Does social learning help or hinder adaptive response to human-induced rapid environmental change?

Human-induced rapid environmental change (HIREC), such as climate change, habitat fragmentation, and pollution, poses a potential threat to a variety of wildlife species. If or how it changes animals’ traits is a question of central importance bridging evolutionary ecology and conservation management. Researchers recently explored how social learning can shape organismal responses to HIREC to understand when social learning can be harmful or helpful.

Social learning allows organisms to learn behaviors on a timescale that closely tracks environmental change while minimizing the costs of individual learning. A common assumption in behavioral ecology is that social learning is generally an adaptive way to cope with HIREC by facilitating the rapid spread of innovative responses to change. While this can be true, at the other end of the continuum, social learning can be maladaptive. It may hinder the spread of adaptive responses by causing a carryover of old, formerly adaptive behaviors that slow the response to HIREC or even promote the spread of misinformation and maladaptive behaviors. In order to understand which side of the continuum social learning will fall, researchers highlighted several key components.

To understand a species’ social learning response to HIREC, you need to consider the environment in which the social learning process evolved. Each species’ social learning process is adapted to maximize the transfer of accurate information while minimizing the costs associated with gathering or disseminating the information. This results in certain heuristics, or shortcuts, that allow animals to identify the best type of individual to learn from and which generation to learn from (e.g. parent or a sibling) at a relatively low cognitive cost. For example, black rats (Rattus rattus) learn to prefer foods they’ve smelled on their mothers [1]. This innate social learning strategy allows black rats to avoid the costs associated with learning from their siblings, or other potentially inexperienced, uninformed individuals. In addition to the evolution of these heuristics, a species’ evolutionary environment influences how they transmit information. This is exemplified in the green hylia (Hylia prasina), a small bird found across a wide range of tropical Africa. Regions within this range have different climates, vegetation, and communities of species which impact how noise travels within them. Due to these varying acoustic environments, populations of hylia living in different regions have evolved different songs frequencies to maximize the propagation of their vocalizations [2]. Insight into the evolutionary environment in which a species’ social learning process evolved allows us to understand how the process may be affected in a new, post-HIREC environment.

Ultimately, whether a species’ social learning response to HIREC is adaptive or maladaptive depends on the mismatch between its evolved social learning process and its environment after HIREC. For instance, when the post-HIREC environment does not change the benefits of the evolved heuristics (i.e. who to learn from) or interfere with the information transmission process, social learning can result in the rapid spread of adaptive information. This is often the case when social learners are exposed to novel resources (e.g. human food). In 1921, researchers observed great tits (Parus major) opening the foil top and drinking out of milk bottles at one site in the UK. Twenty-five years later, this innovative behavior had spread to almost 30 different sites. Hinde and Fisher suggested [3], and later research confirmed [4], this rapid spread of adaptive behavior was due to social learning among the great tits. Similarly, social learning is also responsible for the transfer of novel foraging behavior from black bear mothers to their cubs. Cubs learn to scavenge in dumpsters after observing their mothers doing so [5]. In these examples, despite the introduction of a novel food, HIREC did not result in a mismatch between the environment and the social learning process. Instead, the evolved heuristics and transmission processes continued to be adaptive in the post-HIREC environment allowing these animals to take advantage of resources, likely increasing their chance of survival and reproduction.

On the other hand, when HIREC causes a mismatch between the post-HIREC environment and the evolved social learning process it results in a maladaptive behavioral response. For example, bison (Bison bison) follow experienced herd members to find new foraging patches, a type social learning called local enhancement where individuals are attracted the location of others. Historically, bison would avoid areas where wolves, their natural predator, were actively hunting making the presence of conspecifics (i.e. other individuals of the same species) an indicator of both good food and no predators. However, in Prince Albert National Park, this strategy led to a 50% population decline when misinformed individuals led others to agricultural lands where they were killed by farmers, a “predator” the bison had not learned to identify as such [6]. Post-HIREC, the bison’s formerly adaptive social learning process was mismatched to the current environment, because the visual conspecific cue was no longer indicative of a safe place to forage. Other mismatches occur when some aspect of HIREC disrupts the information transmission process. For instance, banded killifish (Fundulus diaphanous) use conspecific chemical cues to identify conspecifics, find food, and learn about the presence of predators. When these fish are exposed to 4-nonylphenol, a contaminant used in the production household products and commonly found in natural systems, they lose the ability to respond to their conspecifics’ chemical cues [7]. Since these fished have evolved to be reliant on social information, loss in the ability to receive information from other individuals will likely result in fewer foraging opportunities and increased susceptibility to predation.

As the number of species impacted by HIREC continues to rise, researchers need to understand how populations, species, and communities will respond to these changes. Given that social learning can have a profound effect on an individual’s ability to survive and reproduce, exploring how social learning interacts with HIREC will be an important part of predicting how animals will cope.

For more information:

Barrett, B.J.**, Zepeda, E.*, Pollack, L., Munson, A*., & Sih, A.*, (2019). Counter-culture: Does social learning help or hinder adaptive response to human-induced rapid environmental change?. Frontiers in Ecology and Evolution, 7. 183. doi:10.3389/fevo.2019.00183

*Denotes an ABGG-affiliated author, **Denotes an ABGG alumnus author

References:

[1] Chou, L.-S., Marsh, R. E., & Richerson, P. J. (2000). Constraints on social transmission of food selection by roof rats, Rattus rattus. Acta Zool. Taiwan. 11, 95–109.

[2] Kirschel, A.N., Blumstein, D.T., Cohen, R.E., Buermann, W., Smith, T.B., & Slabbekoorn, H., (2009). Birdsong tuned to the environment: Green hylia song varies with elevation, tree cover, and noise. Behavioral Ecology, 20(5), 1089-1095.

[3] Hinde, R. A., & Fisher, J. (1951). Further observations on the opening of milk bottles by birds. Br. Birds, 44, 393–396.

[4] Aplin, L. M., Sheldon, B. C., & Morand-Ferron, J. (2013). Milk bottles revisited: social learning and individual variation in the blue tit, Cyanistes caeruleus. Animal Behaviour, 85(6), 1225-1232.

[5] Mazur, R., & Seher, V. (2008). Socially learned foraging behaviour in wild black bears, Ursus americanus. Animal behaviour, 75(4), 1503-1508.

[6] Sigaud, M., Merkle, J.A., Cherry, S.G., Fryxell, J.M., Berdahl, A., & Fortin, D. (2017). Collective decision‐making promotes fitness loss in a fusion‐fission society. Ecology letters, 20(1), 33-40.

[7] Ward, A. J., Duff, A. J., Horsfall, J. S., & Currie, S. (2008). Scents and scentsability: Pollution disrupts chemical social recognition and shoaling in fish. Proc. R. Soc. Lond. B Biol. Sci., 275, 101–105.