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    Six decades of warming and drought in the world’s top wheat-producing countries offset the benefits of rising CO2 to yield

    Wheat production and yield vis-à-vis climate trendsWheat is currently grown in all six continents except Antarctica. The leading producers include China, the Russian Federation, Ukraine, Kazakhstan (RUK), India, USA, France, Canada, Pakistan, Germany, Argentina, Turkey, Australia, and United Kingdom (Fig. 1 and Supplementary Table 1). The total grain production of these twelve countries is estimated at 600 megatons (2019 data), which accounts for over 78% of the global wheat production. The top three producers are China with 133.6 megatons per year (Mt y−1), RUK with 114.1 Mt y−1, and India with 103.6 Mt y−1. RUK contains the largest harvested area of 45.8 million hectares, followed by India with 29.3 million hectares and China with 23.7 million hectares (Fig. 1A). Despite a relatively small harvested area of 10.1 million hectares (only 22% of RUK’s harvested area), the United Kingdom, France, and Germany account for the world’s highest yields per hectare, with 8.93 tons ha−1, 7.74 tons ha−1, and 7.40 tons ha−1, respectively (compared with the world’s average yield of only 3.2 tons ha−1), accounting for a total yearly production of 79.9 Mt y−1.Figure 1Global wheat area and trends in wheat yield and climate in top-twelve global wheat producers (1961–2019). (A) Worldwide wheat cropping area (%)29, total harvested area (106 hectares in 2019), and wheat production (megatons for 2019) of the top 12 global wheat producers (China, RUK—Russia, Ukraine, and Kazakhstan, India, USA—hard red winter (HRW) and hard red spring (HRS), France, Canada, Pakistan, Germany, Argentina, Turkey, Australia, and United Kingdom) (Map was generated in Python 3.8.5; http://www.python.org). (B) Changes in wheat yield (tons per hectare) and (C) climate—mean daily temperature (red dashed line; °C) and the seasonal water balance represented as potential evaporation minus precipitation (blue line; PET—P in millimeters of H2O). A positive trend in PET-P indicates an increase in water deficit. The seasonal atmospheric [CO2] in μmol CO2 per mol−1 air is also shown in the insert of C (black line). Temperature, PET-P, and [CO2] shown in C are averaged values over the wheat-growing period and the shared area of the wheat-growing areas of the top 12 global wheat producers. Decadal trends in temperature (red) and PET-P (blue) as well as the significance levels of these trends are presented in C.Full size imageWhile all these twelve major wheat producers saw an increase in yield during the last six decades (Fig. 1B), China displayed the most noteworthy increase with a nearly sevenfold higher yield in 2019 than in 1961 and a mean total increase of 5.19 tons ha−1 for the period of 1961–2019. Germany, the UK, and France reported comparable yield increases of 5.20 tons ha−1, 5.19 tons ha−1, and 4.81 tons ha−1, respectively, during this period, suggesting an approximately 1.6-fold improvement since 1961 (Fig. 1B). Australia, RUK, and Turkey reported the lowest gains with only 0.87 tons ha−1, 1.26 tons ha−1, and 1.71 tons ha−1, respectively, representing improvements of 67%, 150%, and 175% in yield per hectare since 1961.Yield increase occurred despite the steep rise in temperature (nearly 1.2 °C) in the twelve countries during the last six decades (Fig. 1C). Water deficit—calculated as the difference between potential evaporative demand and precipitation (PET—P; mm H2O y−1)—also increased by an average of (sim) 29 mm of H2O for the same period. Increases in yield since the early 1960s were likely due to breeding and agrotechnological advances, improved management, and a steep rise in atmospheric [CO2] of (sim) 98 μmol mol−1, from 315.9 μmol mol−1 in 1961 to 413.4 μmol mol−1 in 2019 (insert in Fig. 1C).Unraveling the impacts of climate and [CO2] on yieldBased on previous studies30,31, we used a log-linear model to quantify the impact of [CO2] and daily minimum (Tmin), maximum (Tmax), and mean (Tmean) temperatures, as well as seasonal water deficit (PET-P), and rainfall distribution on wheat yield. Climate variables were obtained from the TerraClimate data set32, while monthly records of [CO2] from the Mauna Loa station were used to model the effects of CO2 (see “Methods”). To quantify wheat yield as a function of climate variables and [CO2], we included all 12 countries in the regression analysis. Supplementary Table 2 presents summary statistics of all variables, while Supplementary Fig. 1 depicts trends in Tmean and PET-P per country.Since climate variables tend to be correlated over time (Supplementary Table 3), controlling for all of these variables in the model facilitates the estimation of their distinct effect on yield. We used country-specific trends to distinguish changes in wheat yield related to climate and [CO2] from those attributed to agrotechnological advancements, changes in country-specific policies, and other local-changing factors (e.g., economic and population growth; more information on how this was done can be found in “Methods”). We also included country-specific effects across all models to account for unobserved time-invariant heterogeneity at the country level, such as geographical properties, edaphic characteristics, and other local-specific features (see “Methods”).Table 1 reports the estimated regression coefficients of four models, (1) using only temperature variables (T), (2) temperature and water-related (i.e., seasonal rainfall distribution and water deficit as PET-P) variables (T + W), (3) including [CO2] (T + W + C), and (4) the interaction between [CO2] and climate variables (T + W + C + interactions).Table 1 Effects of climate variables and [CO2] on log wheat yields of the world’s major wheat producers.Full size tableAmong the temperature measures, only Tmean had a consistently significant effect on yield (p  More

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    Validation of quantitative fatty acid signature analysis for estimating the diet composition of free-ranging killer whales

    Springer, A. M. et al. Sequential megafaunal collapse in the North Pacific Ocean: an ongoing legacy of industrial whaling?. Proc. Natl. Acad. Sci. 100, 12223–12228. https://doi.org/10.1073/pnas.1635156100 (2003).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Estes, J. A., Heithaus, M., McCauley, D. J., Rasher, D. B. & Worm, B. Megafaunal impacts on structure and function of ocean ecosystems. Annu. Rev. Environ. Resour. 41, 83–116. https://doi.org/10.1146/annurev-environ-110615-085622 (2016).Article 

    Google Scholar 
    Newsome, S. D., Clementz, M. T. & Koch, P. L. Using stable isotope biogeochemistry to study marine mammal ecology. Mar. Mamm. Sci. 26, 509–572. https://doi.org/10.1111/j.1748-7692.2009.00354.x (2010).CAS 
    Article 

    Google Scholar 
    Bowen, W. D. & Iverson, S. J. Methods of estimating marine mammal diets: a review of validation experiments and sources of bias and uncertainty. Mar. Mamm. Sci. 29, 719–754. https://doi.org/10.1111/j.1748-7692.2012.00604.x (2013).Article 

    Google Scholar 
    Krahn, M. M. et al. Use of chemical tracers in assessing the diet and foraging regions of eastern North Pacific killer whales. Mar. Environ. Res. 63, 91–114. https://doi.org/10.1016/j.marenvres.2006.07.002 (2007).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Remili, A. et al. Individual prey specialization drives PCBs in Icelandic killer whales. Environ. Sci. Technol. 55, 4923–4931. https://doi.org/10.1021/acs.est.0c08563 (2021).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Foote, A. D., Vester, H., Vikingsson, G. A. & Newton, J. Dietary variation within and between populations of northeast Atlantic killer whales, Orcinus orca, inferred from d13C and d15N analyses. Mar. Mamm. Sci. 28, E472–E485. https://doi.org/10.1111/j.1748-7692.2012.00563.x (2012).CAS 
    Article 

    Google Scholar 
    Remili, A. et al. Humpback whales (Megaptera novaeangliae) breeding off Mozambique and Ecuador show geographic variation of persistent organic pollutants and isotopic niches. Environ. Pollut. 267, 115575. https://doi.org/10.1016/j.envpol.2020.115575 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Pinzone, M., Damseaux, F., Michel, L. N. & Das, K. Stable isotope ratios of carbon, nitrogen and sulphur and mercury concentrations as descriptors of trophic ecology and contamination sources of Mediterranean whales. Chemosphere 237, 124448. https://doi.org/10.1016/j.chemosphere.2019.124448 (2019).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Bourque, J. et al. Feeding habits of a new Arctic predator: insight from full-depth blubber fatty acid signatures of Greenland, Faroe Islands, Denmark, and managed-care killer whales Orcinus orca. Mar. Ecol. Prog. Ser. 603, 1–12. https://doi.org/10.3354/meps12723 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    Krahn, M. M., Pitman, R. L., Burrows, D. G., Herman, D. P. & Pearce, R. W. Use of chemical tracers to assess diet and persistent organic pollutants in Antarctic Type C killer whales. Mar. Mamm. Sci. 24, 643–663. https://doi.org/10.1111/j.1748-7692.2008.00213.x (2008).CAS 
    Article 

    Google Scholar 
    Groß, J. et al. Interannual variability in the lipid and fatty acid profiles of east Australia-migrating humpback whales (Megaptera novaeangliae) across a 10-year timeline. Sci. Rep. 10, 18274. https://doi.org/10.1038/s41598-020-75370-5 (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Jory, C. et al. Individual and population dietary specialization decline in fin whales during a period of ecosystem shift. Sci. Rep. 11, 17181. https://doi.org/10.1038/s41598-021-96283-x (2021).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Iverson, S. J., Field, C., Bowen, W. D. & Blanchard, W. Quantitative fatty acid signature analysis: a new method of estimating predator diets. Ecol. Monogr. 74, 211–235. https://doi.org/10.1890/02-4105 (2004).Article 

    Google Scholar 
    McKinney, M. A. et al. Global change effects on the long-term feeding ecology and contaminant exposures of East Greenland polar bears. Glob. Change Biol. 19, 2360–2372. https://doi.org/10.1111/gcb.12241 (2013).ADS 
    Article 

    Google Scholar 
    Nordstrom, C. A., Wilson, L. J., Iverson, S. J. & Tollit, D. J. Evaluating quantitative fatty acid signature analysis (QFASA) using harbour seals Phoca vitulina richardsi in captive feeding studies. Mar. Ecol. Prog. Ser. 360, 245–263. https://doi.org/10.3354/meps07378 (2008).ADS 
    Article 

    Google Scholar 
    Bourque, J., Atwood, T. C., Divoky, G. J., Stewart, C. & McKinney, M. A. Fatty acid-based diet estimates suggest ringed seal remain the main prey of southern Beaufort Sea polar bears despite recent use of onshore food resources. Ecol. Evol. https://doi.org/10.1002/ece3.6043 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Thiemann, G. W., Derocher, A. E. & Stirling, I. Polar bear Ursus maritimus conservation in Canada: an ecological basis for identifying designatable units. Oryx 42, 504–515. https://doi.org/10.1017/S0030605308001877 (2008).Article 

    Google Scholar 
    Choy, E. S. et al. A comparison of diet estimates of captive beluga whales using fatty acid mixing models with their true diets. J. Exp. Mar. Biol. Ecol. 516, 132–139. https://doi.org/10.1016/j.jembe.2019.05.005 (2019).ADS 
    Article 

    Google Scholar 
    Kirsch, P. E., Iverson, S. J. & Bowen, W. D. Effect of a low-fat diet on body composition and blubber fatty acids of captive Juvenile Harp Seals (Phoca groenlandica). Physiol. Biochem. Zool. 73, 45–59. https://doi.org/10.1086/316723 (2000).CAS 
    Article 
    PubMed 

    Google Scholar 
    Koopman, H. N. Phylogenetic, ecological, and ontogenetic factors influencing the biochemical structure of the blubber of odontocetes. Mar. Biol. 151, 277–291. https://doi.org/10.1007/s00227-006-0489-8 (2007).Article 

    Google Scholar 
    Strandberg, U. et al. Stratification, composition, and function of marine mammal blubber: the ecology of fatty acids in marine mammals. Physiol. Biochem. Zool 81, 473–485. https://doi.org/10.1086/589108 (2008).CAS 
    Article 
    PubMed 

    Google Scholar 
    Choy, E. S. et al. Variation in the diet of beluga whales in response to changes in prey availability: insights on changes in the Beaufort Sea ecosystem. Mar. Ecol. Prog. Ser. 647, 195–210 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    Koopman, H. N., Iverson, S. J. & Gaskin, D. E. Stratification and age-related differences in blubber fatty acids of the male harbour porpoise (Phocoena phocoena). J. Comp. Physiol. B. 165, 628–639. https://doi.org/10.1007/BF00301131 (1996).CAS 
    Article 
    PubMed 

    Google Scholar 
    Budge, S. M., Iverson, S. J. & Koopman, H. N. Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Mar. Mamm. Sci. 22, 759–801. https://doi.org/10.1111/j.1748-7692.2006.00079.x (2006).Article 

    Google Scholar 
    Krahn, M. M. et al. Stratification of lipids, fatty acids and organochlorine contaminants in blubber of white whales and killer whales. J. Cetacean Res. Manag. 6, 175–189 (2004).
    Google Scholar 
    Loseto, L. L. et al. Summer diet of beluga whales inferred by fatty acid analysis of the eastern Beaufort Sea food web. J. Exp. Mar. Biol. Ecol. 374, 12–18. https://doi.org/10.1016/j.jembe.2009.03.015 (2009).CAS 
    Article 

    Google Scholar 
    Heide-Jørgensen, M.-P. Occurrence and hunting of killer whales in Greenland. Rit Fiskedeildar 11, 115–135 (1988).
    Google Scholar 
    Nøttestad, L. et al. Prey selection of offshore killer whales Orcinus orca in the Northeast Atlantic in late summer: spatial associations with mackerel. Mar. Ecol. Prog. Ser. 499, 275–283 (2014).ADS 
    Article 

    Google Scholar 
    Nikolioudakis, N. et al. Drivers of the summer-distribution of Northeast Atlantic mackerel (Scomber scombrus) in the Nordic Seas from 2011 to 2017; a Bayesian hierarchical modelling approach. ICES J. Mar. Sci. 76, 530–548. https://doi.org/10.1093/icesjms/fsy085 (2019).Article 

    Google Scholar 
    Olafsdottir, A. H. et al. Geographical expansion of Northeast Atlantic mackerel (Scomber scombrus) in the Nordic Seas from 2007 to 2016 was primarily driven by stock size and constrained by low temperatures. Deep Sea Res. Part II 159, 152–168. https://doi.org/10.1016/j.dsr2.2018.05.023 (2019).Article 

    Google Scholar 
    Jansen, T. et al. Ocean warming expands habitat of a rich natural resource and benefits a national economy. Ecol. Appl. 26, 2021–2032. https://doi.org/10.1002/eap.1384 (2016).Article 
    PubMed 

    Google Scholar 
    Ferguson, S. H., Higdon, J. W. & Westdal, K. H. Prey items and predation behavior of killer whales (Orcinus orca) in Nunavut, Canada based on Inuit hunter interviews. Aquat. Biosyst. 8, 3–3. https://doi.org/10.1186/2046-9063-8-3 (2012).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Laidre, K. L., Heide-Jørgensen, M. P. & Orr, J. R. Reactions of narwhals, Monodon monoceros, to killer whale, Orcinus orca, attacks in the eastern Canadian Arctic. Can. Field-Naturalist 120, 457–465 (2006).Article 

    Google Scholar 
    Willoughby, A. L., Ferguson, M. C., Stimmelmayr, R., Clarke, J. T. & Brower, A. A. Bowhead whale (Balaena mysticetus) and killer whale (Orcinus orca) co-occurrence in the U.S. Pacific Arctic, 2009–2018: evidence from bowhead whale carcasses. Polar Biol. 43, 1669–1679. https://doi.org/10.1007/s00300-020-02734-y (2020).Article 

    Google Scholar 
    Bloch, D. & Lockyer, C. Killer whales (Orcinus orca) in Faroese waters. Rit Fiskideildar 11, 55–64 (1988).
    Google Scholar 
    Pedro, S. et al. Blubber-depth distribution and bioaccumulation of PCBs and organochlorine pesticides in Arctic-invading killer whales. Sci. Total Environ. 601, 237–246. https://doi.org/10.1016/j.scitotenv.2017.05.193 (2017).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Samarra, F. I. P. et al. Prey of killer whales (Orcinus orca) in Iceland. PLoS ONE 13, 20. https://doi.org/10.1371/journal.pone.0207287 (2018).CAS 
    Article 

    Google Scholar 
    Jourdain, E. et al. Isotopic niche differs between seal and fish-eating killer whales (Orcinus orca) in northern Norway. Ecol. Evol. 10, 4115–4127. https://doi.org/10.1002/ece3.6182 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bromaghin, J. F., Budge, S. M., Thiemann, G. W. & Rode, K. D. Assessing the robustness of quantitative fatty acid signature analysis to assumption violations. Methods Ecol. Evol. 7, 51–59. https://doi.org/10.1111/2041-210X.12456 (2016).Article 

    Google Scholar 
    Jefferson, T. A., Stacey, P. J. & Baird, R. W. A review of Killer Whale interactions with other marine mammals: predation to co-existence. Mamm. Rev. 21, 151–180. https://doi.org/10.1111/j.1365-2907.1991.tb00291.x (1991).Article 

    Google Scholar 
    Bromaghin, J. F. QFASAR: quantitative fatty acid signature analysis with R. Methods Ecol. Evol. 8, 1158–1162. https://doi.org/10.1111/2041-210x.12740 (2017).Article 

    Google Scholar 
    Stewart, C., Iverson, S. & Field, C. Testing for a change in diet using fatty acid signatures. Environ. Ecol. Stat. 21, 775–792. https://doi.org/10.1007/s10651-014-0280-9 (2014).MathSciNet 
    CAS 
    Article 

    Google Scholar 
    Zhang, J. et al. Review of estimating trophic relationships by quantitative fatty acid signature analysis. J. Marine Sci. Eng. 8, 1030 (2020).Article 

    Google Scholar 
    Budge, S. M., Penney, S. N., Lall, S. P. & Trudel, M. Estimating diets of Atlantic salmon (Salmo salar) using fatty acid signature analyses; validation with controlled feeding studies. Can. J. Fish. Aquat. Sci. 69, 1033–1046. https://doi.org/10.1139/f2012-039 (2012).CAS 
    Article 

    Google Scholar 
    Happel, A. et al. Evaluating quantitative fatty acid signature analysis (QFASA) in fish using controlled feeding experiments. Can. J. Fish. Aquat. Sci. 73, 1222–1229. https://doi.org/10.1139/cjfas-2015-0328 (2016).CAS 
    Article 

    Google Scholar 
    Bromaghin, J. F. Simulating realistic predator signatures in quantitative fatty acid signature analysis. Eco. Inform. 30, 68–71. https://doi.org/10.1016/j.ecoinf.2015.09.011 (2015).Article 

    Google Scholar 
    Bromaghin, J. F., Budge, S. M., Thiemann, G. W. & Rode, K. D. Simultaneous estimation of diet composition and calibration coefficients with fatty acid signature data. Ecol. Evol. 7, 6103–6113. https://doi.org/10.1002/ece3.3179 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Burns, J. M., Costa, D. P., Frost, K. & Harvey, J. T. Development of body oxygen stores in harbor seals: effects of age, mass, and body composition. Physiol. Biochem. Zool. 78, 1057–1068. https://doi.org/10.1086/432922 (2005).CAS 
    Article 
    PubMed 

    Google Scholar 
    Noren, D. P. & Mocklin, J. A. Review of cetacean biopsy techniques: Factors contributing to successful sample collection and physiological and behavioral impacts. Mar. Mamm. Sci. 28, 154–199. https://doi.org/10.1111/j.1748-7692.2011.00469.x (2012).Article 

    Google Scholar  More

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    Cohort dominance rank and “robbing and bartering” among subadult male long-tailed macaques at Uluwatu, Bali

    Study siteWe conducted this research at the Uluwatu temple site in Bali, Indonesia. Uluwatu is located on the Island’s southern coast, in the Badung Regency. The temple at Uluwatu is a Pura Luhur, which is a significant temple for Balinese Hindus across the island and is therefore visited regularly for significant regional, community, family, and household rituals by Balinese people from different regions throughout the year18. During the period of data collection hundreds of tourists also visit the Uluwatu temple each day. The temple sits on top of a promontory cliff edge, with walking paths in front of it that continue in loops to the North and South. These looping pathways surround scrub forests, which the macaques frequently inhabit but the humans rarely enter.In 2017–2018 there were five macaque groups at Uluwatu, which ranged throughout the temple complex area, and beyond. All groups are provisioned daily with a mixed diet of corn, cucumbers, and bananas by temple staff members. The two groups included in this research are the Celagi and Riting groups. We selected these groups because they previously exhibited significant differences in robbing frequencies whereby Riting was observed exhibiting robbing and bartering more frequently than Celagi1. Furthermore, both groups include the same highly trafficked tourist areas in their overlapping home ranges relative to the other groups at Uluwatu, theoretically minimizing between group differences in the contexts of human interaction1,19.Data collectionJVP collected data from May, 2017 to March, 2018 totaling 197 focal observation hours on all 13 subadult males in Celagi and Riting that were identified in May–June 2017. Subadult male long-tailed macaques exhibit characteristic patterns of incomplete canine eruption, sex organ development, and body size growth, which achieves a maximum of 80% of total adult size18. Mean sampling effort per individual was 15.2 hours (h), with a range of 1.75 h, totaling 102.75 h for Riting and 94.75 h for Celagi. The data collection protocol consisted of focal-animal sampling and instantaneous scan sampling20 on all six subadult males in the Celagi group, and all seven subadult males in the Riting group. Focal follows were 15 minutes in length. Sampling effort per individual is presented in Table 1. A random number generator determined the order of focal follows each morning. In the event a target focal animal could not be located within 10 minutes of locating the group, the next in line was located and observed. Data presented here come from focal animal sampling records of state and event behaviors. Relevant event behaviors consist of agonistic gestures used for calculating dominance relationships, including the target, or interaction partner, of all communicative event behaviors and the time of its occurrence. All changes in the focal animal’s state behavior were noted, recording the time of the change to the minute.Table 1 Focal Subadult male long-tailed macaques in Celagi and Riting at Uluwatu, Bali, Indonesia.Full size tableDuring focal samples we recorded robbing and bartering as a sequence of mixed event and state behaviors. We scored both the robbery and exchange phases as event behaviors, and the interim phase of item possession as a state behavior. We record a robbery as successful if the focal animal took an object from a human and established control of the object with their hands or teeth, and as unsuccessful if the focal animal touched the object but was not able to establish control of it. For each successful robbery we recorded the object taken. Unsuccessful robberies end the sequence, whereas successful robberies are typically followed by various forms of manipulating the object.The robbing and bartering sequence ends with one of several event behavior exchange outcomes: (1) “Successful exchanges” consist of the focal animal receiving a food reward from a human and releasing the stolen object; (2) “forced exchanges” are when a human takes the object back without a bartering event; (3) “dropped objects” describe when the macaque loses control of the object while carrying it or otherwise locomoting, and is akin to an “accidental drop”; (4) “no exchange” includes instances of the macaque releasing the object for no reward after manipulating it; and (5) “expired observation” consists of instances in which the final result of the robbing and bartering event was unobserved in the sample period (i.e., the sample period ended while the macaque still had possession of the object). A 6th exchange outcome is “rejected exchange,” which occurs when the focal animal does not drop the stolen object after being offered, or in some cases even accepting, a food reward. The “rejected exchange” outcome is unique in that it does not end the robbing and bartering sequence because a human may have one or more exchange attempts rejected before eventually facilitating a successful exchange, or before one of the other outcomes (2–5) occurs. For each successful exchange we recorded the food item the macaques received. Food items are grouped into four categories: fruits, peanuts, eggs, and human snacks. Snacks include packaged and processed food items such as candy or chips.Data analysisWe grouped the broad range of stolen items into classes of general types. “Eyewear” combines eyeglasses and sunglasses, while “footwear” combines sandals and shoes. “Ornaments” includes objects attached to and/or hanging from backpacks, such as keychains, while “accessories” includes decorative objects attached to an individual’s body or clothing like bracelets and hair ties. “Electronics” covers cellular phones and tablets. “Hats” encompasses removable forms of headwear, most typically represented by baseball-style hats or sun hats. “Plastics” is an item class consisting of lighters and bottles, which may be filled with water, soda, or juice. The “unidentified” category is used for stolen items which could not be clearly observed during or after the robbing and bartering sequence.“Robbery attempts” refers to the combined total number of successful and unsuccessful robberies. “Robbery efficiency” is a novel metric referring to the number of successful robberies divided by the total number of robbery attempts. The “Exchange Outcome Index” is calculated by dividing the number of successful exchanges by the total number of robbery attempts. We make this calculation using robbery attempts instead of successful robberies to account for total robbery effort because failed robberies still factor into an individual’s total energy expenditure toward receiving a bartered food reward and their total exposure to the risks (e.g., physical retaliation) of stealing from humans relative to achieving the desired end result of a food reward.Social rank was measured with David’s Score, calculated using dyadic agonistic interactions. We coded “winners” of contests as those who exhibited the agonistic behavior, while “losers” were the recipients of those agonistic behaviors21,22. We excluded intergroup agonistic interactions in our calculations of David’s Score.To account for potential variation in the overall patterns of interaction with humans between groups we calculated a Human Interaction Rate, which is the sum of human-directed interactions from focal animals in each group divided by the total number of observation hours on focal animals in that group.Statistical analysisWe ran statistical tests in SYSTAT software with a significance level set at 0.05. We used chi-square goodness-of-fit tests to assess the significance of differences in successful robberies between individuals for each group. To avoid having cells with values of zero, two focal subjects, Minion and Spot from Celagi, are excluded from this test because neither were observed making a successful robbery during the observation period. We also used chi-square goodness-of-fit tests to assess exchange outcome occurrences within each group, as well as a Fisher’s exact to test for significant differences in robbery outcomes between groups due to low expected counts in 40% of the cells. “Rejected exchange” events were not included in the analysis of robbery outcomes because they do not end the sequence and are therefore not mutually exclusive with the other robbery outcomes.We further tested for the effect of dominance position on robbery outcomes. Due to our small sample size and the preliminary nature of this investigation, we used Spearman correlations to assess the relationship between subadult male dominance position via David’s Score and (1) robbing efficiency and (2) the Exchange Outcome Index.Compliance with ethical standardsThis research complied with the standards and protocols for observational fieldwork with nonhuman primates and was approved by the University of Notre Dame Compliance IACUC board (protocol ID: 16-02-2932), where JVP and AF were affiliated at the time of this research. This study did not involve human subjects. This research further received a research permit from RISTEK in Indonesia (permit number: 2C21EB0881-R), and complied with local laws and customary practices in Bali. More

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    Physiological and morphological effects of a marine heatwave on the seagrass Cymodocea nodosa

    IPCC: IPCC Special Report on the Ocean and Cryosphere in a Changing Climate [Pörtner, H.-O. et al.] In press (2019).Oliver, E. C. J. et al. Longer and more frequent marine heatwaves over the past century. Nat. Commun. 9, 1324 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Gibble, C. et al. Investigation of a largescale Common Murre (Uria aalge) mortality event in California, USA, in 2015. J. Wildl. Dis. 54, 569–574 (2018).PubMed 
    Article 

    Google Scholar 
    Brodeur, R. D., Auth, T. D. & Phillips, A. J. Major shifts in pelagic micronekton and macrozooplankton community structure in an upwelling ecosystem related to an unprecedented marine heatwave. Front. Mar. Sci. 6, 212 (2019).Article 

    Google Scholar 
    Le Nohaïc, M. et al. Marine heatwave causes unprecedented regional mass bleaching of thermally resistant corals in northwestern Australia. Sci. Rep. 7, 1–11 (2017).ADS 
    Article 
    CAS 

    Google Scholar 
    Hughes, T. P. et al. Global warming transforms coral reef assemblages. Nature 556, 492–496 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Genevier, L. G., Jamil, T., Raitsos, D. E., Krokos, G. & Hoteit, I. Marine heatwaves reveal coral reef zones susceptible to bleaching in the Red Sea. Glob. Change Biol. 25, 2338–2351 (2019).ADS 
    Article 

    Google Scholar 
    Leggat, W. P. et al. Rapid coral decay is associated with marine heatwave mortality events on reefs. Curr. Biol. 29, 2723–2730 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Green, E. P. & Short, F. T. World Atlas of Seagrasses (University of California Press, 2003).Duarte, C. M. The future of seagrass meadows. Environ. Conserv. 29, 192–206 (2002).Article 

    Google Scholar 
    Alongi, D. M. Blue Carbon: Coastal Sequestration for Climate Change Mitigation (Springer, Berlin, 2018).Book 

    Google Scholar 
    Blandon, A. & ZuErmgassen, P. S. Quantitative estimate of commercial fish enhancement by seagrass habitat in southern Australia. Estuarine Coast. Shelf Sci. 141, 1–8 (2014).ADS 
    Article 

    Google Scholar 
    Boudouresque, C. F., Mayot, N. & Pergent, G. The outstanding traits of the functioning of the Posidonia oceanica seagrass ecosystem. Biol. Mar. Medit. 13, 109–113 (2006).
    Google Scholar 
    Carr, J., D’odorico, P., McGlathery, K. & Wiberg, P. L. Stability and bistability of seagrass ecosystems in shallow coastal lagoons: Role of feedbacks with sediment resuspension and light attenuation. J. Geophys. Res. Biogeosci. https://doi.org/10.1029/2009JG001103 (2010).Article 

    Google Scholar 
    Welsh, D. T. Nitrogen fixation in seagrass meadows: regulation, plant–bacteria interactions and significance to primary productivity. Ecol. Lett. 3, 58–71. https://doi.org/10.1046/j.1461-0248.2000.00111.x (2000).Article 

    Google Scholar 
    Duarte, C. M. et al. Seagrass community metabolism: Assessing the carbon sink capacity of seagrass meadows. Glob. Biogeochem. Cycles. https://doi.org/10.1029/2010GB003793 (2010).Article 

    Google Scholar 
    Cabaço, S. & Santos, R. Human-induced changes of the seagrass Cymodocea nodosa in Ria Formosa lagoon (Southern Portugal) after a decade. Cah. Biol. Mar. 55, 101–108 (2014).
    Google Scholar 
    Marbà, N., Krause-Jensen, D., Masqué, P. & Duarte, C. M. Expanding Greenland seagrass meadows contribute new sediment carbon sinks. Sci. Rep. 8, 1–8 (2018).Article 
    CAS 

    Google Scholar 
    Bañolas, G., Fernández, S., Espino, F., Haroun, R. & Tuya, F. Evaluation of carbon sinks by the seagrass Cymodocea nodosa at an oceanic island: Spatial variation and economic valuation. Ocean Coast. Manag. 187, 105112 (2020).Article 

    Google Scholar 
    Duarte, C. M. & Krause-Jensen, D. Export from seagrass meadows contributes to marine carbon sequestration. Front. Mar. Sci. 4, 13 (2017).
    Google Scholar 
    Duarte, C. M., Middelburg, J. J. & Caraco, N. Major role of marine vegetation on the oceanic carbon cycle. Biogeosci. 2, 1–8 (2005).ADS 
    CAS 
    Article 

    Google Scholar 
    Kennedy, H. et al. Seagrass sediments as a global carbon sink: Isotopic constraints. Glob. Biogeochem. Cycles https://doi.org/10.1029/2010GB003848 (2010).Article 

    Google Scholar 
    Orth, R. J. et al. A global crisis for seagrass ecosystems. Bioscience 56, 987–996 (2006).Article 

    Google Scholar 
    Waycott, M. et al. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc. Natl. Acad. Sci. 106, 12377–12381 (2009).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Arias-Ortiz, A. et al. A marine heatwave drives massive losses from the world’s largest seagrass carbon stocks. Nat. Clim. Change 8, 338 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    Collier, C. J. et al. Optimum temperatures for net primary productivity of three tropical seagrass species. Front. Plant Sci. 8, 1446 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    George, R., Gullström, M., Mangora, M. M., Mtolera, M. S. & Björk, M. High midday temperature stress has stronger effects on biomass than on photosynthesis: a mesocosm experiment on four tropical seagrass species. Ecol. Evol. 8, 4508–4517 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Savva, I., Bennett, S., Roca, G., Jordà, G. & Marbà, N. Thermal tolerance of Mediterranean marine macrophytes: Vulnerability to global warming. Ecol. Evol. 8, 12032–12043 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Massa, S. I., Arnaud-Haond, S., Pearson, G. A. & Serrão, E. A. Temperature tolerance and survival of intertidal populations of the seagrass Zostera noltii (Hornemann) in Southern Europe (Ria Formosa, Portugal). Hydrobiologia 619, 195–201 (2009).Article 

    Google Scholar 
    Bergmann, N. et al. Population-specificity of heat stress gene induction in northern and southern eelgrass Zostera marina populations under simulated global warming. Mol. Ecol. 19, 2870–2883 (2010).PubMed 
    Article 

    Google Scholar 
    Franssen, S. U. et al. Genome-wide transcriptomic responses of the seagrasses Zostera marina and Nanozostera noltii under a simulated heatwave confirm functional types. Mar. Genomics 15, 65–73 (2014).PubMed 
    Article 

    Google Scholar 
    Qin, L. Z. et al. Influence of regional water temperature variability on the flowering phenology and sexual reproduction of the seagrass Zostera marina in Korean coastal waters. Estuaries Coasts 43, 449–462 (2020).CAS 
    Article 

    Google Scholar 
    Gao, Y. et al. Photosynthetic and metabolic responses of eelgrass Zostera marina L. to short-term high-temperature exposure. J. Oceanol. Limnol. 37, 199–209 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    Marín-Guirao, L. et al. Carbon economy of Mediterranean seagrasses in response to thermal stress. Mar. Pollut. Bull. 135, 617–629 (2018).PubMed 
    Article 
    CAS 

    Google Scholar 
    Costa, M. M., Silva, J., Barrote, I. & Santos, R. Heatwave effects on the photosynthesis and antioxidant activity of the seagrass Cymodocea nodosa under contrasting light regimes. Oceans 2, 448–460 (2021).Article 

    Google Scholar 
    de los Santos, C. et al. Recent trend reversal for declining European seagrass meadows. Nat. Commun. 10, 3356 (2019).Cunha, A. H., Assis, J. F. & Serrão, E. A. Reprint of “Seagrasses in Portugal: A most endangered marine habitat”. Aquat. Bot. 115, 3–13 (2014).Article 

    Google Scholar 
    Olsen, Y. S., Sánchez-Camacho, M., Marbà, N. & Duarte, C. M. Mediterranean seagrass growth and demography responses to experimental warming. Estuaries Coasts 35, 1205–1213 (2012).Article 

    Google Scholar 
    Marín-Guirao, L., Ruiz, J. M., Dattolo, E., Garcia-Munoz, R. & Procaccini, G. Physiological and molecular evidence of differential short-term heat tolerance in Mediterranean seagrasses. Sci. Rep. 6, 1–13 (2016).Article 
    CAS 

    Google Scholar 
    Lüning, K. Seaweeds. Their Environment, Biogeography, and Ecophysiology (Wiley-Interscience, New York, 1990).Lee, K. S., Park, S. R. & Kim, Y. K. Effects of irradiance, temperature, and nutrients on growth dynamics of seagrasses: a review. J. Exp. Mar. Biol. Ecol. 350, 144–175 (2007).Article 

    Google Scholar 
    Franssen, S. U. et al. Transcriptomic resilience to global warming in the seagrass Zostera marina, a marine foundation species. Proc. Natl. Acad. Sci. 108, 19276–19281 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Winters, G., Nelle, P., Fricke, B., Rauch, G. & Reusch, T. B. H. Effects of a simulated heat wave on photophysiology and gene expression of high- and low-latitude populations of Zostera marina. Mar. Ecol. Prog. Ser. 435, 83–95 (2011).ADS 
    Article 

    Google Scholar 
    Maxwell, K. & Johnson, G. N. Chlorophyll fluorescence—A practical guide. J. Exp. Bot. 51, 659–668 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Schubert, N. et al. Photoacclimation strategies in northeastern Atlantic seagrasses: Integrating responses across plant organizational levels. Sci. Rep. 8, 1–14 (2018).CAS 
    Article 

    Google Scholar 
    Miyake, C., Yonekura, K., Kobayashi, Y. & Yokota, A. Cyclic electron flow within PSII functions in intact chloroplasts from spinach leaves. Plant Cell Physiol. 43, 951–957 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    Rasmusson, L. M., Gullström, M., Gunnarsson, P. C. B., George, R. & Björk, M. Estimation of a whole plant Q10 to assess seagrass productivity during temperature shifts. Sci. Rep. 9, 1–9 (2019).CAS 
    Article 

    Google Scholar 
    Buapet, P. & Björk, M. The role of O2 as an electron acceptor alternative to CO2 in photosynthesis of the common marine angiosperm Zostera marina L. Photosynth. Res. 129, 59–69 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Mehler, A. H. Studies on reactions of illuminated chloroplasts. II Stimulation and inhibition of the reaction with molecular oxygen. Arch. Biochem. Biophys. 34, 339–51 (1951).CAS 
    PubMed 
    Article 

    Google Scholar 
    Apel, K. & Hirt, H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373–399 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    Chalanika De Silva, H. C. & Asaeda, T. Effects of heat stress on growth, photosynthetic pigments, oxidative damage and competitive capacity of three submerged macrophytes. J. Plant Interact. 12, 228–236 (2017).Article 
    CAS 

    Google Scholar 
    Beer, S., Björk, M., Gademann, R. & Ralph, P. Measurements of photosynthetic rates in seagrasses. In Global Seagrass Research Methods pp. 183–198 (Elsevier Science, 2001).Brodersen, K. E., Kühl, M., Nielsen, D. A., Pedersen, O. & Larkum, A. W. Rhizome, root/sediment interactions, aerenchyma and internal pressure changes in seagrasses. In Seagrasses of Australia pp. 393–418; https://doi.org/10.1007/978-3-319-71354-0_13 (Springer, Cham, 2018).Purnama, P. R., Purnama, E. R., Manuhara, Y. S. W., Hariyanto, S. & Purnobasuki, H. Effect of high temperature stress on changes in morphology, anatomy and chlorophyll content in tropical seagrass Thalassia hemprichii. AACL Bioflux 11, 1825–1833 (2018).
    Google Scholar 
    Rosalina, D., Herawati, E. Y., Musa, M., Sofarini, D. & Risjani, Y. Anatomical changes in the roots, rhizomes and leaves of seagrass (Cymodocea serrulata) in response to lead. Biodiversitas 20, 2583–2588; https://doi.org/10.13057/biodiv/d200921 (2019).Beca-Carretero, P., Olesen, B., Marbà, N. & Krause-Jensen, D. Response to experimental warming in northern eelgrass populations: comparison across a range of temperature adaptations. Mar. Ecol. Progr. Ser. 589, 59–72; https://doi.org/10.3354/meps12439 (2018).Beca-Carretero, P., Guihéneuf, F., Krause-Jensen, D. & Stengel, D. B. Seagrass fatty acid profiles as a sensitive indicator of climate settings across seasons and latitudes. Mar. Env. Res. 161, 105075; https://doi.org/10.1016/j.marenvres.2020.105075 (2020).Pérez, M. & Romero, J. Photosynthetic response to light and temperature of the seagrass Cymodocea nodosa and the prediction of its seasonality. Aquat. Bot. 43, 51–62; https://doi.org/10.1016/0304-3770(92)90013-9 (1992).Saha, M. et al. Response of foundation macrophytes to near‐natural simulated marine heatwaves. Global Change Biol. 26, 417–430; https://doi.org/10.1111/gcb.14801 (2020).Tutar, O., Marín-Guirao, L., Ruiz, J. M. & Procaccini, G. Antioxidant response to heat stress in seagrasses. A gene expression study. Mar. Environ. Res. 132, 94–102; https://doi.org/10.1016/j.marenvres.2017.10.011 (2017).Moreno‐Marín, F., Brun, F. G. & Pedersen, M. F. Additive response to multiple environmental stressors in the seagrass Zostera marina L. Limnol. Oceanogr. 63, 1528–1544; https://doi.org/10.1002/lno.10789 (2018).Kim, M. et al. Influence of water temperature anomalies on the growth of Zostera marina plants held under high and low irradiance levels. Estuaries Coasts 43, 463–476; https://doi.org/10.1007/s12237-019-00578-2 (2020).Egea, L. G., Jiménez-Ramos, R., Vergara, J. J., Hernández, I. & Brun, F. G. Interactive effect of temperature, acidification and ammonium enrichment on the seagrass Cymodocea nodosa. Mar. Pollut. Bull. 134, 14–26; https://doi.org/10.1016/j.marpolbul.2018.02.029 (2018).Newton, A. & Mudge, S. M. Temperature and salinity regimes in a shallow, mesotidal lagoon, the Ria Formosa, Portugal. Estuarine Coastal Shelf Sci. 57, 73–85; https://doi.org/10.1016/S0272-7714(02)00332-3 (2003).Instituto Hidrográfico. Marés 81/82 Ria de Faro. Estudo das marés de oito estacões da Ria de Faro pp. 13 (Lisbon: Instituto Hidrográfico, 1986).Andrade, J. P. Aspectos Geomorfológicos, Ecológicos e Socioeconómicos da Ria Formosa pp. 91 (Faro: Universidade do Algarve, 1985).Hobday, A.J. et al. A hierarchical approach to defining marine heatwaves. Prog. Oceanogr. 141, 227–238; https://doi.org/10.1016/j.pocean.2015.12.014 (2016).Hobday, A. J. et al. Categorizing and naming marine heatwaves. Oceanogr. 31, 162–173; https://doi.org/10.5670/oceanog.2018.205 (2018).Cunha, A. H., Paulo, D. S., Sousa, I. & Serrão, E. The rediscovery of Caulerpa prolifera in Ria Formosa, Portugal, 60 years after the previous record. Cah. Biol. Mar. 54, 359–364 (2013).
    Google Scholar 
    Huang, B. et al. Improvements of the daily optimum interpolation sea surface temperature (DOISST) Version 2.1. J. Clim. 34, 2923–2939 (2020).ADS 
    Article 

    Google Scholar 
    Reynolds, R. W. et al. Daily high-resolution-blended analyses for sea surface temperature. J. Clim. 20, 5473–5496 (2007).ADS 
    Article 

    Google Scholar 
    Banzon, V., Smith, T. M., Chin, T. M., Liu, C. & Hankins, W. A long-term record of blended satellite and in situ sea-surface temperature for climate monitoring, modelling and environmental studies. Earth Syst. Sci. Data 8, 165–176 (2016).ADS 
    Article 

    Google Scholar 
    Schlegel, R. W. Marine Heatwave Tracker. http://www.marineheatwaves.org/tracker; 10.5281/zenodo.3787872 (2020).Field, C. B., Barros, V., Stocker, T. F. & Dahe, Q. (Eds.). Managing the risks of extreme events and disasters to advance climate change adaptation: special report of the intergovernmental panel on climate change (IPCC) (Cambridge University Press, 2012).Silva, J., Barrote, I., Costa, M. M., Albano, S. & Santos, R. Physiological responses of Zostera marina and Cymodocea nodosa to light-limitation stress. PLoS One 8, e81058 (2013).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Silva, J. & Santos, R. Can chlorophyll fluorescence be used to estimate photosynthetic production in the seagrass Zostera noltii?. J. Exp. Mar. Biol. Ecol. 307, 207–216 (2004).CAS 
    Article 

    Google Scholar 
    Jassby, A. D. & Platt, T. Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol. Oceanogr. 21, 540–547 (1976).ADS 
    CAS 
    Article 

    Google Scholar 
    Henley, W. J. Measurement and interpretation of photosynthetic light-response curves in algae in the context of photoinhibition and diel changes. J. Phycol. 29, 729–739 (1993).Article 

    Google Scholar 
    Genty, B., Briantais, J. M. & Baker, N. R. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 990, 87–92 (1989).CAS 
    Article 

    Google Scholar 
    Folin, O. & Ciocalteu, V. On tyrosine and tryptophane determinations in proteins. J. Biol. Chem. 73, 627–650 (1927).CAS 
    Article 

    Google Scholar 
    Booker, F. L. & Miller, J. E. Phenylpropanoid metabolism and phenolic composition of soybean [Glycine max (L) Merr] leaves following exposure to ozone. J. Exp. Bot. 49, 1191–1202 (1998).CAS 
    Article 

    Google Scholar 
    Re, R. et al. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biol. Med. 26, 1231–1237 (1999).CAS 
    Article 

    Google Scholar 
    Gillespie, K. M., Chae, J. M. & Ainsworth, E. A. Rapid measurement of total antioxidant capacity in plants. Nat. Protoc. 2, 867–870 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Huang, D., Ou, B., Hampsch-Woodill, M., Flanagan, J. A. & Prior, R. L. High-Throughput Assay of Oxygen Radical Absorbance Capacity (ORAC) Using a Multichannel Liquid Handling System Coupled with a Microplate Fluorescence Reader in 96-Well Format. J. Agric. Food Chem. 50, 4437–4444 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hodges, D. M., DeLong, J. M., Forney, C. F. & Prange, R. K. Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207, 604–611 (1999).CAS 
    Article 

    Google Scholar 
    Rasband, W.S. ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, 1997–2018. https://imagej.nih.gov/ij/ (1997).R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/ (2014).Devore, J. & Farnum, N. Applied Statistics for Engineers and Scientists (ed. Brooks/Cole) pp. 656 (Pacific Grove, CA, USA, 1999). More

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    Shifting agriculture is the dominant driver of forest disturbance in threatened forest species’ ranges

    Our results show that the effects of the forest disturbance drivers on biodiversity are likely to be different from those simply expected from the baseline proportions of the forest disturbance drivers if we take into account the threatened species’ distributions. The amount of forest habitat is a primary factor for species diversity of many taxa, including mammals, amphibians, reptiles, birds, insects, and plants18. Indeed, our results revealed that threatened forest species have been exposed to a disproportional decrease in their habitat amount globally (i.e., lower proportions of forest with no or minor loss in all regions when species ranges were considered). Although this finding may be intuitive as population size and/or species range are part of the criteria in the IUCN assessment19, the detected pattern supports the validity of our approach of combining a forest disturbance map and species ranges for evaluating the impact of forest disturbances on threatened species. Moreover, we found that the dominant drivers differ among regions: the proportion of forestry, for example, increased in northern regions such as North America and Europe, whereas that of shifting agriculture increased in tropical regions when threatened species’ distributions were considered. These facts indicate although several influential international schemes for conservation have been implemented for regulating forestry20,21, different mechanisms aiming to directly tackle the over land use for local agriculture may increase their importance when we consider conservation in tropical regions. Our findings suggest that the social and economic drivers underlying the forest disturbance that impacts biodiversity differ among regions or nations, and it is important to establish specific conservation strategies in order to be effective.Based on the findings, we further emphasize that the combinations of multiple interacting drivers are likely to vary among regions. For example, the frequency and extent of stand-replacing natural disturbances such as wildfires have clearly been magnified by climate change, particularly in the Northern Hemisphere (e.g.,22). After such natural disturbances, societal demand for timber and/or pest reduction compels forest managers to ‘salvage’ timber by logging before it deteriorates, a common practice even in locations otherwise exempt from conventional green-tree harvesting, such as national parks or wilderness areas23. Thus, salvage logging clearly mediates the interaction between disturbances by forestry and wildfires and is likely to further affect biodiversity under climate change. Especially in regions where infrastructure (e.g., irrigation systems) has not been well developed, unpredictable changes in precipitation due to climate change was reported to increase forest disturbance by unregulated increases of agricultural land use24. Such regions largely overlapped with regions where shifting agriculture was identified as a dominant disturbance driver for threatened species in this study. Moreover, species themselves shift their ranges in response to climate change25, which would also shift major disturbance drivers and influential interactions of drivers to which the species are exposed, given the region-specific driver patterns. These examples clearly suggest the necessity to understand both the region-specific interrelations among multiple drivers and species’ responses for better prediction of land-use change and thus its effects on biodiversity.Shifting agriculture was the most dominant driver in all tropical regions corresponding to the recent estimates suggesting that the cover of regenerating secondary forest is increasing worldwide26. We demonstrated that this tendency is more drastic especially within the range of threatened species. The effect of shifting agriculture per unit area might be more limited than that of commodity-driven deforestation, which permanently alters forests into other land uses, since habitat structure might recover as the forest vegetation regenerates to a secondary state following the abandonment of the small clearings. However, ample evidence shows that many types of agricultural activities significantly degrade the conservation value of primary forest, especially in the tropics27, which often recovers very slowly if ever28 with the loss of irreplaceable conservation values. Therefore, given the wide areas of dominance of shifting agriculture across all tropical regions, its effect is likely to be pervasive. Consistently, our results show that species extinction risk (i.e., IUCN Red List status) is positively related to the proportional coverage of shifting agriculture (Fig. 2). In addition, as expected, a larger current proportion of shifting agriculture within a species range worsens the change rate in IUCN Red List status of the species (Fig. 4b). Furthermore, the effect is anticipated to be magnified for forest specialists because they are exposed to larger proportions of shifting agriculture than are forest generalist (Fig. 2), and they are also reported to recover more slowly than do forest habitat generalists27,28.A guideline for forest restoration suggested that appropriately sized landscapes should contain ≥40% forest cover (higher percentages are likely needed in the tropics), with about 10% in a very large forest patch and the remaining 30% in many evenly dispersed smaller patches and semi-natural wooded elements (e.g., vegetation corridors)29. Importantly, the guideline also suggests that the patches should be embedded in a high-quality matrix. Although younger secondary forest cannot be a substitute for pristine forest until 50 years or more after a disturbance, it can help to improve the quality of matrix in agricultural landscapes30. Indeed, we show that the negative impacts of shifting agriculture and forestry on IUCN status change have improved over time (Fig. 4b, c), presumably corresponding to the forest regenerating and recovery process. In contrast, the pattern of commodity-driven deforestation, a land use accompanied with permanent forest loss, showed a prolonged negative impact on IUCN status change (Fig. 4a). Notably, whether regenerating forests can move towards a highly diverse and structurally complex state or towards a state of low to intermediate levels of biodiversity and structural complexity depends on the amount of remaining intact mature forest in the landscape29. Therefore, a promising direction for future research would be to develop our analysis further to include spatiotemporal relationships among mature forest remnants, secondary forests, disturbance drivers, and threatened species populations.For conserving the core patches of mature forests, the establishment of protected areas (PAs) is one of the most effective legal measures that has been widely used to regulate land use for biodiversity31. On the other hand, for improving matrix quality, balancing conservation and use of the ecosystem would be critically important; shifting agriculture, for example, causes forest degradation, but it also contributes to food supply chains sourced from smallholder farmers and to food security of local communities8. In fact, establishing mechanisms for managing biodiversity-friendly landscapes has been intensively discussed recently, given the large potential influence of these landscapes on conservation32. These mechanisms include setting an international target on OECMs15. Our finding of a disproportional decrease in forest proportions with minor or no loss within species ranges supports the urgency of the discussion. At the same time, our results highlight an opportunity because large portions of the disturbed forests for threatened species are dominated by shifting agriculture at the global scale, especially in the tropics. As suggested above, if manged properly, such landscapes can still retain or improve functions as essential habitats and/or matrix for a variety of forest-dwelling species. Our analytical method provides a tool set to identify and prioritize areas where such attempts are urgently needed.Global demands for natural resources and ecosystem services drive land use in forests33 and thus affect biodiversity. Therefore, connecting the supply chains to the five major drivers of forest disturbance and their spatial overlaps with biodiversity is essential to inform how we should regulate and design material flows from forest ecosystems to keep them sustainable by minimizing the effects on biodiversity. Existing studies examining the impacts of resource consumption on biodiversity through supply chains of various sectors have often been assessed at the country scale (e.g.,12), partly because the availability of statistics needed to estimate material flows in supply chains is usually limited at finer (i.e., subnational) scales (but see34). We believe that our study provides the first basis for filling the resolution gap between trade statistics and local biodiversity effects by identifying patterns of the local co-occurrence of biodiversity and the forest disturbance drivers that can be directly linked to resource production at the national scale. Note, however, that downscaling a remotely sensed global data set into finer scales inevitably propagates errors and biases which include both those in the original maps and those in the processed data produced by analyses. Thus, preparation of more high-resolution data sets is essential, especially for disturbance drivers and threatened species’ distributions in our case, to keep the errors and biases at a reasonable level at focal spatial scales.The effectiveness of area-based conservation measures to regulate land use for conservation including PAs and OECMs also depends strongly on social and ecosystem conditions. For example, a few studies show that the effectiveness of PAs in halting or slowing forest disturbances depends on PA characteristics such as size and history, as well as on the management entities such as subnational governments or indigenous peoples35,36,37. Moreover, there has been no attempt to elucidate whether PAs and OECMs are effective at regulating supply chains as a supply-side measure by balancing resource production, ecosystem services for local communities, and biodiversity conservation; to tackle this issue, it will be necessary to conduct extensive analyses integrating spatial and temporal patterns of biodiversity, forest loss, its drivers, and material flows in global food supply chains. Though it is challenging and beyond the scope of this paper, solving this issue is urgent and raises a promising opportunity for future research. More

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    Understanding the diversity and biogeography of Colombian edible plants

    Carvalho, A. M. & Barata, A. M. The consumption of wild edible plants. In Wild plants, mushrooms and nuts: functional food properties and applications (eds Isabel, C. F. R. et al.) (John Wiley & Sons, New York City, 2017).
    Google Scholar 
    Diazgranados, M. et al. World checklist of useful plant species. Royal Botanic Gardens, Kew. (Richmond, UK, 2020).
    Google Scholar 
    Ulian, T. et al. Unlocking plant resources to support food security and promote sustainable agriculture. Plants People Planet 12(5), 421–445 (2020).Article 

    Google Scholar 
    Shaheen, S., Ahmad, M., Haroon, N. Edible wild plants: a solution to overcome food insecurity. In: Edible Wild Plants: An alternative approach to food security (eds Shaheen, S., et al.) 41–57. Springer, Cham. https://doi.org/10.1007/978-3-319-63037-3_2 (2017).Chapter 

    Google Scholar 
    Food and Agriculture Organization. World programme for the census of agriculture 2020, Vol. 1. FAO, (Rome, Italy, 2015).
    Google Scholar 
    Wolff, F. Legal factors driving agrobiodiversity loss. Environ. Law Netw. Int. 1, 1–11 (2004).
    Google Scholar 
    Padulosi, S., Heywood, V., Hunter, D. & Jarvis, A. Underutilized species and climate change: current status and outlook. In Crop Adaptation to Climate Change (eds Shyam, S. Y. et al.) 507–517 (Blackwell Publishers, 2011).Chapter 

    Google Scholar 
    Kalamandeen, M., Gloor, E. & Mitchard, E. Pervasive raise of small-scale deforestation in Amazonia. Sci. Rep. 8(1600), 1–10 (2018).CAS 

    Google Scholar 
    Kor, L., Homewood, K., Dawson, T. P. & Diazgranados, M. Sustainability of wild plant use in the Andean community of South America. Ambio 50, 1681–1697 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Nogueira, S. & Nogueira-Filho, S. Wildlife farming: an alternative to unsustainable hunting and deforestation in neotropical forests?. Biodivers. Consrv. 20, 1385–1397 (2011).Article 

    Google Scholar 
    Pilgrim, S. E., Cullen, L. C., Smith, D. J. & Pretty, J. Ecological knowledge is lost in wealthier communities and countries. Environ. Sci. Technol. 42(4), 1004–1009 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Sánchez-Cuervo, A. M. & Mitchell-Aide, T. Consequences of the armed conflict forced human displacement, and land abandonment on forest cover change in Colombia: a multi-scaled analysis. Ecosystems 16, 1052–1070 (2013).Article 

    Google Scholar 
    Rodriguez-Eraso, N., Armenteras-Pascual, D. & Retana-Alumbreros, J. Land use and land cover change in the Colombian Andes: dynamics and future scenarios. J. Land Use Sci. 8(2), 154–174 (2013).Article 

    Google Scholar 
    Food and Agriculture Organization. in The State of the World’s biodiversity for food and agriculture. FAO Commission on Genetic Resources for Food and Agriculture Assessments (eds Bélanger, J., Pilling, D.). (FAO, Rome, Italy, 2019).Borelli, T. et al. Local solutions for sustainable food systems: the contribution of orphan crops and wild edible species. Agronomy 10(2), 231–256 (2020).CAS 
    Article 

    Google Scholar 
    Padulosi, S., Thompson, J. & Rudebjer, P. Fighting poverty, hunger and malnutrition with neglected and underutilized species (NUS): needs, challenges and the way forward (Bioversity International, 2013).
    Google Scholar 
    Hunter, D. et al. The potential of neglected and underutilized species for improving diets and nutrition. Planta 250, 709–729 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Brehmy, J. M., Maxted, N., Martin-Louçao, M. A. & Frod-Lloyd, B. V. New approaches for establishing conservation priorities for socio-economically important plant species. Biodivers. Conserv. 19(9), 2715–2740 (2010).Article 

    Google Scholar 
    N’Danikou, S., Achigan-Dako, E. G. & Wong, J. L. G. Eliciting local values of wild edible plants in Southern Benin to identify priority species for conservation. Econ. Bot. 65, 381–395 (2011).Article 

    Google Scholar 
    Dulloo, M. E. et al. Conserving agricultural biodiversity for use in sustainable food systems. (2017).de Oliveira Beltrame, D. M. et al. Brazilian underutilised species to promote dietary diversity, local food procurement, and biodiversity conservation: a food composition gap analysis. Lancet Planet. Health. 2, S22. (2018).Article 

    Google Scholar 
    Raven, P. H. et al. The distribution of biodiversity richness in the tropics. Sci. Adv. 6(37), 1–5 (2020).Article 

    Google Scholar 
    Renjifo, L. M., Amaya-Villareal, A. M. & Butchart, S. H. M. Tracking extinction risk trends and patterns in a mega-diverse country: a red list index for birds in Colombia. PLoSONE 15(1), 1–19 (2020).Article 

    Google Scholar 
    Clerici, N., Salazar, C., Pardo-Díaz, C., Jiggins, C. D. & Linares, M. Peace in Colombia is a critical moment for neotropical connectivity and conservation: save the northern Andes-Amazon biodiversity bridge. Conserv. Lett. 12, 1–7 (2019).Article 

    Google Scholar 
    Hurtado-Bermudez, L. J., Vélez-Torres, I. & Méndez, F. No land for food: prevalence of food insecurity in ethnic communities enclosed by sugarcane monocrop in Colombia. Int. J. Public Health 65, 1087–1096 (2020).PubMed 
    Article 

    Google Scholar 
    Boron, V., Payan, E., McMillan, D. & Tzanopulos, J. Achieving sustainable development in rural areas in Colombia: future scenarios for biodiversity conservation under land use change. Land Use Policy 59, 27–37 (2016).Article 

    Google Scholar 
    Grau, H. R. & Aide, M. Globalization and land-use transitions in Latin America. Ecol. Soc. 13(2), 1–16 (2008).Article 

    Google Scholar 
    Rivas Abadía, X., Pazos, S. C., Castillo, S. K. & Pachón, H. Indigenous foods of the indigenous and Afro-descendant communities of Colombia (International Center for Tropical Agriculture (CIAT), Cali, 2010) ((In Spanish, English summary)).
    Google Scholar 
    López Diago, D. & García, N. Wild edible fruits of Colombia: diversity and use prospects. Biota Colomb. 22(2), 16–55 (2021).Article 

    Google Scholar 
    Pieroni, A., Pawera, L. & Shah, G. M. Gastronomic ethnobiology. In Introduction to Ethnobiology (eds Albuquerque, U. P. & Alves, R. N.) 53–62 (Springer, 2016).Chapter 

    Google Scholar 
    Castañeda, R. R. Frutas silvestres de Colombia. Instituto Colombiano de Cultura Hispánica. (1991).Medina, C. I., Martínez, E. & López, C. A. Phenological scale for the mortiño or agraz (Vaccinium meridionale Swartz) in the high Colombian Andean area. Revista Facultad Nacional de Agronomía Medellín 72(3), 8897–8908 (2019).Article 

    Google Scholar 
    Asprilla-Perea, J. & Díaz-Puente, J. M. Traditional use of wild edible food in rural territories within tropical forest zones: a case study from the northwestern Colombia. New Trends Issues Proc. Humanit. Soc. Sci. 5(1), 162–181 (2018).
    Google Scholar 
    López Estupiñán, L. Potatoes and land in Boyacá: ethnobotanical and ethnohistorical research of one of the main products of Colombian food. Boletín de Antropología Universidad de Antioquia 30(50), 170–190 (2015) ((In Spanish)).
    Google Scholar 
    Marín Santamaría, C.M. Potential for food use for human consumption of wild fruits in Encenillo Biological Reserve, Guasca, Cundinamarca. Thesis in Biological Sciences. Pontificia Universidad Javeriana. Bogotá, Colombia. (2010) (In Spanish).Molina Samacá, J. R. Ancestral Food Plant Heritage: Construction of the Baseline in the Province of Sumapaz. Master thesis in Agricultural Sciences. University of Cundinamarca, Colombia (2019) (In Spanish).Pasquini, M. W., Sánchez-Ospina, C. & Mendoza, J. S. Traditional food plant knowledge and use in three afro-descendant communities in the Colombian Caribbean Coast: Part II drivers of change. Econ. Bot. 72(3), 295–310 (2018).Article 

    Google Scholar 
    Villa Villegas, M. Análisis del conocimiento asociado al uso de la flora alimenticia y medicinal en la comunidad de San Francisco, Acandí (Chocó. Pontificia Universidad Javeriana, 2020).
    Google Scholar 
    Cook, E. M. F. Economic botany data collection standard (Royal Botanic Gardens, Kew, Richmond, 1995).
    Google Scholar 
    Diazgranados, M. & Kor, L. Notes on the biogeographic distribution of the useful plants of Colombia. In: Catalogue of useful plants of Colombia (eds Negrão, R. et al.) 147–161. Royal Botanic Gardens, Kew. Kew Publishing, London (in press).Diazgranados, M. et al. Annotated checklist of useful plants of Colombia. In: Catalogue of useful plants of Colombia (eds Negrão, R. et al.) 165–473. Royal Botanic Gardens, Kew. Kew Publishing, London (in press).R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. Available at: https://www.R-project.org/. (2021)POWO. Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. Retrieved on 14 April, 2021, from: http://www.plantsoftheworldonline.org/ (2021).Missouri Botanical Gardens. Tropicos.org. Retrieved on 10 April 2021, https://tropicos.org (2021)Wickham, H. The split-apply-combine strategy for data analysis. J. Stat. Softw. 40(1), 1–29 (2011).Article 

    Google Scholar 
    Wickham, H., Francois, R. Dplyr: A Grammar of Data Manipulation. R Package Version 0.4.3 (2021).GBIF Sectretaria. GBIF backbone taxonomy. Retrieved on 22 April 2021, from: https://www.gbif.org/ (2021)Food and Agriculture Organization. The second report on the State of The World’s plant genetic resources for food and agriculture. (FAO, Rome, Italy, 2015).Bystriakova, N. et al. Colombia’s bioregions as a source of useful plants. PLoS One 16(8), 1–19 (2021).Article 

    Google Scholar 
    Olson, D. M. et al. Terrestrial ecoregions of the world: A new map of life on earth a new global map of terrestrial ecoregions provides an innovative tool for conserving biodiversity. BioScience 51(11), 933–938 (2001).Article 

    Google Scholar 
    Chamberlain, S., Oldoni, D., Barve, V., Desmet, P., Geffert, L., Mcglinn, D., Ram, K. Rgbif: interface to the global “Biodiversity” information facility API. R Package Version 3.6.0. (2021)Ondo, I. et al. ShinyCCleaner: an interactive app for cleaning species occurrence records. Unpublished (2021).Bivand, R., Keitt, T., Rowlingson, B., Pebesma, E., Summer, M., Hijmans, R., Baston, D., Rouault, E., et al. Rgdal: bindings for the “Geospatial” data abstraction library. R Package Version 1.5-23. Retrieved from: https://cran.r-project.org/web/packages/rgdal/index.html (2021)Hijmans, R. J., van Etten, J. Raster: geographic analysis and modeling with raster data. R package version 2.0-12. Available at: http://CRAN.R-project.org/package=raster (2012)Bivand, R.S., Pebesma, E., Gomez-Rubio, V. Applied spatial data analysis with R, Second edition. Springer, NY. Available at: https://asdar-book.org/ (2013)Brown, J. L., Bennett, J. & French, C. M. SDMtoolbox: the next generation python-based GIS toolkit for landscape genetic, biogeographic and species distribution model analyses. PeerJ 5, e4095 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    DANE. Indigenous population of Colombia. In: Results of the national population and housing census 2018 (eds DANE). (Bogotá, Colombia, 2019) (In Spanish).Minority Rights Home Minorities and indigenous peoples in Colombia. Retrieved on 20 October, 2021, from: Colombia – World Directory of Minorities & Indigenous Peoples (minorityrights.org) (2021).Maffi, L. & Woodley, E. Biocultural diversity conservation: a global sourcebook 304 (Routledge, 2012).Book 

    Google Scholar 
    van Zonnevelda, M. et al. Human diets drive range expansion of megafauna-dispersed fruit species. PNAS 115(13), 3326–3331 (2018).Article 

    Google Scholar 
    Diazgranados, M., Mendoza, J. E., Peñuela, M., Ramírez, W. Comida, identidad, paisaje… ¿articulación o antagonismo? Universitas Humanistica pp. 119–127. ISSN-0120-4807 (1997).Rojas, T.M., Cortés, C., Pizano, M.N., Ulian, T., Diazgranados, M. Evaluación del estado de los desarrollos bioeconómicos colombianos en plantas y hongos. Royal Botanic Gardens, Kew and Instituto de Investigaciones en Recursos Biológicos Alexander von Humboldt (2020).Departamento Administrativo de la Función Pública. Decree 690 of 2021, Article 10. Bogotá, Colombia (2021).Ahoyo, C. C. et al. A quantitative ethnobotanical approach toward biodiversity conservation of useful woody species in Wari-Maro forest reserve (Benin, West Africa). Environ. Dev. Sustain. https://doi.org/10.1007/s10668-017-9990-0 (2017).Article 

    Google Scholar 
    Suwardi, A. B., Navia, Z. I., Harmawan, T. & Syamsuardi, E. Ethnobotany and conservation of indigenous edible fruit plants in South Aceh, Indonesia. Biodiversitas 12(5), 1850–1860 (2020).
    Google Scholar 
    Pei, S., Alan, H. & Wang, Y. Vital roles for ethnobotany in conservation and sustainable development. Plant Divers. 42(6), 399 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bernal, M. H. Y. & Correa, Q. J. E. Erythrina edulis. In Promising plant species from countries of the Convenio Andrés Bello Vol. 8 (eds Bernal, M. H. Y. & Correa, Q. J. E.) 231–278 (Editora Guadalupe Ltda, Bogotá, 1992) ((In Spanish)).
    Google Scholar 
    Bernal, M.H.Y., Correa, Q.J.E. Food plants of Colombia. in Promising plant species from the Andrés Bello Convention countries (andean countries). First edition. (eds Bernal M.H.Y., Correa, Q.J.E.) Editora Guadalupe Ltda. Bogotá, D.C., Colombia. Volume I, p. 547; Volume II, 462; Volume III, 485; Volume IV, 489; Volume V, 569; Volume VI, 507; Volume VII, p. 684; Volume VIII, p. 547; Volume IX, p. 482; Volume X, 549; Volume XI, p. 516 and Volume XII, p. 621 (1989–1998) (In Spanish).Bernal, M.H.Y., Farfán, M.M. Guide for the cultivation and use of the “chachafruto” or “balú” (Erythrina edulis Triana ex Micheli). Bogotá: Editoria Guadalupe Ltda. 50 p. (1996) (In Spanish).Bernal, M.H.Y., Jiménez, L.C. The “Creole bean” Canavalia ensiformis (Linnaeus) De Candolle (Fabaceae-Faboideae). Bogotá: Editoria Guadalupe Ltda. 533 p. (1990) (In Spanish).Jiménez, B.L.C., Bernal, M.H.Y. The “inchi” Caryodendron orinocense Karsten (Euphorbiaceae). Bogotá: Editora Guadalupe Ltda. p. 429 (1992) (In Spanish).Melgarejo, L.M., Hernández, M.S., Barrera, J.A., Carrillo, M. Offers and potential of a germplasm bank of the genus Theobroma for the enrichment of Amazonian systems. Instituto de Investigaciones Científicas Sinchi. Universidad Nacional de Colombia. Bogotá, Colombia. p. 225 (2006) (In Spanish).Bernal, R., Galeano, G., Rodríguez, A., Sarmiento, H., Gutiérrez, M. Nombres Comunes de las Plantas de Colombia. Retrieved 15 June, 2021, from: http://www.biovirtual.unal.edu.co/nombrescomunes/ (2017)Food Plants International. Retrieved on 14 March 2021 at Articles & Books – Food Plants International (2021).Lorenzi, H., Bacher, L., Lacerda, M. & Sartori, S. Brazilian fruits and cultivated exotics (Instituto Plantarum De Estudos Da Flora LTDA, Nova Odessa, 2000).
    Google Scholar 
    Martín, F.W., Campbell, C.W., Ruberté, R.M. Perennial Edible Fruits of the Tropics: An Inventory. U.S. Department of Agriculture, Agricultural Research Service. (1987)Marrugo, S. L. Como Pepa’e Guama: Lo que no sabías acerca de la vida de los guamos (Royal Botanic Gardens Kew, Richmond, 2019).
    Google Scholar 
    Leon, J. Central American and West Indian Species of Inga (Leguminosae). Ann. Mo. Bot. Gard. 53(3), 265–359 (1966).Article 

    Google Scholar 
    Blombery, A. & Rodd, T. Palms of the world (Angus and Robertson, 1992).
    Google Scholar 
    Wickens, G. E. Edible nuts: non-wood forest products, handbook 5 (FAO, 1995).
    Google Scholar 
    Chízmar, C. Plantas comestibles de Centroamérica. Santo Domingo de Heredia, Costa Rica: Editorial INBio. p. 358 (2009)Rodríguez, L. M. G. Growth and fruit production study of Bactris guineesis (güiscoyol) in Agroforestry Systems as development potential in the Chorotega Region (Universidad Técnica Nacional Investigación y transferencia, 2019).
    Google Scholar 
    Bax, V. & Francesconi, W. Conservation gaps and priorities in the Tropical Andes biodiversity hotspot: Implications for the expansion of protected areas. J. Environ. Manage. 232, 387–396 (2019).PubMed 
    Article 

    Google Scholar 
    Noh, J. K. et al. Warning about conservation status of forest ecosystems in tropical Andes: National assessment based on IUCN criteria. PLoS One 15(8), e0237877 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Brooks, M. T. et al. Habitat loss and extinction in the hotspots of biodiversity. Biodivers. Conserv. 16(4), 909–923 (2002).
    Google Scholar 
    Ocampo, J. Diversidad y distribución de las Passifloraceae en el departamento del Huila en Colombia. Acta biologica Colombiana 18(3), 511–516 (2013).
    Google Scholar 
    Durán-Izquierdo, M. & Olivero-Verbel, J. Vulnerability assessment of Sierra Nevada de Santa Marta Colombia World’s most irreplaceable nature reserve. Glob. Ecol. Conserv. 28, e01592 (2021).Article 

    Google Scholar 
    Cabrera Gaviria, L.D., Gil Pereira, L.F. Comparative analysis of the loss of natural coverage in the protected areas Nukak and Puinawai and their effects on the ecosystems present in the period between the years 2000–2020. Thesis in Environmental and Sanitary Engineering. Universidad de La Salle, Bogotá. Available at: https://ciencia.lasalle.edu.co/ing_ambiental_sanitaria/1943 (2021) (In Spanish).Castillo, H. M. N. A story of the indigenous struggle against mining: the creation of the Yaigojé-Apaporis National Natural Park in the Colombian Amazon (Universidade Federal De Minas Gerais, 2018) ((In Portuguese)).
    Google Scholar 
    Walsh, J. & Sanchez, G. The spreading of illicit crops in Colombia (Instituto de Estudios para el Desarrollo y la Paz, Bogotá, 2008).
    Google Scholar 
    MAPS, OPS, ICBF. Encuesta Nacional de la Situacion Nutricional-ENSIN. Retrieved on 12 October, 2-21, from: http://www.ensin.gov.co/Documents/Documento-metodologico-ENSIN-2015.pdf (2015)Correa-García, E., Vélez-Correa, J., Zapata-Caldas, E., Vélez-Torres, I. & Figueroa-Casas, A. Territorial transformations produced by the sugarcane agroindustry in the ethnic communities of López Adentro and El Tiple, Colombia. Land Use Policy 76, 847–860 (2018).Article 

    Google Scholar 
    Hurtado, D. & Vélez-Torres, I. Toxic dispossession: on the social impacts of the aerial use of glyphosate by the sugarcane agroindustry in Colombia. Crit. Criminol. 28, 557–576 (2020).Article 

    Google Scholar 
    Vélez-Torres, I., Varela-Corredor, D., Rátiva-Gaona, S., Salcedo-Fidalgo, A. Agroindustry and extractivism in the Alto Cauca: impact on the livelihood systems of Afro-descendent Farmers and Resistance (1950–2011). CS, 12: 157–188. (2013) (In Spanish, English summary).Fernández Lucero, M. Protocol for the use of Guáimaro (Brosimum alicastrum Sw.) seeds in Montes de María and Serranía del Perijá, Colombian Caribbean. Bogotá: Instituto de Investigación de Recursos Biológicos Alexander von Humboldt (2021) (In Spanish).Santillán-Fernández, A. et al. Brosimum alicastrum Swartz as an alternative for the productive reconversion of agrosilvopastoral areas in Campeche. Revista Mexicana de Ciencias Forestales 11(61), 51–69 (2020).Article 

    Google Scholar 
    Subiria-Cueto, R. et al. Brosimum alicastrum Sw. (Ramón): an alternative to improve the nutritional properties and functional potential of the wheat flour tortilla. Foods 8(12), 613 (2019).CAS 
    PubMed Central 
    Article 

    Google Scholar 
    Quiñones-Hoyos, C., Rengifo-Fernández, A., Bernal-Galeano, S., Peña, R., Fernández, M., Tatiana Rojas, M., Diazgranados, M. A look at useful plants and fungi in three biodiverse areas of Colombia. Royal Botanic Gardens, Kew and Instituto de Investigaciones en Recursos Biológicos Alexander von Humboldt. Bogotá, Colombia (2021) (In Spanish)Royal Botanic Gardens, Kew. Discovering the Guáimaro trails: promote a market for native species. Retrieved on 18 February 2022 from https://storymaps.arcgis.com/stories/f540b764fc6c47db886b38515560852f (2022)Gottesch, B. et al. Extinction risk of Mesoamerican crop wild relatives. Plants People Planet 3, 775–795 (2021).Article 

    Google Scholar 
    French, B. Food plants international database of edible plants of the world, a free resource for all. Acta Hort. 1241, 1–6 (2019).
    Google Scholar 
    Meyers, N., Mittermeier, R., Mittermeier, C. G. & Kent, J. Biodiversity hotspot for conservation priority. Nature 403(6772), 853–858 (2000).Article 

    Google Scholar  More

  • in

    We can have biodiversity and eat too

    Godfray, H. C. J. et al. Science 327, 812–818 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    Pimm, S. L. et al. Science 344, 1246752 (2014).CAS 
    Article 

    Google Scholar 
    Chung, M. G. & Liu, J. Nat. Food https://doi.org/10.1038/s43016-022-00499-7 (2022).Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. & Kent, J. Nature 403, 853–858 (2000).ADS 
    CAS 
    Article 

    Google Scholar 
    A complex prairie ecosystem. National Park Service https://www.nps.gov/tapr/learn/nature/a-complex-prairie-ecosystem.htm (2022)Davalos, L. M. et al. Environ. Sci. Technol. 45, 1219–1227 (2011).ADS 
    CAS 
    Article 

    Google Scholar 
    Vijay, V., Pimm, S. L., Jenkins, C. N. & Smith, S. J. PLoS ONE 11, e0159668 (2016).Article 

    Google Scholar 
    Liu, J. et al. Ecol. Soc. 18, 26 (2013).CAS 
    Article 

    Google Scholar 
    Liu, J. Consumption patterns and biodiversity. The Royal Society https://go.nature.com/3M19vup (2020).Xu, Z. et al. Nat. Sustain. 3, 964–971 (2020).Article 

    Google Scholar 
    Dou, Y., da Silva, R. F. B., Yang, H. & Liu, J. J. Geogr. Sci. 28, 1715–1732 (2018).Article 

    Google Scholar  More

  • in

    Want to prevent pandemics? Stop spillovers

    Spillover events, in which a pathogen that originates in animals jumps into people, have probably triggered every viral pandemic that’s occurred since the start of the twentieth century1. What’s more, an August 2021 analysis of disease outbreaks over the past four centuries indicates that the yearly probability of pandemics could increase several-fold in the coming decades, largely because of human-induced environmental changes2.Fortunately, for around US$20 billion per year, the likelihood of spillover could be greatly reduced3. This is the amount needed to halve global deforestation in hotspots for emerging infectious diseases; drastically curtail and regulate trade in wildlife; and greatly improve the ability to detect and control infectious diseases in farmed animals.That is a small investment compared with the millions of lives lost and trillions of dollars spent in the COVID-19 pandemic. The cost is also one-twentieth of the statistical value of the lives lost each year to viral diseases that have spilled over from animals since 1918 (see ‘Spillovers: a growing threat’), and less than one-tenth of the economic productivity erased per year1.

    Source: Ref. 1

    Yet many of the international efforts to better defend the world from future outbreaks, prompted by the COVID-19 pandemic, still fail to prioritize the prevention of spillover. Take, for example, the Independent Panel for Pandemic Preparedness and Response, established by the World Health Organization (WHO). The panel was convened in September 2020, in part to ensure that any future infectious-disease outbreak does not become another pandemic. In its 86-page report released last May, wildlife is mentioned twice; deforestation once.We urge the decision-makers currently developing three landmark international endeavours to make the prevention of spillover central to each.First, the G20 group of the world’s 20 largest economies provisionally agreed last month to create a global fund for pandemics. If realized, this could provide funding at levels that infectious-disease experts have been recommending for decades — around $5 per person per year globally (see go.nature.com/3yjitwx). Second, an agreement to improve global approaches to pandemics is under discussion by the World Health Assembly (WHA), the decision-making body of the WHO. Third, a draft framework for biodiversity conservation — the post-2020 global biodiversity framework — is being negotiated by parties to the Convention on Biological Diversity.Designed in the right way, these three international endeavours could foster a more proactive global approach to infectious diseases. This opportunity — to finally address the factors that drive major disease outbreaks, many of which also contribute to climate change and biodiversity loss — might not present itself again until the world faces another pandemic.Four actions The risk of spillover is greater when there are more opportunities for animals and humans to make contact, for instance in the trade of wildlife, in animal farming or when forests are cleared for mining, farming or roads. It is also more likely to happen under conditions that increase the likelihood of infected animals shedding viruses – when they are housed in cramped conditions, say, or not fed properly.Decades of research from epidemiology, ecology and genetics suggest that an effective global strategy to reduce the risk of spillover should focus on four actions1,3.First, tropical and subtropical forests must be protected. Various studies show that changes in the way land is used, particularly tropical and subtropical forests, might be the largest driver of emerging infectious diseases of zoonotic origin globally4. Wildlife that survives forest clearance or degradation tends to include species that can live alongside people, and that often host pathogens capable of infecting humans5. For example, in Bangladesh, bats that carry Nipah virus — which can kill 40–75% of people infected — now roost in areas of high human population density because their forest habitat has been almost entirely cleared6.Furthermore, the loss of forests is driving climate change. This could in itself aid spillover by pushing animals, such as bats, out of regions that have become inhospitable and into areas where many people live7.Yet forests can be protected even while agricultural productivity is increased — as long as there is enough political will and resources8. This was demonstrated by the 70% reduction in deforestation in the Amazon during 2004–12, largely through better monitoring, law enforcement and the provision of financial incentives to farmers. (Deforestation rates began increasing in 2013 due to changes in environmental legislation, and have risen sharply since 2019 during Jair Bolsonaro’s presidency.)Second, commercial markets and trade of live wild animals that pose a public-health risk must be banned or strictly regulated, both domestically and internationally.Doing this would be consistent with the call made by the WHO and other organizations in 2021 for countries to temporarily suspend the trade in live caught wild mammals, and to close sections of markets selling such animals. Several countries have already acted along these lines. In China, the trade and consumption of most terrestrial wildlife has been banned in response to COVID-19. Similarly, Gabon has prohibited the sale of certain mammal species as food in markets.

    A worker in a crowded chicken farm in Anhui province, China.Credit: Jianan Yu/Reuters

    Restrictions on urban and peri-urban commercial markets and trade must not infringe on the rights and needs of Indigenous peoples and local communities, who often rely on wildlife for food security, livelihoods and cultural practices. There are already different rules for hunting depending on the community in many countries, including Brazil, Canada and the United States.Third, biosecurity must be improved when dealing with farmed animals. Among other measures, this could be achieved through better veterinary care, enhanced surveillance for animal disease, improvements to feeding and housing animals, and quarantines to limit pathogen spread.Poor health among farmed animals increases their risk of becoming infected with pathogens — and of spreading them. And nearly 80% of livestock pathogens can infect multiple host species, including wildlife and humans9.Fourth, particularly in hotspots for the emergence of infectious diseases, people’s health and economic security should be improved.People in poor health — such as those who have malnutrition or uncontrolled HIV infection — can be more susceptible to zoonotic pathogens. And, particularly in immunosuppressed individuals such as these, pathogens can mutate before being passed on to others10.What’s more, some communities — especially those in rural areas — use natural resources to produce commodities or generate income in a way that brings them into contact with wildlife or wildlife by-products. In Bangladesh, for example, date palm sap, which is consumed as a drink in various forms, is often collected in pots attached to palm trees. These can become contaminated with bodily substances from bats. A 2016 investigation linked this practice to 14 Nipah virus infections in humans that caused 8 deaths11.Providing communities with both education and tools to reduce the risk of harm is crucial. Tools can be something as simple as pot covers to prevent contamination of date palm sap, in the case of the Bangladesh example.In fact, providing educational opportunities alongside health-care services and training in alternative livelihood skills, such as organic agriculture, can help both people and the environment. For instance, the non-governmental organization Health in Harmony in Portland, Oregon, has invested in community-designed interventions in Indonesian Borneo. During 2007–17, these contributed to a 90% reduction in the number of households that were reliant on illegal logging for their main livelihood. This, in turn, reduced local rainforest loss by 70%. Infant mortality also fell by 67% in the programme’s catchment area12.Systems-oriented interventions of this type need to be better understood, and the most effective ones scaled up.Wise investmentSuch strategies to prevent spillover would reduce our dependence on containment measures, such as human disease surveillance, contact tracing, lockdowns, vaccines and therapeutics. These interventions are crucial, but are often expensive and implemented too late — in short, they are insufficient when used alone to deal with emerging infectious diseases.The COVID-19 pandemic has exposed the real-world limitations of these reactive measures — particularly in an age of disinformation and rising populism. For example, despite the US federal government spending more than $3.7 trillion on its pandemic response as of the end of March, nearly one million people in the United States — or around one in 330 — have died from COVID-19 (see go.nature.com/39jtdfh and go.nature.com/38urqvc). Globally, between 15 million and 21 million lives are estimated to have been lost during the COVID-19 pandemic beyond what would be expected under non-pandemic conditions (known as excess deaths; see Nature https://doi.org/htd6; 2022). And a 2021 model indicates that, by 2025, $157 billion will have been spent on COVID-19 vaccines alone (see go.nature.com/3jqds76).

    A farmer in Myanmar gathers sap from a palm tree to make wine. Contamination of the collection pots with excretions from bats can spread diseases to humans.Credit: Wolfgang Kaehler/LightRocket via Getty

    Preventing spillover also protects people, domesticated animals and wildlife in the places that can least afford harm — making it more equitable than containment. For example, almost 18 months since COVID-19 vaccines first became publicly available, only 21% of the total population of Africa has received at least one dose. In the United States and Canada, the figure is nearly 80% (see go.nature.com/3vrdpfo). Meanwhile, Pfizer’s total drug sales rose from $43 billion in 2020 to $72 billion in 2021, largely because of the company’s COVID-19 vaccine, the best-selling drug of 202113.Lastly, unlike containment measures, actions to prevent spillover also help to stop spillback, in which zoonotic pathogens move back from humans to animals and then jump again into people. Selection pressures can differ across species, making such jumps a potential source of new variants that can evade existing immunity. Some researchers have suggested that spillback was possibly responsible for the emergence of the Omicron variant of SARS-CoV-2 (see Nature 602, 26–28; 2022).Seize the dayOver the past year, the administration of US President Joe Biden and two international panels (one established in 2020 by the WHO and the other in 2021 by the G20) have released guidance on how to improve approaches to pandemics. All recommendations released so far acknowledge spillover as the predominant cause of emerging infectious diseases. None adequately discusses how that risk might be mitigated. Likewise, a PubMed search for the spike protein of SARS-CoV-2 yields thousands of papers, yet only a handful of studies investigate coronavirus dynamics in bats, from which SARS-CoV-2 is likely to have originated14.Spillover prevention is probably being overlooked for several reasons. Upstream animal and environmental sources of pathogens might be being neglected by biomedical researchers and their funders because they are part of complex systems — research into which does not tend to lead to tangible, profitable outputs. Also, most people working in public health and biomedical sciences have limited training in ecology, wildlife biology, conservation and anthropology.There is growing recognition of the importance of cross-sectoral collaboration, including soaring advocacy for the ‘One Health’ approach — an integrated view of health that recognizes links between the environment, animals and humans. But, in general, this has yet to translate into action to prevent pandemics.Another challenge is that it can take decades to realize the benefits of preventing spillover, instead of weeks or months for containment measures. Benefits can be harder to quantify for spillover prevention, no matter how much time passes, because, if measures are successful, no outbreak occurs. Prevention also runs counter to individual, societal and political tendencies to wait for a catastrophe before taking action.The global pandemic fund, the WHA pandemic agreement and the post-2020 global biodiversity framework all present fresh chances to shift this mindset and put in place a coordinated global effort to reduce the risk of spillover alongside crucial pandemic preparedness efforts.Global fund for pandemicsFirst and foremost, a global fund for pandemics will be key to ensuring that the wealth of evidence on spillover prevention is translated into action. Funding for spillover prevention should not be folded into existing conservation funds, nor draw on any other existing funding streams.Investments must be targeted to those regions and practices where the risk of spillover is greatest, from southeast Asia and Central Africa to the Amazon Basin and beyond. Actions to prevent spillover in these areas, particularly by reducing deforestation, would also help to mitigate climate change and reduce loss of biodiversity. But conservation is itself drastically underfunded. As an example, natural solutions (such as conservation, restoration and improved management of forests, wetlands and grasslands) represent more than one-third of the climate mitigation needed by 2030 to stabilize warming to well below 2 °C15. Yet these approaches receive less than 2% of global funds for climate mitigation16. (Energy systems receive more than half.)In short, the decision-makers backing the global fund for pandemics must not assume that existing funds are dealing with the threat of spillover — they are not. The loss of primary tropical forest was 12% higher in 2020 than in 2019, despite the economic downturn triggered by COVID-19. This underscores the continuing threat to forests.Funding must be sustained for decades to ensure that efforts to reduce the risk of spillover are in place long enough to yield results.WHA pandemic agreementIn 2020, the president of the European Council, Charles Michel, called for a treaty to enable a more coordinated global response to major epidemics and pandemics. Last year, more than 20 world leaders began echoing this call, and the WHA launched the negotiation of an agreement (potentially, a treaty or other international instrument) to “strengthen pandemic prevention, preparedness, and response” at the end of 2021.Such a multilateral agreement could help to ensure more-equitable international action around the transfer of scientific knowledge, medical supplies, vaccines and therapeutics. It could also address some of the constraints currently imposed on the WHO, and define more clearly the conditions under which governments must notify others of a potential disease threat. The COVID-19 pandemic exposed the shortcomings of the International Health Regulations on many of these fronts17. (This legal framework defines countries’ rights and obligations in the handling of public-health events and emergencies that could cross borders.)We urge negotiators to ensure that the four actions to prevent spillover outlined here are prioritized in the WHA pandemic agreement. For instance, it could require countries to create national action plans for pandemics that include reducing deforestation and closing or strictly regulating live wildlife markets. A reporting mechanism should also be developed to evaluate progress in implementing the agreement. This could build on experience from existing schemes, such as the WHO Joint External Evaluation process (used to assess countries’ capacities to handle public-health risks) and the verification regime of the Chemical Weapons Convention.Commitments to expand pathogen surveillance at interfaces between humans, domesticated animals and wildlife — from US mink farms and Asian wet markets to areas of high deforestation in South America — should also be wrapped into the WHA agreement. Surveillance will not prevent spillover, but it could enable earlier detection and better control of zoonotic outbreaks, and provide a better understanding of the conditions that cause them. Disease surveillance would improve simply through investing in clinical care for both people and animals in emerging infectious-disease hotspots.Convention on Biological DiversityWe are in the midst of the sixth mass extinction, and activities that drive the loss of biodiversity, such as deforestation, also contribute to the emergence of infectious disease. Meanwhile, epidemics and pandemics resulting from the exploitation of nature can lead to further conservation setbacks — because of economic damage from lost tourism and staff shortages affecting management of protected areas, among other factors18. Also, pathogens that infect people can be transmitted to other animals and decimate those populations. For instance, an Ebola outbreak in the Republic of Congo in 2002–03 is thought to have killed 5,000 gorillas19.Yet the global biodiversity framework currently being negotiated by the Convention on Biological Diversity fails to explicitly address the negative feedback cycle between environmental degradation, wildlife exploitation and the emergence of pathogens. The first draft made no mention of pandemics. Text about spillover prevention was proposed in March, but it has yet to be agreed on.Again, this omission stems largely from the siloing of disciplines and expertise. Just as the specialists relied on for the WHA pandemic agreement tend to be those in the health sector, those informing the Convention on Biological Diversity tend to be specialists in environmental science and conservation.The global biodiversity framework, scheduled to be agreed at the Conference of the Parties later this year, must strongly reflect the environment–health connection. This means explicitly including spillover prevention in any text relating to the exploitation of wildlife and nature’s contributions to people. Failing to connect these dots weakens the ability of the convention to achieve its own objectives around conservation and the sustainable use of resources.Preventive health careA reactive response to catastrophe need not be the norm. In many countries, preventive health care for chronic diseases is widely embraced because of its obvious health and economic benefits. For instance, dozens of colorectal cancer deaths are averted for every 1,000 people screened using colonoscopies or other methods20. A preventive approach does not detract from the importance of treating diseases when they occur.With all the stressors now being placed on the biosphere — and the negative implications this has for human health — leaders urgently need to apply this way of thinking to pandemics. More