More stories

  • in

    Studying the distribution patterns, dynamics and influencing factors of city functional components by gradient analysis

    Data collectionSelection of the case cities and city functional componentsTo make the research results more universal, we set the criteria for the selection of case cities as follows. (1) Large cities: cities in which the built-up area exceeded 1000 km2. We chose Beijing, Shanghai, and Tianjin. Beijing is China’s capital and political centre, Shanghai is China’s largest economic centre, and Tianjin is one of China’s four municipalities directly governed by the Central Government; (2) medium cities: cities in which the built-up area varied between 400 and 1000 km2. We chose two provincial capital cities in central China, Wuhan and Hefei, and an economically developed coastal city, Ningbo; (3) small cities: cities in which the built-up area was smaller than 400 km2. Small cities need to have a complete urban form and functions. We selected three economically developed small cities Changzhou, Nantong and Jiaxing.The selection of city functional component types should cover typical city functional components related to the coupling between humans and the city in urban systems, including production, processing, circulation, decomposition and other functions: Kentucky Fried Chicken (KFC) and McDonald’s (McD), two of the most popular western fast-food restaurants in China; Lanzhou Noodles (LZN) and Shaxian Snacks (SXS), two of the most popular Chinese fast-food restaurants in China; Agricultural Bank of China (ABC), one of the four most widely distributed banks in China; swimming pool (SP), a type of indoor sports venue popular in recent years; Shunfeng (SF) and Shentong (STO) express outlets, two of the most commonly used express service components in China; China National Petroleum Corporation (CNPC) and China Petroleum and Chemical Corporation (Sinopec) gas stations, two gas station enterprises accounting for more than half of the total number of gas stations in China; WTP, a type of waste treatment component; GH, a type of primary biological production component; and DF, a type of secondary biological processing component.Acquisition of city functional component dataLatitude and longitude data of the above city functional components were obtained through electronic maps and remote sensing images and verified through field investigation. AutoNavi and Baidu electronic maps are the two most widely used map suppliers in China due to their high accuracy and practicality46. In particular, the location of service city functional components can be accurately obtained through electronic maps. WTPs have detailed lists and location data on the government websites, and GHs can be accurately identified in Google Earth images due to their unique appearance31. Therefore, these three types of raw data are listed as the main sources of location data for functional components.Latitude and longitude data of the KFC, McD, ABC, SP, LZN, SXS, SF, STO, CNPC, Sinopec and DF locations were retrieved from AutoNavi and Baidu historical electronic maps through Python 3.5 software (https://www.python.org/). The 2012 and 2015 historical electronic map data originated from the East China Normal University Humanities and Social Sciences Big Data Platform47, and the 2018 historical electronic map data originated from the Peking University Open Research Data Platform48. Based on AutoNavi and Baidu, each individual component was strictly filtered by name and type. Please refer to the Supplementary Table S3 for a summary of the detailed filtering conditions.Accurate WTP latitude and longitude data were obtained by using the WTP name and address to query the AutoNavi map coordinate picking system [the WTP name and address were acquired from the Ministry of Ecology and Environment of the People’s Republic of China (www.mee.gov.cn), China Environment Network (www.cenews.com.cn) and Beijing Municipal Ecology and Environment Bureau (sthjj.beijing.gov.cn)]. GH latitude and longitude data were determined via a method commonly used in community ecology, which has previously been reported31. Briefly, ArcGIS 10.3 software was employed to generate grids covering the entire city (the size of each grid was 0.5 × 0.5 km), and these grids were then converted into the keyhole markup language (KML) format and imported into Google Earth for GH visual interpretation. The GHs were characterized as (a) bright white or bluish-white, (b) rectangular-shaped objects, (c) oriented in rows or separated by paths or bare areas. If a GH occurred in a specific grid, the centre of the grid was marked with the landmark tool to obtain the corresponding latitude and longitude data.Land price and housing price are affected by location factors such as population, employment, transportation, and amenities and are important indicators to determine whether a city is monocentric or polycentric49,50. Land price was also used as a determining indicator in our study. The concentric circle model was first established by Von Thünen51 to study the order of agricultural land use from urban to rural areas, and it is still an important method to explore research topics along the urban–rural gradient32,52.To obtain the land price distribution curve along the urban–rural gradient, all the standard land parcel information in each case city through the real-time land price query function provided by the China Land Price Information Service Platform (www.landvalue.com.cn), including land price, latitude and longitude, was obtained, and the parcel with highest land price was defined as the city centre. Concentric circles with an increasing radius of 1-km intervals were generated by adopting the city centre as the circle centre, and the average land price of all standard land parcels in each concentric ring was considered as the land price of the ring. We found that in all the case cities, the land price exhibited an obvious monotonous downward trend from the centre to the edge of the city (Supplementary Fig. S7). Therefore, we assumed a monocentric city model and used the concentric circles to define the urban–rural gradient.To acquire density distribution curves of the city functional components along urban–rural gradients, the latitude and longitude data of the KFC, McD, ABC, SP, LZN, SXS, SF, STO, CNPC, Sinopec, GH, WTP and DF components were applied for map labelling purposes. Concentric circles with the increasing radius of 1-km intervals were generated by adopting the city centre as the circle centre, and the number of each type of component in each concentric ring was counted. Since the overall number of WTPs and DFs was smaller, the concentric circle radius was increased at 5- and 10-km intervals, respectively, and the number of WTPs or DFs in each concentric ring was determined, while the component density in each ring was calculated by dividing the number by the area of the ring.To calculate the ecosystem services per unit area for each type of city functional component, the revenue of each component in the current year was determined. KFC and McD revenue data were retrieved from Yum China Holdings and Askci Corporation, respectively. ABC revenue data originated from the Agricultural Bank of China, Ltd., and SF and STO revenue data were acquired from SF Holding Corporation, Ltd., and STO Express Corporation, Ltd., respectively, while CNPC and Sinopec revenue data were retrieved from PetroChina Company, Ltd., and Sinopec Corporation, respectively. Moreover, LZN and SXS revenue data were obtained via field investigation. Environmental impact data of the KFC, McD, CNPC and Sinopec components originated from the Ministry of Ecology and Environment of the People’s Republic of China (www.mee.gov.cn), while LZN and SXS environmental impact data were obtained via field investigation. The costs of the KFC, McD, LZN, SXS, CNPC and Sinopec environmental impacts were converted according to the Environmental Protection Tax Law, 2018. The WTP ecosystem services were retrieved from Liu et al.53, and the GH ecosystem services originated from Chang et al.54, while the DF ecosystem services were obtained from Fan et al.55. The cultural services of all components were determined through field investigation.Data processingTo intuitively describe the density changes of city functional components along the urban–rural gradient, the density of the components in the above concentric rings were adopted as the ordinate, the distance from the city centre to the edge of the ring was adopted as the abscissa, and scatter plots were created. To compare the characteristic values of the density distribution of each type of component more clearly, a distribution model was used to fit the scatter plots35,36.Fitting of the density distribution curve of the city functional componentsThrough the nonlinear fitting function in OriginPro 2019 software (https://www.originlab.com/), the Gumbel model56,57 was considered to fit the above scatter plots to generate density distribution curves of all city functional components. The goodness-of-fit (choosing the 13 types of components in Beijing as examples) is shown in the Supplementary Fig. S2.The component density (P, individual components km−2) at a given distance from the city centre (d, km) along the urban–rural gradient is calculated as follows:$${P} = {P_{max}} {cdot} {{e^{-{e}}}^{-frac{{{d}}-{d^{*}}}{{w}} , – , frac{{{d}}-{d^{*}}}{{w}} , + , {1}}}$$
    (1)
    where Pmax (individual components km−2) is the peak value of the curve, d* (km) is the peak position of the curve, and w (km) is a parameter controlling the width of the curve.Calculation of the niche width of the density distribution curve of the city functional componentsTo intuitively compare the distance spanned by the density distribution curve of the city functional components, the difference in the abscissa between a density value of 10% of the Pmax value on the density distribution curve was adopted as the niche width W (km).Calculation of the skewness and kurtosis of the density distribution curve of the city functional componentsThe skewness and kurtosis are calculated according to the following equation58:$$text{skewness } = frac{frac{1}{{{n}}}{sum }_{{{i}}= {1}}^{{n}} ,{left({{x}}_{{i}}-{bar{x}}right)}^{3}}{{left(frac{1}{{{n}}}{sum}_{{{i}}= {1} }^{{n}} ,{left({{x}}_{{i}}-{bar{x}}right)}^{2}right)}^{frac{3}{{2}}}}$$
    (2)
    $$text{kurtosis } = frac{frac{1}{{{n}}}{sum }_{{{i}}= {1}}^{{n}} ,{left({{x}}_{{i}}-{bar{x}}right)}^{4}}{left(frac{1}{n}sumnolimits_{i=1}^{n} ,{left({{x}}_{{i}}-{bar{x}}right)}^{2}right)^2}-3$$
    (3)

    where xi (km) is the distance from each individual type of component to the city centre, and ‾x (km) is the average of the distances from all individual types of components to the city centre.Correlation analysis between the characteristic values of the density distribution curveLinear and nonlinear regression analyses in Microsoft Excel 2019 were implemented to study the relationship between the characteristic values of the density distribution curve, and the regression form with the best R2 value was selected.Correlation analysis between the characteristic values of the density distribution curve and the city sizeLinear and nonlinear regression analyses in Microsoft Excel 2019 were implemented to study the relationship between the characteristic values of the density distribution curve and the city size, and the regression form with the best R2 value was selected.Framework for ecosystem service assessment of the city functional componentsAccording to the classification of the Millennium Ecosystem Assessment (MA), ecosystem services include provisioning, regulating, cultural and supporting services59. In this study, the ecosystem services (goods and services) provided by the city functional components (artificial ecosystems) were divided into target and accompanied services (Supplementary Fig. S6), both of which may include provisioning, regulating and cultural services.In this study, the target services of the KFC, McD, LZN, SXS, CNPC, Sinopec, GH, and DF components were provisioning services, the target services of the ABC, SF, STO, and WTP components were regulating services, and the target services of component SP were cultural services. According to the guidance of Liu et al.53, the above regulating and cultural services were divided into positive and negative services (dis-services).The net service (NES, USD m−2 yr−1) is the sum of the positive services (target services + positive regulating services + positive cultural services) and dis-services (negative regulating services + negative cultural services):$${NES} = sum_{{i} = 1}^{n}{ES}_{i}$$
    (4)

    where ESi (USD m−2 yr−1) is the value of a given type of ecosystem service involved in this study, and n is the number of ecosystem service types involved in this study.The ecological index (γ) is calculated as follows:$${gamma } = {TGS}/ |EDS|$$
    (5)

    where TGS (USD m−2 yr−1) denotes the target services of the city functional components, and EDS (USD m−2 yr−1) denotes the dis-services of the city functional components.Calculation of the ecosystem services of the city functional componentsThe calculation methods are provided in the supplementary materials. More

  • in

    DNA-based taxonomy of a mangrove-associated community of fishes in Southeast Asia

    1.Levin, L. A. et al. The function of marine critical transition zones and the importance of sediment biodiversity. Ecosystems 4, 430–451 (2001).CAS 
    Article 

    Google Scholar 
    2.Sarathchandra, C. et al. Significance of mangrove biodiversity conservation in fishery production and living conditions of coastal communities in Sri Lanka. Diversity 10, 20 (2018).Article 

    Google Scholar 
    3.Brown, C. J. et al. The assessment of fishery status depends on fish habitats. Fish Fish. 20, 1–14 (2019).CAS 
    Article 

    Google Scholar 
    4.Kathiresan, K. & Bingham, B. L. Biology of mangroves and mangrove ecosystems. Adv. Mar. Biol. 40, 84–254 (2001).
    Google Scholar 
    5.De La Morinière, E. C., Pollux, B., Nagelkerken, I. & Van der Velde, G. Post-settlement life cycle migration patterns and habitat preference of coral reef fish that use seagrass and mangrove habitats as nurseries. Estuar. Coast. Shelf Sci. 55, 309–321 (2002).ADS 
    Article 

    Google Scholar 
    6.Asaad, I., Lundquist, C. J., Erdmann, M. V. & Costello, M. J. Delineating priority areas for marine biodiversity conservation in the Coral Triangle. Biol. Conserv. 222, 198–211 (2018).Article 

    Google Scholar 
    7.Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. & Kent, J. Biodiversity hotspots for conservation priorities. Nature 403, 853 (2000).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    8.Chong, V. C., Lee, P. K. & Lau, C. M. Diversity, extinction risk and conservation of Malaysian fishes. J. Fish Biol. 76, 2009–2066. https://doi.org/10.1111/j.1095-8649.2010.02685.x (2010).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    9.Wong, S. L. Matang Mangroves: A Century of Sustainable Management (Sasyaz Holdings Private Ltd., Forestry Department Peninsular Malaysia, 2004).
    Google Scholar 
    10.Ong, J. et al. Hutan paya laut Merbok, Kedah: Pengurusan hutan, persekitaran fizikal dan kepelbagaian flora. In Siri Kepelbagaian Biologi Hutan Vol. 23 (eds Ku-Aman, K. A. et al.) 21–33 (Jabatan Perhutanan Semenanjung Malaysia, 2015).
    Google Scholar 
    11.Jamaluddin, J. A. F. et al. DNA barcoding of shrimps from a mangrove biodiversity hotspot. Mitochondrial DNA Part A 30, 618–625. https://doi.org/10.1080/24701394.2019.1597073 (2019).CAS 
    Article 

    Google Scholar 
    12.Mansor, M., Mohammad-Zafrizal, M., Nur-Fadhilah, M., Khairun, Y. & Wan-Maznah, W. Temporal and spatial variations in fish assemblage structures in relation to the physicochemical parameters of the Merbok estuary, Kedah. J. Nat. Sci. Res. 2, 110–127 (2012).
    Google Scholar 
    13.Hookham, B., Shau-Hwai, A. T., Dayrat, B. & Hintz, W. A baseline measure of tree and gastropod biodiversity in replanted and natural mangrove stands in Malaysia: Langkawi Island and Sungai Merbok. Trop. Life Sci. Res. 25, 1 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    14.Mansor, M., Najamuddin, A., Mohammad-Zafrizal, M., Khairun, Y. & Siti-Azizah, M. Length-weight relationships of some important estuarine fish species from Merbok estuary, Kedah. J. Nat. Sci. Res. 2, 8–19 (2012).
    Google Scholar 
    15.Zainal Abidin, D. H. et al. Ichthyofauna of Sungai Merbok Mangrove Forest Reserve, northwest Peninsular Malaysia, and its adjacent marine waters. Check List 17, 601–631 (2021).Article 

    Google Scholar 
    16.Lim, H. C., Zainal Abidin, M., Pulungan, C. P., de Bruyn, M. & Mohd Nor, S. A. DNA barcoding reveals high cryptic diversity of the freshwater halfbeak genus Hemirhamphodon from Sundaland. PLoS ONE 11, e0163596 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    17.Mennesson, M. I., Bonillo, C., Feunteun, E. & Keith, P. Phylogeography of Eleotris fusca (Teleostei: Gobioidei: Eleotridae) in the Indo-Pacific area reveals a cryptic species in the Indian Ocean. Conserv. Genet. 19, 1025–1038 (2018).Article 

    Google Scholar 
    18.Gomes, L. C., Pessali, T. C., Sales, N. G., Pompeu, P. S. & Carvalho, D. C. Integrative taxonomy detects cryptic and overlooked fish species in a neotropical river basin. Genetica 143, 581–588 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    19.Iyiola, O. A. et al. DNA barcoding of economically important freshwater fish species from north-central Nigeria uncovers cryptic diversity. Ecol. Evol. 8, 6932–6951 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    20.Stern, N., Rinkevich, B. & Goren, M. Integrative approach revises the frequently misidentified species of Sardinella (Clupeidae) of the Indo-West Pacific Ocean. J. Fish Biol. 89, 2282–2305 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Hebert, P. D., Ratnasingham, S. & De Waard, J. R. Barcoding animal life: Cytochrome c oxidase subunit 1 divergences among closely related species. Proc. R. Soc. Lond. Ser. B Biol. Sci. 270, S96–S99 (2003).CAS 

    Google Scholar 
    22.Ward, R. D., Zemlak, T. S., Innes, B. H., Last, P. R. & Hebert, P. D. DNA barcoding Australia’s fish species. Philos. Trans. R. Soc. B Biol. Sci. 360, 1847–1857 (2005).CAS 
    Article 

    Google Scholar 
    23.Xu, L. et al. Assessment of fish diversity in the South China Sea using DNA taxonomy. Fish. Res. 233, 105771 (2020).Article 

    Google Scholar 
    24.Lakra, W. et al. DNA barcoding Indian marine fishes. Mol. Ecol. Resour. 11, 60–71 (2011).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    25.Hubert, N. et al. Cryptic diversity in Indo-Pacific coral-reef fishes revealed by DNA-barcoding provides new support to the centre-of-overlap hypothesis. PLoS ONE 7, e28987 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Adibah, A. & Darlina, M. Is there a cryptic species of the golden snapper (Lutjanus johnii)?. Genet. Mol. Res. 13, 8094–8104 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Bakar, A. A. et al. DNA barcoding of Malaysian commercial snapper reveals an unrecognized species of the yellow-lined Lutjanus (Pisces: Lutjanidae). PLoS ONE 13, e0202945 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    28.Farhana, S. N. et al. Exploring hidden diversity in Southeast Asia’s Dermogenys spp. (Beloniformes: Zenarchopteridae) through DNA barcoding. Sci. Rep. 8, 1–11 (2018).
    Google Scholar 
    29.Jaafar, T. N. A. M., Taylor, M. I., Nor, S. A. M., de Bruyn, M. & Carvalho, G. R. DNA barcoding reveals cryptic diversity within commercially exploited Indo-Malay Carangidae (Teleosteii: Perciformes). PLoS ONE 7, e49623 (2012).ADS 
    Article 
    CAS 

    Google Scholar 
    30.Azmir, I., Esa, Y., Amin, S., Salwany, M. & Zuraina, M. DNA barcoding analysis of larval fishes in Peninsular Malaysia. J. Environ. Biol. 41, 1295–1308 (2020).CAS 
    Article 

    Google Scholar 
    31.Chu, C. et al. Using DNA barcodes to aid the identification of larval fishes in tropical estuarine waters (Malacca Straits, Malaysia). Zool. Stud. 58, e30 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    32.Hubert, N., Delrieu-Trottin, E., Irisson, J.-O., Meyer, C. & Planes, S. Identifying coral reef fish larvae through DNA barcoding: A test case with the families Acanthuridae and Holocentridae. Mol. Phylogenet. Evol. 55, 1195–1203 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    33.Ko, H.-L. et al. Evaluating the accuracy of morphological identification of larval fishes by applying DNA barcoding. PLoS ONE 8, e53451 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    34.Chin, T. C., Adibah, A., Hariz, Z. D. & Azizah, M. S. Detection of mislabelled seafood products in Malaysia by DNA barcoding: Improving transparency in food market. Food Control 64, 247–256 (2016).Article 
    CAS 

    Google Scholar 
    35.Hubert, N. et al. Identifying Canadian freshwater fishes through DNA barcodes. PLoS ONE 3, e2490 (2008).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    36.Landi, M. et al. DNA barcoding for species assignment: The case of Mediterranean marine fishes. PLoS ONE 9, e106135 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    37.Russell, D., Thuesen, P. & Thomson, F. A review of the biology, ecology, distribution and control of Mozambique tilapia, Oreochromis mossambicus (Peters 1852) (Pisces: Cichlidae) with particular emphasis on invasive Australian populations. Rev. Fish Biol. Fish. 22, 533–554 (2012).Article 

    Google Scholar 
    38.Hebert, P. D., Cywinska, A. & Ball, S. L. Biological identifications through DNA barcodes. Proc. R. Soc. Lond. B Biol. Sci. 270, 313–321 (2003).CAS 
    Article 

    Google Scholar 
    39.Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. ABGD, automatic barcode gap discovery for primary species delimitation. Mol. Ecol. 21, 1864–1877 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    40.Meier, R., Zhang, G. & Ali, F. The use of mean instead of smallest interspecific distances exaggerates the size of the “barcoding gap” and leads to misidentification. Syst. Biol. 57, 809–813 (2008).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.Ortiz, D. & Francke, O. F. Two DNA barcodes and morphology for multi-method species delimitation in Bonnetina tarantulas (Araneae: Theraphosidae). Mol. Phylogenet. Evol. 101, 176–193 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    42.Hajibabaei, M., Singer, G. A., Hebert, P. D. & Hickey, D. A. DNA barcoding: How it complements taxonomy, molecular phylogenetics and population genetics. Trends Genet. 23, 167–172 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Mecklenburg, C. W., Møller, P. R. & Steinke, D. Biodiversity of arctic marine fishes: taxonomy and zoogeography. Mar. Biodivers. 41, 109–140 (2011).Article 

    Google Scholar 
    44.Puckridge, M., Andreakis, N., Appleyard, S. A. & Ward, R. D. Cryptic diversity in flathead fishes (Scorpaeniformes: Platycephalidae) across the Indo-West Pacific uncovered by DNA barcoding. Mol. Ecol. Resour. 13, 32–42 (2013).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    45.Thirumaraiselvi, R. & Thangaraj, M. Genetic diversity analysis of Indian Salmon, Eleutheronema tetradactylum from South Asian countries based on mitochondrial COI gene sequences. Not. Sci. Biol. 7, 417–422 (2015).CAS 
    Article 

    Google Scholar 
    46.Delrieu-Trottin, E. et al. Biodiversity inventory of the grey mullets (Actinopterygii: Mugilidae) of the Indo-Australian Archipelago through the iterative use of DNA-based species delimitation and specimen assignment methods. Evol. Appl. 13, 1451–1467 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    47.Durand, J.-D., Hubert, N., Shen, K.-N. & Borsa, P. DNA barcoding grey mullets. Rev. Fish Biol. Fish. 27, 233–243 (2017).Article 

    Google Scholar 
    48.Alavi-Yeganeh, M. S., Khajavi, M. & Kimura, S. A new ponyfish, Deveximentum mekranensis (Teleostei: Leiognathidae), from the Gulf of Oman. Ichthyol. Res. 68, 437–444. https://doi.org/10.1007/s10228-020-00794-y (2021).Article 

    Google Scholar 
    49.Carpenter, K. E. & Niem, V. FAO Species Identification Guide for Fishery Purposes. The Living Marine Resources of the Western Central Pacific. Bony Fishes Part 4 (Labridae to Latimeriidae), Estuarine Crocodiles, Sea Turtles, Sea Snakes and Marine Mammals Vol. 6 (FAO Library, 2001).
    Google Scholar 
    50.Chen, W., Ma, X., Shen, Y., Mao, Y. & He, S. The fish diversity in the upper reaches of the Salween River, Nujiang River, revealed by DNA barcoding. Sci. Rep. 5, 1–12 (2015).
    Google Scholar 
    51.Guimarães-Costa, A. J. et al. Fish diversity of the largest deltaic formation in the Americas-a description of the fish fauna of the Parnaíba Delta using DNA Barcoding. Sci. Rep. 9, 1–8 (2019).Article 
    CAS 

    Google Scholar 
    52.Hupało, K. et al. An urban Blitz with a twist: Rapid biodiversity assessment using aquatic environmental DNA. Environ. DNA 3, 200–213 (2020).Article 

    Google Scholar 
    53.Zainal Abidin, D. H. & Noor Adelyna, M. A. Universities as Living Labs for Sustainable Development 211–225 (Springer, 2020).
    Google Scholar 
    54.Ratnasingham, S. & Hebert, P. D. BOLD: The barcode of life data system. Mol. Ecol. Notes 7, 355–364 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    55.Benson, D. A. et al. GenBank. Nucleic Acids Res. 46, D41–D47 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    56.Mansor, M. I. et al. Field Guide to Important Commercial Marine Fishes of the South China Sea (SEAFDEC/MFRDMD, 1998).
    Google Scholar 
    57.Nuruddin, A. A. & Isa, S. M. Trawl Fisheries in Malaysia-Issues, Challenges and Mitigating Measures (Fisheries Research Institute, Department of Fisheries Malaysia, 2013).
    Google Scholar 
    58.Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    59.Kimura, M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111–120 (1980).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    60.Bouckaert, R. et al. BEAST 2: A software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10, e1003537 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    61.Edler, D., Klein, J., Antonelli, A. & Silvestro, D. raxmlGUI 2.0: A graphical interface and toolkit for phylogenetic analyses using RAxML. Methods Ecol. Evol. 12, 373–377 (2021).Article 

    Google Scholar 
    62.Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T. & Calcott, B. PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 34, 772–773 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    63.Miller, M. A., Pfeiffer, W. & Schwartz, T. In Proceedings of the 2011 TeraGrid Conference: Extreme digital discovery 1–8 (2011).64.Rambaut, A. FigTree v1.4.4. Available from: http://tree.bio.ed.ac.uk/software/figtree/ (2018).65.Ratnasingham, S. & Hebert, P. D. A DNA-based registry for all animal species: The Barcode Index Number (BIN) system. PLoS ONE 8, e66213 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    66.Pons, J. et al. Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst. Biol. 55, 595–609 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    67.Glez-Pena, D., Gomez-Blanco, D., Reboiro-Jato, M., Fdez-Riverola, F. & Posada, D. ALTER: Program-oriented conversion of DNA and protein alignments. Nucleic Acids Res. 38, W14–W18 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    68.Team, R. RStudio: integrated development for R (RStudio Inc., 2015).
    Google Scholar 
    69.Fujisawa, T. & Barraclough, T. G. Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: A revised method and evaluation on simulated data sets. Syst. Biol. 62, 707–724 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Global relationships between crop diversity and nutritional stability

    Narrowing crop diversity in the world’s food supplies is a potential threat to food security25; however, there have been few empirical studies to link crop diversity to system-level nutritional measures, especially beyond dietary intake at the household level9. Here we develop a method to link crops to specific micronutrients using a network approach and assess the role of crop production and imports on nutritional stability outcomes in 184 countries between 1961 and 2016. Similar to other scholars25,26, we find that crop diversity has increased over time in many regions, but that in many cases these gains are due to imports. Despite this increase in crop diversity, nutritional stability has remained stagnant or decreased in all regions except Asia, a trend largely attributed to our finding that gains in crop diversity coincide with fewer new nutritional links in a given food system.The general relationship between crop diversity and nutritional stability is contextualized by changes in crop degree and explains why stability does not mirror diversification trends. Improving crop diversity will always increase the size of the crop-nutrient network, but stability depends on the number and pattern of links within this network. As in other diversity–stability relationships functional identity matters, and declines in crop degree could reflect shifts toward networks with less nutrient-rich crops. For example, production-based crop diversity in Senegal increased by 29%, while crop degree dropped by 19% as the composition of its food supply shifted from staples (e.g., millet, groundnuts, sweet potatoes) to include less nutrient-dense crops (e.g., sugar cane, watermelon, cabbage). In light of on-going homogenization of crop diversity26, attaining the benefits of nutritional stability will require further understanding of the topology of crop-nutrient networks.By considering both production and nutritional diversity, our approach advances the quantification of food system resilience—the capacity over time of a food system and its units at multiple levels, to provide sufficient, appropriate, and accessible food to all, in the face of various and even unforeseen disturbances27. Our results have many implications for our understanding of nutritional measures and their relationship to crop diversity. First, our work reaffirms the existing body of research demonstrating that crop diversity is important for agricultural resilience11, and it does so at a national scale. Previous work has examined patterns of crop or nutritional diversity at global scales15,28 or linked crop diversity and nutrition-relevant outcomes at the field or landscape levels9. Our work answers recent calls8 to explore crop diversity and nutrition-relevant outcomes at a larger scale through a country-level analysis and incorporates both production and imports, the latter of which has been significant for driving an increase in the types of crops available in a given country over time. To be clear, we are measuring the relationships of crop diversity to nutrients and their susceptibility to disturbance; we are not measuring nutritional outcomes such as dietary intake, dietary diversity, or other health-related outcomes that are the result of nutrition. Just as nutritional status cannot be determined from dietary intake alone, nutritional stability does not determine the availability, let alone utilization, of nutrients. This is a natural area to expand this work moving forward.Second, our work establishes a functional relationship between crop diversity and nutritional stability. We suggest that this non-linear relationship has important implications for thinking about the types of crops grown or imported in a given region and how they ensure nutrient availability. A foundation shared by ecology and nutrition is that diversity can improve long-term functioning of complex biological systems29,30. Like other ecological diversity–resilience relationships, we observe that diversity loss can result in rapid loss of function31. In countries where diversity is already low, our results indicate that crop failures, either through production failure or an inability to import such crops, could lead to rapid reductions in nutrient availability within a country. Moreover, multiple failures of highly important regional crops, as might occur during a drought or other extreme events, could have catastrophic nutritional impact. Such countries are thus vulnerable to a variety of potential global challenges both ecological (e.g., climate change) and economic (e.g., trade wars).Third, that nutritional stability is stagnant or decreased over time in all regions but Asia highlights that increasing crop diversity—at least at the national level—does not necessarily lead to more stability. Instead, the wide variability in nutritional stability across countries highlights clear vulnerabilities both across and within regions. Africa has the greatest inter-regional variability, demonstrating that in some cases neighboring countries have very different stabilities of crop nutrients in their food supply chain in any given year. This variability is likely driven by multiple factors including the capacity of a country to trade32, in country food availability as a result of war or political/social unrest33,34,35, or exposure to climate-induced disasters36.Finally, the important role of imports in many regions highlights that crop diversity and nutritional stability are market exposed. While trade can positively affect food security37, it can also hinder nutrition efforts38 and could be a vulnerability if imports comprise a significant portion of nutritional stability for a given population. Countries with a high reliance on imports are thus subject to trade wars, market shifts, and price shocks that can occur for a variety of reasons39. Such countries may be more likely to experience increased variability in the future, especially as climate change is expected to affect agricultural production, markets, and trade40.The use of these results could help inform high-level discussions within countries and regions about the key crops for a given place and their availability via import or domestic production. Scenario development using our metric could help target country-specific crop additions that would maximize nutritional stability. Our approach could also be used to identify potential tradeoffs in production and import outcomes, at least as it relates to the availability of a given amount of nutrients in a certain place. In the context of policy interventions, this system-level metric could be applied in panel-type designs to diagnose whether initiatives (e.g., promoting or increasing food production, trade and storage) at different scales of organization (e.g., household, community, national) will effectively promote food system resilience programs41.Such potential applications also highlight the importance of identifying several caveats and important limitations. First, although we are addressing the nutrients available in a given country in a given time, we are not equating this with food security. This “availability” is only one component of food security, with access, utilization, and stability being other critical pillars. Thus, even though nutritional stability is generally high in most regions and remained stagnant (or increased in Asia), this does not mean that people are not food insecure. Adequate food and nutritional security comprises much more than the factors captured in our analysis, which provides a relative measure of nutrient availability not an absolute metric of adequacy. In the present study, we focused on nutrients available from crops, because animal-based products are rarely resolved to the species level and there is large interspecies variability in crop micronutrient composition. Animal-based products nonetheless play a critical role in providing some nutrients, thus there may be greater variability between countries when accounting for animal-based foods. There are also some methodological limitations. Crops are likely to vary in their loss susceptibility according to exogenous factors, such as market value or climate change vulnerability or pest pressure or simply abundance. In our current approach, all crops have equal removal probability; crop removal scenarios that account for these differential vulnerabilities is an exciting next step. Our current approach considers only nutrient presence or absence and may underestimate nutritional stability because ultimately the vulnerability of nutrient provision will also depend on how much of that nutrient is produced. Considering fractional crop loss or removal probabilities based on production levels could add realistic complexity in future analyses. Furthermore, complex system modeling of trade dynamics could explore to what extent import-based network re-orientation rescues nutritional stability by allowing for network rewiring via crop substitutability42,43. Finally, there are recognized shortcomings with the existing FAO data, especially in many low-income countries44. Nevertheless, to our knowledge, it is the best available data of its kind and scale available, so we utilize it knowing that there are many opportunities to improve this work moving forward.Despite these caveats, this work advances a method to assess the relationship between crop diversity and nutrient availability globally over the past 55 years. Future research could expand this work in multiple ways by combining crop-nutrient availability data with nutritional intake data to better assess whether available nutrients in the supply chain are making their way into household consumption. This would more completely link crop diversity with food and nutritional security outcomes, rather than just food availability as this work has done. Furthermore, our network tolerance method could be advanced by exploring the importance of certain crops for a given country or region by considering non-random loss of crops. Finally, with climate change expected to affect the yields of many globally important crops45 and potentially cause multiple crop failures at once36, this type of analysis could advance our understanding of food system vulnerability to specific crop failures and provide guidance on climate adaptation efforts or crop diversification strategies to safeguard against climate change.Resilience is now a central paradigm in many sectors—humanitarian aid, disaster risk reduction, climate change adaptation, social protection. Most analyses of resilience in food systems occur at household or community scales17 or focus on broader patterns of food production and distribution18,39. Erosion of biological diversity typically leads to loss of ecosystem functioning and services, likewise loss of crop diversity may to lead to potentially drastic shifts in nutritional stability. Together this and future analyses have the potential to direct the protection or restoration of crop diversity so as to best support nutrient availability that is stable to current and future challenges. More

  • in

    Polar bears are inbreeding as their icy home disintegrates

    .readcube-buybox { display: none !important;}

    Polar bears in Norway have undergone a staggering loss in genetic diversity in recent decades, as a result of the decline of Arctic sea ice.

    Access options

    Access through your institution

    Change institution

    Buy or subscribe

    /* style specs start */
    style{display:none!important}.LiveAreaSection-193358632 *{align-content:stretch;align-items:stretch;align-self:auto;animation-delay:0s;animation-direction:normal;animation-duration:0s;animation-fill-mode:none;animation-iteration-count:1;animation-name:none;animation-play-state:running;animation-timing-function:ease;azimuth:center;backface-visibility:visible;background-attachment:scroll;background-blend-mode:normal;background-clip:borderBox;background-color:transparent;background-image:none;background-origin:paddingBox;background-position:0 0;background-repeat:repeat;background-size:auto auto;block-size:auto;border-block-end-color:currentcolor;border-block-end-style:none;border-block-end-width:medium;border-block-start-color:currentcolor;border-block-start-style:none;border-block-start-width:medium;border-bottom-color:currentcolor;border-bottom-left-radius:0;border-bottom-right-radius:0;border-bottom-style:none;border-bottom-width:medium;border-collapse:separate;border-image-outset:0s;border-image-repeat:stretch;border-image-slice:100%;border-image-source:none;border-image-width:1;border-inline-end-color:currentcolor;border-inline-end-style:none;border-inline-end-width:medium;border-inline-start-color:currentcolor;border-inline-start-style:none;border-inline-start-width:medium;border-left-color:currentcolor;border-left-style:none;border-left-width:medium;border-right-color:currentcolor;border-right-style:none;border-right-width:medium;border-spacing:0;border-top-color:currentcolor;border-top-left-radius:0;border-top-right-radius:0;border-top-style:none;border-top-width:medium;bottom:auto;box-decoration-break:slice;box-shadow:none;box-sizing:border-box;break-after:auto;break-before:auto;break-inside:auto;caption-side:top;caret-color:auto;clear:none;clip:auto;clip-path:none;color:initial;column-count:auto;column-fill:balance;column-gap:normal;column-rule-color:currentcolor;column-rule-style:none;column-rule-width:medium;column-span:none;column-width:auto;content:normal;counter-increment:none;counter-reset:none;cursor:auto;display:inline;empty-cells:show;filter:none;flex-basis:auto;flex-direction:row;flex-grow:0;flex-shrink:1;flex-wrap:nowrap;float:none;font-family:initial;font-feature-settings:normal;font-kerning:auto;font-language-override:normal;font-size:medium;font-size-adjust:none;font-stretch:normal;font-style:normal;font-synthesis:weight style;font-variant:normal;font-variant-alternates:normal;font-variant-caps:normal;font-variant-east-asian:normal;font-variant-ligatures:normal;font-variant-numeric:normal;font-variant-position:normal;font-weight:400;grid-auto-columns:auto;grid-auto-flow:row;grid-auto-rows:auto;grid-column-end:auto;grid-column-gap:0;grid-column-start:auto;grid-row-end:auto;grid-row-gap:0;grid-row-start:auto;grid-template-areas:none;grid-template-columns:none;grid-template-rows:none;height:auto;hyphens:manual;image-orientation:0deg;image-rendering:auto;image-resolution:1dppx;ime-mode:auto;inline-size:auto;isolation:auto;justify-content:flexStart;left:auto;letter-spacing:normal;line-break:auto;line-height:normal;list-style-image:none;list-style-position:outside;list-style-type:disc;margin-block-end:0;margin-block-start:0;margin-bottom:0;margin-inline-end:0;margin-inline-start:0;margin-left:0;margin-right:0;margin-top:0;mask-clip:borderBox;mask-composite:add;mask-image:none;mask-mode:matchSource;mask-origin:borderBox;mask-position:0% 0%;mask-repeat:repeat;mask-size:auto;mask-type:luminance;max-height:none;max-width:none;min-block-size:0;min-height:0;min-inline-size:0;min-width:0;mix-blend-mode:normal;object-fit:fill;object-position:50% 50%;offset-block-end:auto;offset-block-start:auto;offset-inline-end:auto;offset-inline-start:auto;opacity:1;order:0;orphans:2;outline-color:initial;outline-offset:0;outline-style:none;outline-width:medium;overflow:visible;overflow-wrap:normal;overflow-x:visible;overflow-y:visible;padding-block-end:0;padding-block-start:0;padding-bottom:0;padding-inline-end:0;padding-inline-start:0;padding-left:0;padding-right:0;padding-top:0;page-break-after:auto;page-break-before:auto;page-break-inside:auto;perspective:none;perspective-origin:50% 50%;pointer-events:auto;position:static;quotes:initial;resize:none;right:auto;ruby-align:spaceAround;ruby-merge:separate;ruby-position:over;scroll-behavior:auto;scroll-snap-coordinate:none;scroll-snap-destination:0 0;scroll-snap-points-x:none;scroll-snap-points-y:none;scroll-snap-type:none;shape-image-threshold:0;shape-margin:0;shape-outside:none;tab-size:8;table-layout:auto;text-align:initial;text-align-last:auto;text-combine-upright:none;text-decoration-color:currentcolor;text-decoration-line:none;text-decoration-style:solid;text-emphasis-color:currentcolor;text-emphasis-position:over right;text-emphasis-style:none;text-indent:0;text-justify:auto;text-orientation:mixed;text-overflow:clip;text-rendering:auto;text-shadow:none;text-transform:none;text-underline-position:auto;top:auto;touch-action:auto;transform:none;transform-box:borderBox;transform-origin:50% 50% 0;transform-style:flat;transition-delay:0s;transition-duration:0s;transition-property:all;transition-timing-function:ease;vertical-align:baseline;visibility:visible;white-space:normal;widows:2;width:auto;will-change:auto;word-break:normal;word-spacing:normal;word-wrap:normal;writing-mode:horizontalTb;z-index:auto;-webkit-appearance:none;-moz-appearance:none;-ms-appearance:none;appearance:none;margin:0}.LiveAreaSection-193358632{width:100%}.LiveAreaSection-193358632 .login-option-buybox{display:block;width:100%;font-size:17px;line-height:30px;color:#222;padding-top:30px;font-family:Harding,Palatino,serif}.LiveAreaSection-193358632 .additional-access-options{display:block;font-weight:700;font-size:17px;line-height:30px;color:#222;font-family:Harding,Palatino,serif}.LiveAreaSection-193358632 .additional-login >li:not(:first-child)::before{transform:translateY(-50%);content:”;height:1rem;position:absolute;top:50%;left:0;border-left:2px solid #999}.LiveAreaSection-193358632 .additional-login >li:not(:first-child){padding-left:10px}.LiveAreaSection-193358632 .additional-login >li{display:inline-block;position:relative;vertical-align:middle;padding-right:10px}.BuyBoxSection-683559780{display:flex;flex-wrap:wrap;flex:1;flex-direction:row-reverse;margin:-30px -15px 0}.BuyBoxSection-683559780 .box-inner{width:100%;height:100%}.BuyBoxSection-683559780 .readcube-buybox{background-color:#f3f3f3;flex-shrink:1;flex-grow:1;flex-basis:255px;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .subscribe-buybox{background-color:#f3f3f3;flex-shrink:1;flex-grow:4;flex-basis:300px;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .title-readcube{display:block;margin:0;margin-right:20%;margin-left:20%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .title-buybox{display:block;margin:0;margin-right:29%;margin-left:29%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .title-asia-buybox{display:block;margin:0;margin-right:5%;margin-left:5%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .asia-link{color:#069;cursor:pointer;text-decoration:none;font-size:1.05em;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:1.05em6}.BuyBoxSection-683559780 .access-readcube{display:block;margin:0;margin-right:10%;margin-left:10%;font-size:14px;color:#222;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .access-asia-buybox{display:block;margin:0;margin-right:5%;margin-left:5%;font-size:14px;color:#222;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .access-buybox{display:block;margin:0;margin-right:30%;margin-left:30%;font-size:14px;color:#222;opacity:.8px;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .price-buybox{display:block;font-size:30px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;padding-top:30px;text-align:center}.BuyBoxSection-683559780 .price-from{font-size:14px;padding-right:10px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .issue-buybox{display:block;font-size:13px;text-align:center;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:19px}.BuyBoxSection-683559780 .no-price-buybox{display:block;font-size:13px;line-height:18px;text-align:center;padding-right:10%;padding-left:10%;padding-bottom:20px;padding-top:30px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif}.BuyBoxSection-683559780 .vat-buybox{display:block;margin-top:5px;margin-right:20%;margin-left:20%;font-size:11px;color:#222;padding-top:10px;padding-bottom:15px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:17px}.BuyBoxSection-683559780 .button-container{display:block;padding-right:20px;padding-left:20px}.BuyBoxSection-683559780 .button-container >a:hover,.Button-505204839:hover,.Button-1078489254:hover{text-decoration:none}.BuyBoxSection-683559780 .readcube-button{background:#fff;margin-top:30px}.BuyBoxSection-683559780 .button-asia{background:#069;border:1px solid #069;border-radius:0;cursor:pointer;display:block;padding:9px;outline:0;text-align:center;text-decoration:none;min-width:80px;margin-top:75px}.BuyBoxSection-683559780 .button-label-asia,.ButtonLabel-3869432492,.ButtonLabel-3296148077{display:block;color:#fff;font-size:17px;line-height:20px;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;text-align:center;text-decoration:none;cursor:pointer}.Button-505204839,.Button-1078489254{background:#069;border:1px solid #069;border-radius:0;cursor:pointer;display:block;padding:9px;outline:0;text-align:center;text-decoration:none;min-width:80px;margin-top:10px}.Button-505204839 .readcube-label,.Button-1078489254 .readcube-label{color:#069}
    /* style specs end */Subscribe to JournalGet full journal access for 1 year$199.00only $3.90 per issueSubscribeAll prices are NET prices. VAT will be added later in the checkout.Tax calculation will be finalised during checkout.Rent or Buy articleGet time limited or full article access on ReadCube.from$8.99Rent or BuyAll prices are NET prices.

    Additional access options:

    Log in

    Learn about institutional subscriptions

    doi: https://doi.org/10.1038/d41586-021-02438-1

    References1.Maduna, S. N. et al. Proc. R. Soc. B 288, 20211741 (2021).PubMed 
    Article 

    Google Scholar 
    Download references

    Subjects

    Ecology

    Latest on:

    Ecology

    Pollination advantage of rare plants unveiled
    News & Views 08 SEP 21

    Pollinators contribute to the maintenance of flowering plant diversity
    Article 08 SEP 21

    Widespread woody plant use of water stored in bedrock
    Article 08 SEP 21

    Jobs

    Open Rank, Term Tenure Track

    The University of Texas MD Anderson Cancer Center
    Houston, TX, United States

    Assistant Professor of Bioengineering

    George R. Brown School of Engineering, Rice University
    Houston, TX, United States

    Senior Marketing Manager, Open Research and Agreements

    Springer Nature
    London, United Kingdom

    Research Scientist / Postdoc as Young Investigator Group Leader for in situ surface analytics

    Helmholtz Association.
    Geesthacht, Germany

    Nature Briefing
    An essential round-up of science news, opinion and analysis, delivered to your inbox every weekday.

    Email address

    Yes! Sign me up to receive the daily Nature Briefing email. I agree my information will be processed in accordance with the Nature and Springer Nature Limited Privacy Policy.

    Sign up More

  • in

    Who wants to be a polar bear?

    Download PDF

    As a wildlife-conservation biologist studying climate change, I want to understand the evolving environment through the eyes of large animals. My work — usually in cold, remote places — involves finding animals, and ways to eat, sleep and be warm. I might be miserable, but I get insights that others cannot into what animals are doing.For about 15 years I’ve been interested in musk oxen (Ovibos moschatus), social herd animals that roamed with woolly mammoths. This picture was taken on Wrangel Island, off the northeast coast of Russia, when I was studying how musk oxen react to polar bears. Because polar ice is melting, more polar bears are hunting on land, and they’re known to have killed musk oxen. These herd animals typically don’t flee from predators such as grizzly bears. They tend to form huddles instead, and male musk oxen have killed grizzlies. Would they try to kill polar bears, too?To find out, I dressed as a polar bear, pulling a bear head on and placing a cape over a range finder, camera and data books. I was cold and nervous. I didn’t want to be killed by a charging musk ox — or by anything else. If some oxen charged, I’d throw off my costume and stand up straight, as I’m doing here; so far, that had stopped them. I’d also encountered a female polar bear with newborn cubs, but she’d left me alone. This picture is from the end of a session, and I’d lived another day. Whew!I learnt that musk oxen are more likely to flee from polar bears than from grizzlies. But during this trip to Russia, I was arrested — over a date error on my permits. In court, the only word I understood was ‘CIA’. I was let go, but banned from returning for three years, so I’m now studying the huemul (Hippocamelus bisulcus), an endangered species of deer that lives in the shadows of glaciers at the tip of South America. As glaciers recede, how will huemul populations respond?

    Nature 597, 296 (2021)
    doi: https://doi.org/10.1038/d41586-021-02429-2

    Related Articles

    Tracking Chernobyl’s effects on wildlife

    Chasing bats at dawn

    To look after these birds is to ‘fall in love’ with them

    Subjects

    Careers

    Climate change

    Conservation biology

    Latest on:

    Careers

    Diversity in science workforce an ‘economic imperative’
    Career News 02 SEP 21

    What makes us tick: lab leaders describe their research philosophies
    Career Guide 01 SEP 21

    In memory of a game-changing haematologist
    Correspondence 31 AUG 21

    Climate change

    Freak US winters linked to Arctic warming
    News 03 SEP 21

    Policy, drought and fires combine to affect biodiversity in the Amazon basin
    News & Views 01 SEP 21

    The contribution of insects to global forest deadwood decomposition
    Article 01 SEP 21

    Jobs

    PhD Project – High recovery and chemical-free desalination using advanced electrodialysis schemes

    Wetsus Centre of Excellence for Sustainable Water Technology
    Leeuwarden, Netherlands

    PhD Project – Beyond chlorine: alternative sustainable compounds to remove biofilms in drinking water environments

    Wetsus Centre of Excellence for Sustainable Water Technology
    Leeuwarden, Netherlands

    PhD Project – Sensing strategies for real-time, early warning monitoring of biofilm formation parameters in drinking water distribution systems

    Wetsus Centre of Excellence for Sustainable Water Technology
    Leeuwarden, Netherlands

    Enhancing the local water cycle via evaporation for a sustainable water supply

    Wetsus Centre of Excellence for Sustainable Water Technology
    Leeuwarden, Netherlands

    Nature Briefing
    An essential round-up of science news, opinion and analysis, delivered to your inbox every weekday.

    Email address

    Yes! Sign me up to receive the daily Nature Briefing email. I agree my information will be processed in accordance with the Nature and Springer Nature Limited Privacy Policy.

    Sign up More

  • in

    Socio-demographic correlates of wildlife consumption during early stages of the COVID-19 pandemic

    We focused our research on countries/territories in Asia (specifically, Hong Kong SAR, Japan, Myanmar, Thailand and Vietnam) because COVID-19 had not spread much outside Asia at the time of data collection and the global effects were predominantly concentrated in East and Southeast Asia. Our five survey countries/territories were chosen because they all have relatively high levels of wildlife trade but also represent very different forms of trade (for example, the pet trade in Japan versus the wild-meat trade in Vietnam). Surveying respondents from markets with these different forms of trade thus allowed an examination of how the full variety of wildlife consumption types may be impacted by perceived disease risk. Budgetary constraints precluded the inclusion of further countries, although we believe those that were surveyed provide a valid snapshot of the main regional issues and patterns. The exception to this may be the exclusion of China, a key global player in the wildlife trade and the possible origin of the COVID-19 virus. Conducting research in China requires an extensive process to obtain permission that was not consistent with the opportunistic nature of our survey, which was mobilized quickly to target opinions from a snapshot view of an (at that time) emerging disease. Given the time-sensitive nature of the research, we were therefore unable to wait for the necessary permissions to include China in this survey.Our online survey was conducted between March 3–11, 2020 and surveyed 1,000 respondents in each of the five target countries/territories. We designed and translated our questionnaires with local experts to ensure questions were culturally appropriate, understandable and relevant. The survey was a quantitative data collection instrument that comprised 32 questions, lasted on average 8 minutes, and respondents were offered an incentive for participating. Respondents aged 18+ were invited via email from an online panel of over 2.5 million people in the target countries/territories, and could answer on any internet-capable device (for example smartphone, tablet, laptop) at their convenience. Only respondents aged 18 and over were eligible to take the survey, which was entirely voluntary. Any respondents working in advertising, public relations, marketing, market research or media industries were screened out to prevent possible bias. The email invite that was sent to participants did not specify the exact nature of the survey to avoid skewing the participants towards those that believed they know about the topic. Instead, the invite indicated that the questions would be about ‘consumption and shopping habits’. The panel is maintained by Toluna (https://tolunacorporate.com/), an online data collection group focused on providing high-quality market research data to clients in various business and non-business sectors. Toluna builds and maintains large online consumer panels to collect these data while adhering to stringent global and local guidelines for panel management and data quality, and is a member of the European Society for Opinion and Market Research (https://www.esomar.org).Toluna respects privacy and is committed to protecting personal data. Their privacy policy (https://tolunacorporate.com/legal/privacy-policy/) provides information on how Toluna collects and processes personal data, explains privacy rights and gives an overview of applicable legislation protecting the handling of personal information. Toluna only uses personal data when the law allows the data to be used.Respondents were asked demographic questions, and quotas based on the most recent census data for each country/territory were used to ensure the final sample profile was nationally representative of age and gender, except in Myanmar where internet access skewed online panel members to a younger male demographic. Specifically, participants were excluded once quotas on age and gender were filled, and again, participants working in advertising/public relations, marketing research or media were excluded from the survey as we believed these jobs could influence responses. Respondents were asked about societal, economic and environmental concerns, their perception of COVID-19 and their attitudes towards wildlife and wildlife consumption (Supplementary Methods). We also excluded respondents who stated that they were unsure whether they or anyone in their social circle had recently purchased wildlife products (n = 421), as well as an additional n = 39 respondents who were unable to answer survey questions that were later included as covariates in our models.Because of the potentially sensitive nature of wildlife consumption, we asked about past wildlife purchases indirectly, questioning respondents on whether anyone within their social circle, including themselves, had recently purchased wildlife products. Indirect questions can improve answer rates for questions that people may feel uncomfortable about answering honestly27. During the pandemic, respondents may have felt uncomfortable about revealing wildlife purchases, given links between wildlife consumption and COVID-19. Additionally, although most wildlife consumption is legal (with restrictions) in the markets surveyed, some is not, and researchers can be perceived as having interests contrary to that of the respondent. For less-sensitive questions on future wildlife consumption and changes in consumption resulting from COVID-19, we asked respondents for their own response rather than that of their social group.Previous studies have found a high correlation between an individual’s admission of using a wildlife product and their likelihood of being within a network of individuals who buy such products28, and suggested that this is linked to homophily in social networks, especially in Southeast Asia. The homophily principle states that people’s personal networks are homogeneous with regard to many socio-demographic, behavioural and intrapersonal characteristics29. Research on wildlife consumption in other Southeast Asian contexts suggests that social groups can be a motivator to begin or maintain consumption of wildlife products28,30. Our own previous research supports this, indicating a strong correlation between one’s own tiger and ivory purchases and knowing someone within one’s social circle who has purchased such products. Additionally and recognizing the homophily principle, behaviour change campaigns targeted at social networks rather than individuals per se are likely to achieve better results than non-targeted campaigns. Changing perceptions of acceptability is a key aspect of social marketing and is used in the social mobilization domain of social and behaviour change communications, which has become a popular framework for reducing demand for illegally traded wildlife products31. Influencing people within a wildlife consumer’s social network may therefore have a higher rate of efficacy than attempting to influence the perceptions of individuals who do not know any consumers of wildlife.We used hierarchical Bayesian regression models to assess relationships between socio-demographic explanators and our three response variables: (1) self-reported recent wildlife consumption, (2) change in wildlife consumption as a result of COVID-19 and (3) anticipated future wildlife consumption. Explanatory variables included 22 non-collinear variables in six categories: basic demographics, awareness and level of worry of COVID-19, COVID-19 personal impacts, support for and effectiveness of wildlife market closures, international travel habits and general attitudes towards global issues (Supplementary Table 1). Aside from household income (measured in US dollars per year), age (midpoint of year categories from the survey question) and education (ordinal, reflecting increasing level of schooling), all other variables were categorical; those with more than two categories were collapsed into dummy variables. Income, age and education were standardized and included to investigate whether a person’s general socio-economic status affects wildlife consumption. General attitudes towards global issues were expected to reflect aspects of respondents’ political tendencies, while travel habits were included to test the hypothesis that those who travel internationally more habitually are, and will be, more frequent consumers of wildlife. Questions regarding awareness and impacts of COVID-19, and concern about future disease epidemics, were asked to determine how the pandemic may be shaping wildlife consumption. Finally, support and perceived effectiveness of wildlife market closures were included as predictor variables since this measure has been suggested as a strong policy lever to reduce wildlife consumption.The general structure of all three models was as follows:$$y_{ij}sim {{{mathrm{Bernoulli}}}}left( {theta _{ij}} right)$$
    (1)
    $${mathrm{logit}}left( theta right) = alpha + {{u}_1} + {beta} {mathbf{X}} + {{u}_2}{mathbf{Z}}$$
    (2)
    This model allowed both coefficients and intercepts to vary across countries (that is, a ‘random-slope random-intercept’ model). In equation (1), yij is whether or not individual i in country j reported wildlife consumption, modelled as a Bernoulli trial with probability θij. The logit transformation of θ (equation 2) is a linear function of parameters α and u1 (the fixed intercept term and a vector of the country-specific intercept terms, respectively), as well as a vector of fixed regression coefficients β and a vector of country-specific regression coefficients u2, with X and Z being the corresponding design matrices32. For α and β, we used an improper flat prior over the real numbers, while the group level parameters u1 and u2 were assumed to arise from a multivariate normal distribution with mean 0 and unknown covariance matrix. The covariance matrix was parameterized by a correlation matrix having a Lewandowski–Kurowicka–Joe prior, and a standard deviation with half-Student t prior with three degrees of freedom32.For the three dependent variables, we evaluated the predictive power of a model containing all 22 variables, as well as six subset models, using Watanabe–Akaike Information Criterion and leave-one-out cross-validation33. Each of these six subset models contained all explanatory variables except for those within one of the six categories described above (for example, all explanatory variables except those relating to international travel habits, all explanatory variables except those relating to support for wildlife market closures). We used this model-comparison approach to test whether any of these categories of explanatory variable were more or less important in explaining wildlife consumption; if particular categories of variable are stronger predictors of wildlife consumption, this could help inform where future conservation interventions should focus on. Watanabe–Akaike Information Criterion and leave-one-out cross-validation are both measures of model predictive accuracy (both use log predictive density as the utility function or comparison metric) and have been suggested as useful metrics for Bayesian model selection33. We interpreted variable coefficients whose 95% Bayesian credible intervals did not contain 0 as providing strong evidence for the impact of that variable on the outcome in each of the three models for self-reported wildlife consumption (that is, recent, future and changes due to COVID-19). Models were estimated using the R statistical computing software34, in particular the package brms32, with four chains of 1,000 iterations each, a 500-iteration warm-up period, and with successful convergence verified by confirming that R-hat statistical values were less than or equal to 1.01 (ref. 22).We used the Bayesian hierarchical model of anticipated future wildlife consumption and generated predicted probabilities of future consumption for our sample population (Fig. 2, grey bars). We then predicted future consumption probabilities for a hypothetical behaviour-change intervention (Fig. 2, coloured bars). This intervention was simulated by setting the ‘medical impact’ variable to zero for all individuals, and by assigning all individuals into the ‘aware lots’ and ‘support very likely’ categories for questions related to level of awareness of COVID-19 and level of support for government closure of domestic wildlife markets, respectively. All other variables for individuals were held at the levels recorded in the surveys. We considered the difference between these two predicted probabilities as the impact of the hypothetical behaviour-change intervention, which we examined at the level of the country/territory and within education, age, income and gender demographic classes. Strong evidence for the effectiveness of this hypothetical intervention among countries and demographic classes was suggested where Bayesian credible intervals around the mean predicted difference were less than zero (Supplementary Table 3).Reporting SummaryFurther information on research design is available in the Nature Research Reporting Summary linked to this article. More

  • in

    Ecological memory of recurrent drought modifies soil processes via changes in soil microbial community

    1.Kannenberg, S. A., Schwalm, C. R. & Anderegg, W. R. L. Ghosts of the past: how drought legacy effects shape forest functioning and carbon cycling. Ecol. Lett. 23, 891–901 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    2.Padisak, J. Seasonal succession of phytoplankton in a large shallow lake (Balaton, Hungary)—a dynamic approach to ecological memory, its possible role and mechanisms. J. Ecol. 80, 217–230 (1992).Article 

    Google Scholar 
    3.Power, D. A. et al. What can ecosystems learn? Expanding evolutionary ecology with learning theory. Biol. Direct 10, 69 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    4.Falkowski, P. G., Fenchel, T. & Delong, E. F. The microbial engines that drive Earth’s biogeochemical cycles. Science 320, 1034–1039 (2008).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    5.Reichstein, M. et al. Climate extremes and the carbon cycle. Nature 500, 287 (2013).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    6.Seneviratne, S. I. et al. Changes in climate extremes and their impacts on the natural physical environment. In Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation. A Special Report of Working Groups I and II of the Intergovernmental Panel on Climate Change (IPCC) (eds. Field, C.B. et al.) 109–230 (Cambridge University Press, 2017).7.Pappas, C., Mahecha, M. D., Frank, D. C., Babst, F. & Koutsoyiannis, D. Ecosystem functioning is enveloped by hydrometeorological variability. Nat. Ecol. Evol. 1, 1263–1270 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    8.Hawkes, C. V. & Keitt, T. H. Resilience vs. historical contingency in microbial responses to environmental change. Ecol. Lett. 18, 612–625 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    9.Johnstone, J. F. et al. Changing disturbance regimes, ecological memory, and forest resilience. Front. Ecol. Environ. 14, 369–378 (2016).Article 

    Google Scholar 
    10.Ochoa‐Hueso, R. et al. Drought consistently alters the composition of soil fungal and bacterial communities in grasslands from two continents. Glob. Chang. Biol. 24, 2818–2827 (2018).11.Bastida, F. et al. Differential sensitivity of total and active soil microbial communities to drought and forest management. Glob. Chang. Biol. 23, 4185–4203 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    12.Evans, S. E., Wallenstein, M. D. & Burke, I. C. Is bacterial moisture niche a good predictor of shifts in community composition under long-term drought? Ecology 95, 110–122 (2014).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.de Vries, F. T. et al. Soil bacterial networks are less stable under drought than fungal networks. Nat. Commun. 9, 3033 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    14.Rousk, J., Smith, A. R. & Jones, D. L. Investigating the long-term legacy of drought and warming on the soil microbial community across five European shrubland ecosystems. Glob. Chang. Biol. 19, 3872–3884 (2013).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Kaisermann, A., de Vries, F. T., Griffiths, R. I. & Bardgett, R. D. Legacy effects of drought on plant–soil feedbacks and plant–plant interactions. New Phytol. 215, 1413–1424 (2017).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Fuchslueger, L. et al. Drought history affects grassland plant and microbial carbon turnover during and after a subsequent drought event. J. Ecol. 104, 1453–1465 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    17.Meisner, A., De Deyn, G. B., de Boer, W. & van der Putten, W. H. Soil biotic legacy effects of extreme weather events influence plant invasiveness. Proc. Natl Acad. Sci. USA 110, 9835–9838 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    18.de Nijs, E. A., Hicks, L. C., Leizeaga, A., Tietema, A. & Rousk, J. Soil microbial moisture dependences and responses to drying–rewetting: the legacy of 18 years drought. Glob. Chang. Biol. 25, 1005–1015 (2019).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    19.Fuchslueger, L., Bahn, M., Fritz, K., Hasibeder, R. & Richter, A. Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow. New Phytol. 201, 916–927 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.Mooshammer, M., Wanek, W., Zechmeister-Boltenstern, S. & Richter, A. Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources. Front. Microbiol. 5, 22 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    21.Waring, B. G., Weintraub, S. R. & Sinsabaugh, R. L. Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry 117, 101–113 (2014).CAS 
    Article 

    Google Scholar 
    22.Sinsabaugh, R. L. et al. Stoichiometry of soil enzyme activity at global scale. Ecol. Lett. 11, 1252–1264 (2008).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    23.Douglas, G. M. et al. PICRUSt2 for prediction of metagenome functions. Nat. Biotechnol. 38, 685–688, (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    24.Csonka, L. N. Physiological and genetic responses of bacteria to osmotic stress. Microbiol. Mol. Biol. Rev. 53, 121–147 (1989).CAS 

    Google Scholar 
    25.Whitfield, G. B., Marmont, L. S. & Howell, P. L. Enzymatic modifications of exopolysaccharides enhance bacterial persistence. Front. Microbiol. 6, 471 (2015).26.Byrd, M. S. et al. Genetic and biochemical analyses of the Pseudomonas aeruginosa Psl exopolysaccharide reveal overlapping roles for polysaccharide synthesis enzymes in Psl and LPS production. Mol. Microbiol. 73, 622–638 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    27.El Zoeiby, A., Sanschagrin, F. & Levesque, R. C. Structure and function of the Mur enzymes: development of novel inhibitors. Mol. Microbiol. 47, 1–12 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    28.Lebre, P. H., De Maayer, P. & Cowan, D. A. Xerotolerant bacteria: surviving through a dry spell. Nat. Rev. Microbiol. 15, 285–296 (2017).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    29.Delgado-Baquerizo, M. et al. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat. Commun. 7, 10541 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    30.Hughes, T. P. et al. Ecological memory modifies the cumulative impact of recurrent climate extremes. Nat. Clim. Chang. 9, 40–43 (2019).31.Seidl, R., Donato, D. C., Raffa, K. F. & Turner, M. G. Spatial variability in tree regeneration after wildfire delays and dampens future bark beetle outbreaks. Proc. Natl Acad. Sci. USA 113, 13075–13080 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    32.Hillebrand, H. & Kunze, C. Meta-analysis on pulse disturbances reveals differences in functional and compositional recovery across ecosystems. Ecol. Lett. 23, 575–585 (2020).33.Meisner, A., Jacquiod, S., Snoek, B. L., ten Hooven, F. C. & van der Putten, W. H. Drought legacy effects on the composition of soil fungal and prokaryote communities. Front. Microbiol. 9, 294 (2018).34.Bardgett, R. D. & Caruso, T. Soil microbial community responses to climate extremes: resistance, resilience and transitions to alternative states. Philos. Trans. R. Soc. B Biol. Sci. 375, 20190112 (2020).CAS 
    Article 

    Google Scholar 
    35.Isobe, K., Bouskill, N. J., Brodie, E. L., Sudderth, E. A. & Martiny, J. B. H. Phylogenetic conservation of soil bacterial responses to simulated global changes. Philos. Trans. R. Soc. B Biol. Sci. 375, 20190242 (2020).CAS 
    Article 

    Google Scholar 
    36.Barberán, A., Caceres Velazquez, H., Jones, S. & Fierer, N. Hiding in plain sight: mining bacterial species records for phenotypic trait information. mSphere 2, e00237–17 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    37.Bouskill, N. J. et al. Pre-exposure to drought increases the resistance of tropical forest soil bacterial communities to extended drought. ISME J. 7, 384 (2012).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    38.Taketani, R. G. et al. Dry season constrains bacterial phylogenetic diversity in a semi-arid rhizosphere system. Microb. Ecol. 73, 153–161 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    39.Naylor, D., DeGraaf, S., Purdom, E. & Coleman-Derr, D. Drought and host selection influence bacterial community dynamics in the grass root microbiome. ISME J. 11, 2691 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    40.Xu, L. et al. Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria. Proc. Natl Acad. Sci. USA 115, E4284–E4293 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    41.Taniguchi, T., Kitajima, K., Douhan, G. W., Yamanaka, N. & Allen, M. F. A pulse of summer precipitation after the dry season triggers changes in ectomycorrhizal formation, diversity, and community composition in a Mediterranean forest in California, USA. Mycorrhiza 28, 665–677 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    42.Ren, C. et al. Responses of soil total microbial biomass and community compositions to rainfall reductions. Soil Biol. Biochem. 116, 4–10 (2018).CAS 
    Article 

    Google Scholar 
    43.Furze, J. R. et al. Resistance and resilience of root fungal communities to water limitation in a temperate agroecosystem. Ecol. Evol. 7, 3443–3454 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    44.Deveautour, C., Donn, S., Power, S. A., Bennett, A. E. & Powell, J. R. Experimentally altered rainfall regimes and host root traits affect grassland arbuscular mycorrhizal fungal communities. Mol. Ecol. 27, 2152–2163 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    45.Averill, C., Turner, B. L. & Finzi, A. C. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505, 543–545 (2014).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    46.Dijkstra, F. A., He, M., Johansen, M. P., Harrison, J. J. & Keitel, C. Plant and microbial uptake of nitrogen and phosphorus affected by drought using 15N and 32P tracers. Soil Biol. Biochem. 82, 135–142 (2015).CAS 
    Article 

    Google Scholar 
    47.Kakumanu, M. L., Ma, L. & Williams, M. A. Drought-induced soil microbial amino acid and polysaccharide change and their implications for C–N cycles in a climate change world. Sci. Rep. 9, 10968 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    48.Sleator, R. D. & Hill, C. Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol. Rev. 26, 49–71 (2002).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    49.Warren, C. R. Response of osmolytes in soil to drying and rewetting. Soil Biol. Biochem. 70, 22–32 (2014).ADS 
    CAS 
    Article 

    Google Scholar 
    50.Bouskill, N. J. et al. Belowground response to drought in a tropical forest soil. I. Changes in microbial functional potential and metabolism. Front. Microbiol. 7, 525 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    51.Flemming, H.-C. et al. Biofilms: an emergent form of bacterial life. Nat. Rev. Microbiol. 14, 563 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    52.Malik, A. A. et al. Drought and plant litter chemistry alter microbial gene expression and metabolite production. ISME J. 14, 2236–2247 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    53.Nunan, N., Raynaud, X. & Schmidt, H. The ecology of heterogeneity: soil bacterial communities and C dynamics. Philos. Trans. R. Soc. B Biol. Sci. 375, 20190249 (2020).54.Li, J. et al. Predictive genomic traits for bacterial growth in culture versus actual growth in soil. ISME J. 13, 2162–2172 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    55.Maestre, F. T. et al. Plant species richness and ecosystem multifunctionality in global drylands. Science 335, 214–218 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    56.Grigulis, K. et al. Relative contributions of plant traits and soil microbial properties to mountain grassland ecosystem services. J. Ecol. 101, 47–57 (2013).Article 

    Google Scholar 
    57.Lau, J. A. & Lennon, J. T. Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc. Natl Acad. Sci. USA 109, 14058–14062 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    58.Fitzpatrick, C. R. et al. Assembly and ecological function of the root microbiome across angiosperm plant species. Proc. Natl Acad. Sci. USA 115, E1157–E1165 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    59.Huang, S. et al. Autotrophic and heterotrophic soil respiration responds asymmetrically to drought in a subtropical forest in the Southeast China. Soil Biol. Biochem. 123, 242–249 (2018).CAS 
    Article 

    Google Scholar 
    60.López-Ballesteros, A. et al. Enhancement of the net CO2 release of a semiarid grassland in SE Spain by rain pulses. J. Geophys. Res. Biogeosci. 121, 52–66 (2016).Article 
    CAS 

    Google Scholar 
    61.Schimel, J. P. Life in dry soils: effects of drought on soil microbial communities and processes. Annu. Rev. Ecol. Evol. Syst. 49, 409–432 (2018).Article 

    Google Scholar 
    62.Canarini, A., Kaiser, C., Merchant, A., Richter, A. & Wanek, W. Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Front. Plant Sci. 10, 157 (2019).63.de Vries, F. T. et al. Changes in root-exudate-induced respiration reveal a novel mechanism through which drought affects ecosystem carbon cycling. New Phytol. 224, 132–145 (2019).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    64.Teste, F. P. et al. Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands. Science 355, 173–176 (2017).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    65.Hu, L. et al. Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat. Commun. 9, 2738 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    66.Canarini, A., Merchant, A. & Dijkstra, F. A. Drought effects on Helianthus annuus and Glycine max metabolites: from phloem to root exudates. Rhizosphere 2, 85–97 (2016).67.Canarini, A. & Dijkstra, F. A. Dry-rewetting cycles regulate wheat carbon rhizodeposition, stabilization and nitrogen cycling. Soil Biol. Biochem. 81, 195–203 (2015).68.Morecroft, M. D. et al. Changing precipitation patterns alter plant community dynamics and succession in an ex-arable grassland. Funct. Ecol. 18, 648–655 (2004).Article 

    Google Scholar 
    69.Strickland, M. S., Osburn, E., Lauber, C., Fierer, N. & Bradford, M. A. Litter quality is in the eye of the beholder: initial decomposition rates as a function of inoculum characteristics. Funct. Ecol. 23, 627–636 (2009).Article 

    Google Scholar 
    70.Allison, S. D. et al. Microbial abundance and composition influence litter decomposition response to environmental change. Ecology 94, 714–725 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    71.Walker, T. W. N. et al. A systemic overreaction to years versus decades of warming in a subarctic grassland ecosystem. Nat. Ecol. Evol. 4, 101–108 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    72.Ogle, K. et al. Quantifying ecological memory in plant and ecosystem processes. Ecol. Lett. 18, 221–235 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    73.Bahn, M., Knapp, M., Garajova, Z., Pfahringer, N. & Cernusca, A. Root respiration in temperate mountain grasslands differing in land use. Glob. Chang. Biol. 12, 995–1006 (2006).ADS 
    Article 

    Google Scholar 
    74.Bahn, M. et al. Soil respiration at mean annual temperature predicts annual total across vegetation types and biomes. Biogeosciences 7, 2147 (2010).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    75.Schmitt, M., Bahn, M., Wohlfahrt, G., Tappeiner, U. & Cernusca, A. Land use affects the net ecosystem CO2 exchange and its components in mountain grasslands. Biogeosciences 7, 2297 (2010).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    76.Estiarte, M. et al. Few multiyear precipitation–reduction experiments find a shift in the productivity–precipitation relationship. Glob. Chang. Biol. 22, 2570–2581 (2016).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    77.Spohn, M., Klaus, K., Wanek, W. & Richter, A. Microbial carbon use efficiency and biomass turnover times depending on soil depth—Implications for carbon cycling. Soil Biol. Biochem. 96, 74–81 (2016).CAS 
    Article 

    Google Scholar 
    78.Manzoni, S., Taylor, P., Richter, A., Porporato, A. & Ågren, G. I. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol. 196, 79–91 (2012).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    79.Schinner, F., Öhlinger, R., Kandeler, E., Margesin, R. & Kaiser, P. Methods in soil biology. Bull. Inst. Pasteur 4, 311–312 (1996).
    Google Scholar 
    80.Kuo, S. Phosphorus. In Methods of Soil Analysis, Part 3 (eds. Sparks, D. L. et al.) Ch. 32, 869–919 (SSSA, 1996).81.Vance, E. D., Brookes, P. C. & Jenkinson, D. S. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19, 703–707 (1987).CAS 
    Article 

    Google Scholar 
    82.Brookes, P. C., Landman, A., Pruden, G. & Jenkinson, D. S. Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol. Biochem. 17, 837–842 (1985).CAS 
    Article 

    Google Scholar 
    83.Doyle, A., Weintraub, M. N. & Schimel, J. P. Persulfate digestion and simultaneous colorimetric analysis of carbon and nitrogen in soil extracts. Soil Sci. Soc. Am. J. 68, 669–676 (2004).ADS 
    CAS 
    Article 

    Google Scholar 
    84.Kandeler, E. & Gerber, H. Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol. Fertil. Soils 6, 68–72 (1988).CAS 
    Article 

    Google Scholar 
    85.Hood-Nowotny, R., Umana, N. H.-N., Inselbacher, E., Oswald- Lachouani, P. & Wanek, W. Alternative methods for measuring inorganic, organic, and total dissolved nitrogen in soil. Soil Sci. Soc. Am. J. 74, 1018–1027 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    86.Jones, D. L., Owen, A. G. & Farrar, J. F. Simple method to enable the high resolution determination of total free amino acids in soil solutions and soil extracts. Soil Biol. Biochem. 34, 1893–1902 (2002).CAS 
    Article 

    Google Scholar 
    87.Prommer, J. et al. Biochar decelerates soil organic nitrogen cycling but stimulates soil nitrification in a temperate arable field trial. PLoS ONE 9, e86388 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    88.Kaiser, C., Frank, A., Wild, B., Koranda, M. & Richter, A. Negligible contribution from roots to soil-borne phospholipid fatty acid fungal biomarkers 18:2ω6,9 and 18:1ω9. Soil Biol. Biochem. 42, 1650–1652 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    89.Kaiser, C. et al. Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil. New Phytol. 187, 843–858 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    90.Olsson, P. A. Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol. Ecol. 29, 303–310 (1999).CAS 
    Article 

    Google Scholar 
    91.Ngosong, C., Gabriel, E. & Ruess, L. Use of the signature fatty acid 16:1ω5 as a tool to determine the distribution of arbuscular mycorrhizal fungi in soil. J. Lipids 2012, 236807 (2012).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    92.Quideau, S. A. et al. Extraction and analysis of microbial phospholipid fatty acids in soils. J. Vis. Exp. 2016, 54360 (2016).93.García-Orenes, F., Morugán-Coronado, A., Zornoza, R., Cerdà, A. & Scow, K. Changes in soil microbial community structure influenced by agricultural management practices in a mediterranean agro-ecosystem. PLoS ONE 8, e80522–e80522 (2013).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    94.Herbold, C. et al. A flexible and economical barcoding approach for highly multiplexed amplicon sequencing of diverse target genes. Front. Microbiol. 6, 731 (2015).95.Apprill, A., McNally, S., Parsons, R. & Weber, L. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat. Microb. Ecol. 75, 129–137 (2015).Article 

    Google Scholar 
    96.Parada, A. E., Needham, D. M. & Fuhrman, J. A. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18, 1403–1414 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    97.White, T. J., Bruns, T., Lee, S. & Taylor, J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications 315–322 (Academic Press, 1990).98.Paymaneh, Z., Sarcheshmehpour, M., Bukovská, P. & Jansa, J. Could indigenous arbuscular mycorrhizal communities be used to improve tolerance of pistachio to salinity and/or drought? Symbiosis 79, 269–283 (2019).99.Smith, D. P. & Peay, K. G. Sequence depth, not PCR replication, improves ecological inference from next generation DNA sequencing. PLoS ONE 9, e90234 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    100.Tedersoo, L. & Lindahl, B. Fungal identification biases in microbiome projects. Environ. Microbiol. Rep. 8, 774–779 (2016).PubMed 
    Article 

    Google Scholar 
    101.Krüger, M., Stockinger, H., Krüger, C. & Schüßler, A. DNA‐based species level detection of Glomeromycota: one PCR primer set for all arbuscular mycorrhizal fungi. New Phytol. 183, 212–223 (2009).PubMed 
    Article 
    CAS 

    Google Scholar 
    102.Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    103.Bengtsson‐Palme, J. et al. Improved software detection and extraction of ITS1 and ITS 2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol. Evol. 4, 914–919 (2013).
    Google Scholar 
    104.Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    105.Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267 (2007).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    106.Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541 (2009).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    107.Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2012).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    108.Deshpande, V. et al. Fungal identification using a Bayesian classifier and the Warcup training set of internal transcribed spacer sequences. Mycologia 108, 1–5 (2016).PubMed 
    Article 

    Google Scholar 
    109.R Core Team. R: A Language and Environment for Statistical Computing (R Core Team, 2017).110.McMurdie, P. J. & Holmes, S. phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS ONE 8, e61217 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    111.Chen, L. et al. GMPR: a robust normalization method for zero-inflated count data with application to microbiome sequencing data. PeerJ 6, e4600–e4600 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    112.Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    113.Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).114.Kozak, M. & Piepho, H. What’s normal anyway? Residual plots are more telling than significance tests when checking ANOVA assumptions. J. Agron. Crop Sci. 204, 86–98 (2018).Article 

    Google Scholar 
    115.Ben-Shachar, M. S., Lüdecke, D. & Makowski, D. effectsize: Estimation of effect size indices and standardized parameters. J. Open Source Softw. 5, 2815 (2020).ADS 
    Article 

    Google Scholar 
    116.Oksanen, J. et al. Package ‘vegan’. Community Ecol. Packag. 2, 1–295 (2013).
    Google Scholar 
    117.Hedges, L. V., Gurevitch, J. & Curtis, P. S. The meta‐analysis of response ratios in experimental ecology. Ecology 80, 1150–1156 (1999).Article 

    Google Scholar 
    118.Barbera, P. et al. EPA-ng: massively parallel evolutionary placement of genetic sequences. Syst. Biol. 68, 365–369 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    119.Czech, L. & Stamatakis, A. Scalable methods for analyzing and visualizing phylogenetic placement of metagenomic samples. PLoS ONE 14, e0217050–e0217050 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    120.Louca, S. & Doebeli, M. Efficient comparative phylogenetics on large trees. Bioinformatics 34, 1053–1055 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    121.McMurdie, P. J. & Paulson, J. N. biomformat: An interface package for the BIOM file format. R/Bioconductor Package, version 1.0.0. (Bioconductor, 2015). More

  • in

    Agrobiodiversity Index scores show agrobiodiversity is underutilized in national food systems

    1.Living Planet Report 2020: Bending the Curve on Biodiversity Loss (WWF, 2020).2.Routledge Handbook of Agricultural Biodiversity (Routledge, 2017).3.Ulian, T. et al. Unlocking plant resources to support food security and promote sustainable agriculture. Plants People Planet 2, 421–445 (2020).Article 

    Google Scholar 
    4.Jarvis, D. I. et al. A global perspective of the richness and evenness of traditional crop-variety diversity maintained by farming communities. Proc. Natl Acad. Sci. USA 105, 5326–5331 (2008).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    5.The State of the World’s Biodiversity for Food and Agriculture (FAO Commission on Genetic Resources for Food and Agriculture, 2019); https://doi.org/10.4060/ca3129en6.Soroye, P., Newbold, T. & Kerr, J. Climate change contributes to widespread declines among bumble bees across continents. Science 367, 685–688 (2020).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    7.Willett, W. et al. Food in the Anthropocene: the EAT–Lancet Commission on healthy diets from sustainable food systems. Lancet 393, 447–492 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    8.Lachat, C. et al. Dietary species richness as a measure of food biodiversity and nutritional quality of diets. Proc. Natl Acad. Sci. USA 115, 127–132 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    9.Afshin, A. et al. Health effects of dietary risks in 195 countries, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet 393, 1958–1972 (2019).Article 

    Google Scholar 
    10.Altieri, M. A. & Nicholls, C. I. Biodiversity and Pest Management in Agroecosystems (Food Products, 2004).11.McDaniel, M. D., Tiemann, L. K. & Grandy, A. S. Does agricultural crop diversity enhance soil microbial biomass and organic matter dynamics? A meta-analysis. Ecol. Appl. 24, 560–570 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    12.Beillouin, D., Ben-Ari, T. & Makowski, D. Evidence map of crop diversification strategies at the global scale. Environ. Res. Lett. 4, 123001 (2019).ADS 
    Article 
    CAS 

    Google Scholar 
    13.Stomph, T. J. et al. Designing intercrops for high yield, yield stability and efficient use of resources: are there principles? Adv. Agron. 160, 1–50 (2020).Article 

    Google Scholar 
    14.Raseduzzaman, M. & Jensen, E. S. Does intercropping enhance yield stability in arable crop production? A meta-analysis. Eur. J. Agron. 91, 25–33 (2017).Article 

    Google Scholar 
    15.Renard, D. & Tilman, D. National food production stabilized by crop diversity. Nature 571, 257–260 (2019).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.International Food Policy Research Institute. Global spatially-disaggregated crop production statistics data for 2010 version 1.1. Harvard Dataverse v.3 (Harvard Dataverse, 2019).17.You, L., Wood, S., Wood-Sichra, U. & Wu, W. Generating global crop distribution maps: from census to grid. Agric. Syst. 127, 53–60 (2014).Article 

    Google Scholar 
    18.Tedesco, P. A. et al. Data Descriptor: a global database on freshwater fish species occurrence in drainage basins. Sci. Data 4, 170141 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    19.Sibhatu, K. T., Krishna, V. V. & Qaim, M. Production diversity and dietary diversity in smallholder farm households. Proc. Natl Acad. Sci. USA 2015, 201510982 (2015).
    Google Scholar 
    20.Allen, T., Prosperi, P., Cogill, B. & Flichman, G. Agricultural biodiversity, social–ecological systems and sustainable diets. Proc. Nutr. Soc. 73, 498–508 (2014).PubMed 
    Article 

    Google Scholar 
    21.Massawe, F., Mayes, S. & Cheng, A. Crop diversity: an unexploited treasure trove for food security. Trends Plant Sci. 21, 365–368 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    22.Dwivedi, S. L. et al. Diversifying food systems in the pursuit of sustainable food production and healthy diets. Trends Plant Sci. 22, 842–856 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    23.Frison, E. A. et al. Agricultural biodiversity is essential for a sustainable improvement in food and nutrition security. Sustainability 3, 238–253 (2011).Article 

    Google Scholar 
    24.Klein, A.-M. et al. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B 274, 303–313 (2007).PubMed 
    Article 

    Google Scholar 
    25.Orgiazzi, A. et al. Global Soil Biodiversity Atlas (European Commission, Publications Office of the European Union, 2016); https://doi.org/10.2788/79918226.Kremen, C., Iles, A. & Bacon, C. Diversified farming systems: an agroecological, systems-based alternative to modern industrial agriculture. Ecol. Soc. 17, 44 (2012).
    Google Scholar 
    27.Khoury, C. K. et al. Comprehensiveness of conservation of useful wild plants: an operational indicator for biodiversity and sustainable development targets. Ecol. Indic. 98, 420–429 (2019).Article 

    Google Scholar 
    28.Castañeda-Álvarez, N. P. et al. Global conservation priorities for crop wild relatives. Nat. Plants 2, 16022 (2016).PubMed 
    Article 

    Google Scholar 
    29.A Global Database for the Distributions of Crop Wild Relatives v.1.12 (Centro Internacional de Agricultura Tropical, 2018); https://doi.org/10.15468/jyrthk30.Shannon, C. E. & Weaver, W. The Mathematical Theory of Communication (Univ. of Illinois Press, 1949).31.Milla, R. Crop Origins and Phylo Food: a database and a phylogenetic tree to stimulate comparative analyses on the origins of food crops. Glob. Ecol. Biogeogr. 29, 606–614 (2020).Article 

    Google Scholar 
    32.Hoelzel, A. R., Bruford, M. W. & Fleischer, R. C. Conservation of adaptive potential and functional diversity. Conserv. Genet. 20, 1–5 (2019).Article 

    Google Scholar 
    33.Tamburini, G. et al. Agricultural diversification promotes multiple ecosystem services without compromising yield. Sci. Adv. 6, eaba1715 (2020).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    34.Garibaldi, L. A. et al. Working landscapes need at least 20% native habitat. Conserv. Lett. 14, e12773 (2020).
    Google Scholar 
    35.Shackelford, G. et al. Comparison of pollinators and natural enemies: a meta-analysis of landscape and local effects on abundance and richness in crops. Biol. Rev. 88, 1002–1021 (2013).PubMed 
    Article 

    Google Scholar 
    36.Tuck, S. L. et al. Land-use intensity and the effects of organic farming on biodiversity: a hierarchical meta-analysis. J. Appl. Ecol. 51, 746–755 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    37.Rader, R. et al. Organic farming and heterogeneous landscapes positively affect different measures of plant diversity. J. Appl. Ecol. 51, 1544–1553 (2014).Article 

    Google Scholar 
    38.Palm, C., Blanco-Canqui, H., DeClerck, F., Gatere, L. & Grace, P. Conservation agriculture and ecosystem services: an overview. Agric. Ecosyst. Environ. 187, 87–105 (2014).Article 

    Google Scholar 
    39.Altieri, M. A. & Nicholls, C. I. Agroecology and the emergence of a post COVID-19 agriculture. Agric. Human Values 37, 525–526 (2020).Article 

    Google Scholar 
    40.Gemmill-Herren, B. Closing the circle: an agroecological response to COVID-19. Agric. Human Values 37, 613–614 (2020).Article 

    Google Scholar 
    41.Tester, M. & Langridge, P. Breeding technologies to increase crop production in a changing world. Science 327, 818–822 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    42.Swaminathan, M. S. in In Search of Biohappiness: Biodiversity and Food, Health and Livelihood Security (eds Sardar, D. & Yun, A.) Ch. 9 (World Scientific, 2015).43.Brown, C., Alexander, P., Arneth, A., Holman, I. & Rounsevell, M. Achievement of Paris climate goals unlikely due to time lags in the land system. Nat. Clim. Change 9, 203–208 (2019).ADS 
    Article 

    Google Scholar 
    44.Love, B. & Spaner, D. Agrobiodiversity: its value, measurement, and conservation in the context of sustainable agriculture. J. Sustain. Agric. 31, 53–82 (2007).Article 

    Google Scholar 
    45.Zimmerer, K. S. et al. The biodiversity of food and agriculture (agrobiodiversity) in the Anthropocene: research advances and conceptual framework. Anthropocene 25, 100192 (2019).Article 

    Google Scholar 
    46.Béné, C. et al. Global map and indicators of food system sustainability. Sci. Data 6, 279 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    47.Béné, C. et al. Global drivers of food system (un)sustainability: a multi-country correlation analysis. PLoS ONE 15, e0231071 (2020).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    48.Hickey, G. M., Pouliot, M., Smith-Hall, C., Wunder, S. & Nielsen, M. R. Quantifying the economic contribution of wild food harvests to rural livelihoods: a global-comparative analysis. Food Policy 62, 122–132 (2016).Article 

    Google Scholar 
    49.Mainstreaming Agrobiodiversity in Sustainable Food Systems: Scientific Foundations for an Agrobiodiversity Index (Bioversity International, 2017).50.The Agrobiodiversity Index Methodology Report Version 1.0 (Bioversity International, 2018).51.Guidelines for the Preparation of the Country Reports for the State of the World’s Biodiversity for Food and Agriculture (SOWBFA) (FAO, 2013); https://doi.org/10.5812/jjm.3480452.Juventia, S. D. et al. Text mining national commitments towards agrobiodiversity conservation and use. Sustainability 12, 715 (2020).Article 

    Google Scholar 
    53.Singh, R. K., Murty, H. R., Gupta, S. K. & Dikshit, A. K. An overview of sustainability assessment methodologies. Ecol. Indic. 9, 189–212 (2009).Article 

    Google Scholar 
    54.Gan, X. et al. When to use what: methods for weighting and aggregating sustainability indicators. Ecol. Indic. 81, 491–502 (2017).Article 

    Google Scholar 
    55.Gómez-Limón, J. A. & Sanchez-Fernandez, G. Empirical evaluation of agricultural sustainability using composite indicators. Ecol. Econ. 69, 1062–1075 (2010).Article 

    Google Scholar 
    56.Nardo, M., Saisana, M., Saltelli, A. & Tarantola, S. Tools for Composite Indicators Building (Joint Research Centre of the European Commission, 2005).57.Wilson, M. C. & Wu, J. The problems of weak sustainability and associated indicators. Int. J. Sustain. Dev. World Ecol. 24, 44–51 (2017).Article 

    Google Scholar 
    58.Blaser, W. J. et al. Climate-smart sustainable agriculture in low-to-intermediate shade agroforests. Nat. Sustain. 1, 234–239 (2018).Article 

    Google Scholar 
    59.Standard Country or Area Codes for Statistical Use (M49) (United Nations Statistics Division, 2012); https://unstats.un.org/unsd/methodology/m49/60.De Mendiburu, F. Una Herramienta de Analisis Estadistico para la Investigacion Agricola (Universidad Nacional de Ingenieria (UNI-PERU), 2009).61.Dinno, A. dunn.test: Dunn’s test of multiple comparisons using rank sums. R package v.1.3.4 (CRAN, 2017).62.Warner, R. M. Applied Statistics: From Bivariate Through Multivariate Techniques (SAGE, 2008).63.R Core Team R: A language and environment for statistical computing (R Foundation for Statistical Computing, 2018); https://www.r-project.org/64.Jones, S. K. et al. Agrobiodiversity Index Scores for 80+ Countries (Harvard Dataverse, 2020); https://doi.org/10.7910/DVN/SKZSQD65.Kennedy, G. et al. in Mainstreaming Agrobiodiversity in Sustainable Food Systems: Scientific Foundations for an Agrobiodiversity Index (ed Bailey, A.) 23–52 (Bioversity International, 2017).66.Minimum Dietary Diversity for Women: A Guide for Measurement (FAO, FHI, 2016).67.Ojiewo, C., Tenkouano, C., Hughes, J. & Keatinge, J. D. H. in Diversifying Food and Diets: Using Agricultural Biodiversity to Improve Nutrition and Health (eds Fanzo, J. et al.) 291–302 (Routledge, 2013).68.Snyder, L. D., Gómez, M. I. & Power, A. G. Crop varietal mixtures as a strategy to support insect pest control, yield, economic, and nutritional services. Front. Sustain. Food Syst. 4, 60 (2020).Article 

    Google Scholar 
    69.Maureaud, A. et al. Biodiversity–ecosystem functioning relationships in fish communities: biomass is related to evenness and the environment, not to species richness. Proc. R. Soc. B 286, 20191189 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    70.Wang, L. et al. Diversifying livestock promotes multidiversity and multifunctionality in managed grasslands. Proc. Natl Acad. Sci. USA 116, 6187–6192 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Khumairoh, U., Lantinga, E. A., Schulte, R. P. O., Suprayogo, D. & Groot, J. C. J. Complex rice systems to improve rice yield and yield stability in the face of variable weather conditions. Sci. Rep. 8, 14746 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    72.Lavorel, S. Plant functional effects on ecosystem services. J. Ecol. 101, 4–8 (2013).Article 

    Google Scholar 
    73.Wood, S. A. et al. Functional traits in agriculture: agrobiodiversity and ecosystem services. Trends Ecol. Evol. 30, 531–539 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    74.Martin, A. R. & Isaac, M. E. Functional traits in agroecology: advancing description and prediction in agroecosystems. J. Appl. Ecol. 55, 5–11 (2018).Article 

    Google Scholar 
    75.Stark, J. C. & Thornton, M. in Potato Production Systems (eds Stark, J. et al.) 87–100 (Springer International, 2020).76.Taylor, M., Jaenicke, H., Hunter, D., McGregor, A. & Lyon, G. Diversity for sustaining livelihoods: examples, constraints and lessons learnt. Acta Hortic. 1101, 105–112 (2015).Article 

    Google Scholar 
    77.Mulumba, J. W. et al. A risk-minimizing argument for traditional crop varietal diversity use to reduce pest and disease damage in agricultural ecosystems of Uganda. Agric. Ecosyst. Environ. 157, 70–86 (2012).Article 

    Google Scholar 
    78.Bartomeus, I. et al. Contribution of insect pollinators to crop yield and quality varies with agricultural intensification. PeerJ 2014, e328 (2014).Article 

    Google Scholar 
    79.Fahrig, L. et al. Farmlands with smaller crop fields have higher within-field biodiversity. Agric. Ecosyst. Environ. 200, 219–234 (2015).Article 

    Google Scholar 
    80.Maxted, N., Dulloo, M. E. & Ford Lloyd, B. Enhancing Crop Genepool Use: Capturing Wild Relative and Landrace Diversity for Crop Improvement (CABI, 2016).81.Li, Y. et al. Investigating drought tolerance in chickpea using genome-wide association mapping and genomic selection based on whole-genome resequencing data. Front. Plant Sci. 9, 190 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    82.Hunter, D. et al. The potential of neglected and underutilized species for improving diets and nutrition. Planta 250, 709–729 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar  More