To test whether bees might cooperate during string pulling, we needed to compare whether experienced bees performed more efficiently when paired with another experienced individual than when foraging alone. Because the diffusion experiment contained only trials with dyads of foragers, the only way to make a direct comparison was to use trials in which an experienced demonstrator was paired with a fully naïve individual that had not shown any pulling action (PA, PAa, RP, or RPa) and thus did not interact or interfere with the skilled forager, who pulled the string singly. Such pairings were compared with instances where both bees were experienced (had already displayed a pulling action). We hypothesized that if cooperation was occurring, strings would be pulled faster and reward obtained quicker in such dyads. However, when paired with an experienced bee, demonstrators (n = 16 randomly chosen individuals) took 2.5 times longer to pull the string and obtain the reward (39.9 ± 9 s) than when the same individual demonstrators were paired with an experienced observer who did not interact or interfere with them (15.6 ± 2.1 s; Wilcoxon test, Z 30 = 3.409, p < 0.001). These results suggest that bees do not cooperate to pull the string but in fact hinder each other’s efforts to some degree. 
   
   Of particular interest for culture-like phenomena is the question of whether a socially learnt behavior routine persists in the population for longer than the original knowledgeable individual can serve as a demonstrator, so that former observers can themselves become demonstrators. If this is the case, then group-specific behavior routines can at least potentially be retained over biological generations. Our network analysis indeed indicates that the technique spread across sequential sets of learners, whereby some bees that learnt the technique never interacted with the seeded demonstrator. In fact, despite the death of the seeded demonstrator in one of the test colonies (Colony 6) after 58 paired foraging bouts, the technique continued to spread among foragers. Moreover we found that there were up to four sequential learning “generations” (as opposed to true biological generations) in two of the three colonies (Fig 5). Learners had string pulling demonstrated to them by up to eight different demonstrators (2.1 ± 0.13), and each demonstrator displayed the technique to 5.3 ± 0.93 learners. Overall, seeded demonstrators displayed eight times more string pulling (119.7 ± 26.5) than the other foragers (14.6 ± 3) (Mann–Whitney, U 68 = 4, p = 0.004) and demonstrated the technique to five times more foragers (19 ± 2.8) than the other foragers (4.2 ± 0.7) (Mann–Whitney, U 36 = 2, p = 0.006). This preponderance of the pretrained demonstrators could be a result of higher motivation simply because they obtained reward with every bout, whereas untrained bees often (in the beginning of the experiment) were unrewarded (i.e., unsuccessful until they were paired with a demonstrator or until they learned to pull the string themselves). 
   
   To test whether string pulling was diffused socially, we performed network-based diffusion analysis (NBDA). We used the time-based approach described by Hoppitt et al [49]. The Aikake Information Criterion (AIC) was used to determine if string pulling was diffused socially by comparing a social and a nonsocial model for each of the diffusion experiments. We found that for all three experiments, social transmission was more likely than asocial transmission (Table 2). 
   
   PPT PowerPoint slide 
   
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   larger image TIFF original image Download: Table 2. Results of network-based diffusion analysis (NBDA). The difference between the fit of the nonsocial model and the fit for the social model is denoted by the change in AIC (ΔAIC). Therefore, positive values indicate a better fit for the social model (p values indicate significance). The social transmission estimate reflects the degree to which social interactions between bees influence the diffusion of string pulling. Positive social transmission estimates that do not cross zero (intervals) indicate significant influence of social interactions. https://doi.org/10.1371/journal.pbio.1002564.t002 
   
   We also analyzed the structure of the social networks using exponential-family random graph modeling [50] and found that for all diffusion experiments as well as the control experiments without a demonstrator bee, the structure of the networks was significantly different from random (see Table 3). This indicates that certain bees were more likely to forage together than other bees. Although this could be interpreted as certain individuals preferentially foraging together, given the open-diffusion paradigm and experimental design (in which bees could not freely distribute themselves in space but were forced through the “bottleneck” of the nest entrance tunnel to the foraging arena), this likely reflects temporal factors such differences in when bees began to forage each day, daily changes in foraging activity across bees, and how long each bee takes to return to foraging from the hive. ||||| Scientists taught bumblebees to pull a string to get a food reward, and then those bees spread the learned technique to others. The groundbreaking study is the first to show that insects have the ability to learn and pass on knowledge and skills. (Reuters) 
   
   The bumblebee brain is puny, at least compared with the massive and fatty organ locked in your skull. At about 0.0002 percent the volume of yours, bee brains are close in size to the seeds stuck on a hamburger bun. Thinking about insect brains in terms of size alone, however, is a trap. The intelligence of sesame-brained bugs should not be underestimated. 
   
   A study reported in the journal PLOS Biology on Tuesday, for instance, takes bee smarts in a surprising direction: Scientists from the Queen Mary University of London suggest that the “insects possess the essential cognitive elements for cultural transmission,” as they wrote in their new paper. It is possible to teach a single bee a new trick, in other words, and a different bee can learn that behavior from her peer. 
   
   That ability is not the only ace found up the clever bee’s sleeves. A recent experiment published in the journal Science, for instance, suggested that bees have their own version of optimism, as The Washington Post reported at the end of September. (Unless they were just buzzed on sugar.) Bees are also capable of an intricate form of communication called a waggle dance, with which they signal the location of nearby food. Every 75 milliseconds a waggle lasts, roughly speaking, indicates to other honeybees that a nectar source is an additional 330 feet further from the colony. 
   
   “Bees have some amazing cognitive abilities,” wrote Clint Perry, a behavioral ecologist at Queen Mary University and an author of the paper, in an email to The Washington Post. They can count, he pointed out, at least up to four. 
   
   It has long been understood that some animals can teach their peers to perform new tasks. But the most famous examples involve stereotypically brainy critters, like primates or ravens: Japanese macaques show other monkeys how to wash sweet potatoes in streams. A certain group of chimps knows to fish for insects by prodding termite mounds with sticks, nibbled into brushes for maximum scoopage. 
   
   [‘Like it’s been nuked’: Millions of bees dead after South Carolina sprays for Zika mosquitoes] 
   
   In their paper, the researchers demonstrate for the first time that a new skill can pass from bee to bee. To that end, they had to teach bumblebees to do something strange, a task the insects would not know how to perform in nature. The scientists turned to a “coiled-string test,” similar to other tests used previously in animal cognition research. 
   
   “We wanted to know whether bees, with a dynamic social structure and the ability to socially learn from each other, might have the basic capacities for cultural transmission of a novel behavior,” Perry said. “And this is what we showed.” 
   
   During the test, a bee needed to extract a blue disc, hidden beneath a clear Plexiglas table, by tugging on a string attached to the puck. These bees had an incentive. The blue disc mimicked a flower, to which the scientists added a tasty drop of sugar water in its center. 
   
   When left to their own devices, however, zero out of 50 bees could figure out how to pull the disc out from under the table. (Given a second chance, two out of 25 managed to figure it out, but they were sluggish tuggers.) 
   
   [As bees vanish, bee heists multiply] 
   
   So the scientists trained a batch of bees in several steps. First they familiarized the animals with the flower mimic, leaving it out in the open. The researchers then tucked the disc progressively further under the table, until the only way for the bee to reach the sugar water would be to yank on the disc’s string. 
   
   The scientists successfully trained 23 of 40 bees. (It took about 5-and-a-quarter hours per bee.) Of the 23 pulling bees, three were selected as demonstrators. The scientists put an untrained bee in a separate cage, and let her watch the demonstrator. Out of these bees, 15 in 25 figured out how to pull on the string. 
   
   [Morning Mix Bees from hive of 800,000 kill Arizona landscaper, injure others] 
   
   Once trained bees were allowed to interact with their colonies, knowledge of the string-pulling behavior spread. In two colonies, the researchers recorded the pulling behavior at four degrees of social separation. In other words, bee D learned to pull the string from bee C, who learned from bee B, who learned from bee A. 
   
   If that is the case, why don’t we see more honey bees dragging strings around the garden? It is not necessarily that insects lack the intelligence, or their undersized brains, wrote Perry’s colleague and co-author Sylvain Alem in an email to The Post. Instead, “the reason we don’t see string-pulling culture in wild bees and other insects is not lack of ability,” the scientist said, “but lack of opportunity and adequate challenges.” 
   
   The takeaway, to hear the scientists tell it, is that “cultural transmission does not require the high cognitive sophistication specific to humans, nor is it a distinctive feature of humans.” Despite our flashcards and our SAT-prep books, we should not feel special in our ability to learn. 
   
   [Bee hotels: One way to help native bees] 
   
   This post has been updated.
target: – Ever wondered how tiny a bumble bee's brain is? Imagine a sesame seed clinging to a burger bun, reports the Washington Post—in other words, it's about 0.0002% the volume of a human brain, as calculated by Science. But that doesn't mean you can't teach a bee a new trick, as behavioral ecologist Clint Perry tells the paper: "Bees have some amazing cognitive abilities," including counting up to at least four. And now he and colleagues from Queen Mary University of London are reporting in the journal Plos Biology that bees can not only learn an entirely new skill to get food but also pass on their knowledge, which is one of the basic aspects of culture. In their study, researchers placed blue discs with sugar water beneath a clear plastic table, just out of reach, but affixed a string to each one that, if tugged, would move it within reach. Out of 110 bumble bees individually introduced to the task, some tugged at the strings before eventually quitting, and only two sorted out how to pull on the string to get the sugar water. However, when bees got to watch the ones retrieving the sugar water, more than 60% of them were able to pull the string when it was their turn. One of the researchers tells Science that, as exciting as the findings are, the explanation isn't necessarily that bees are smart, but that "culturelike phenomena might actually be based on relatively simple mechanisms." (One type of bumblebee has nearly gone extinct in 20 years.)