Downloaded by guest on September 29, 2021 ot mrc,nrhetAaoi,adNwGie being in services New medicinal and all the Amazonia, in of northwest uniqueness 84% America, and linguistic 91%, North of 73%, pattern with strong regions, a exhibits a of (e.g., System). subcategory combination Digestive medicinal the a as and service” Methods ). and plant “medicinal (Materials a defined indigenous We 236 asso- services with plant 12,495 ciated and north- data species these three plant (11), Together, medicinal analyzed (13). 3,597 America Guinea span we New this, North and (12), of for Amazonia west extent datasets the ethnobotanical assess large To shared. knowl- such is whom lan- with edge be indigenous languages still surviving would some other knowledge if in plant safeguarded even medicinal their knowledge is, extinct, That go languages, guages high. different be would speak resilience that (10). among groups widely orally shared indigenous is knowledge medicines about transmit resilience knowledge if cultures its Therefore, indigenous for Most implications important (9). has this services been medicinal how has extinction and ecological knowledge by result unique posed 1). may (Fig. that limited linguistically languages to indigenous of compares of risk of loss the loss discovery of the the poten- understanding the in which our full and however, to the people far, degree limit to So uses. may contributions unanticipated nature’s century of coming (7, plant tial the crops useful geographic in and within reductions the plants and species constrain extinction endemic associated will Together, human-utilized On 8). strongly change many (6). of global is plants ranges about hand, disuse knowledge other language extinctions indigenous the species hand, in and one decreases (3) with On loss 5). language (4, increas- by in is encoded threatened however, knowledge, is ingly Indigenous (1)—that (2). benefits languages health their significant confers that I languages indigenous than knowledge be medicinal of will loss. extinction loss biodiversity the to language critical coupling that more strong suggests even of and languages finding knowledge threatened Our indigenous with languages are. in most knowledge uniqueness threatened, unique high linguis- linguistically not report with are that associated knowledge biocul- one species medicinal unique to high plant 12,495 tically known all most a only of Whereas unique—i.e., have 75% language. linguistically over are that that services regions plant show go we three plants diversity, and on tural much languages how is Focusing as quantify plants vanish extinct. and may medicinal knowledge languages of indigenous individual knowledge with indigenous ask associated loss degree we under- the Here, what our limited. in however, remains to result knowledge far, may unique So extinction be linguistically century. of longer language the no whether will of of world 2021) end standing the 24, the February in review languages by for (received 7,400 spoken 2021 the 9, of May approved 30% and Over AZ, Tempe, University, State Turner, L. B. by Edited a C Rodrigo unique knowledge of medicinal loss the triggers extinction Language PNAS eateto vltoayBooyadEvrnetlSuis nvriyo uih H85 uih Zurich, CH-8057 Zurich, of University Studies, Environmental and Biology Evolutionary of Department deaotpat n hi evcsicuigknowledge services—including their knowl- and sophisticated plants a about accumulated edge have people ndigenous u eut hwta nieoskoldeaotmedicinal about knowledge indigenous that show results Our about knowledge indigenous of structure the Unraveling 01Vl 1 o 4e2103683118 24 No. 118 Vol. 2021 amara-Leret ´ | csse services ecosystem a,1 n od Bascompte Jordi and | iclua diversity biocultural iu insipida Ficus a + fuiu nweg soitdwt hetndlnugsin languages threatened percentage with the Guinea. associated language-threat New underestimate knowledge our likely unique that (15) of suggests Glottolog generation from single data a not con- language do in in mostly who decline in skills dramatic students uses a fluent the Such few languages. in students indigenous species a speak plant to by nonnative known in replaced centrated Guinea uses are of languages New plant 91% Crucially, indigenous medicinal Papua (14). to languages varied in compared indigenous students, in the study fluent 6,190 are recent of parents, 58% their A only assess. that showed to languages Guinea’s New difficult of status unique is island- true an all the of survey, By absence of linguistic the efforts. wide in 31% However, documentation Guinea. for New future in account knowledge and, for languages languages) area threatened threatened priority contrast, most key to and (i.e., a linked America hotspot thus, is that knowledge North knowledge indigenous highlights in an medicinal result are knowledge This unique the respectively. all Amazonia, of northwest 100% and that languages in question found the mostly threatened. raises is are knowledge knowledge America, unique unique North of find- whether pattern in of Our strong 50% respectively. a Guinea, and of differ- ing New 18%, using and 56%, language Amazonia, is northwest each species), as (i.e., species), plant turnover same ent species the to of (i.e., fraction turnover knowledge opposed The cultural different by 2). having explained (Fig. is languages respectively that knowledge language, unique one of only by cited doi:10.1073/pnas.2103683118/-/DCSupplemental at online information supporting contains article This 1 ulse ue8 2021. 8, June Published BY-NC-ND) (CC 4.0 NoDerivatives License distributed under is article access open This Submission.y Direct PNAS a is article This interest.y research; competing performed no paper.y declare the R.C.-L. authors wrote The J.B. research; and designed R.C.-L. and J.B. data; analyzed and R.C.-L. R.C.-L. contributions: Author owo orsodnemyb drse.Eal [email protected] Email: addressed. be may correspondence whom To tn o naeigadcnevn auescnrbtosto Rosetta contributions nature’s knowledge—a people. conserving medicinal and there- unraveling of for is reservoir stone language unique indigenous a Each fore plants. language— threatened than single languages with threatened a with knowledge associated by strongly medicinal more known ecosys- and in most unique—i.e., that such plants linguistically find of of is we example use Here, relevant The services. particularly provide. tem a they is services surrounding medicine their the about and have plants for communities the that importance contain knowledge languages and Indigenous global endangerment development. raise sustainable their to aims about Languages awareness Indigenous of Interna- the Decade as 2022–2032 tional of proclamation Nations United The Significance u nlssidctsta hetndlnugsspot86% support languages threatened that indicates analysis Our https://doi.org/10.1073/pnas.2103683118 . y raieCmosAttribution-NonCommercial- Commons Creative . y https://www.pnas.org/lookup/suppl/ | f5 of 1

SUSTAINABILITY ECOLOGY SCIENCE Fig. 1. Medicinal plant knowledge and its association with indigenous languages. The figure illustrates a regional pharmacy with remedies (jars with plants) cited by languages (jar labels). In this paper, we assess to what degree the knowledge contained in this pharmacy would be eroded by the extinction of either indigenous languages or plants.

Once we have quantified the overall amount of unique knowl- three regions (Fig. 3; SI Appendix, Table S1). This indicates that edge, we next proceed by mapping how it is distributed across the when planning for medicinal knowledge conservation, the entire linguistic phylogeny. This will serve to identify whether unique linguist spectrum—rather than a few “hot” branches—needs to knowledge is uniformly distributed across all linguistic groups be considered. or whether a few linguistic groups deserve more protection than So far, we have focused on how unique knowledge is dis- others. First, we built language phylogenies for all of the indige- tributed along the cultural dimension. Let us turn now to nous languages in our sample. Next, we calculated the degree examine the other component of the indigenous knowledge of phylogenetic clustering of unique knowledge using Pagel’s network (9), namely, the plants. To understand the degree of lambda (λ) (16); values of λ close to one indicate strong phy- threat faced by medicinal plants, we queried the International logenetic clustering, whereas values close to zero indicate data Union for Conservation of Nature (IUCN) Red List of Threat- without phylogenetic dependence. We did not find clustering of ened Species (17). We found conservation assessments for 22%, unique knowledge along the language phylogenies in any of the 31%, and 32% of the medicinal species recorded in North

Fig. 2. Most medicinal knowledge is unique to a single language. Histograms depict the number of indigenous languages that cite a medicinal service. (A) . (B) Northwest Amazonia. (C) New Guinea. Red bars show medicinal plant services only known to one language. Dots within the maps indicate the distribution of languages.

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SUSTAINABILITY ECOLOGY SCIENCE that study, the probability of a medicinal species belonging to from Richard E. Schultes’s book on the medicinal plants of northwest Ama- a threatened category ranged from 0.0002 to 0.8341 in North zonia, which integrates nearly half a century of his field research (12); and America (mean ± SD, 0.156 ± 0.158), 0.149 to 0.822 in north- 3) New Guinea: from an ethnobotanical review of 488 references and 854 west Amazonia (mean 0.483 ± 0.119), and 0.063 to 0.679 in New herbarium specimens (13). Guinea (mean 0.357 ± 0.141), respectively. In summary, both We classified uses from the three data sources into medicinal subcate- gories following the classification in the Economic Botany Data Collection the IUCN conservation assessments and machine-learning pre- Standard (31), with modifications explained by Camara-Leret´ et al. (32). dictions suggest that most medicinal plant species in our sample Medicinal subcategories included Blood and cardio-vascular system; Cultural are not threatened. Finally, we found that about 1% of all unique diseases and disorders; Dental health; Digestive system; Endocrine system; knowledge in each region was associated with both threatened General ailments with unspecified symptoms; Infections and infestations; languages and threatened plants (SI Appendix, Table S3). How- Metabolic system and nutrition; Muscular-skeletal system; Nervous system ever, there is considerable uncertainty about the potential loss of and mental health; Poisoning; Pregnancy, birth and puerperium; Reproduc- unique knowledge from the extinction of plants because 64% and tive system and reproductive health; Respiratory system; Sensory system; 69% of the unique knowledge in North America and northwest Skin and subcutaneous tissue; Urinary system; Veterinary; Not specified; Amazonia that is associated with threatened languages belongs and Other medicinal uses. We defined “unique knowledge” as a medicinal service cited exclusively by one indigenous language. to plants that lack plant-conservation assessments. IUCN con- The amount of unique knowledge may change as more indigenous servation assessments are urgently needed for these plant groups are studied and as more in-depth studies are made on indige- species. nous groups already reported in the literature. We hypothesize that it will To assess whether unique knowledge is strongly clustered increase, for three reasons. First, research in indicates that biologically, we built phylogenies of the medicinal floras of the amount of unique knowledge is positively correlated with the total each region and calculated Pagel’s lambda (Fig. 4). We only number of medicinal uses registered in a community (33). This is confirmed found significant clustering of unique knowledge in North Amer- in New Guinea by a study that showed that linguistic uniqueness occurs ica, although values were low (SI Appendix, Table S1). This even among the best-studied indigenous groups who occupy montane habi- relatively weak phylogenetic signal across the three regions tats with a similar flora (34). Therefore, any undersampling in our study regions—especially in New Guinea—would, in fact, underestimate unique suggests that when planning for biocultural conservation, the knowledge because generalist knowledge tends to be the first that is docu- entire medicinal flora—rather than a few clades—must be mented in the field. Second, our classification of medicinal plant services considered. is conservative because it omits “plant parts” (e.g., bark, leaf, fruit, and Here, we have shown that in North America, northwest Ama- seed). Because different plant parts may be used for different purposes zonia, and New Guinea, indigenous knowledge of medicinal [different plant parts may have different chemical compounds (35)], our plant services exhibits a low redundancy across languages that classification underestimates the detection of medicinal knowledge that is typical of systems with high information content (19, 20). is restricted to one language. Third, our classification of medicinal plant This low redundancy in medicinal knowledge among languages services is based on 20 medicinal subcategories that are broad in scope. does not support the notion of high cross-cultural consensus— For example, “Infections and infestations” encompasses reports related to, e.g., malaria, leishmaniasis, and measles. This means that if one indigenous i.e., that cultures resemble each other in their knowledge—but language cites plant A as a remedy for malaria and another indigenous lan- instead highlights the unique biocultural heritage each culture guage cites plant A for measles, both reports would be classified as “Plant holds. The invention and diversification of languages involve A: Infections and Infestations” and considered shared, rather than unique, two opposing forces. On the one hand, sharing facilitates the knowledge. exchange of information and the spread of valuable ideas that may enhance the fitness within populations. On the other hand, Language Phylogenies and Threat. Medicinal services in the literature were the diversification of languages is the result of innovations, and associated with 119 indigenous languages in North America, 37 lan- eventually linguistic barriers may limit information spread. In guages in northwest Amazonia, and 80 languages in New Guinea. For areas of high linguistic or biological diversity and/or geographic each region, we built language trees through phylogenetic inference barriers, the balance between sharing and innovating may tip using machine-learning techniques on the word lists of the Automated toward the latter. This may result in the amplification of dif- Similarity Judgment Program (ASJP) database (36) and used the Glot- ferences among cultures, as we have shown here for the case of tolog classification as a constraint (30). The ASJP list consists of the medicinal knowledge. 40 most stable items, as determined by Holman et al. (37), from the Only about 6% of higher plants have been screened for biolog- 100-item list of Swadesh (38). To assess the degree of threat faced by languages in our sample, we queried the Glottolog (15), which derives ical activity (21). Therefore, assessing to what degree linguisti- an Agglomerated Endangerment Status (AES) from the databases of The cally unique medicinal services are truly effective in the Western Catalog of Endangered Languages, United Nations Educational, Scientific, sense is beyond the scope of this paper. In many instances, these and Cultural Organization Atlas of the World’s Languages in Danger, plants have been proven medicinally effective (12, 22–27), albeit and Ethnologue. For a list of the languages analyzed, see SI Appendix, there are also exceptions (28, 29). Regardless of that, here, we Table S2. treat this knowledge as what it is: part of the cultural heritage of indigenous people. Phylogenies and Threat. We verified plant-species The United Nations declared 2022–2032 as the International using recently published checklists to the vascular plants of the Americas Decade of Indigenous Languages to raise awareness about their (39) and New Guinea (40). Using the list of medicinal plant species in each importance for sustainable development and their endanger- region, we queried the mega-tree GBOTB.-extended of Smith and Brown ment across the world. Our study suggests that each indigenous (41) with the phylo.maker function of the R package V.PhyloMaker (42). language brings unique insights that may be complementary to The phylogenies used in all subsequent analyses comprised 2,475 species other societies that seek potentially useful medicinal remedies. in North America, 645 species in northwest Amazonia, and 477 species in Therefore, the predicted extinction of up to 30% of indigenous New Guinea. To assess the threat faced by medicinal plant species, we queried the conservation assessments published by the IUCN Red List of languages by the end of the 21st century (3) would substantially Threatened Species (17), which classifies species as Data Deficient, Least compromise humanity’s capacity for medicinal discovery. Concern, Near Threatened, Vulnerable, Endangered, Critically Endangered, Extinct in the Wild, and Extinct. Following IUCN, species assessed to be Materials and Methods Near Threatened, Vulnerable, and Endangered were considered threat- Plant Services. We obtained a list of medicinal plant species and services ened. Because most plant species lack IUCN conservation assessments, associated with individual indigenous groups from three regions: 1) North we also obtained endangerment probabilities from a recent study that America: from the Native American Ethnobotany database (11)—the largest used machine-learning to predict the conservation status of 30,497 plant repository of indigenous knowledge for the region; 2) northwest Amazonia: species (18).

4 of 5 | PNAS Camara-Leret´ and Bascompte https://doi.org/10.1073/pnas.2103683118 Language extinction triggers the loss of unique medicinal knowledge Downloaded by guest on September 29, 2021 Downloaded by guest on September 29, 2021 1 .Vrore hraons ntenwmlenu:Lafidn n biotechnol- and Leadfinding millennium: new the in Pharmacognosy Verpoorte, biology. R. in theory 21. Information Margalef, R. communications. 20. of theory mathematical A Shannon, E. C. 19. 8 .A elte,B .Crtn,D .Tn,J ulvn .Esp A. Sullivan, J. Tank, C. D. Carstens, C. threatened B. of Pelletier, list A. T. red 18. IUCN The Nature. of Conservation for Union International 17. evolution. biological of patterns historical the Inferring Pagel, Mark. 16. 5 .Hammarstr H. 15. Kik A. 14. C R. 13. dyes Raffauf, F. drugs, R. foods, Schultes, E. of R. database 12. A ethnobotany: American Native Moerman, D. 11. 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A change. global of face change. climate Adv. Sci. . of Zapotecs Isthmus the Ethnomed. among knowledge ethnoecological implications. future and Amsterdam, Benjamins, John species. Series, Companion 3–19. pp. Language 142, vol. in 2013), , (Studies Eds. ley, Endangerment Language to Responses Societies Traditional 2014). in Animals and Amazon. Bolivian the in health 6Arl2021). April (Accessed 26 https://doi.org/10.1101/2021.04.12.439439 (2021). [Preprint] bioRxiv threat. Amazonia naeb.brit.org/. Northwest (2020). plants from derived 2020. peoples, May American 24 Accessed Native of fibers and 2000). UK, Oxford, Demand, on Press University mr-ee,M .Frua .Bsope nieoskoldentok nthe in networks knowledge Indigenous Bascompte, J. Fortuna, A. M. amara-Leret, amara-Leret mr-ee,Z enh,Idgnu nweg fNwGie’ sflplants: useful Guinea’s New of knowledge Indigenous Dennehy, Z. amara-Leret, ´ ´ ´ .Pam Pharmacol. Pharm. 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