Animal Cultures Matter for Conservation on March 21, 2019 Understanding the Rich Social Lives of Animals Benefits International Conservation Efforts

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Animal cultures matter for conservation on March 21, 2019 Understanding the rich social lives of animals benefits international conservation efforts

By Philippa Brakes, Sasha R. X. Dall, Lucy M. Aplin, Stuart Bearhop, Emma L. Carroll, Paolo Ciucci, Vicki Fishlock, John K. B. Ford, Ellen C. Garland, Sally A. Keith, Peter K. McGregor, Sarah L. Mesnick, Michael J. Noad, Giuseppe Notarbartolo di Sciara, Martha M. Robbins, Mark P. Simmonds, Fernando Spina, Alex Thornton, Paul R. Wade, Martin J. Whiting, James Williams, Luke Rendell, Hal Whitehead, Andrew Whiten, Christian Rutz

nimal culture, defined as “informa- and other aspects of sociality (3) is now af- CONSEQUENCES OF SOCIAL KNOWLEDGE tion or behavior—shared within a fording critical insights into what should An important aspect of social learning is community—which is acquired from be conserved (going beyond the protection the speed with which new behaviors can po- conspecifics through some form of of genetic diversity, to consider adaptive tentially spread through populations, with social learning” (1), can have impor- aspects of phenotypic variation), and why effects that may be positive (e.g., adaptive tant consequences for the survival specific conservation programs succeed exploitation of a new food source) or nega- Aand reproduction of individuals, social (e.g., through facilitating the resilience of tive (e.g., increasing conflict with humans, groups, and potentially, entire populations cultural diversity) while others fail (e.g., such as when sperm whales learn to remove (1, 2). Yet, until recently, conservation strat- by neglecting key repositories of socially fish from longlines) (2). Transmission can egies and policies have focused primarily transmitted knowledge). Here, we high- be mediated by an inherent propensity to on broad demographic responses and the light how international legal instruments, adopt innovations [e.g., “lobtail” feeding in preservation of genetically defined, evolu- such as the Convention on the Conserva- humpback whales (1)], or curbed by cultural tionarily significant units. A burgeoning tion of Migratory Species of Wild Animals conservatism [e.g., southern resident killer body of evidence on cultural transmission (CMS), can facilitate smart, targeted con- whales’ persistent foraging specialization servation of a wide range of taxa, by explic- on Chinook salmon (2)]. Author affiliations are listed in the supplementary materials. itly considering aspects of their sociality Social learning can result in the emer-

Email: [email protected]; [email protected] and cultures. gence of subpopulations with distinctive ELEPHANTS FOR TRUST FISHLOCK/AMBOSELI V. PHOTO:

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Published by AAAS An African elephant matriarch (center) servation and management of migratory can lead, and shape the success of, a family species in CMS Appendix II. Although, like for three decades or more. many other international agreements, CMS does not have a compliance mechanism, its Positive conservation outcomes can de- standing committee is in the process of crit- pend on the restoration of cultural knowl- ically reviewing the impacts of its decisions, edge. For example, because whooping to improve effectiveness (background CMS cranes learn migratory routes socially, hu- documents are available in the supplemen- man surrogates in ultralight aircraft can tary materials). guide naïve, captive-bred birds along their Impetus for an animal culture initiative first migration, potentially boosting the ef- was provided by a growing body of evidence fectiveness of reintroduction programs (8, for social learning and culture in cetaceans 9). Similarly, without the benefit of socially that raised important questions about inherited knowledge, bighorn sheep and how best to conserve these animals (12). moose translocated to unfamiliar habitats The CMS Scientific Council’s preexisting can take generations to master the skill of expertise in evaluating threats to aquatic tracking the seasonal distribution of high- mammals made CMS a natural avenue for quality forage (10). Social learning can also examining these issues further. In 2014, be exploited to ameliorate human-wildlife a formal consultation revealed an exten- conflict, for example, by artificially “seed- sive range of circumstances in which so- Downloaded from ing” desirable behavior, such as avoidance cial structure, social learning, and cultural of particular foods or sites (3, 11). variation in whales and dolphins can affect To improve the efficacy of conservation the planning or outcomes of conservation efforts, we therefore argue that it is criti- efforts. This culminated in the adoption of a cal to consider the interplay between social ground-breaking resolution, through which structure and the transmission of social the CMS signatories formally acknowledged information. This may be particularly im- the importance of social learning and cul- http://science.sciencemag.org/ portant if different categories of individu- ture for the conservation of some highly als vary in their propensity to innovate, or social species. are more likely to be copied by naïve group Following the 2014 resolution, the CMS members (11). In some cases, populations Scientific Council established an expert may be structured into distinct cultural group to broaden the scope of this initiative units with differing resource requirements. beyond cetaceans. The group determined For instance, cultural transmission of vocal that social learning has conservation rel- behavioral profiles, erecting social barriers, patterns among sperm whales in the East- evance across a wide range of vertebrate as observed in distinct vocal clans of sperm ern tropical Pacific results in distinct vocal taxa, including birds, fishes, and many ma- whales (see the figure) . Culturally mediated clans (1) (see the figure). Clans vary in their rine and terrestrial mammals (1, 3 ). At a on March 21, 2019 population structure has important impli- feeding success during El Niño and La Niña 2018 cross-taxa CMS culture workshop in cations for conservation efforts (4), as it can oceanographic cycles (1), meaning that if Parma, Italy, the authors of the present influence species-wide phenotypic diversity these cycles increase, as predicted under cli- article reviewed relevant evidence, with and adaptability to changing conditions (5). mate change, population-level impacts may a particular focus on species in which so- In some cases, such as humpback or blue not be uniform. cial learning has the potential to strongly whale song, cultural variation can reflect influence migratory behavior, habitat use, demography and facilitate more efficient, CETACEANS, AND BEYOND foraging, or interaction with human activi- or less invasive, assays of contemporary Despite mounting evidence that aspects of ties. On the basis of this work, we recom- genetic population structure (1, 4). Most sociality can have far-reaching implications mend, among other things (for details, see profoundly, culture can play a causal role in for wildlife conservation, international table S1): augmenting the designation of establishing and maintaining distinct evo- policy forums—where most large-scale con- evolutionarily significant units; conserving lutionary trajectories (6). servation strategies are conceived—have individuals that are critical repositories Another consequence of social learning so far not engaged substantially with the of social knowledge; refining the criteria can be the increased importance of key challenges and opportunities presented by used for identifying and prioritizing spe- individuals as repositories of accumulated this new scientific perspective. A notable cies and populations for assessment; im- knowledge, making their targeted protec- exception is the CMS Scientific Council, proving reintroduction schemes through tion particularly important for the per- which has conducted work at the interface strategic management of social knowledge; sistence of social units. For example, the of cutting-edge science and international planning effective mitigation strategies for experience of African elephant matriarchs policy-making. anthropogenic impacts using aspects of (see the photo) has been shown to posi- The CMS signatories work to develop sociality; systematically cataloging the di- tively influence the fertility rates of younger collaboration between range states for the mensions of cultural diversity; and raising females in their social group, through the conservation of species that move across awareness about the value of conserving transmission of information about the so- jurisdictional boundaries. They agree to animal cultures. cial and ecological landscape (7). Yet, tradi- support research, to endeavor to provide The overall aim of this initiative is to tional approaches to species conservation immediate protection for migratory spe- maximize the efficacy of conservation efforts often prioritize younger individuals for cies listed in CMS Appendix I, and to work through enhanced consideration of sociality their direct reproductive potential. toward developing agreements for the con- in general, and social learning and (both

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Published by AAAS INSIGHTS | POLICY FORUM adaptive, and seemingly arbitrary) cultural triggered cameras, as exemplified by a will be to determine if evidence warrants processes in particular. Understanding recent attempt to chart putative cultural explicitly recognizing some distinct cultural the importance of behavioral diversity will variation in wild chimpanzees (14) in the units listed in the CMS Appendices, and benefit conservation policies both when as- face of urgent threats from habitat destruc- how insights from this work can be used to sessing the status of potentially vulnerable tion and poaching (see fig. S1). In addition, inform conservation efforts across the en- populations (e.g., when delineating units appropriately parameterized formal models tire CMS portfolio of agreements. to conserve, by accounting for cultural seg- may provide reliable predictions about the Within the broader context of interna- regation) and when devising effective con- impact of specific conservation interven- tional wildlife law (15), it is important to servation strategies (e.g., by identifying key tions on sociocultural processes (5). The consider the relevance of animal culture repositories of social knowledge). Achieving field of animal social learning is now suf- for scientific assessments and policy de- these ambitious goals will require a con- ficiently mature to provide key parameters cision-making across a range of relevant siderable amount of work. For example, for robust modeling of some systems, where multilateral environmental agreements, although there is broad agreement that suc- relevant data are available from long-term such as the Convention on International cessful reintroduction programs require in- field studies and controlled experiments. Trade in Endangered Species of Wild dividuals to be behaviorally competent (8), Fauna and Flora (CITES) and the Conven- for many species it will still be necessary to tion on Biological Diversity (CBD). We see establish the degree to which key behaviors Sperm whale vocal clans opportunities to extend our approach be- are socially learned [e.g., migratory routes Subpopulations in the eastern tropical Pacific. Clan yond species and issues currently covered in birds (9, 13)]. To facilitate progress, we names are derived from their culturally transmitted by CMS, for example, when assessing the highlight a few additional opportunities, sustainability of exports and trade through

vocal dialects. Colored lines indicate confirmed Downloaded from both in terms of particular species that may movements of photo-identified individuals of known CITES processes. Such consideration is merit further consideration and promising clans across jurisdictional boundaries (conceptual timely, because 2020 is the final year of research approaches. map, not to scale). See supplementary materials. the United Nations Decade on Biodiversity, The CMS encourages its signatories to when governments will negotiate the Post- engage in collective conservation measures 2020 Biodiversity Framework. Given the Costa Rica through its “concerted action” mechanism. prevalence of social learning and cultures

Panama http://science.sciencemag.org/ This process is particularly relevant when across a wide range of taxa, a comprehen- considering collaboration between range Colombia sive, integrated approach is essential to states for gathering and sharing data on maintaining the natural diversity and in- cultural diversity for populations that move tegrity of Earth’s rich ecosystems. j predictably across national borders. In 2017, Ecuador CMS adopted a concerted action for Eastern REFERENCES AND NOTES 1. H. Whitehead, L. Rendell, The Cultural Lives of Whales and tropical Pacific sperm whales (see the figure). Dolphins (Univ. of Chicago Press, 2015). A variety of species may benefit from similar 2. H. Whitehead, Learn. Behav. 38, 329 (2010). consideration, to evaluate the importance of 3. A. Whiten, Interface Focus 7, 20160142 (2017). 4. E. C. Garland et al., Conserv. Biol. 29, 1198 (2015). aspects of their sociality for their conserva- Peru 5. S. A. Keith, J. W. Bull, Ecography 40, 296 (2017). tion. This includes species as diverse as cod Regular 6. A. D. Foote et al., Nat. Commun. 7, 11693 (2016). on March 21, 2019 (not currently listed in the CMS Appendi- Plus-one 7. K. McComb, C. Moss, S. M. Durant, L. Baker, S. Sayialel, ces), which appear to socially learn migra- Science 292, 491 (2001). Short 8. T. Mueller, R. B. O’Hara, S. J. Converse, R. P. Urbanek, W. F. tory routes, and chimpanzees (recently listed Fagan, Science 341, 999 (2013). Four-plus Chile in the CMS Appendices), where a culture of 9. C. S. Teitelbaum, S. J. Converse, T. Mueller, Conserv. Lett. nut-cracking tool use thrives in a small area CMS Signatory 12, e12599 (2019). Non-Signatory 10. B. R. Jesmer et al., Science 361, 1023 (2018). of Western Africa (see fig. S1), yet spans mul- 11. A. L. Greggor, A. Thornton, N. S. Clayton, Behav. Ecol. tiple national jurisdictions and may provide Sociobiol. 71, 16 (2017). access to an important food source during 12. H. Whitehead, L. Rendell, R. W. Osborne, B. Würsig, Biol. Conserv. 120, 427 (2004). the dry season (3). 13. B.-U. Meyburg et al., J. Exp. Biol. 220, 2765 (2017). An important challenge is to identify 14. H. S. Kühl et al., Sci. Rep. 6, 22219 (2016). those populations, or social units, that 15. A. Trouwborst et al., BioScience 67, 784 (2017). would most benefit from our proposed ap- ACKNOWLEDGMENTS proach, and to predict how specific biologi- MOVING FORWARD We are grateful to the CMS executive secretary and the CMS cal processes may influence conservation Our growing understanding of the conser- secretariat for organizing the Parma workshop; the hosts and outcomes (11). Recent studies illustrate how vation relevance of cultural variation urges sponsors of the workshop (the Appennino Tosco-Emiliano National Park, the Fondazione Monteparma, and the Principality innovative rapid-assessment techniques that scientists and policy-makers collabo- of Monaco); M. Prideaux for helpful policy discussions; S. could aid the identification of distinct cul- rate closely to ensure that policy is informed Smart for graphic design; and the experts that have supported tural units, which may be particularly vul- by the latest scientific advances. Many cul- this initiative. G.N.d.S. is the CMS Conference of the Parties Appointed Councillor for Aquatic Mammals. F.S. is the chair of nerable (e.g., as a result of socially learned tural systems are highly complex, and the the CMS Scientific Council and is the councillor for Italy. J.W. foraging strategies). Where socially trans- conservation impact of cultural processes is the UK scientific councillor for CMS and works for the Joint mitted traits—such as foraging tactics (and is context dependent, necessitating careful Nature Conservation Committee, which is a statutory adviser to hence resource requirements) and vocal case-by-case consideration. Recommenda- the UK Government. behavior—covary (1), it may be possible to tions from the Parma workshop will inform SUPPLEMENTARY MATERIALS SCIENCE document cultural variation with well-es- discussions at the November 2019 Meeting www.sciencemag.org/cgi/content/full/science.aaw3557/DC1 tablished, inexpensive survey protocols (4). of the Sessional Committee of the CMS Sci- Another approach is to harness new survey entific Council and the 2020 CMS Confer- Published online 26 February 2019

technologies, such as autonomous motion- ence of the Parties in India. A key challenge 10.1126/science.aaw3557 DESAI/ N. GRAPHIC:

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Published by AAAS Animal cultures matter for conservation Philippa Brakes, Sasha R. X. Dall, Lucy M. Aplin, Stuart Bearhop, Emma L. Carroll, Paolo Ciucci, Vicki Fishlock, John K. B. Ford, Ellen C. Garland, Sally A. Keith, Peter K. McGregor, Sarah L. Mesnick, Michael J. Noad, Giuseppe Notarbartolo di Sciara, Martha M. Robbins, Mark P. Simmonds, Fernando Spina, Alex Thornton, Paul R. Wade, Martin J. Whiting, James Williams, Luke Rendell, Hal Whitehead, Andrew Whiten and Christian Rutz

Science 363 (6431), 1032-1034. DOI: 10.1126/science.aaw3557originally published online February 26, 2019 Downloaded from

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