Social learning in animals
Social learning refers to learning that is facilitated by observation of, or interaction with, another animal or its products. Social learning has been observed in a variety of animal taxa, such as insects, fish, birds, reptiles, amphibians and mammals (including primates).
Social learning is fundamentally different from individual learning, or asocial learning, which involves learning the appropriate responses to an environment through experience and trial and error. Though asocial learning may result in the acquisition of reliable information, it is often costly for the individual to obtain. Therefore, individuals that are able to capitalize on other individuals' self-acquired information may experience a fitness benefit. However, because social learning relies on the actions of others rather than direct contact, it can be unreliable. This is especially true in variable environments, where appropriate behaviors may change frequently. Consequently, social learning is most beneficial in stable environments, in which predators, food, and other stimuli are not likely to change rapidly.
When social learning is actively facilitated by an experienced individual, it is classified as teaching. Mechanisms of inadvertent social learning relate primarily to psychological processes in the observer, whereas teaching processes relate specifically to activities of the demonstrator. Studying the mechanisms of information transmission allows researchers to better understand how animals make decisions by observing others' behaviors and obtaining information.
Social learning mechanisms
Social learning occurs when one individual influences the learning of another through various processes. In local enhancement and opportunity providing, the attention of an individual is drawn to a specific location or situation. In stimulus enhancement, emulation, observational conditioning, the observer learns the relationship between a stimulus and a result but does not directly copy the behavior of the experienced individual. In imitation, the observer directly copies the behavior of the animal in order to complete a novel task. In emulation, the observer learns a goal from the observed animal’s behavior and seeks to achieve the same results while not following all of the same steps. All of these mechanisms are possible through inadvertent social learning, without active facilitation from the experienced individual. When an individual more actively influences another's behavior through any one of these mechanisms, the individual becomes a teacher.
In local enhancement, a demonstrator attracts an observer's attention to a particular location. One seminal study with guppies (Poecilia reticulata) demonstrated how local enhancement influenced foraging behavior. Untrained adult female guppies (observers) were given five days of experience swimming with demonstrator fish trained to take one of two equivalent routes to food. When these observers were later isolated, they preferentially used the route their demonstrators had used. These results indicate that guppies learn about their local environments through the social learning mechanism of local enhancement.
Local enhancement has also been observed to transmit foraging information in among birds, rats, and pigs.
Opportunity providing is a social learning mechanism in which the experienced individual puts the observer in a situation that facilitates the acquisition of knowledge or a new skill. A well known example of unintentional opportunity providing is the transmission of feeding behavior in black rats (Rattus rattus). One pilot study determined that black rats living in the forests of Israel preferentially fed on pine cones instead of other fresh fruits and vegetation nearby. These rats also methodically stripped pine cones rather than gnawing at them randomly. To determine how these food preferences developed, researchers provided naive adult black rats with fresh pine cones in captivity and observed their behavior. After three months of experimentation, they found that none of the rats had successfully opened the pine cones and had instead haphazardly and inefficiently attempted to feed on the cones. In further experiments, the rats were allowed to observe experienced individuals opening the pine cones but were still unable to pick up the skill of pinecone stripping. Eventually, the researchers determined that naive adult rats could learn to strip pine cones efficiently if presented with an already partially stripped cone. This is consistent with opportunity providing because experienced individuals inadvertently provide naive rats with partially stripped cones that facilitate their learning without altering the experienced rats' behavior.
Opportunity providing has also been found to be important in the acquisition of tool use by chimpanzees, in which a mother chimpanzee may contribute to the development of her offspring's nut cracking technique by leaving "hammer", either hard wood or rocks, and nuts in the nest. The infant is thus given the chance to use the hammer in the “proper” context. The mother chimpanzee may provide this opportunity unknowing or actively depending on the situation.
Stimulus enhancement and observational conditioning
In stimulus enhancement, a demonstrator exposes an observer to a particular stimulus, leading to the observer learning the relationship between a stimulus and its result. A study investigating stimulus enhancement in greylag geese (Anser anser) found that individuals that had previously observed a human opening a box preferentially spent more time investigating the box and attempting to open it via trial and error. These geese were also more successful at eventually opening the box in comparison to control geese that had not previously observed a human opening the box.
Observational conditioning is a phenomenon similar to stimulus enhancement. In observational conditioning, the behavior of the demonstrator exposes the learner to a new relationship between stimuli that it had not previously known, and causes the learner to form an association between them. In an experiment with rhesus macaques (Macaca mulatta), young monkeys that observed their parents fearfully responding to model snakes also developed a fear of snakes without direct contact. After three months, the observer rhesus macaques still showed strong fearful reactions toward snakes, suggesting that they had formed a strong connection from just observing their parents’ behavior. Another example of this is how blackbirds learn to identify predators; they observe other birds mobbing unfamiliar objects they haven't seen before.
Imitation and emulation
Though the exact definition of imitation is a topic of debate within scientific literature, broadly, in imitation a learner observes a unique action performed by the demonstrator and learns to reproduce the behavior with detectable behavior matching. (This differs from "copying" in which the learner reproduces that same action but this is performed with a different part of the body e.g. the left paw is used instead of the right paw.)
Emulation is similar to imitation in that after observing a demonstrator interacting with objects in its environment, an observer is more likely to act to bring about a similar effect on those objects, but not necessarily through the same method. For example, emulation may include using a tool to achieve a goal such as reaching otherwise inaccessible food after observing another to do such a task but using the tool in a different way than the model. The term 'emulation' encompasses a scope of distinct social learning processes, including object movement re-enactment, end-state emulation, and affordance learning. Object movement re-enactment is the extraction and copying of certain steps of a process of a model moving an object. End-state emulation is the copying of the results of a model's actions using the observer's own unique means. Affordance learning deals with the idea that an observer can gain information about physical properties of the environment and objects within it and how those may interact and then use such information to complete a task.
One key distinction between imitation and emulation is copying fidelity. High-fidelity is associated with imitation. In studies comparing behaviors of chimpanzees and human children, the human children were typically shown to perform high-fidelity imitation, what may even be considered 'over-imitation.' Meanwhile chimpanzee responses depended more on context such as causal relevance of actions. Fidelity of behavior copying and transfer reportedly plays a role in cultural transmission, so understanding copying fidelity in non-human animals may be important for understanding their capacity for cultural transmission and cumulative culture.
Much of the research that has been conducted on imitation and emulation in animals has centered around primates due to their advanced cognitive capacities and evolutionary proximity to humans. Examples of studies that have explored these capacities and tendencies in primates are listed in a table within the ‘Research on Imitation and Emulation in Primates’ section below.
Beyond the studies listed, in a naturalistic environment, imitative learning is seen in many animal species. Many species of songbirds learn their songs through imitation, and it has been hypothesized that chimpanzees' understanding of intentionality of action in other members of a social group influences their imitative behaviors.
Imitation of birdsong
As a sexually selected trait, variation in learning of songbird calls is often studied. Lahti et al. performed a study on swamp sparrows (Melospiza georgiana) where young sparrows were exposed to song models with controlled trill rates. Higher trill rates are more difficult to perform and thus are likely more desired in birdsong performance. When exposed to low-performance models, it was found that the learner sparrows sacrificed imitative accuracy for higher performance, while when exposed to high-performance models, imitation was very accurate. The researchers suggest that this study may provide insight into how behaviors learned through imitation can still be selected for due to level of performance.
Sewall explored the variation in learned bird songs in relation to social and genetic intermixing of families of red crossbills (Loxia curvirostra). When given to foster parents, it was shown that fledgling crossbills will imitate the particular variations in their foster parents' calls. It was thus hypothesized that such idiosyncrasies in call could aid in creating familial cohesion and that when such call variants are passed down generations, those variants are direct signals of the crossbill's genetic and familial history.
MacDougall-Shackleton summarized research that suggests developmental stressors affect bird song learning, and that such discrepancies in call can be identified and selected against in some species of birds. He suggests that while many studies have shown that several species of songbirds prefer the song dialect of their local area, current data is lacking in explaining why this is so. It has been argued that genetic factors may play into this preference as well as social learning. In this study, three separate groups of laboratory-raised house finches (Carpodacus mexicanus) were raised hearing the local song dialect, a foreign song dialect, or no song. When adults, all finches showed sexual preference for the local dialect, suggesting an inherited component to song preference.
Visual behavioral imitation
Pigeons are able to learn behaviors that lead to the delivery of a reward by watching a demonstrator pigeon. A demonstrator pigeon was trained to peck a panel in response to one stimulus (e.g. a red light) and hop on the panel in response to a second stimulus (e.g. a green light). After proficiency in this task was established in the demonstrator pigeon, other learner pigeons were placed in a video-monitored observation chamber. After every second observed trial, these learner pigeons were then individually placed in the demonstrator pigeon's box and presented the same test. The learner pigeons displayed competent performance on the task, and thus it was concluded that the learner pigeons had formed a response-outcome association while observing. However, the researchers noted that an alternative interpretation of these results could be that the learner pigeons had instead acquired outcome-response associations that guided their behavior and that further testing was needed to establish if this was a valid alternative.
The performance of opening an artificial fruit after watching a demonstrator was tested in groups of adult pig-tailed macaques (Macaca nemestrina) and compared to adult humans. The macaques showed weak evidence of imitative learning compared to the adult humans. It was hypothesized that because the macaques were adults, they were less likely to imitate than juvenile monkeys, as accurate imitation may be an adaptation that is more useful to juveniles.
Mechanisms for imitative learning
Mechanisms that support imitative learning have been studied on the neurological level. Roberts et al. performed research on zebra finches (Taeniopygia guttata) that explored the importance of neural motor circuitry on birdsong learning. If the premotor nucleus was disrupted while a juvenile finch was learning a song from an older finch, the song was not copied. Images of a finch undergoing various neural manipulations showed that premotor circuits aid in encoding information about songs.
Mirror neurons have been implicated as the link in primate brains between visual observation and motor representation. These special neurons, originally discovered in area F5 of the ventral premotor cortex of monkeys, are activated when an individual performs a certain action and when that individual observes another (human or monkey) performing a similar action. Ferrari, Bonini, and Fogassi worked to explain how the mirror neuron framework could account for imitation of a multiple phenomena with ranging complexities and cognitive demands; they proposed a ‘direct mirror pathway’ for earlier, more automatic imitation and an ‘indirect mirror pathway’ that seems important for more complex and efficient imitative behaviors.
Behavioral mechanisms have also been studied. Cecilia Heyes at the University of Oxford argues that the mechanisms underlying social learning in both humans and nonhumans are analogous to those of non-social learning. Observational learning, then, only becomes social when perceptual, attentional, and motivational factors are focused on other organisms by genetic or developmental forces.
Research on Imitation and Emulation in Primates
In considering imitation and emulation in non-human animals, much of the research has centered around the presence or absence of these abilities in primates. The table below provides an overview of the field of research related to possible imitation and emulation in primates.
|Likely learning mechanism||Positive or negative support||Genus||Behavior(s)||Citation|
|Imitation||Positive||Pongo (Orangutan)||Kiss imitation||Abel (1818) |
|Digging with spade||Furness (1916)|
|Lifting lid of sewage tank||Yerkes and Yerkes (1927)|
|Building nests, feeding habits||Harrison (1960)|
|Flaking stone tools||Wright (1972)|
|Tool use||Galdikas (1982)|
|Macaca (Macaque)||Opening oysters with stones||Carpenter (1887)|
|Plug pulling, lever pressing, box opening||Kinnaman (1902)|
|Botanical collection (assisting experimenter)||Carner (1955)|
|Potato washing, rice throwing, consumption of caramel||Imanishi (1957)|
|Jumping over barrier to avoid electric shock||Presley and Riopelle (1959)|
|Fear response||Miller et al. (1959)|
|Throwing tool at unreachable food||Beck (1976)|
|Reaching food with metal rods||Anderson (1985)|
|Fear of snakes||Cook et al. (1985)|
|Pan (Specifically Chimpanzees)||Door opening, using keys in locks, regulating water supply with lever, scrubbing floor, sweeping with broom||Rothman and Teuber (1915)|
|Opening watch||Shepherd (1915)|
|Digging with spade, screwing screw, scrubbing, sweeping||Furness (1916)|
|Wiping nose with handkerchief, hammering nails, sewing||Sheak (1923)|
|Using paintbrush, stacking boxes to reach banana||Kohler (1925)|
|Washing clothes||Kearton (1925)|
|Brushing hair, opening cupboards||Kellogg and Kellogg (1933)|
|Spitting, imitating facial expressions||Yerkes (1943)|
|Brushing hair, applying lipstick, brushing teeth, sharpening pencils||Hayes (1951)|
|Imitation on command||Hayes and Hayes (1951)|
|Solving stick and tunnel problems, solving stick and string problems, throwing ball||Hayes and Hayes (1952)|
|Patting head, clapping hands, sticking out tongue||Hayes and Hayes (1953)|
|Termite Fishing||van Lawick-Goodall (1973)|
|Cracking nuts with stones, techniques for reaching lower tree branches||Sugiyama and Koman (1979)|
|Limping gait||De Waal (1982)|
|Ant species selection||Nishida and Hiraiwa (1982)|
|Cracking walnuts with stones||Sumita et al. (1985)|
|Sign language||Fouts et al (1989)|
|Play initiation by throwing chips||Tomasello et al. (1989)|
|Trigger light or sound by using head, foot, or sitting (greater imitation when observed was hands free and making unconstrained action)||Buttelmann et al. (2007)|
|Action imitation||Carrasco et al. (2009)|
|Gorilla||Matching moods and play behaviors||Carpenter (1937)|
|Papio (Baboon)||Digging in certain locations||Hall (1963)|
|Fruit cracking with stones||Marais (1969)|
|Fishing||Hamilton and Tilson (1985)|
|Ateles (Spider Monkey)||Putting things in mouth, bell ringing, object examination, bucket interactions||Chevalier-Skolnikoff (1989)|
|Cebus (Capuchin)||Banging objects together, putting tub in moat, putting cloth on branch||Chevalier-Skolnikoff (1989)|
|Negative||Cebus||Box opening||Thorndike (1901)|
|Cracking nuts||Antinucci and Visalberghi (1986)|
|Cracking nuts||Visalberghi (1987)|
|Probing for syrup||Westergaard and Fragaszy (1987)|
|Puzzle solving||Adams-Curtis (1987)|
|Moving reward in tube||Visalberghi and Trinca (1987)|
|Nut cracking, moving reward in tube with stick||Fragaszy and Visalberghi (1989)|
|Papio||Reaching food with tool||Beck (1972)|
|Macaca||Reaching pan using stick||Beck (1974)|
|Emulation||Positive||Pan (Specifically chimpanzees)||Reaching food with tool||Tomasello et al. (1987)|
|Reaching food with tool||Nagell et al. (1993)|
|Tube opening||Call et al. (2005)|
|Accessing food reward from puzzle box (in clear condition when causal vs irrelevant steps could be observed)||Horner and Whiten (2005)|
|Pongo||Reaching food with tool||Call and Tomasello (1994)|
At different life stages
Rats use social learning in a wide range of situations, but perhaps especially so in acquiring food preferences. Learning about suitable foods can be divided into four life stages.
- Before birth: In utero, fetal rats detect odor-bearing particles that come from their mother's diet and cross the placental barrier. Shortly after birth, newborn rats respond positively to these foods.
- During nursing: Nursing rats receive information about their mother's diet through her milk. They prefer the foods she ate during lactation.
- Weaning: When young rats are weaning and eating solid foods for the first time, they use adult rats as guides. They forage where the adults are foraging or where adults have previously scent-marked.
- Adolescence and adulthood: When rats forage on their own, their food choices are influenced by social interactions that may take place far away from foraging sites. They smell foods on the fur, whiskers and especially the breath of other rats and strongly prefer the foods those rats had previously eaten.
Many of the mechanisms involved in inadvertent social learning are also employed during teaching; the distinction is drawn based upon the role of the demonstrator. From the perspective of the pupil, teaching would be identical to its inadvertent social learning equivalent, but in teaching, a tutor actively demonstrates a behavior pattern or draws attention to a location with the specific function of transmitting information to the pupil. An individual must meet three criteria to qualify as a “teacher”: it modifies its behavior only in the presence of a naive observer, it incurs some cost (or at least, no benefit) to itself in doing so, and the naive observer acquires knowledge or skill more rapidly or efficiently than it might otherwise. All of these criteria are rarely met in animals, and only recently have convincing examples been adequately described. Most identified examples have still not been conclusively proven to meet all criteria and primarily serve to suggest that teaching may occur while acknowledging that further research is needed.
Adult killer whales (Orcinus orca) teach the predatory technique of “stranding” to their young. Stranding in these circumstances is a behavior in which a whale temporarily beaches itself to reach prey on land near to the shoreline. Adult whales have been observed helping juveniles with many aspects of this behavior by pushing them up and down the beach, guiding them towards prey, and intervening when the juveniles find themselves in danger. Adults only engage in this behavior with apparently naive juveniles. They are more successful when hunting alone than when teaching juveniles, but case studies suggest that juveniles taught the stranding technique by adults are able to master it more than a year earlier than their non-taught peers.
Coaching appears to occur in other species as well. In domestic chickens, adult hens encourage safe food choices by responding with increased pecking and scratching at palatable food when chicks consume apparently unpalatable food.
Adult meerkats (Suricata suricatta) have been shown to teach pups essential prey-handling skills. Meerkats often consume dangerous prey (such as venomous scorpions) that inexperienced pups appear unable to safely subdue and consume without assistance from older individuals. Adults only display teaching behavior in response to pup begging calls, and adults modify their specific teaching behaviors based upon the age of the pup begging (providing more assistance to younger, presumably less experienced pups). In some instances, providing prey to pups appears costly to adults. Pups are initially unable to find and consume any of their own prey and more rapidly gain predatory abilities through learning experiences from a “teacher”, suggesting that adult teaching facilitates both the speed and efficiency of skill acquisition.
Other species appear to similarly teach their young through the provisioning of weakened or otherwise subdued prey. In both cheetahs and domestic cats, adults catch live prey animals and transport them back to cubs, allowing the cubs to learn and practice hunting skills.
Using local enhancement
Tandem running in ants provides evidence that teaching can occur even without a large brain with complex cognitive abilities. This behavior is shown by an ant who has located a food source in order to guide a naive ant to the desired location. The leading ant only continues the tandem run if the following ant frequently taps on the leader's body, showing that the leader (teacher) modifies its behavior in the presence of the naive follower. Tandem running appears to impose a significant cost on the leader, slowing its speed to ¼ of what it would be if running alone. But the benefit is clear: evidence suggests that followers find food much more quickly through tandem running than from searching alone.
Other evidence of teaching through local enhancement can be seen in a variety of species. In bees, knowledgeable workers perform a waggle dance to guide naive workers to an identified food source. This dance provides information about the direction, distance and quality of the food source. In callitrichid monkeys, adults emit "food-offering" vocalizations only in the presence of infants that appear to indicate the presence of food or discovery of a hidden prey item.
Social learning is a beneficial means to gather information if asocial learning is particularly costly and would increase risk of predation, parasitism, or of expending unnecessary energy. In these types of scenarios, social learners may observe the behaviors of an experienced individual. This allows the observer to gain information about the environment without individually being put at risk.
Learning about predators
An animal generally learns its natural predators through direct experience. Thus, predator learning is very costly and increases the predation risk for each individual. In group learning scenarios, a few members can experience the danger of predation and transmit this acquired predator recognition throughout the group. Consequently, in future encounters, the entire group can recognize the threat of predation and respond accordingly. This social learning method has been shown in group mobbing behavior in the common blackbird (Turdus merula). Blackbird groups were more likely to mob an object if a member of the group had previously been conditioned to recognize it as a predator. This behavior has also been recorded in guppies, where naive guppies from environments with less natural predators significantly improved their anti-predator behavior when placed in a group with guppies from a high predation environment.
Learning about brood parasites
Learning about brood parasites through direct experience can also be costly and error-prone. Birds can actively defend themselves against brood parasitism from cuckoos and cowbirds via a variety of behaviors, including mobbing, and these too can be socially learned. For example, a study on Eurasian reed warblers (Acrocephalus scirpaceus) showed that individuals that observed their neighbors mob of common cuckoo (Cuculus canorus) were subsequently more likely to mob cuckoos but not harmless controls. These results indicate that social learning provides a mechanism by which hosts can rapidly increase their nest defense against brood parasites, enabling the hosts to track fine-scale spatiotemporal variation in the local risk of brood parasitism.
Learning about foraging opportunities
Social learning also provides individuals with information about food sources in an environment. This can include information on where to find food, what to eat, and how to eat it. There are several examples in the animal kingdom in which animals utilize social learning to find food. For example, birds are more likely to forage in areas where they already see birds feeding. The Norway rat (Rattus norvegicus) also utilizes social learning behaviors to find food sources. Mature rats leave sensory trails to and from food sources that are preferentially followed by naive pups. Animals can also learn what to eat from social learning with conspecifics. Experimentally discerning harmful foods from edible foods can be dangerous for a naive individual; however, inexperienced individuals can avoid this cost through observing older individuals that already have acquired this knowledge. For example, several species of bird will avoid food if they see another individual eat it and become ill. Observation can also educate the observer about how to eat particular foods. Red squirrels (Sciurus vulgaris) have been shown to more successfully open hickory nuts after watching more experienced squirrels open the nuts.
Social learning does not necessarily mean that the transmitted behavior is the most efficient response to a stimulus. If a socially learned behavior expends unnecessary energy, and there is a more efficient strategy that is not being utilized, employing social learning is maladaptive. This has been experimentally demonstrated in guppies. After a group of guppies was trained to swim a more energetically costly route to food, naive guppies were added to the group. These new members were more likely to follow the larger group even if a shorter, more effective route was provided; however, if the naive guppies were not introduced to the trained individuals, they preferentially used the more efficient route to the food source. Norway rats have been shown to abandon previously individually learned habits due to the actions of conspecifics. Rats modified established aversions to certain foods if they observed conspecifics eating those same foods. If this previous aversion was formed for adaptive reasons (i.e. the food was nutrient-poor), reversion to consumption of this food source could reduce the fitness of the individual. More theoretically, social learning can become maladaptive after a certain point in animal populations. If there are more social learners than asocial learners in a particular group, the information transferred between individuals is less likely to be reliable. This could result in maladaptive information transfer to social learners, decreasing the fitness for social learners in comparison to that of asocial learners. Therefore, social learning is only an adaptive strategy if the number of individual learners is equal to or greater than the number of social learners.
When many individuals residing within the same area employ social learning, local traditions can be formed and cultural transmission can occur. These learned behavior complexes shared by individuals appear in the population generation after generation and persist in the behavioral repertoire of individual organisms even following removal from the immediate learning situation. One of the most commonly recognized examples of tradition in animals is found in songbirds, in which the same song pattern is transmitted from generation to generation by vocal imitation. Even "alien" syllable types not produced by their biological parents can be learned by finches raised by foster canaries in the lab.
If copying errors are common, or if each observer adds individually learned modifications to a new behavior pattern, stable traditions are unlikely to develop and persist over time. However, even when no longer adaptive, traditions can be passed down if individuals learn primarily through observing experienced individuals rather than through asocial learning techniques. This was observed in guppies in the laboratory, in the group foraging example explained above. Even when the originally trained “founder” guppies were removed from the group and only initially naive individuals (trained by the founders) were present, the tradition persisted and new guppies learned the costly path. Socially learning the more costly route also resulted in slower learning of the more efficient route when it was subsequently presented, suggesting that even maladaptive strategies can be socially learned and incorporated into local traditions.
- Hoppitt, William; Laland, Kevin N. (2013). Social Learning: An Introduction to Mechanisms, Methods, and Models. Princeton University Press. ISBN 978-1-4008-4650-4.[page needed]
- Galef, Bennett G.; Laland, Kevin N. (2005). "Social learning in animals: Empirical studies and theoretical models". BioScience. 55 (6): 489. doi:10.1641/0006-3568(2005)055[0489:SLIAES]2.0.CO;2.
- Galef, Bennett G.; Giraldeau, Luc-Alain (2001). "Social influences on foraging in vertebrates: Causal mechanisms and adaptive functions". Animal Behaviour. 61 (1): 3–15. doi:10.1006/anbe.2000.1557. PMID 11170692. S2CID 38321280.
- Alem, Sylvain; Perry, Clint J.; Zhu, Xingfu; Loukola, Olli J.; Ingraham, Thomas; Søvik, Eirik; Chittka, Lars (2016-10-04). "Associative Mechanisms Allow for Social Learning and Cultural Transmission of String Pulling in an Insect". PLOS Biology. 14 (10): e1002564. doi:10.1371/journal.pbio.1002564. ISSN 1545-7885. PMC 5049772. PMID 27701411.
- Brown, Culum; Kevin Laland (2003). "Social Learning in Fishes: A review". Fish and Fisheries. 4 (3): 280–288. doi:10.1046/j.1467-2979.2003.00122.x.
- Slagsvold, Tore; Wiebe, Karen L. (2011-04-12). "Social learning in birds and its role in shaping a foraging niche". Philosophical Transactions of the Royal Society of London B: Biological Sciences. 366 (1567): 969–977. doi:10.1098/rstb.2010.0343. ISSN 0962-8436. PMC 3049099. PMID 21357219.
- Ferrari, Maud C. O.; Messier, François; Chivers, Douglas P. (June 2007). "First Documentation of Cultural Transmission of Predator Recognition by Larval Amphibians". Ethology. 113 (6): 621–627. doi:10.1111/j.1439-0310.2007.01362.x. ISSN 0179-1613.
- Whiten, Andrew; van de Waal, Erica (November 2017). "Social learning, culture and the 'socio-cultural brain' of human and non-human primates". Neuroscience & Biobehavioral Reviews. 82: 58–75. doi:10.1016/j.neubiorev.2016.12.018. hdl:10023/12387. ISSN 0149-7634. PMID 28034660. S2CID 32051.
- Metz, Alexander; Shultz, Thomas R. (2010). "Spatial Factors of Social and Asocial Learning". In Ohlsson, Stellan; Catrambone, Richard (eds.). Proceedings of the 32nd Annual Conference of the Cognitive Science Society. pp. 1685–90.
- Kendal, Rachel L.; Coolen, Isabelle; Van Bergen, Yfke; Laland, Kevin N. (2005). "Trade‐Offs in the Adaptive Use of Social and Asocial Learning". Advances in the Study of Behavior. Vol. 35. pp. 333–79. doi:10.1016/S0065-3454(05)35008-X. ISBN 978-0-12-004535-8.
- Kameda, Tatsuya; Nakanishi, Daisuke (2002). "Cost–benefit analysis of social/cultural learning in a nonstationary uncertain environment". Evolution and Human Behavior. 23 (5): 373–93. doi:10.1016/S1090-5138(02)00101-0.
- Hoppitt, W; Brown, G; Kendal, R; Rendell, L; Thornton, A; Webster, M; Laland, K (2008). "Lessons from animal teaching". Trends in Ecology & Evolution. 23 (9): 486–93. doi:10.1016/j.tree.2008.05.008. PMID 18657877.
- Reader, Simon; Kendal, Jeremy; Laland, Kevin (2003). "Social learning of foraging sites and escape routes in wild Trinidadian guppies". Animal Behaviour. 66 (4): 729–739. doi:10.1006/anbe.2003.2252. S2CID 53169300.
- Aisner, R.; Terkel, J. (1992). "Ontogeny of pine cone opening behaviour in the black rat, Rattus rattus". Animal Behaviour. 44: 327–36. doi:10.1016/0003-3472(92)90038-B. S2CID 53148456.
- Terkel, Joseph (1996). "Cultural Transmission of Feeding Behavior in the Black Rat (Rattus rattus)". In Heyes, Cecilia M.; Galef, Bennett G. (eds.). Social Learning In Animals: The Roots of Culture. Elsevier. pp. 17–47. ISBN 978-0-08-054131-0.
- Hirata, Satoshi; Celli, Maura L. (2003). "Role of mothers in the acquisition of tool-use behaviours by captive infant chimpanzees". Animal Cognition. 6 (4): 235–44. doi:10.1007/s10071-003-0187-6. PMID 13680401. S2CID 362220.
- Fritz, Johannes; Bisenberger, Agnes; Kotrschal, Kurt (2000). "Stimulus enhancement in greylag geese: Socially mediated learning of an operant task". Animal Behaviour. 59 (6): 1119–1125. doi:10.1006/anbe.2000.1424. PMID 10877890. S2CID 20465133.
- Mineka, Susan; Davidson, Mark; Cook, Michael; Keir, Richard (1984). "Observational conditioning of snake fear in rhesus monkeys". Journal of Abnormal Psychology. 93 (4): 355–72. doi:10.1037/0021-843X.93.4.355. PMID 6542574.
- Curio, E.; Ernst, U.; Vieth, W. (1978). "Cultural Transmission of Enemy Recognition: One Function of Mobbing". Science. 202 (4370): 899–901. Bibcode:1978Sci...202..899C. doi:10.1126/science.202.4370.899. PMID 17752463. S2CID 33299917.
- Whiten, Andrew; McGuigan, Nicola; Marshall-Pescini, Sarah; Hopper, Lydia M. (2009-08-27). "Emulation, imitation, over-imitation and the scope of culture for child and chimpanzee". Philosophical Transactions of the Royal Society B: Biological Sciences. 364 (1528): 2417–2428. doi:10.1098/rstb.2009.0069. ISSN 0962-8436. PMC 2865074. PMID 19620112.
- Call, Josep; Carpenter, Malinda; Tomasello, Michael (July 2005). "Copying results and copying actions in the process of social learning: chimpanzees (Pan troglodytes) and human children (Homo sapiens)". Animal Cognition. 8 (3): 151–163. doi:10.1007/s10071-004-0237-8. ISSN 1435-9448. PMID 15490290. S2CID 17599865.
- Horner, Victoria; Whiten, Andrew (July 2005). "Causal knowledge and imitation/emulation switching in chimpanzees (Pan troglodytes) and children (Homo sapiens)". Animal Cognition. 8 (3): 164–181. doi:10.1007/s10071-004-0239-6. ISSN 1435-9448. PMID 15549502. S2CID 1949770.
- Call, Josep (2009). "Contrasting the Social Cognition of Humans and Nonhuman Apes: The Shared Intentionality Hypothesis". Topics in Cognitive Science. 1 (2): 368–379. doi:10.1111/j.1756-8765.2009.01025.x. PMID 25164939.
- Lahti, David C.; Moseley, Dana L.; Podos, Jeffrey (2011). "A Tradeoff Between Performance and Accuracy in Bird Song Learning". Ethology. 117 (9): 802–811. doi:10.1111/j.1439-0310.2011.01930.x.
- Sewall, Kendra B. (2011). "Early learning of discrete call variants in red crossbills: implications for reliable signaling". Behavioral Ecology and Sociobiology. 65 (2): 157–166. doi:10.1007/s00265-010-1022-0. PMC 6191197. PMID 30337770.
- MacDougall-Shackleton, Scott A. (2009). "The importance of development: What songbirds can teach us". Canadian Journal of Experimental Psychology. 63 (1): 74–79. doi:10.1037/a0015414. PMID 19271818.
- Hernandez, Alexandra M.; MacDougall-Shackleton, Scott A. (2004). "Effects of early song experience on song preferences and song control and auditory brain regions in female house finches (Carpodacus mexicanus)". Journal of Neurobiology. 59 (2): 247–258. doi:10.1002/neu.10312. PMID 15085541.
- Saggerson, A. L.; George, David N.; Honey, R. C. (2005). "Imitative Learning of Stimulus-Response and Response-Outcome Associations in Pigeons" (PDF). Journal of Experimental Psychology: Animal Behavior Processes. 31 (3): 289–300. doi:10.1037/0097-7403.31.3.289. PMID 16045384.
- Custance, Deborah; Prato-Previde, Emanuela; Spiezio, Caterina; Rigamonti, Marco M.; Poli, Marco (2006). "Social learning in pig-tailed macaques (Macaca nemestrina) and adult humans (Homo sapiens) on a two-action artificial fruit". Journal of Comparative Psychology. 120 (3): 303–313. doi:10.1037/0735-7036.120.3.303. PMID 16893268.
- Roberts, Todd F.; Gobes, Sharon M. H.; Murugan, Malavika; Ölveczky, Bence P.; Mooney, Richard (2012). "Motor circuits are required to encode a sensory model for imitative learning". Nature Neuroscience. 15 (10): 1454–1459. doi:10.1038/nn.3206. PMC 3458123. PMID 22983208.
- Rizzolatti, Giacomo; Fogassi, Leonardo; Gallese, Vittorio (September 2001). "Neurophysiological mechanisms underlying the understanding and imitation of action". Nature Reviews Neuroscience. 2 (9): 661–670. doi:10.1038/35090060. ISSN 1471-003X. PMID 11533734. S2CID 6792943.
- Ferrari, P. F.; Bonini, L.; Fogassi, L. (2009-08-27). "From monkey mirror neurons to primate behaviours: possible 'direct' and 'indirect' pathways". Philosophical Transactions of the Royal Society B: Biological Sciences. 364 (1528): 2311–2323. doi:10.1098/rstb.2009.0062. ISSN 0962-8436. PMC 2865083. PMID 19620103.
- Heyes, Cecilia (2012). "What's social about social learning?". Journal of Comparative Psychology. 126 (2): 193–202. CiteSeerX 10.1.1.401.6757. doi:10.1037/a0025180. PMID 21895355.
- Abel, Clarke (1818). Narrative of a Journey in the Interior of China. Longman, Hurst, Rees, Orme, and Brown.
- Furness, William H. (1916). "Observations on the Mentality of Chimpanzees and Orang-Utans". Proceedings of the American Philosophical Society. 55 (3): 281–290. ISSN 0003-049X. JSTOR 984118.
- Harrisson, Barbara (1962). "A STUDY OF ORANG‐UTAN BEHAVIOUR IN THE 1959‐60". International Zoo Yearbook. 3 (1): 57–68. doi:10.1111/j.1748-1090.1962.tb03396.x. ISSN 1748-1090.
- Wright, R. V. S. (2009-02-10). "Imitative Learning of a Flaked Stone Technology-The Case of an Orangutan". Mankind. 8 (4): 296–306. doi:10.1111/j.1835-9310.1972.tb00451.x.
- Galdikas, Biruté M.F. (January 1982). "Orang-utan tool-use at Tanjung Puting Reserve, Central Indonesian Borneo (Kalimantan Tengah)". Journal of Human Evolution. 11 (1): 19–33. doi:10.1016/S0047-2484(82)80028-6.
- Carpenter, Alfred (May 1887). "Monkeys opening Oysters". Nature. 36 (916): 53. Bibcode:1887Natur..36...53C. doi:10.1038/036053d0. ISSN 0028-0836. S2CID 4112014.
- Kinnaman, A. J. (April 1902). "Mental Life of Two Macacus rhesus Monkeys in Captivity. II". The American Journal of Psychology. 13 (2): 173–218. doi:10.2307/1412738. JSTOR 1412738.
- Carner, R (1955). "Botanical Collecting with Monkeys". Proc. Roy. Instil. 36.
- Imanishi, Kinji (March 1957). "Identification : A process of enculturation in the subhuman society ofMacaca fuscata". Primates. 1 (1): 1–29. doi:10.1007/BF01667196. ISSN 0032-8332. S2CID 30040660.
- Presley, W. J.; Riopelle, A. J. (December 1959). "Observational Learning of an Avoidance Response". The Journal of Genetic Psychology. 95 (2): 251–254. doi:10.1080/00221325.1959.10534265. ISSN 0022-1325. PMID 14434758.
- Miller, Robert E.; Murphy, John V.; Mirsky, I. Arthur (1959). "Non-verbal communication of affect". Journal of Clinical Psychology. 15 (2): 155–158. doi:10.1002/1097-4679(195904)15:2<155::AID-JCLP2270150211>3.0.CO;2-P. ISSN 1097-4679. PMID 13631102.
- Beck, Benjamin B. (July 1976). "Tool use by captive pigtailed macaques". Primates. 17 (3): 301–310. doi:10.1007/bf02382787. ISSN 0032-8332. S2CID 35080987.
- Anderson, James R. (November 1985). "Development of tool-use to obtain food in a captive group of Macaca tonkeana". Journal of Human Evolution. 14 (7): 637–645. doi:10.1016/S0047-2484(85)80072-5.
- Cook, Michael; Mineka, Susan; Wolkenstein, Bonnie; Laitsch, Karen (1985). "Observational conditioning of snake fear in unrelated rhesus monkeys". Journal of Abnormal Psychology. 94 (4): 591–610. doi:10.1037/0021-843X.94.4.591. ISSN 1939-1846. PMID 4078162.
- Rothman, M; Teuber, E (1915). Einzelausgabe aus der Anthropoidenstaton auf Teneriffa. Ziele und Aufgaben der Station sowie rste Beobachtungen an den auf ihr gehaltenen Schimpansen. Berlin: Abh Preuss. pp. 1–20.
- Shepherd, W. T. (1915). "Some observations on the intelligence of the chimpanzee". Journal of Animal Behavior. 5 (5): 391–396. doi:10.1037/h0070497. ISSN 0095-9928.
- Sheak, W.H. (1923). "Anthropoid apes I have known". Natural History. 23: 45–55.
- Köhler, Wolfgang (1925). The Mentality of Apes. Harcourt, Brace.
- Kearton, Cherry (1925). My friend Toto: The adventures of a chimpanzee and the story of his journey from the Congo to London. London: Arrowsmith.
- Kellogg, WN; Kellogg, LA (1933). The Ape and the Child: A Study of Environmental Influence Upon Early Behaviour. Whittlesey House.
- Yerkes, R. M. (1943). Chimpanzees: a laboratory colony. New Haven: Yale University Press.
- Hayes, Cathy (1951). The Ape in Our House. Harper.
- Hayes, Keith J.; Hayes, Catherine (1951). "The Intellectual Development of a Home-Raised Chimpanzee". Proceedings of the American Philosophical Society. 95 (2): 105–109. ISSN 0003-049X. JSTOR 3143327.
- Hayes, Keith J.; Hayes, Catherine (1952). "Imitation in a home-raised chimpanzee". Journal of Comparative and Physiological Psychology. 45 (5): 450–459. doi:10.1037/h0053609. ISSN 0021-9940. PMID 13000013.
- Hayes, Keith J.; Hayes, Catherine (1953). "Picture perception in a home-raised chimpanzee". Journal of Comparative and Physiological Psychology. 46 (6): 470–474. doi:10.1037/h0053704. ISSN 0021-9940. PMID 13109075.
- van Lawick-Goodall, Jane (1973). "Cultural elements in a chimpanzee community". Precultural Primate Behavior: 144–184.
- Sugiyama, Yukimaru; Koman, Jeremy (October 1979). "Tool-using and -making behavior in wild chimpanzees at Bossou, Guinea". Primates. 20 (4): 513–524. doi:10.1007/BF02373433. ISSN 0032-8332. S2CID 22621124.
- Waal, Frans de; Waal, Frans B. M. (2000-04-10). Chimpanzee Politics: Power and Sex Among Apes. JHU Press. ISBN 978-0-8018-6336-3.
- Nishida, Toshisada; Uehara, Shigeo (October 1980). "Chimpanzees, Tools, and Termites: Another Example From Tanzania". Current Anthropology. 21 (5): 671–672. doi:10.1086/202545. ISSN 0011-3204. S2CID 145349296.
- Sumita, Kyoko; Kitahara-Frisch, Jean; Norikoshi, Kohshi (April 1985). "The acquisition of stone-tool use in captive chimpanzees". Primates. 26 (2): 168–181. doi:10.1007/BF02382016. ISSN 0032-8332. S2CID 25897929.
- Gardner, R. Allen; Gardner, Beatrix T.; Cantfort, Thomas E. Van (1989-01-01). Teaching Sign Language to Chimpanzees. SUNY Press. ISBN 978-0-88706-965-9.
- Tomasello, Michael; Gust, Deborah; Frost, G. Thomas (January 1989). "A longitudinal investigation of gestural communication in young chimpanzees". Primates. 30 (1): 35–50. doi:10.1007/BF02381209. ISSN 0032-8332. S2CID 21156104.
- Buttelmann, David; Carpenter, Malinda; Call, Josep; Tomasello, Michael (July 2007). "Enculturated chimpanzees imitate rationally". Developmental Science. 10 (4): F31–F38. doi:10.1111/j.1467-7687.2007.00630.x. ISSN 1363-755X. PMID 17552931.
- Carrasco, Lara; Posada, Sandra; Colell, Montserrat (2009). "New evidence on imitation in an enculturated chimpanzee (Pan troglodytes)". Journal of Comparative Psychology. 123 (4): 385–390. doi:10.1037/a0016275. ISSN 1939-2087. PMID 19929107.
- Carpenter, Clarence Ray (1937). "An Observational Study of Two Captive Mountain Gorillas (Gorilla Beringei)". Human Biology. 9: 175–200 – via ProQuest.
- Hall, K. R. L. (August 1963). "Observational Learning in Monkeys and Apes". British Journal of Psychology. 54 (3): 201–226. doi:10.1111/j.2044-8295.1963.tb00877.x. PMID 14051442.
- Marais, Eugène Nielen (1990). The Soul of the Ape. Penguin Books. ISBN 978-0-14-012848-2.
- Hamilton, W. J.; Tilson, R. L. (1985). "Fishing baboons at desert waterholes". American Journal of Primatology. 8 (3): 255–257. doi:10.1002/ajp.1350080308. ISSN 0275-2565. PMID 31986808. S2CID 84278221.
- Chevalier-Skolnikoff, Suzanne (September 1989). "Spontaneous tool use and sensorimotor intelligence in Cebus compared with other monkeys and apes". Behavioral and Brain Sciences. 12 (3): 561–588. doi:10.1017/S0140525X00057678. ISSN 0140-525X. S2CID 145467809.
- Thorndike, Edward L. (1901). The mental life of the monkeys by Edward L. Thorndike: This Monograph is also Vol. IX, No. 1, of Columbia University Contributions to Philosophy, Psychology and Education. Macmillan.
- Antinucci, Francesco; Visalberghi, Elisabetta (August 1986). "Tool use inCebus apella: A case study". International Journal of Primatology. 7 (4): 351–363. doi:10.1007/bf02693700. ISSN 0164-0291. S2CID 23901545.
- Visalberghi, Elisabetta (1987). "Acquisition of Nut-Cracking Behaviour by 2 Capuchin Monkeys (Cebus apella)". Folia Primatologica. 49 (3–4): 168–181. doi:10.1159/000156320. ISSN 1421-9980.
- Westergaard, Gregory C.; Fragaszy, Dorothy M. (1987). "The manufacture and use of tools by capuchin monkeys (Cebus apella)". Journal of Comparative Psychology. 101 (2): 159–168. doi:10.1037/0735-7036.101.2.159. ISSN 0735-7036.
- Adams-Curtis, L.E. (1987). "Social context of manipulative behaviour in Cebus apella". American Journal of Primatology. 12: 325.
- Visalberghi, Elisabetta; Trinca, Loredana (October 1989). "Tool use in capuchin monkeys: Distinguishing between performing and understanding". Primates. 30 (4): 511–521. doi:10.1007/bf02380877. ISSN 0032-8332. S2CID 19285572.
- Fragaszy, Dorothy M.; Visalberghi, Elisabetta (1989). "Social influences on the acquisition of tool-using behaviors in tufted capuchin monkeys (Cebus apella)". Journal of Comparative Psychology. 103 (2): 159–170. doi:10.1037/0735-7036.103.2.159. ISSN 1939-2087. PMID 2736909.
- Beck, Benjamin B. (September 1972). "Tool use in captive hamadryas baboons". Primates. 13 (3): 277–295. doi:10.1007/bf01730574. ISSN 0032-8332. S2CID 42897869.
- Beck, Benjamin B. (November 1974). "Baboons, chimpanzees, and tools". Journal of Human Evolution. 3 (6): 509–516. doi:10.1016/0047-2484(74)90011-6. ISSN 0047-2484.
- Tomasello, M.; Davis-Dasilva, M.; Camak, L.; Bard, K. (April 1987). "Observational learning of tool-use by young chimpanzees". Human Evolution. 2 (2): 175–183. doi:10.1007/bf02436405. ISSN 0393-9375. S2CID 84211164.
- Nagell, Katherine; Olguin, Raquel S.; Tomasello, Michael (1993). "Processes of social learning in the tool use of chimpanzees (Pan troglodytes) and human children (Homo sapiens)". Journal of Comparative Psychology. 107 (2): 174–186. doi:10.1037/0735-7036.107.2.174. ISSN 1939-2087. PMID 8370271.
- Call, J.; Tomasello, M. (October 1994). "The social learning of tool use by orangutans (Pongo pygmaeus)". Human Evolution. 9 (4): 297–313. doi:10.1007/bf02435516. ISSN 0393-9375. S2CID 84534346.
- Hanson, Anne (2012). "How do rats choose what to eat?". Rat behavior and biology. Retrieved 24 August 2014.
- Caro, TM; Hauser, MD (1992). "Is there teaching in nonhuman animals?". The Quarterly Review of Biology. 67 (2): 151–74. doi:10.1086/417553. JSTOR 2831436. PMID 1635977. S2CID 40567375.
- Bauer, Gordon B.; Harley, Heidi E. (2001). "The mimetic dolphin". Behavioral and Brain Sciences. 24 (2): 326–7. doi:10.1017/S0140525X01243969. S2CID 144947666.
- Nicol, Christine J.; Pope, Stuart J. (1996). "The maternal feeding display of domestic hens is sensitive to perceived chick error". Animal Behaviour. 52 (4): 767. doi:10.1006/anbe.1996.0221. S2CID 53162892.
- Thornton, A.; McAuliffe, K (2006). "Teaching in Wild Meerkats". Science. 313 (5784): 227–9. Bibcode:2006Sci...313..227T. doi:10.1126/science.1128727. PMID 16840701. S2CID 11490465.
- Franks, Nigel R.; Richardson, Tom (2006). "Teaching in tandem-running ants". Nature. 439 (7073): 153. Bibcode:2006Natur.439..153F. doi:10.1038/439153a. PMID 16407943. S2CID 4416276.
- Kelley, Jennifer L.; Evans, Jonathan P.; Ramnarine, Indar W.; Magurran, Anne E. (2003). "Back to school: Can antipredator behavior in guppies be enhanced through social learning?". Animal Behaviour. 65 (4): 655–62. doi:10.1006/anbe.2003.2076. S2CID 53186108.
- Davies, N. B.; Welbergen, J. A. (2009). "Social Transmission of a Host Defense Against Cuckoo Parasitism". Science. 324 (5932): 1318–1320. Bibcode:2009Sci...324.1318D. doi:10.1126/science.1172227. PMID 19498167. S2CID 206519140.
- Welbergen, J.A; Davies, N.B (2009). "Strategic variation in mobbing as a front line of defense against brood parasitism". Current Biology. 19 (3): 235–240. doi:10.1016/j.cub.2008.12.041. PMID 19185495.
- Galef, Bennett G. (1982). "Studies of social learning in norway rats: A brief review". Developmental Psychobiology. 15 (4): 279–95. doi:10.1002/dev.420150402. PMID 7049794.
- Griffin, A. S. (2004). "Social learning about predators: A review and prospectus". Animal Learning & Behavior. 32 (1): 131–40. doi:10.3758/BF03196014. PMID 15161148.
- Laland, Kevin N.; Williams, Kerry (1998). "Social transmission of maladaptive information in the guppy". Behavioral Ecology. 9 (5): 493–9. doi:10.1093/beheco/9.5.493.
- Galef, Bennett G. (1986). "Social interaction modifies learned aversions, sodium appetite, and both palatability and handling-time induced dietary preference in rats (Rattus norvegicus)". Journal of Comparative Psychology. 100 (4): 432–9. doi:10.1037/0735-7036.100.4.432. PMID 3802787.
- Rendell, Luke; Fogarty, Laurel; Laland, Kevin N. (2010). "Rogers' Paradox Recast and Resolved: Population Structure and the Evolution of Social Learning Strategies". Evolution. 64 (2): 534–48. doi:10.1111/j.1558-5646.2009.00817.x. PMID 19674093.
- Giraldeau, L.-A.; Valone, T. J.; Templeton, J. J. (2002). "Potential disadvantages of using socially acquired information". Philosophical Transactions of the Royal Society B: Biological Sciences. 357 (1427): 1559–66. doi:10.1098/rstb.2002.1065. PMC 1693065. PMID 12495513.
- Mundinger, Paul C. (1980). "Animal cultures and a general theory of cultural evolution". Ethology and Sociobiology. 1 (3): 183–233. doi:10.1016/0162-3095(80)90008-4.