More stories

  • in

    Cumulative effects of human footprint, natural features and predation risk best predict seasonal resource selection by white-tailed deer

    1.Eisner, R., Seabrook, L. M. & McAlpine, C. A. Are changes in global oil production influencing the rate of deforestation and biodiversity loss?. Biol. Conserv. 196, 147–155. https://doi.org/10.1016/j.biocon.2016.02.017 (2016).Article 

    Google Scholar 
    2.Fahrig, L. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. Syst. 34, 487–515. https://doi.org/10.1146/132419 (2003).Article 

    Google Scholar 
    3.Pfeifer, M. et al. Creation of forest edges has a global impact on forest vertebrates. Nature 551, 187–191. https://doi.org/10.1038/nature24457 (2017).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    4.Tilman, D., May, R., Lehman, C. & Nowak, M. Habitat destruction and the extinction debt. Nature 371, 65–66. https://doi.org/10.1038/371065a0 (1994).ADS 
    Article 

    Google Scholar 
    5.Fisher, J. T. & Burton, C. A. Wildlife winners and losers in an oil sands landscape. Front Ecol. Environ. https://doi.org/10.1002/fee.1807 (2018).Article 

    Google Scholar 
    6.Heim, N., Fisher, J. T., Volpe, J., Clevenger, A. P. & Paczkowski, J. Carnivore community response to anthropogenic landscape change: species-specificity foils generalizations. Landscape Ecol. 34, 2493–2507. https://doi.org/10.1007/s10980-019-00882-z (2019).Article 

    Google Scholar 
    7.Pereira, H. M., Navarro, L. & Martins, I. Global biodiversity change: the bad, the good, and the unknown. Annu. Rev. Environ. Resour. https://doi.org/10.1146/annurev-environ-042911-093511 (2012).Article 

    Google Scholar 
    8.Northrup, J. M., Anderson, C. R. Jr. & Wittemyer, G. Quantifying spatial habitat loss from hydrocarbon development through assessing habitat selection patterns of mule deer. Glob Change Biol. 21, 3961–3970. https://doi.org/10.1111/gcb.13037 (2015).ADS 
    Article 

    Google Scholar 
    9.Holbrook, S. J. & Schmitt, R. J. The combined effects of predation risk and food reward on patch selection. Ecology 69, 125–134. https://doi.org/10.2307/1943167 (1988).Article 

    Google Scholar 
    10.Moody, A. L., Houston, A. I. & McNamara, J. M. Ideal free distributions under predation risk. Behav. Ecol. Sociobiol. 38, 131–143 (1996).Article 

    Google Scholar 
    11.Dietz, H. & Edwards, P. J. Recognition that causal processes change during plant invasion helps explain conflicts in evidence. Ecology 87, 1359–1367 (2006).Article 

    Google Scholar 
    12.Hobbs, R. J. & Huenneke, L. F. Disturbance, diversity, and invasion: implications for conservation. Conserv. Biol. 6, 324–337 (1992).Article 

    Google Scholar 
    13.Van der Graaf, S., Stahl, J., Klimkowska, A. & Drent, J. P. B. Surfing on a green wave—How plant growth drives spring migration in the Barnacle Goose Branta leucopsis. Ardea -Wageningen- 94, 567 (2006).
    Google Scholar 
    14.Parker, I. M. et al. Impact: toward a framework for understanding the ecological effects of invaders. Biol. Invasions 1, 3–19. https://doi.org/10.1023/A:1010034312781 (1999).Article 

    Google Scholar 
    15.Pimentel, D., Zuniga, R. & Morrison, D. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol. Econ. 52, 273–288. https://doi.org/10.1016/j.ecolecon.2004.10.002 (2005).Article 

    Google Scholar 
    16.Shackelford, N. et al. Primed for change: developing ecological restoration for the 21st Century. Restor. Ecol. 21, 297–304. https://doi.org/10.1111/rec.12012 (2013).Article 

    Google Scholar 
    17.Pickell, P. D., Pickell, P. D., Andison, D. W., Coops, N. C. & Gergel, S. E. The spatial patterns of anthropogenic disturbance in the western Canadian boreal forest following oil and gas development. Can. J. For. Res. 45, 732–743. https://doi.org/10.1139/cjfr-2014-0546 (2015).Article 

    Google Scholar 
    18.Fisher, J. T. & Wilkinson, L. The response of mammals to forest fire and timber harvest in the North American boreal forest. Mammal Rev. 35, 51–81 (2005).Article 

    Google Scholar 
    19.Wittische, J., Heckbert, S., James, P. M. A., Burton, A. C. & Fisher, J. T. Community-level modelling of boreal forest mammal distribution in an oil sands landscape. Sci. Total Environ. 755, 142500. https://doi.org/10.1016/j.scitotenv.2020.142500 (2021).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    20.Hewitt, D. G. Biology and management of white-tailed deer (CRC Press, Boca Raton, 2011).Book 

    Google Scholar 
    21.McCabe, R. E. & McCabe, T. R. in White tailed deer: ecology and management Ch. Chapter 2, 19–72 (Stackpole, A Wildlife Management Institute Book, 1984).22.Webb, R. The range of white-tailed deer in Alberta (Alberta Fish and Wildlife Division Edmonton, Alberta, 1967).
    Google Scholar 
    23.Dawe, K. L. & Boutin, S. Climate change is the primary driver of white-tailed deer (Odocoileus virginianus) range expansion at the northern extent of its range; land use is secondary. Ecol. Evol. 6, 6435–6451. https://doi.org/10.1002/ece3.2316 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    24.DeCesare, N. J., Hebblewhite, M., Robinson, H. S. & Musiani, M. Endangered, apparently: the role of apparent competition in endangered species conservation. Anim. Conserv. 13, 353–362. https://doi.org/10.1111/j.1469-1795.2009.00328.x (2010).Article 

    Google Scholar 
    25.Latham, A. D. M., Latham, M. C., McCutchen, N. A. & Boutin, S. Invading white-tailed deer change wolf-caribou dynamics in northeastern Alberta. J. Wildl. Manag. 75, 204–212. https://doi.org/10.1002/jwmg.28 (2011).Article 

    Google Scholar 
    26.Latham, A. D. M., Latham, M. C., Boyce, M. C. & Boutin, S. Movement responses by wolves to industrial linear features and their effect on woodland caribou in northeastern Alberta. Ecol. Appl. 21, 11 (2011).Article 

    Google Scholar 
    27.Fisher, J. T., Burton, A. C., Nolan, L. & Roy, L. Influences of landscape change and winter severity on invasive ungulate persistence in the Nearctic boreal forest. Sci. Rep. 10, 8742. https://doi.org/10.1038/s41598-020-65385-3 (2020).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    28.Dabros, A., Pyper, M. & Castilla, G. Seismic lines in the boreal and arctic ecosystems of North America: environmental impacts, challenges, and opportunities. Environ. Rev. 26, 214–229. https://doi.org/10.1139/er-2017-0080 (2018).Article 

    Google Scholar 
    29.Dickie, M., Serrouya, R., McNay, R. S., Boutin, S. & du Toit, J. Faster and farther: wolf movement on linear features and implications for hunting behaviour. J. Appl. Ecol. 54, 253–263. https://doi.org/10.1111/1365-2664.12732 (2017).Article 

    Google Scholar 
    30.Finnegan, L., MacNearney, D. & Pigeon, K. E. Divergent patterns of understory forage growth after seismic line exploration: implications for caribou habitat restoration. For. Ecol. Manag. 409, 634–652. https://doi.org/10.1016/j.foreco.2017.12.010 (2018).Article 

    Google Scholar 
    31.Prokopenko, C. M., Boyce, M. S., Avgar, T. & Tulloch, A. Characterizing wildlife behavioural responses to roads using integrated step selection analysis. J. Appl. Ecol. 54, 470–479. https://doi.org/10.1111/1365-2664.12768 (2017).Article 

    Google Scholar 
    32.Waring, G. H., Griffis, J. L. & Vaughn, M. E. White-tailed deer roadside behavior, wildlife warning reflectors, and highway mortality. Appl. Anim. Behav. Sci. 29, 215–223. https://doi.org/10.1016/0168-1591(91)90249-W (1991).Article 

    Google Scholar 
    33.Bowman, J., Ray, J. C., Magoun, A. J., Johnson, D. S. & Dawson, F. N. Roads, logging, and the large-mammal community of an eastern Canadian boreal forest. Can. J. Zool. 88, 454–467. https://doi.org/10.1139/z10-019 (2010).Article 

    Google Scholar 
    34.Munro, K. G., Bowman, J. & Fahrig, L. Effect of paved road density on abundance of white-tailed deer. Wildl. Res. 39, 478. https://doi.org/10.1071/wr11152 (2012).Article 

    Google Scholar 
    35.Fisher, J. T. & Burton, A. C. Spatial structure of reproductive success infers mechanisms of ungulate invasion in Nearctic boreal landscapes. Ecol. Evol. 11, 900–911. https://doi.org/10.1002/ece3.7103 (2021).Article 
    PubMed 

    Google Scholar 
    36.Kie, J. G. Optimal foraging and risk of predation effects on behavior and social structure in ungulates. J. Mammal. 80, 1114–1129 (1999).Article 

    Google Scholar 
    37.Brown, J. S., Laundré, J. W. & Gurung, M. The ecology of fear: optimal foraging, game theory, and trophic interactions. J. Mammal. 80, 385–399. https://doi.org/10.2307/1383287 (1999).Article 

    Google Scholar 
    38.Kittle, A. M., Fryxell, J. M., Desy, G. E. & Hamr, J. The scale-dependent impact of wolf predation risk on resource selection by three sympatric ungulates. Oecologia 157, 163–175. https://doi.org/10.1007/s00442-008-1051-9 (2008).ADS 
    Article 
    PubMed 

    Google Scholar 
    39.Moen, A. N. Energy conservation by white-tailed deer in the winter. Ecology 57, 192–198. https://doi.org/10.2307/1936411 (1976).Article 

    Google Scholar 
    40.Schmidt, K. Winter ecology of nonmigratory Alpine red deer. Oecologia 95, 226–233. https://doi.org/10.1007/BF00323494 (1993).ADS 
    Article 
    PubMed 

    Google Scholar 
    41.Kilgo, J. C., Ray, H. S., Vukovich, M., Goode, M. J. & Ruth, C. Predation by coyotes on white-tailed deer neonates in South Carolina. J. Wildl. Manag. https://doi.org/10.1002/jwmg.393 (2012).Article 

    Google Scholar 
    42.Laurent, M., Dickie, M., Becker, M., Serrouya, R. & Boutin, S. Evaluating the mechanisms of landscape change on white-tailed deer populations. J. Wildl. Manag. 85, 340–353. https://doi.org/10.1002/jwmg.21979 (2020).Article 

    Google Scholar 
    43.Schneider, R. R., Hauer, G., Adamowicz, W. L. & Boutin, S. Triage for conserving populations of threatened species: the case of woodland caribou in Alberta. Biol. Conserv. 143, 1603–1611. https://doi.org/10.1016/j.biocon.2010.04.002 (2010).Article 

    Google Scholar 
    44.Kilkenny, C., Browne Wj Fau – Cuthill, I. C., Cuthill Ic Fau – Emerson, M., Emerson M Fau – Altman, D. G. & Altman, D. G. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS biol. 8(6), e1000412 (2010).45.DelGiudice, G. D., Mangipane, B. A., Sampson, B. A. & Kochanny, C. O. Chemical immobilization, body temperature, and post-release mortality of white-tailed deer captured by clover trap and net-gun. Wildl. Soc. Bull. (1973-2006) 29, 1147–1157 (2001).
    Google Scholar 
    46.Droge, E., Creel, S., Becker, M. S. & M’Soka, J. Risky times and risky places interact to affect prey behaviour. Nat. Ecol. Evol. 1, 1123–1128. https://doi.org/10.1038/s41559-017-0220-9 (2017).Article 
    PubMed 

    Google Scholar 
    47.Kunkel, K. E. & Mech, L. D. Wolf and bear predation on white-tailed deer fawns in northeastern Minnesota. Can. J. Zool. 72, 1557–1565 (1994).Article 

    Google Scholar 
    48.Latham, A., Latham, M., Knopff, K., Hebblewhite, M. & Boutin, S. Wolves, white-tailed deer, and beaver: Implications of seasonal prey switching for woodland caribou declines. Ecography https://doi.org/10.1111/j.1600-0587.2013.00035.x (2013).Article 

    Google Scholar 
    49.Alberta Environment and Sustainable Resource Development. Alberta Vegetation Index. Accessed October 2016. https://geodiscover.alberta.ca/50.Manly, B., McDonald, L., Thomas, D., McDonald, T. & Erickson, W.Resource selection by animals: statistical design and analysis for field studies. Vol. 63, pp. 1-10 (Springer Science & Business Media, 2007).51.Boyce, M. S., Vernier, P. R., Nielsen, S. E. & Schmiegelow, F. K. A. Evaluating resource selection functions. Ecol. Model. 157, 281–300. https://doi.org/10.1016/S0304-3800(02)00200-4 (2002).Article 

    Google Scholar 
    52.Hijmans, R. & van Etten, J. Raster: Geographic data analysis and modeling. CRAN R package 2 (2016).53.R: A language and environment for statistical computing. (Vienna, Austria, 2013).54.Zuur, A., Hilbe, J. & Ieno, E. A Beginner’s Guide to GLM and GLMM with R: a frequentist and Bayesian perspective for ecologists. (Highland Statistics, 2013).55.Gillies, C. S. et al. Application of random effects to the study of resource selection by animals. J. Anim. Ecol. 75, 887–898. https://doi.org/10.1111/j.1365-2656.2006.01106.x (2006).Article 
    PubMed 

    Google Scholar 
    56.Craney, T. A. & Surles, J. G. Model-dependent variance inflation factor cutoff values. Qual. Eng. 14, 391–403. https://doi.org/10.1081/QEN-120001878 (2002).Article 

    Google Scholar 
    57.Akaike, H. Information theory and an extension of the maximum likelihood principle. Selected papers of hirotugu akaike 199–213 (Springer, New York, 1998).Book 

    Google Scholar 
    58.Burnham, K. P. & Anderson, D. R. Multimodel inference: understanding AIC and BIC in model selection. Sociol. Methods Res. 33, 261–304. https://doi.org/10.1177/0049124104268644 (2004).MathSciNet 
    Article 

    Google Scholar 
    59.Boulanger, Y. et al. Climate change impacts on forest landscapes along the Canadian southern boreal forest transition zone. Landscape Ecol. 32, 1415–1431. https://doi.org/10.1007/s10980-016-0421-7 (2017).Article 

    Google Scholar 
    60.Sulla-Menashe, D., Woodcock, C. E. & Friedl, M. A. Canadian boreal forest greening and browning trends: an analysis of biogeographic patterns and the relative roles of disturbance versus climate drivers. Environ. Res. Lett. 13, 014007. https://doi.org/10.1088/1748-9326/aa9b88 (2018).ADS 
    Article 

    Google Scholar 
    61.St-Pierre, F., Drapeau, P. & St-Laurent, M.-H. Drivers of vegetation regrowth on logging roads in the boreal forest: Implications for restoration of woodland caribou habitat. For. Ecol. Manag. 482, 118846. https://doi.org/10.1016/j.foreco.2020.118846 (2021).Article 

    Google Scholar 
    62.Berger, J. Fear, human shields and the redistribution of prey and predators in protected areas. Biol. Let. 3, 620–623. https://doi.org/10.1098/rsbl.2007.0415 (2007).Article 

    Google Scholar 
    63.Heyes, A., Leach, A. & Mason, C. F. The economics of Canadian oil sands. Rev. Environ. Econ. Policy 12, 242–263. https://doi.org/10.1093/reep/rey006 (2018).Article 

    Google Scholar 
    64.Komers, P. E. & Stanojevic, Z. Rates of disturbance vary by data resolution: implications for conservation schedules using the Alberta boreal forest as a case study. Global Change Biol. 19, 2916–2928 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    65.Hebblewhite, M. & Merrill, E. H. Trade-offs between predation risk and forage differ between migrant strategies in a migratory ungulate. Ecology 90, 3445–3454. https://doi.org/10.1890/08-2090.1 (2009).Article 
    PubMed 

    Google Scholar 
    66.Mech, D. L. & Boitani, L. Wolves: behavior, ecology, and conservation Vol. 57 (University of Chicago Press, Chicago, 2004).
    Google Scholar 
    67.Creel, S., Winnie, J. A., Christianson, D. & Liley, S. Time and space in general models of antipredator response: tests with wolves and elk. Anim. Behav. 76, 1139–1146. https://doi.org/10.1016/j.anbehav.2008.07.006 (2008).Article 

    Google Scholar 
    68.Steenweg, R. et al. Scaling-up camera traps: monitoring the planet’s biodiversity with networks of remote sensors. Front. Ecol. Environ. 15, 26–34. https://doi.org/10.1002/fee.1448 (2017).Article 

    Google Scholar 
    69.Hebblewhite, M. Billion dollar boreal woodland caribou and the biodiversity impacts of the global oil and gas industry. Biol. Cons. 206, 102–111. https://doi.org/10.1016/j.biocon.2016.12.014 (2017).Article 

    Google Scholar 
    70.Côté, S. D., Rooney, T. P., Tremblay, J.-P., Dussault, C. & Waller, D. M. Ecological impacts of deer overabundance. Annu. Rev. Ecol. Evol. Syst. 35, 113–147 (2004).Article 

    Google Scholar 
    71.McCullough, D. R. Evaluation of night spotlighting as a deer study technique. J. Wildl. Manag. 46, 963–973. https://doi.org/10.2307/3808229 (1982).Article 

    Google Scholar 
    72.Preston, T., Wildhaber, M., Green, N., Albers, J. & Debenedetto, G. Enumerating white-tailed deer using unmanned aerial vehicles. Wildlife Soc. Bull. https://doi.org/10.1002/wsb.1149 (2021).Article 

    Google Scholar 
    73.Parks, A. E. Provincial woodland caribou range plan. 212 (Edmonton, Alberta, 2017).74.Tattersall, E. R., Burgar, J. M., Fisher, J. T. & Burton, A. C. Boreal predator co-occurrences reveal shared use of seismic lines in a working landscape. Ecol. Evol. 10, 1678–1691. https://doi.org/10.1002/ece3.6028 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    75.Diaz, S. et al. Pervasive human-driven decline of life on Earth points to the need for transformative change. Science (New York N.Y.) https://doi.org/10.1126/science.aax3100 (2019).Article 
    PubMed Central 

    Google Scholar 
    76.Bayoumi, T. & Muhleisen, M. Energy, the exchange rate, and the economy: macroeconomic benefits of Canada’s oil sands production (International Monetary Fund, Washington, 2006).
    Google Scholar 
    77.Zhu, K., Song, Y. & Qin, C. Forest age improves understanding of the global carbon sink. Proc. Natl. Acad. Sci. 116, 3962. https://doi.org/10.1073/pnas.1900797116 (2019).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    Effects of Chinese medicine herbal residues on antibiotic resistance genes and the bacterial community in chicken manure composting

    1.Zhang QQ, Ying GG, Pan CG, Liu YS, Zhao JL. Comprehensive evaluation of antibiotics emission and fate in the river basins of China: source analysis, multimedia modeling, and linkage to bacterial rResistance. Environ Sci Technol. 2015;49:6772–82.CAS 
    Article 

    Google Scholar 
    2.Zhao WX, Wang B, Yu G. Antibiotic resistance genes in China: occurrence, risk, and correlation among different parameters. Environ Sci Pollut R. 2018;25:21467–82.CAS 
    Article 

    Google Scholar 
    3.Han XM, Hu HW, Chen QL, Yang LY, Li HL, Zhu YG, et al. Antibiotic resistance genes and associated bacterial communities in agricultural soils amended with different sources of animal manures. Soil Biol Biochem. 2018;126:91–102.CAS 
    Article 

    Google Scholar 
    4.Huerta B, Marti E, Gros M, López P, Pompêo M, Armengol J, et al. Exploring the links between antibiotic occurrence, antibiotic resistance, and bacterial communities in water supply reservoirs. Sci Total Environ. 2013;456:161–70.Article 

    Google Scholar 
    5.Martinez JL, Sánchez MB, Martínez-Solano L, Hernandez A, Garmendia L, Fajardo A, et al. Functional role of bacterial multidrug efflux pumps in microbial natural ecosystems. Fems Microbiol Rev. 2009;33:430–49.CAS 
    Article 

    Google Scholar 
    6.Wright GD. The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol. 2007;5:175–86.CAS 
    Article 

    Google Scholar 
    7.Meng F, Yang S, Wang X, Chen T, Wang X, Tang X, et al. Reclamation of Chinese herb residues using probiotics and evaluation of their beneficial effect on pathogen infection. J Infect Public Health. 2017;10:749–54.Article 

    Google Scholar 
    8.Zhou Y, Selvam A, Wong JWC. Chinese medicinal herbal residues as a bulking agent for food waste composting. Bioresour Technol. 2018;249:182–8.CAS 
    Article 

    Google Scholar 
    9.Wu HW, Sun XQ, Liang BW, Chen JB, Zhou XF. Analysis of livestock and poultry manure pollution in China and its treatment and resource utilization. J Agro-Environ Sci. 2020;39:1168–76.
    Google Scholar 
    10.Chen J, Yu Z, Michel FC Jr., Wittum T, Morrison M. Development and application of real-time PCR assays for quantification of erm genes conferring resistance to macrolides-lincosamides-streptogramin B in livestock manure and manure management systems. Appl Environ Microbiol. 2007;73:4407–16.CAS 
    Article 

    Google Scholar 
    11.Duan M, Gu J, Wang X, Li Y, Zhang S, Yin Y, et al. Effects of genetically modified cotton stalks on antibiotic resistance genes, intI1, and intI2 during pig manure composting. Ecotoxicol Environ Saf. 2018;147:637–42.CAS 
    Article 

    Google Scholar 
    12.Cui E, Wu Y, Zuo Y, Chen H. Effect of different biochars on antibiotic resistance genes and bacterial community during chicken manure composting. Bioresour Technol. 2016;203:11–7.CAS 
    Article 

    Google Scholar 
    13.Ma Y, Wilson CA, Novak JT, Riffat R, Aynur S, Murthy S, Pruden A. Effect of various sludge digestion conditions on sulfonamide, macrolide, and tetracycline Resistance Genes and Class I Integrons. Environ Sci Technol. 2011;45:7855–61.CAS 
    Article 

    Google Scholar 
    14.Tien YC, Li B, Zhang T, Scott A, Murray R, Sabourin L, et al. Impact of dairy manure pre-application treatment on manure composition, soil dynamics of antibiotic resistance genes, and abundance of antibiotic-resistance genes on vegetables at harvest. Sci Total Environ. 2017;581-582:32–9.CAS 
    Article 

    Google Scholar 
    15.Zhang L, Sun XY. Effects of waste lime and Chinese medicinal herbal residue amendments on physical, chemical, and microbial properties during green waste composting. Environ Sci Pollut Res. Int. 2018;25:31381–95.CAS 
    Article 

    Google Scholar 
    16.Wang YQ, Wu XQ, Zhu TT, Ma QG, Chen HG. Study on utilization of solid slag compost of Chinese medicinal herbal. J Chin Medicinal Mater. 2008;31:1622–4.CAS 

    Google Scholar 
    17.Wu DL, Liu P, Luo YZ, Tian GM, Mahmood Q. Nitrogen transformations during co-composting of herbal residues, spent mushrooms, and sludge. J Zhejiang Univ Sci B. 2010;11:497–505.Article 

    Google Scholar 
    18.Ward T, Larson J, Meulemans J, Hillmann B, Lynch J, Sidiropoulos D, et al. BugBase predicts organism-level microbiome phenotypes. bioRxiv. 2017;133462.19.Chao A. Nonparametric estimation of the number of classes in a population. Scand J Stat. 1984;11:265–70.
    Google Scholar 
    20.Chao A, Yang MCK. Stopping rules and estimation for recapture debugging with unequal failure rates. Biometrika. 1993;80:193–201.Article 

    Google Scholar 
    21.Shannon CE. A mathematical theory of communication. Bell Syst Tech J. 1948;27:623–56.Article 

    Google Scholar 
    22.Simpson EH. Measurement of diversity. Nature 1949;163:688.Article 

    Google Scholar 
    23.Huang K, Xia H, Wu Y, Chen J, Cui G, Li F, et al. Effects of earthworms on the fate of tetracycline and fluoroquinolone resistance genes of sewage sludge during vermicomposting. Bioresour Technol. 2018;259:32–9.CAS 
    Article 

    Google Scholar 
    24.Qian X, Sun W, Gu J, Wang XJ, Sun JJ, Yin YN, et al. Variable effects of oxytetracycline on antibiotic resistance gene abundance and the bacterial community during aerobic composting of cow manure. J Hazard Mater. 2016;315:61–9.CAS 
    Article 

    Google Scholar 
    25.Zhang R, Gu J, Wang X, Li Y, Zhang K, Yin Y, Zhang X. Contributions of the microbial community and environmental variables to antibiotic resistance genes during co-composting with swine manure and cotton stalks. J Hazard Mater. 2018;358:82–91.CAS 
    Article 

    Google Scholar 
    26.Wang H, Sangwan N, Li HY, Su JQ, Oyang WY, Zhang ZJ, et al. The antibiotic resistome of swine manure is significantly altered by association with the Musca domestica larvae gut microbiome. Isme J. 2017;11:100–11.Article 

    Google Scholar 
    27.Li J, Xin Z, Zhang Y, Chen J, Yan J, Li H, Hu H. Long-term manure application increased the levels of antibiotics and antibiotic resistance genes in a greenhouse soil. Appl Soil Ecol. 2017;121:193–200.Article 

    Google Scholar 
    28.Su JQ, Wei B, Ou-Yang WY, Huang FY, Zhao Y, Xu HJ, et al. Antibiotic resistome and its association with bacterial communities during sewage sludge composting. Environ Sci Technol. 2015;49:7356–63.CAS 
    Article 

    Google Scholar 
    29.Li H, Duan M, Gu J, Zhang Y, Qian X, Ma J, et al. Effects of bamboo charcoal on antibiotic resistance genes during chicken manure composting. Ecotoxicol Environ Saf. 2017;140:1–6.Article 

    Google Scholar 
    30.Zhang J, Lin H, Ma J, Sun W, Yang Y, Zhang X. Compost-bulking agents reduce the reservoir of antibiotics and antibiotic resistance genes in manures by modifying bacterial microbiota. Sci Total Environ. 2019;649:396–404.CAS 
    Article 

    Google Scholar 
    31.Ghosh S, Ramsden SJ, LaPara TM. The role of anaerobic digestion in controlling the release of tetracycline resistance genes and class 1 integrons from municipal wastewater treatment plants. Appl Microbiol Biotechnol. 2009;84:791–6.CAS 
    Article 

    Google Scholar 
    32.Selvam A, Xu D, Zhao Z, Wong JW. Fate of tetracycline, sulfonamide and fluoroquinolone resistance genes and the changes in bacterial diversity during composting of swine manure. Bioresour Technol. 2012;126:383–90.CAS 
    Article 

    Google Scholar 
    33.Antunes P, Machado J, Sousa JC, Peixe L. Dissemination of sulfonamide resistance genes (sul1, sul2, and sul3) in Portuguese Salmonella enterica strains and relation with integrons. Antimicrob Agents Chemother. 2005;49:836–9.CAS 
    Article 

    Google Scholar 
    34.Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, Stedtfeld RD, et al. Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci USA. 2013;110:3435–40.CAS 
    Article 

    Google Scholar 
    35.Chen Q, An X, Li H, Su J, Ma Y, Zhu YG. Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil. Environ Int. 2016;92-93:1–10.CAS 
    Article 

    Google Scholar  More

  • in

    A global coral-bleaching database, 1980–2020

    The GCBD is stored at figshare23. Below we describe 20 Tables (also see Fig. 3 schematic) that comprise the GCBD: (1) Site_Info_tbl, (2) Sample_Event_tbl, (3) R_Scripts_tbl, (4) Cover_tbl, (5) Bleaching_tbl, (6) Environmental_tbl, (7) Authors_LUT, (8) Bleaching_Level_LUT, (9) City_Town_Name_LUT, (10) Country_Name_LUT, (11) Data_Source_LUT, (12) Ecoregion_Name_LUT, (13) Exposure_LUT, (14) Ocean_Name_LUT, (15) Realm_Name_LUT, (16) State_Island_Province_Name_LUT, (17) Substrate_Type_LUT, (18) Relevant_Papers_tbl, (19) Severity_Code_LUT, and (20) Bleaching_Prevalence_Score_LUT, where LUT stands for look-up table.

    1)

    Site Information (Site_Info_tbl)
    Latitude_Degrees: latitude coordinates in decimal degrees.
    Longitude_Degrees: longitude coordinates in decimal degrees.
    Ocean_Name: the ocean in which the sampling took place.
    Realm_Name: identification of realm as defined by the Marine Ecoregions of the World (MEOW)12.
    Ecoregion_Name: identification of the Ecoregions (150) as defined by Veron et al.13.
    Country_Name: the country where sampling took place.
    State_Island_Province_Name: the state, territory (e.g., Guam) or island group (e.g., Hawaiian Islands) where sampling took place.
    City_Town_Name: the region, city, or nearest town, where sampling took place.
    Site_Name: the accepted name of the site or the name given by the team that sampled the reef.
    Distance_to_Shore: the distance (m) of the sampling site from the nearest land.
    Exposure: a site was considered exposed if it had >20 km of fetch, if there were strong seasonal winds, or if the site faced the prevailing winds. Otherwise, the site was considered sheltered or ‘sometimes’. ‘Sometimes’ refers to a few sites with a >20 km fetch through a narrow geographic window, and therefore we considered that the site was potentially exposed during cyclone seasons. We left the category ‘sometimes’ in the database because those sites were not clearly exposed sites, nor were they clearly sheltered sites, and future researchers may be interested in temporary exposure.
    Turbidity: kd490 with a 100-km buffer.
    Cyclone_Frequency: number of cyclone events from 1964 to 2014.
    Comments: comments of any issues with the site or additional information.

    2)

    Sample Event Information (Sample_Event_tbl)
    Site_ID: site ID field from Site_Info_tbl.
    Reef_ID: name of reef site that was adopted by sampling group (from ReefCheck).
    Quadrat_No: quadrat number (from McClanahan et al.)20.
    Date_Day: the date of the sampling event.
    Date_Month: the month of sampling event.
    Date_Year: the year of sampling event.
    Depth: depth (m) of sampling site. Comments: comments of any issue or additional information of sampling event.

    3)

    R Code (R_Scripts_tbl)
    Relevant_Papers_ID: relevant papers ID field from Relevant_Papers_tbl.
    Project name: name of project associated with R code.
    Paper_Title: title of paper where R code was published.
    Code_Name: name of R code file.
    Description: description of the R code.
    Data_Source: data source ID field from Data_Source_LUT.
    R_Code: attachment of R code file.
    URL: hyperlink to R code or link to github.

    4)

    Coral Cover Information (Cover_tbl)
    Sample_ID: sampled ID field from Sample_Event_tbl.
    Substrate_Type: substrate type ID field from Substrate_LUT.
    S1: Reef Check breaks down transects into four 20 m × 5 m segments, point data from segment one of transect.
    S2: Reef Check breaks down transects into four 20 m × 5 m segments, point data from segment two of transect.
    S3: Reef Check breaks down transects into four 20 m × 5 m segments, point data from segment three of transect.
    S4: Reef Check breaks down transects into four 20 m × 5 m segments, point data from segment four of transect.
    Perc_hardcoral: percent hard coral cover from McClanahan et al.20 data source.
    Perc_macroalgae: percent macroalgae cover from McClanahan et al.20 data source.
    Average_Ellipse_Transect: calculated percent hard coral cover per 10 m × 1 m transect using ellipse equation.
    Average_Ellipse_Site: calculated percent hard coral cover per site using ellipse equation.
    Comments: comments of any issue or additional information of sampling event

    5)

    Bleaching Information (Bleaching_tbl)
    Sample_ID: sample ID field from Sample_Event_tbl.
    Bleaching_Level: Reef Check data, coral population or coral colony.
    S1: Reef Check breaks down transects into four 20 m × 5 m segments, percent bleaching from segment one of transect.
    S2: Reef Check breaks down transects into four 20 m × 5 m segments, percent bleaching from segment two of transect.
    S3: Reef Check breaks down transects into four 20 m × 5 m segments, percent bleaching from segment three of transect.
    S4: Reef Check breaks down transects into four 20 m × 5 m segments, percent bleaching from segment four of transect.
    Percent_Bleaching_RC_Old_Method: old method of determining percent bleaching from Reef_Check.
    Severity_Code: coded range of bleaching severity from Donner et al.10.
    Percent_Bleached: percent of coral bleaching.
    Number_Bleached_colonies: number of bleached corals from McClanahan et al.20 data source.
    Bleaching_intensity: from McClanahan et al.20 data source.
    Bleaching_Prevalence_Score: coded range of bleaching prevalence from Safaie et al.21.

    6)

    Environmental Parameter Information (Environmental_tbl)
    Sample_ID: sample ID field from Sample_Event_tbl.
    ClimSST: CoRTAD. [Climatological Sea-Surface Temperature (SST)] based on weekly SSTs for the study time frame, created using a harmonics approach.
    Temperature_ Kelvin: CoRTAD. SST in Kelvin.
    Temperature_Mean: CoRTAD. Mean SST in degrees Celsius.
    Temperature_Minimum: CoRTAD. Minimum SST in degrees Celsius.
    Temperature_Maximum: CoRTAD. Maximum SST in degrees Celsius.
    Temperature_Kelvin_Standard_Deviation: CoRTAD. Standard deviation of SST in Kelvin.
    Windspeed: CoRTAD. meters per hour.
    SSTA: CoRTAD. (Sea-Surface Temperature Anomaly) weekly SST minus weekly climatological SST.
    SSTA_Standard_Deviation: CoRTAD. The Standard Deviation of weekly SSTA in degrees Celsius over the entire period.
    SSTA_Mean: CoRTAD. The mean SSTA in degrees Celsius over the entire period.
    SSTA_Minimum: CoRTAD. The minimum SSTA in degrees Celsius over the entire period.
    SSTA_Maximum: CoRTAD. The maximum SSTA in degrees Celsius over the entire period.
    SSTA_Frequency: CoRTAD. (Sea Surface Temperature Anomaly Frequency) number of times over the previous 52 weeks that SSTA  >  = 1 degree Celsius.
    SSTA_Frequency_Standard_Deviation: CoRTAD. The standard deviation of SSTA Frequency in degrees Celsius over the entire time period of 40 years.
    SSTA_FrequencyMax: CoRTAD. The maximum SSTA Frequency in degrees Celsius over the entire time period.
    SSTA_FrequencyMean: CoRTAD. The mean SSTA Frequency in degrees Celsius over the entire time period of 40 years.
    SSTA_DHW: CoRTAD. (Sea Surface Temperature Degree Heating Weeks) sum of previous 12 weeks when SSTA  >  = 1 degree Celsius.
    SSTA_DHW_Standard_Deviation: CoRTAD. The standard deviation SSTA DHW in degrees Celsius over the entire period.
    SSTA_DHWMax: CoRTAD. The maximum SSTA DHW in degrees Celsius over the entire time period of 40 years.
    SSTA_DHWMean: CoRTAD. The mean SSTA DHW in degrees Celsius over the entire time period of 40 years.
    TSA: CoRTAD. (Thermal Stress Anomaly) weekly SSTs minus the maximum of weekly climatological SSTs in degrees Celsius.
    TSA_Standard_Deviation: CoRTAD. The standard deviation of TSA in degrees Celsius over the entire time period of 40 years.
    TSA_Minimum: CoRTAD. The minimum TSA in degrees Celsius over the entire time period of 40 years.
    TSA_Maximum: CoRTAD. The maximum TSA in degrees Celsius over the entire time period of 40 years.
    TSA_Mean: CoRTAD. The mean TSA in degrees Celsius over the entire time period of 40 years.
    TSA_Frequency: CoRTAD. The number of times over previous 52 weeks that TSA  >  = 1 degree Celsius.
    TSA_Frequency_Standard_Deviation: CoRTAD. The standard deviation of frequency of TSA in degrees Celsius over the entire time period of 40 years.
    TSA_FrequencyMax: CoRTAD. The maximum TSA frequency in degrees Celsius over the entire time period of 40 years.
    TSA_FrequencyMean: CoRTAD. The mean TSA frequency in degrees Celsius over the entire time period of 40 years.
    TSA_DHW: CoRTAD. (Thermal Stress Anomaly Degree Heating Weeks) sum of previous 12 weeks when TSA  >  = 1 degree Celsius.
    TSA_DHW_Standard_Deviation: CoRTAD. The standard deviation of TSA DHW in degrees Celsius over the entire time period of 40 years.
    TSA_DHWMax: CoRTAD. The maximum TSA DHW in degrees Celsius over the entire time period of 40 years.
    TSA_DHWMean: CoRTAD. The mean TSA DHW in degrees Celsius over the entire time period of 40 years.

    7)

    Author Names (Authors_LUT)
    Last_Name: author’s last name.
    First_Name: author’s first name.
    Middle_Initial: author’s middle initial.

    8)

    Bleaching Level Information (Bleaching_Level_LUT)
    Bleaching_Level: Reef Check data, coral population or coral colony.

    9)

    City, Town Names (City_Town_Name_LUT)
    City_Town_Name: the region, city, or town, where sampling took place.

    10)

    Country names (Country_Name_LUT)
    Country_Name: name of the country where sampling took place.

    11)

    Data Source Information (Data_Source_LUT)
    Data_Source: name of source of original data set.
    Sample_Method: Description of the sampling methods used to collect the data. If more than one method was used then we stated that an amalgamation of methods were used to collect the data, and the original papers are found in “Relevant_Papers_tbl”, and can be referenced therein.

    12)

    Ecoregion Names (Ecoregion_Name_LUT)
    Ecoregion_Name: name of Ecoregion from Veron et al.13.

    13)

    Exposure Type (Exposure_LUT)
    Exposure_Type: site exposure to fetch.

    14)

    Ocean Name Information (Ocean_Name_LUT)
    Ocean_Name: name of ocean where sampling took place.

    15)

    Name of Realm (Realm_Name_LUT)
    Realm_Name: name of realm as identified by the Marine Ecoregions of the World (MEOW)12.

    16)

    State, Island, Province Name (State_Island_Province_Name_LUT)
    State_Island_Province_Name, Name of the state, territory (e.g. Guam) or island group (e.g. Hawaiian Islands) where sampling took place.

    17)

    Substrate Type (Substrate_Type_LUT)
    Substrate_Type: type of substrate from Reef Check data.

    18)

    Relevant Publications (Relevant_Papers_tbl)
    Data_Source: source associated with publication.
    Author_ID: author ID field from Authors_LUT.
    Title: title of published work.
    Journal_Name: name of publication journal.
    Year_Published: year of publication.
    Volume: volume number of journal.
    Issue: issue number of journal.
    Pages: page range of publication.
    URL: hyperlink to publication.
    DOI: DOI number of publication.
    pdf: pdf attachment of publication.

    19)

    Severity Index Code (Severity_Code_LUT)
    Severity_Code: coded range of bleaching severity from Donner et al.10.

    20)

    Bleaching Prevalence Code (Bleaching_Prevalence_Score_LUT)

    Bleaching_Prevalence_Score: coded range of bleaching prevalence from Safaie et al. 21. More

  • in

    Global gridded crop harvested area, production, yield, and monthly physical area data circa 2015

    Here we describe methods for the GAEZ+ 2015 Annual Crop Data, and the GAEZ+ 2015 Monthly Cropland Data. The Annual Crop Data was generated first, then the Monthly Cropland Data was calculated based on the Harvest Area results of the Annual Data (Fig. 1).Fig. 1Schematic overview of annual and monthly data production methods. The GAEZ+ 2015 products described in this paper are in dark blue boxes; publicly available data used are in light blue. Dark blue arrows indicate which data are used in each processing step, and grey arrows from steps to data show which steps result in final GAEZ+ 2015 data products. The processing steps listed here are referred to in the Methods section text.Full size imageGAEZ+ 2015 Annual Crop Data MethodsThe GEAZ+ 2015 Annual Crop Data updates the 2010 GAEZ v4 crop harvest area, yield, and production maps6,7 (identified as Theme 5 in ref. 7) using national-scale data on the change in crop harvested area and livestock numbers from 2010 to 2015, based on statistics for 160 crop groups, and cattle and buffalo, from FAOSTAT5.Three datasets were used to produce GAEZ+ 2015 Annual Crop Data:

    1.

    FAOSTAT crop production domain: annual, country-level data on crop harvested area (H) and crop production (P) for each crop from the FAOSTAT database (Table 1)Table 1 GAEZ and FAOSTAT crop harmonization.Full size table

    2.

    GAEZ v46,7 gridded global annual harvested area, yield, and production by crop for the 26 FAOSTAT crops and crop categories at 5-minute resolution

    3.

    Global Administrative Unit Layer (GAUL 2012)13 data. GAUL 2012 reports the fraction of each global 5-minute grid cell that falls within a given country or disputed territory. There are 275 unique global administrative units.

    Step 1. Calculate crop changes from 2010 to 2015 by country:
    For each country, we extracted the harvested area (H) and crop production (P) for each of the 160 FAOSTAT crop categories, c, from the FAOSTAT database. We averaged three years (2009–2011) of annual national crop harvested area data to represent 2010 national crop harvest area, H2010, and three years (2014–2016) of annual crop harvested area data to represent 2015 national crop harvest area, H2015, then calculated a ratio, rHc, of 2015 to 2010 harvested areas for each crop c in each country, and equivalently, for crop production:$$r{H}_{c}={H}_{2015}/{H}_{2010}$$
    (1)
    $$r{P}_{c}={P}_{2015}/{P}_{2010}$$
    (2)
    This results in 160 rH and rP values per country. If harvest area and production values for a particular crop are zero or unreported in the FAOSTAT data, then rHc and rPc are both set to 1.0 (i.e., no change from 2010 to 2015). Three years of data are averaged (2009 – 2011 and 2014 – 2016) to account for missing data for some country/year combinations and to avoid emphasizing reported outliers.
    Step 2. Aggregate FAOSTAT-based ratios to the GAEZ crop categories:
    We followed the crop aggregation methods of the GAEZ model to aggregate the FAOSTAT crop list (160 unique crops as of 2019) to 26 crops (see Table 1). For each of the 26 GAEZ crop categories, if there is more than one matching FAOSTAT crop (see Table 1) then we applied an area-weighted average (based on FAOSTAT year 2015 harvested area) of the FAOSTAT crops within each country to the rH and rP values for that crop and country. This results in 26 rH and rP values per country. There was one exception to this: the GAEZ_2010 crop category ‘fodder crops’ was an aggregate of 17 FAOSTAT crops (see Table 1) for which harvest area data are no longer reported on FAOSTAT; i.e., GAEZ_2010 had obtained FAOSTAT data on fodder crops circa 2010, but FAOSTAT no longer provides any data on fodder crops for any year. We assumed that the 2010 to 2015 fractional change in fodder crop harvest area in each country was proportional to the change in the FAOSTAT reported national herd sizes for cattle and buffalo livestock data5 for that country, following the same methodology as for crop harvested area change (see Step 2 below). This method assumes a negligible international trade of fodder crops as indicated by bilateral trade matrices available from FAOSTAT.
    Step 3. Apply country-level ratios to grid cells:
    Calculated country-level ratios were then applied to each grid cell k, using the GAUL_201213 definitions for which grid cells fall within which countries. Some grid cells are split between two or more countries. In this case, all model output variables for the grid cell are divided between the countries based on the fraction of grid cell area falling within the country i:$${H}_{c,2015}^{k}={H}_{c,2010}^{k}{sum }_{i},{f}_{i}^{k}r{H}_{c,i}$$
    (3)
    $${P}_{c,2015}^{k}={P}_{c,2010}^{k}{sum }_{i},{f}_{i}^{k}r{P}_{c,i}$$
    (4)
    where ({H}_{c,2015}^{k}) is the year 2015 harvested area (or production) for crop c in grid cell k; ({f}_{i}^{k}) is the fraction of country i in grid cell k, and rHc,i and rPc,i are the ratios for crop c in country i as calculated in Eqs. 1 and 2. This results in 26 H and P values per grid cell. If the sum of all crop harvest areas exceeds 99% of the grid cell area, all crop harvest areas are reduced equally to fit within 99% of the area.
    Special Case: Sudan
    FAOSTAT data for years before 2011 report data for Sudan, and for South Sudan and Sudan after 2011. To compute the ratios for these grid cells, we split the 2010 data for Sudan into a virtual ‘North’ Sudan and ‘South_Sudan’, using the data for the year 2012, which was reported for both countries. We then used these generated 2010 data and applied the same methodology as described above to calculate changes in harvested areas and production in all grid cells in both countries.
    Special Case: Small regions and islands
    Forty-nine countries – generally small regions or islands – had no data reported for crop harvested area by FAOSTAT. We assumed that there was no change in crop harvested area for the grid cells in these countries. Note that many may have had zero ha as previously-reported crop area in GAEZ v4. These countries are (the number following each region is the region’s number in ADM0_CODE in the GAUL_2012 data13):Anguilla (9), Aruba (14), Ashmore_and_Cartier_Islands (16), Azores_Islands (74578), Baker_Island (22), Bassas_da_India (25), Bird_Island (32), Bouvet_Island (36), British_Indian_Ocean_Territory (38), Christmas_Island (54), Clipperton_Island (55), Cocos (Keeling)_Islands (56), Europa_Island (80), French_Southern_and_Antarctic_Territories (88), Glorioso_Island (96), Greenland (98), Guernsey (104), Heard_Island_and_McDonald_Islands (109), Howland_Island (112), Isle_of_Man (120), Jarvis_Island (127), Jersey (128), Johnston_Atoll (129), Juan_de_Nova_Island (131), Kingman_Reef (134), Kuril_islands (136), Madeira_Islands (151), Mayotte (161), Midway_Island (164), Navassa_Island (174), Netherlands_Antilles (176), Norfolk_Island (184), Northern_Mariana_Islands (185), Palmyra_Atoll (190), Paracel_Islands (193), Pitcairn (197), Saint_Helena (207), Scarborough_Reef (216), Senkaku_Islands (218), South_Georgia_and_the_South_Sandwich_Islands (228), Spratly_Islands (230), Svalbard_and_Jan_Mayen_Islands (234), Tromelin_Island (247), Turks_and_Caicos_Islands (251), United_States_Virgin_Islands (258), Wake_Island (265), Gibraltar (95), Holy_See (110), Liechtenstein (146).
    Special Case: Disputed Areas
    Some grid cells in the GAUL_201213 cell-table database are assigned to nine disputed areas, rather than to specific countries. We assumed that there was no change in crop harvested area or production from 2010 to 2015 for grid cells these disputed areas. These areas are (the number following each region is the region’s number of the ADM0_CODE in the GAUL_201213 data):Abyei (102), Aksai_Chin (2), Arunachal_Pradesh (15), China/India (52), Hala’ib_Triangle (40760), Ilemi_Triangle (61013), Jammu_and_Kashmir (40781), Ma’tan_al-Sarra (40762), Falkland_Islands_(Malvinas) (81).
    Step 4. Compute 2015 crop yields:
    Crop yields were computed for each crop, c, and grid cell, k, as the ratio of crop production to crop harvest area (if harvest area, Hc,k,2015, is zero, then yield, Yc,k,2015, is set to zero):$${Y}_{c,k,2015}={P}_{c,k,2015}/{H}_{c,k,2015}$$
    (5)
    The resulting gridded global data are:

    A.

    GAEZ+ 2015 Crop Harvest Area14

    B.

    GAEZ+ 2015 Crop Yield15

    C.

    GAEZ+ 2015 Crop Production16

    This new data product consists of 156 data files in geotiff format, one rainfed harvested area file and one irrigated harvested area file for each crop harvest area (1000 ha (107 m2) per 5-minute grid cell), crop production (1000 tonnes (106 kg) per 5-minute grid cell), and crop yield (tonnes per ha (10−1 kg m−2) per 5-minute grid cell), for each of the 26 GAEZ crops or crop categories in Table 1.GAEZ+ 2015 monthly cropland area methodsTwo datasets were used to produce monthly cropland area by crop and by irrigated vs rainfed management. These are:

    1.

    GAEZ+ 2015 Annual Harvested Area14 (as developed above)

    2.

    MIRCA2000 cropland area4

    Step 5. Harmonize the GAEZ+ 2015 and MIRCA2000 crop lists
    The MIRCA20004 cropland product provides monthly growing area grids (gridded physical cropland area) for 26 irrigated and rainfed crops and crop categories, as well as cropping calendars that identify the planting month and harvesting month for each crop (via ‘subcrops’ – see below). However, the MIRCA2000 crop list is not the same as the GAEZ+ 2015 crop list; we matched each crop type in the GAEZ+ 2015 crop list to a crop type in the MIRCA2000 crop list to enable the application of MIRCA2000 crop calendars to GAEZ+ 2015 crops (Table 2). Out of the 26 GAEZ+ 2015 crops, 18 had clear 1:1 matching crop categories within MIRCA2000. The remaining 8 crops were matched based on general crop characteristics, i.e., annual vs. perennial, or to unmatched MIRCA2000 cereals.Table 2 List of GAEZ crop categories used in all GAEZ+ 2015 products, as well as the matching between GAEZ+ 2015 crops and MIRCA20004 crop categories for the purposes of producing GAEZ+ 2015 monthly cropland data.Full size tableAn essential component of the MIRCA2000 cropland dataset is the identification of subcrop categories within each crop category to split crops into areas grown in different seasons, or crops with different planting and harvesting dates within the same season. Up to 5 subcrops can be defined to represent such multi-cropping practices. Below, we use the following notation:HG = annual harvested area from the GAEZ+ 2015 product for a given cropHM = annual harvested area calculated from the MIRCA2000 data for a given cropAM,n = cropland area of MIRCA2000 crop, subcrop n, by monthAG,n = cropland area of GAEZ+ 2015 crop, subcrop n, by monthAG = cropland area of GAEZ+ 2015 crop, by month
    Step 6. Apply MIRCA2000 monthly crop calendars to GAEZ+ 2015 annual data
    To generate the monthly cropland physical area of GAEZ+ 2015 crops, we followed these steps for each GAEZ crop in each grid cell:

    1.

    For a given GAEZ crop in a given grid cell, is the area reported >0 for the matching MIRCA2000 crop?

    a.

    If YES, then use the MIRCA2000 data for the grid cell and crop considered.

    b.

    If NO, then find the closest grid cell with the matching MIRCA2000 crop category, and apply the MIRCA2000 crop rotation from that grid cell to the given crop/grid cell combination for the following steps.

    2.

    Does the matching MIRCA2000 crop category (Table 1) have more than 1 subcrop?

    a.

    If NO, then AG = HG for all months of the cropping season, as defined by the MIRCA2000 crop calendar.

    b.

    If YES, then for each subcrop category n, apply the ratio of AM,n/HM to HG, then sum the subcrop areas within each month such that:

    $${A}_{G}=sum _{n}frac{{A}_{M,n}}{{H}_{M}}{H}_{G}$$

    3.

    For each month and each grid cell, check if the sum of all crops (irrigated and rainfed) is greater than the 99% of area of the grid cell. We assume that at least 1% of land must be retained as non-cropland for agricultural infrastructure such as roads, buildings, irrigation infrastructure, and other landcovers (e.g. rivers, wetlands).

    a.

    If NO, then no further processing is done.

    b.

    If YES, then reduce crop area by the excess value based on a removal order (Table 2). Rainfed crops have higher removal order numbers for the excess truncation (starting with 1) before removing irrigated crops, until the cell area is not exceeded. A large removal number (e.g., 20) indicates that the crop’s land is unlikely to be removed. Large priority numbers are given to the staple crops to ensure these important food producing lands are consistent with FAOSTAT country data.

    The maximum monthly amount of physical cropland that was removed by step 3 is 711,543 ha, which is 0.05% of total global cropland physical area.The resulting global gridded data from Step 6 are monthly time series of cropland physical area by crop, subcrop, and production system, called GAEZ+_2015 Monthly Cropland Data17. Combining the MIRCA2000 crop calendar and subcrop rotation information with the GAEZ+ 2015 annual data allows for the representation of crop seasonality; e.g., Fig. 2 shows the aggregate monthly cropland physical area for Rice 1 and Rice 2 (two sub-crops of rice) over the northern hemisphere, clearly illustrating the two main rice-growing seasons.Fig. 2Aggregate monthly cropland physical area for Rice 1 and Rice 2 subcrops from monthly GAEZ+ 2015 over the northern hemisphere shows the two main rice-growing seasons. This seasonality is the result of combining GAEZ+ 2015 annual data with the MIRCA20004 crop calendars and subcrop divisions.Full size image More

  • in

    Complex marine microbial communities partition metabolism of scarce resources over the diel cycle

    1.Ottesen, E. A. et al. Pattern and synchrony of gene expression among sympatric marine microbial populations. Proc. Natl Acad. Sci. USA 110, E488–E497 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    2.Muñoz-Marín, M. D. C. et al. The transcriptional cycle is suited to daytime N2 fixation in the unicellular cyanobacterium “Candidatus Atelocyanobacterium thalassa” (UCYN-A). mBio 10, e02495-18 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    3.Vislova, A., Sosa, O. A., Eppley, J. M., Romano, A. E. & DeLong, E. F. Diel oscillation of microbial gene transcripts declines with depth in oligotrophic ocean waters. Front. Microbiol. 10, 2191 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    4.Harke, M. J. et al. Periodic and coordinated gene expression between a diazotroph and its diatom host. ISME J. 13, 118–131 (2019).CAS 
    PubMed 

    Google Scholar 
    5.Hernández Limón, M. D. et al. Transcriptional patterns of Emiliania huxleyi in the North Pacific Subtropical Gyre reveal the daily rhythms of its metabolic potential.Environ. Microbiol. 22, 381–396 (2020).PubMed 

    Google Scholar 
    6.Becker, K. W. et al. Daily changes in phytoplankton lipidomes reveal mechanisms of energy storage in the open ocean. Nat. Commun. 9, 5179 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    7.Frischkorn, K. R., Haley, S. T. & Dyhrman, S. T. Coordinated gene expression between Trichodesmium and its microbiome over day–night cycles in the North Pacific Subtropical Gyre. ISME J. 12, 997–1007 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    8.Ottesen, E. A. et al. Ocean microbes. Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages. Science 345, 207–212 (2014).CAS 
    PubMed 

    Google Scholar 
    9.Wilson, S. T. et al. Coordinated regulation of growth, activity and transcription in natural populations of the unicellular nitrogen-fixing cyanobacterium Crocosphaera. Nat. Microbiol. 2, 17118 (2017).CAS 
    PubMed 

    Google Scholar 
    10.Saito, M. A. et al. Iron conservation by reduction of metalloenzyme inventories in the marine diazotroph Crocosphaera watsonii. Proc. Natl Acad. Sci. USA 108, 2184–2189 (2011).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    11.Strenkert, D. et al. Multiomics resolution of molecular events during a day in the life of Chlamydomonas. Proc. Natl Acad. Sci. USA 116, 2374–2383 (2019).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    12.Boysen, A. K. et al. Particulate metabolites and transcripts reflect diel oscillations of microbial activity in the surface ocean. mSystems 6, e00896-20 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    13.White, A. E., Barone, B., Letelier, R. M. & Karl, D. M. Productivity diagnosed from the diel cycle of particulate carbon in the North Pacific Subtropical Gyre: optically derived productivity. Geophys. Res. Lett. 44, 3752–3760 (2017).CAS 

    Google Scholar 
    14.DeLong, E. F. et al. Community genomics among stratified microbial assemblages in the ocean’s interior. Science 311, 496–503 (2006).CAS 
    PubMed 

    Google Scholar 
    15.Sunagawa, S. et al. Ocean plankton. Structure and function of the global ocean microbiome. Science 348, 1261359 (2015).PubMed 

    Google Scholar 
    16.Coles, V. J. et al. Ocean biogeochemistry modeled with emergent trait-based genomics. Science 358, 1149–1154 (2017).CAS 
    PubMed 

    Google Scholar 
    17.Walbauer, J. R., Rodrigue, S., Coleman, M. L. & Chisholm, S. W. Transcriptome and proteome dynamics of a light–dark synchronized bacterial cell cycle.PLoS ONE 7, e43432 (2012).
    Google Scholar 
    18.Steiner, P. A. et al. Highly variable mRNA half-life time within marine bacterial taxa and functional genes. Environ. Microbiol. 21, 3873–3884 (2019).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    19.Moran, M. A. et al. Sizing up metatranscriptomics. ISME J. 7, 237–243 (2013).CAS 
    PubMed 

    Google Scholar 
    20.Tamames, J., Cobo-Simón, M. & Puente-Sánchez, F. Assessing the performance of different approaches for functional and taxonomic annotation of metagenomes. BMC Genomics 20, 960 (2019).21.DiTullio, G. R. & Laws, E. A. Diel periodicity of nitrogen and carbon assimilation in five species of marine phytoplankton: accuracy of methodology for predicting N-assimilation rates and N/C composition ratios. Mar. Ecol. Prog. Ser. 32, 123–132 (1986).CAS 

    Google Scholar 
    22.Granum, E., Kirkvold, S. & Myklestad, S. M. Cellular and extracellular production of carbohydrates and amino acids by the marine diatom Skeletonema costatum: diel variations and effects of N depletion. Mar. Ecol. Prog. Ser. 242, 83–94 (2002).CAS 

    Google Scholar 
    23.Lacour, T., Sciandra, A., Talec, A., Mayzaud, P. & Bernard, O. Diel variations of carbohydrates and neutral lipids in nitrogen-sufficient and nitrogen-starved cyclostat cultures of Isochrysis sp. J. Phycol. 48, 966–975 (2012).PubMed 

    Google Scholar 
    24.Follett, C. L., Dutkiewicz, S., Karl, D. M., Inomura, K. & Follows, M. J. Seasonal resource conditions favor a summertime increase in North Pacific diatom–diazotroph associations. ISME J. 12, 1543–1557 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    25.Chen, W.-N. U. et al. Diel rhythmicity of lipid-body formation in a coral-Symbiodinium endosymbiosis. Coral Reefs 31, 521–534 (2012).
    Google Scholar 
    26.Zhou, X. & Mopper, K. Photochemical production of low-molecular-weight carbonyl compounds in seawater and surface microlayer and their air-sea exchange. Mar. Chem. 56, 201–213 (1997).CAS 

    Google Scholar 
    27.Durham, B. P. et al. Sulfonate-based networks between eukaryotic phytoplankton and heterotrophic bacteria in the surface ocean.Nat. Microbiol. 4, 1706–1715 (2019).CAS 
    PubMed 

    Google Scholar 
    28.Lambert, S. et al. Rhythmicity of coastal marine picoeukaryotes, bacteria and archaea despite irregular environmental perturbations. ISME J. 13, 388–401 (2019).PubMed 

    Google Scholar 
    29.Kolody, B. C. et al. Diel transcriptional response of a California Current plankton microbiome to light, low iron, and enduring viral infection. ISME J. 13, 2817–2833 (2019).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    30.Aylward, F. O. et al. Microbial community transcriptional networks are conserved in three domains at ocean basin scales. Proc. Natl Acad. Sci. USA 112, 5443–5448 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    31.Rusch, D. B. et al. The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol. 5, e77 (2007).PubMed 
    PubMed Central 

    Google Scholar 
    32.Bork, P. et al. Tara Oceans studies plankton at planetary scale. Science 348, 873 (2015).CAS 
    PubMed 

    Google Scholar 
    33.Delmont, T. O. et al. Nitrogen-fixing populations of Planctomycetes and Proteobacteria are abundant in surface ocean metagenomes. Nat. Microbiol. 3, 804–813 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    34.Fuhrman, J. A. et al. Annually reoccurring bacterial communities are predictable from ocean conditions. Proc. Natl Acad. Sci. USA 103, 13104–13109 (2006).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    35.Morris, R. M. et al. Temporal and spatial response of bacterioplankton lineages to annual convective overturn at the Bermuda Atlantic Time‐series Study site. Limnol. Oceanogr. 50, 1687–1696 (2005).CAS 

    Google Scholar 
    36.Mende, D. R. et al. Environmental drivers of a microbial genomic transition zone in the ocean’s interior. Nat. Microbiol. 2, 1367–1373 (2017).CAS 
    PubMed 

    Google Scholar 
    37.Keeling, P. J. et al. The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol. 12, e1001889 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    38.Kanehisa, M., Sato, Y., Kawashima, M., Furumichi, M. & Tanabe, M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res. 44, D457–D462 (2016).CAS 

    Google Scholar 
    39.Thaben, P. F. & Westermark, P. O. Detecting rhythms in time series with RAIN. J. Biol. Rhythms 29, 391–400 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    40.Cuhel, R. L., Ortner, P. B. & Lean, D. R. S. Night synthesis of protein by algae. Limnol. Oceanogr. 29, 731–744 (1984).CAS 

    Google Scholar 
    41.Coesel, S. N. et al. Diel transcriptional oscillations of light-sensitive regulatory elements in open-ocean eukaryotic plankton communities. Proc. Natl Acad. Sci. USA 118, e2011038118 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    42.Bolay, P., Muro-Pastor, M. I., Florencio, F. J. & Klähn, S. The distinctive regulation of cyanobacterial glutamine synthetase. Life (Basel) 8, 52 (2018).CAS 

    Google Scholar 
    43.Karl, D. M., Church, M. J., Dore, J. E., Letelier, R. M. & Mahaffey, C. Predictable and efficient carbon sequestration in the North Pacific Ocean supported by symbiotic nitrogen fixation. Proc. Natl Acad. Sci. USA 109, 1842–1849 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    44.Berman, T. & Bronk, D. A. Dissolved organic nitrogen: a dynamic participant in aquatic ecosystems. Aquat. Microb. Ecol. 31, 279–305 (2003).
    Google Scholar 
    45.Lee, C. & Bada, J. L. Amino acids in equatorial Pacific Ocean water. Earth Planet. Sci. Lett. 26, 61–68 (1975).CAS 

    Google Scholar 
    46.Bada, J. L. & Lee, C. Decomposition and alteration of organic compounds dissolved in seawater. Mar. Chem. 5, 523–534 (1977).CAS 

    Google Scholar 
    47.Poretsky, R. S., Sun, S., Mou, X. & Moran, M. A. Transporter genes expressed by coastal bacterioplankton in response to dissolved organic carbon. Environ. Microbiol. 12, 616–627 (2010).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    48.Berthelot, H. et al. NanoSIMS single cell analyses reveal the contrasting nitrogen sources for small phytoplankton. ISME J. 13, 651–662 (2019).CAS 
    PubMed 

    Google Scholar 
    49.Moore, L. R., Post, A. F., Rocap, G. & Chisholm, S. W. Utilization of different nitrogen sources by the marine cyanobacteria Prochlorococcus and Synechococcus. Limnol. Oceanogr. 47, 989–996 (2002).CAS 

    Google Scholar 
    50.Hu, S. K., Connell, P. E., Mesrop, L. Y. & Caron, D. A. A hard day’s night: diel shifts in microbial eukaryotic activity in the North Pacific Subtropical Gyre. Front. Mar. Sci. https://doi.org/10.3389/fmars.2018.00351 (2018).51.Hannides, C. C. S., Popp, B. N., Choy, C. A. & Drazen, J. C. Midwater zooplankton and suspended particle dynamics in the North Pacific Subtropical Gyre: a stable isotope perspective. Limnol. Oceanogr. 58, 1931–1946 (2013).CAS 

    Google Scholar 
    52.Becker, K. W. et al. Combined pigment and metatranscriptomic analysis reveals highly synchronized diel patterns of phenotypic light response across domains in the open oligotrophic ocean.ISME J. 15, 520–533 (2021).CAS 
    PubMed 

    Google Scholar 
    53.Mruwat, N. et al. A single-cell polony method reveals low levels of infected Prochlorococcus in oligotrophic waters despite high cyanophage abundances. ISME J. 15, 41–54 (2021).CAS 
    PubMed 

    Google Scholar 
    54.Chesson, P. L. & Warner, R. R. Environmental variability promotes coexistence in lottery competitive systems. Am. Nat. 117, 923–943 (1981).
    Google Scholar 
    55.Shmida, A. & Ellner, S. Coexistence of plant species with similar niches. Vegetatio 58, 29–55 (1984).
    Google Scholar 
    56.Ellner, S. P., Snyder, R. E. & Adler, P. B. How to quantify the temporal storage effect using simulations instead of math. Ecol. Lett. 19, 1333–1342 (2016).PubMed 

    Google Scholar 
    57.Adler, P. B., Fajardo, A., Kleinhesselink, A. R. & Kraft, N. J. B. Trait-based tests of coexistence mechanisms. Ecol. Lett. 16, 1294–1306 (2013).PubMed 

    Google Scholar 
    58.Adler, P. B., HilleRisLambers, J., Kyriakidis, P. C., Guan, Q. & Levine, J. M. Climate variability has a stabilizing effect on the coexistence of prairie grasses. Proc. Natl Acad. Sci. USA 103, 12793–12798 (2006).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    59.Cáceres, C. E. Temporal variation, dormancy, and coexistence: a field test of the storage effect. Proc. Natl Acad. Sci. USA 94, 9171–9175 (1997).PubMed 
    PubMed Central 

    Google Scholar 
    60.Padisák, J. Identification of relevant time-scales in non-equilibrium community dynamics: conclusions from phytoplankton surveys. N. Z. J. Ecol. 18, 169–176 (1994).
    Google Scholar 
    61.Anderies, J. M. & Beisner, B. E. Fluctuating environments and phytoplankton community structure: a stochastic model. Am. Nat.155, 556–569 (2000).PubMed 

    Google Scholar 
    62.Wagg, C. et al. Functional trait dissimilarity drives both species complementarity and competitive disparity. Funct. Ecol. 31, 2320–2329 (2017).
    Google Scholar 
    63.Bligh, E.G. & Dyer, W. J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917 (1959).CAS 
    PubMed 

    Google Scholar 
    64.Boysen, A. K., Heal, K. R., Carlson, L. T. & Ingalls, A. E. Best-matched internal standard normalization in liquid chromatography–mass spectrometry metabolomics applied to environmental samples. Anal. Chem. 90, 1363–1369 (2018).CAS 
    PubMed 

    Google Scholar 
    65.MacLean, B. et al. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26, 966–968 (2010).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    66.Fountoulakis, M. & Lahm, H. W. Hydrolysis and amino acid composition analysis of proteins. J. Chromatogr. A 826, 109–134 (1998).CAS 
    PubMed 

    Google Scholar 
    67.Popendorf, K. J., Fredricks, H. F. & Van Mooy, B. A. S. Molecular ion-independent quantification of polar glycerolipid classes in marine plankton using triple quadrupole MS. Lipids 48, 185–195 (2013).CAS 
    PubMed 

    Google Scholar 
    68.Collins, J. R., Edwards, B. R., Fredricks, H. F. & Van Mooy, B. A. S. LOBSTAHS: an adduct-based lipidomics strategy for discovery and identification of oxidative stress biomarkers. Anal. Chem. 88, 7154–7162 (2016).CAS 
    PubMed 

    Google Scholar 
    69.Hummel, J. et al. Ultra performance liquid chromatography and high resolution mass spectrometry for the analysis of plant lipids. Front. Plant Sci. 2, 54 (2011).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    70.Smith, C. A., Want, E. J., O’Maille, G., Abagyan, R. & Siuzdak, G. XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal. Chem. 78, 779–787 (2006).CAS 
    PubMed 

    Google Scholar 
    71.Kuhl, C., Tautenhahn, R., Böttcher, C., Larson, T. R. & Neumann, S. CAMERA: an integrated strategy for compound spectra extraction and annotation of liquid chromatography/mass spectrometry data sets. Anal. Chem. 84, 283–289 (2012).CAS 
    PubMed 

    Google Scholar 
    72.Biller, S. J. et al. Prochlorococcus extracellular vesicles: molecular composition and adsorption to diverse microbes.Environ. Microbiol. https://doi.org/10.1111/1462-2920.15834 (2021).Article 
    PubMed 

    Google Scholar 
    73.Aylward, F. O. et al. Diel cycling and long-term persistence of viruses in the ocean’s euphotic zone. Proc. Natl Acad. Sci. USA 114, 11446–11451 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    74.Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    75.Masella, A. P., Bartram, A. K., Truszkowski, J. M., Brown, D. G. & Neufeld, J. D. PANDAseq: paired-end assembler for illumina sequences. BMC Bioinformatics 13, 31 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    76.Joshi, N. & Fass, J. Sickle: A sliding-window, adaptive, quality-based trimming tool for FastQ files. Version 1.33. GitHub https://github.com/najoshi/sickle (2015).77.Kopylova, E., Noé, L. & Touzet, H. SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28, 3211–3217 (2012).CAS 

    Google Scholar 
    78.Kiełbasa, S. M., Wan, R., Sato, K., Horton, P. & Frith, M. C. Adaptive seeds tame genomic sequence comparison. Genome Res. 21, 487–493 (2011).PubMed 
    PubMed Central 

    Google Scholar 
    79.Li, H. & Durbin, R. Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 26, 589–595 (2010).PubMed 
    PubMed Central 

    Google Scholar 
    80.Alexander, H. et al. Functional group-specific traits drive phytoplankton dynamics in the oligotrophic ocean. Proc. Natl Acad. Sci. USA 112, E5972–E5979 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    81.Anders, S., Pyl, P. T. & Huber, W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169 (2015).CAS 

    Google Scholar 
    82.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 

    Google Scholar 
    83.Meinicke, P. UProC: tools for ultra-fast protein domain classification. Bioinformatics 31, 1382–1388 (2015).CAS 
    PubMed 

    Google Scholar 
    84.Mende, D. R., Boeuf, D. & DeLong, E. F. Persistent core populations shape the microbiome throughout the water column in the North Pacific Subtropical Gyre. Front. Microbiol. 10, 2273 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    85.White, A. E. et al. Phenology of particle size distributions and primary productivity in the North Pacific subtropical gyre (Station ALOHA). J. Geophys. Res. Oceans 120, 7381–7399 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    86.Borchers, H. W. pracma: Practical numerical math functions. R package version 2 https://cran.r-project.org/web/packages/pracma/index.html (2019).87.Maechler, M., Rousseeuw, P., Struyf, A., Hubert, M. & Hornik, K. cluster: Cluster analysis basics and extensions. R package version 1.56 (2012).88.Wehrens, R. & Buydens, L. M. C. Self- and super-organizing maps in R: the Kohonen package. J. Stat. Softw. 21, 1–19 (2007).
    Google Scholar 
    89.Hennig, C. fpc: Flexible procedures for clustering. R package version 2.2-9 (2010).90.Muratore, D. Code for complex marine microbial communities partition metabolism of scarce resources over the diel cycle. Zenodo https://doi.org/10.5281/zenodo.3817416 (2020). More

  • in

    Leaf plasticity across wet and dry seasons in Croton blanchetianus (Euphorbiaceae) at a tropical dry forest

    1.Holechek, J. L., Pieper, R. D. & Herbel, C. H. Range management: Principles and practices 6th edn. (Pearson Education, Inc., 2011).
    Google Scholar 
    2.Dombroski, J. L. D., Praxedes, S. C., de Freitas, R. M. O. & Pontes, F. M. Water relations of Caatinga trees in the dry season. S. Afr. J. Bot. 77, 430–434 (2011).
    Google Scholar 
    3.Santos, M. G. et al. Caatinga, the Brazilian dry tropical forest: can it tolerate climate changes?. Theor. Experim. Plant Physiol. 26, 83–99 (2014).
    Google Scholar 
    4.Mendes, K. et al. Croton blanchetianus modulates its morphophysiological responses to tolerate drought in a tropical dry forest. Funct. Plant Biol. 10, 1–13 (2017).
    Google Scholar 
    5.Smith, W. K. & Nobel, P. S. Influences of seasonal changes in leaf morphology on water-use efficiency for three desert broad leaf shrubs. Ecology 58, 1033–1043 (1977).
    Google Scholar 
    6.Kyparissis, A. & Manetas, Y. Seasonal leaf dimorphism in a semi-deciduous Mediterranean shrub-ecophysiological comparisons between winter and summer leaves. Acta Oecol.-Oecol. Plantarum 14, 23–32 (1993).
    Google Scholar 
    7.Kloeppel, B. D., Abrams, M. D. & Kubiske, M. E. Seasonal ecophysiology and leaf morphology of four successional Pennsylvania barrens species in open versus understory environments. Can. J. For. Res. 23(2), 181–189 (1993).
    Google Scholar 
    8.Coley, P. D. Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia 74, 531–536 (1988).ADS 
    CAS 
    PubMed 

    Google Scholar 
    9.Reich, P., Walters, M. & Ellsworth, D. From tropics to tundra: global convergence in plant functioning. Proc. Natl. Acad. Sci. USA 94, 13730–13734 (1997).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    10.Pompelli, M. F. et al. Allometric models for non-destructive leaf area estimation of the Jatropha curcas. Biomass Bioenerg. 36, 77–85 (2012).
    Google Scholar 
    11.Duan, B., Yang, Y., Lu, Y., Korpelainen, H. & Berninger, F. C. L. Interactions between drought stress, ABA and genotypes in Picea asperata. J. Exp. Bot. 58, 3025–3036 (2007).CAS 
    PubMed 

    Google Scholar 
    12.Kwon, M. Y. & Woo, S. Y. Plants’ responses to drought and shade environments. Afr. J. Biotech. 15, 29–31 (2016).CAS 

    Google Scholar 
    13.Santos, J. C., Leal, I. R., Almeida-Cortez, J. S., Fernandes, G. W. & Tabarelli, M. Caatinga: the scientific negligence experienced by a dry tropical forest. Tropical Conservation Science 4, 276–286 (2011).
    Google Scholar 
    14.Almazroui, M., Islanm, M. N., Saeed, F., Alkhalaf, A. K. & Dambul, R. Assessing the robustness and uncertainties of projected changes in temperature and precipitation in AR5 Global Climate Models over the Arabian Peninsula. Atmos. Res. 194, 202–213 (2017).
    Google Scholar 
    15.Angulo-Brown, F., Sánchez-Salas, N., Barranco-Jiménez, M. A. & Rosales, M. A. Possible future scenarios for atmospheric concentration of greenhouse gases: A simplified thermodynamic approach. Renewable Energy 34, 2344–2352 (2009).CAS 

    Google Scholar 
    16.Glotfelty, T. & Zhang, Y. Impact of future climate policy scenarios on air quality and aerosol-cloud interactions using an advanced version of CESM/CAM5: Part II. Future trend analysis and impacts of projected anthropogenic emissions. Atmos. Environ. 152, 531–552 (2017).ADS 
    CAS 

    Google Scholar 
    17.O’Neill, B. C. et al. IPCC reasons for concern regarding climate change risks. Nat. Clim. Change 7, 28–37 (2017).ADS 

    Google Scholar 
    18.Hulshof et al. Plant Functional Trait Variation in Tropical Dry Forests: A Review and Synthesis in Tropical Dry Forests in the Americas (ed. Sánchez-Azofeifa, A. et al.) 129–140 (2014).19.Mendes, K. R. et al. Seasonal variation in net ecosystem CO2 exchange of a Brazilian seasonally dry tropical forest. Sci. Rep. 10, 9454 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    20.Poulter, B. et al. Contribuition of semi-arid ecosystems to interannual variability of the global carbon cycle. Nature 509, 600–604 (2014).ADS 
    CAS 
    PubMed 

    Google Scholar 
    21.Campos, S. et al. Closure and partitioning of the energy balance in a preserved area of a Brazilian seasonally dry tropical forest. Agric. For. Meteorol. 471, 398–412 (2019).ADS 

    Google Scholar 
    22.Zappi, D. et al. Growing knowledge: An overview of seed plant diversity in Brazil. Rodriguésia 66, 1085–1113 (2015).
    Google Scholar 
    23.Pompelli, M. F., Pompelli, G. M., Cabrini, E. C., Alves, C. J. L. & Ventrella, M. C. Leaf anatomy, ultrastructure and plasticity of Coffea arabica L. in response to light and nitrogen availability. Biotemas 25, 13–28 (2012).
    Google Scholar 
    24.Rossatto, D. R. & Kolb, R. M. (2010) Gochnatia polymorpha (Less) Cabrera (Asteraceae) changes in leaf structure due to differences in light and edaphic conditions. Acta Bot. Bras. 24, 605–612 (2010).
    Google Scholar 
    25.Liu, Y. et al. Does greater specific leaf area plasticity help plants to maintain a high performance when shaded?. Ann. Bot. 118, 1329–1336 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    26.Pompelli, M. F., Martins, S. C., Celin, E. F., Ventrella, M. C. & Da Matta, F. M. What is the influence of ordinary epidermal cells and stomata on the leaf plasticity of coffee plants grown under full-sun and shady conditions?. Braz. J. Biol. 70, 1083–1088 (2010).CAS 
    PubMed 

    Google Scholar 
    27.Björkman, O. Responses to different quantum flux densities. In Encyclopaedia of Plant Physiology (eds Lange, O. L. et al.) (Springer, Berlin, 1981).
    Google Scholar 
    28.Robakowski, P., Wyka, T., Samardakiewicz, S. & Kierzkowski, D. Growth, photosynthesis, and needle structure of silver fir (Abies alba Mill) seedlings under different canopies. For. Ecol. Manag. 201, 211–227 (2004).
    Google Scholar 
    29.Sam, O., Jeréz, E., Dell’Amico, J. & Ruiz-Sanchez, M. C. Water stress induced changes in anatomy of tomato leaf epidermes. Biol. Plant. 43, 275–277 (2000).
    Google Scholar 
    30.Shao, H. B., Chu, L.-Y., Jaleel, C. A. & Zhao, D. Water-deficit stress-induced anatomical changes in higher plants. C.R. Biol. 331, 215–225 (2008).PubMed 

    Google Scholar 
    31.Chartzoulakis, K., Patakas, A., Kofidis, G., Bosabalidis, A. & Nastou, A. Water stress affects leaf anatomy, gas exchange, water relations and growth of two avocado cultivars. Sci. Hortic. 95, 39–50 (2002).CAS 

    Google Scholar 
    32.Ennajeh, M., Vadel, A. M., Cochard, H. & Khemira, H. Comparative impacts of water stress on the leaf anatomy of a drought-resistant and a drought-sensitive olive cultivar. J. Hortic. Sci. Biotechnol. 85, 289–294 (2010).
    Google Scholar 
    33.Oguchi, R., Hikosaka, K. & Hirose, T. Does the photosynthetic light-acclimation need change in leaf anatomy?. Plant Cell Environ. 26, 505–512 (2003).
    Google Scholar 
    34.Johnson, D., Meinzer, F., Woodruff, D. & McCulloh, K. Leaf xylem embolism, detected acoustically and by cryo-SEM, corresponds to decreases in leaf hydraulic conductance in four evergreen species. Plant Cell Environ. 32, 828–836 (2009).PubMed 

    Google Scholar 
    35.Tyree, M. & Sperry, J. B. Vulnerability of xylem to cavitation and embolism. Annu. Rev. Plant Biol. 40, 19–36 (1989).
    Google Scholar 
    36.McKown, A., Cochard, H. & Sack, L. Decoding leaf hydraulics with a spatially explicit model: principles of venation architecture and implications for its evolution. Am. Nat. 175, 447–460 (2010).PubMed 

    Google Scholar 
    37.Nardini, A., Pedà, G. & Rocca, N. Trade-offs between leaf hydraulic capacity and drought vulnerability: Morpho-anatomical bases, carbon costs and ecological consequences. New Phytol. 196, 788–798 (2012).PubMed 

    Google Scholar 
    38.Nunes, A. et al. Plants used to feed ruminants in semi-arid Brazil: A study of nutritional composition guided by local ecological knowledge. J. Arid Environ. 135, 96–103 (2016).ADS 

    Google Scholar 
    39.Santos, A. C. J. & Melo, J. I. M. Flora vascular de uma área de caatinga no estado da Paraíba – Nordeste do Brasil. Revista Caatinga 23, 32–40 (2010).
    Google Scholar 
    40.Flexas, J. et al. Mesophyll conductance to CO2 and Rubisco as targets for improving intrinsic water use efficiency in C3 plants. Plant Cell Environ. 39, 965–982 (2016).CAS 
    PubMed 

    Google Scholar 
    41.Flexas, J. & Medrano, H. Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann. Bot. 89, 183–189 (2002).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    42.He, W. & Zhang, X. Responses of an evergreen shrub Sabina vulgaris to soil water and nutrient shortages in the semi-arid Mu Us Sandland in China. J. Arid Environ. 53, 307–316 (2003).ADS 

    Google Scholar 
    43.Pinho-Pessoa, A. C. B. et al. Interannual variation in temperature and rainfall can modulate the physiological and photoprotective mechanisms of a native semiarid plant species. Indian J. Sci. Technol. 11, 1–17 (2018).CAS 

    Google Scholar 
    44.Reddy, T., Reddy, V. & Anbumozhi, V. Physiological responses of groundnut (Arachis hypogea L.) to drought stress and its amelioration: A critical review. Plant Growth Regul. 41, 75–88 (2003).CAS 

    Google Scholar 
    45.Thakur, P. & Sood, R. Drought tolerance of multipurpose agroforestry tree species during first and second summer droughts after transplanting. Indian J. Plant Physiol. 10, 32–40 (2005).
    Google Scholar 
    46.Leigh, A., Sevanto, S., Close, J. D. & Nicotra, A. B. The influence of leaf size and shape on leaf thermal dynamics: Does theory hold up under natural conditions?. Plant, Cell Environ. 40, 237–248 (2016).
    Google Scholar 
    47.Markesteijn, L., Poorter, L. & Bongers, F. Light-dependent leaf trait variation in 43 tropical dry forest tree species. Am. J. Bot. 94, 515–525 (2007).PubMed 

    Google Scholar 
    48.Gotsch, S., Powers, J. & Lerdau, M. Leaf traits and water relations of 12 evergreen species in Costa Rican wet and dry forests: patterns of intra-specific variation across forests and seasons. Plant Ecol. 211, 133–146 (2010).
    Google Scholar 
    49.Popma, J. & Bongers, F. The effect of canopy gaps on growth and morphology of seedlings of rain forest species. Oecologia 75, 625–632 (1988).ADS 
    CAS 
    PubMed 

    Google Scholar 
    50.Evans, J. R. & Poorter, H. Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant Cell Environ. 24, 755–767 (2001).CAS 

    Google Scholar 
    51.Pompelli, M. F. et al. Mesophyll thickness and sclerophylly among Calotropis procera morphotypes reveal water-saved adaptation to environments. J Arid Land. 11, 795–810 (2019).
    Google Scholar 
    52.Leigh, A., Sevanto, S., Close, J. & D & Nicotra A. B.,. The influence of leaf size and shape on leaf thermal dynamics: Does theory hold up under natural conditions?. Plant Cell Environ. 40, 237–248 (2016).PubMed 

    Google Scholar 
    53.Gil-Pelegrín, E., Saz, M. A., Cuadrat, J. M., Peguero-Pina, J. J. & Sancho-Knapik, D. Oaks Under Mediterranean-Type Climates: Functional Response to Summer Aridity. In Oaks Physiological Ecology Exploring the Functional Diversity of Genus Quercus L (eds Gil-Pelegrín, E. et al.) 137–193 (Springer, London, 2017).
    Google Scholar 
    54.Chazdon, R. L. & Kaufmann, S. Plasticity of leaf anatomy of two rain forest shrubs in relation to photosynthetic light acclimation. Funct. Ecol. 7, 385–394 (1993).
    Google Scholar 
    55.Smith, W., Vogelmann, T., De Lucia, E., Bell, D. & Shepherd, K. Leaf form and photosynthesis: Do leaf structure and orientation interact to regulate internal light and carbon dioxide?. Bioscience 47, 785–793 (1997).
    Google Scholar 
    56.Boanares, D., Isaias, R. R. M. S., Sousa, H. C. & Kozovits, A. R. Strategies of leaf water uptake based on anatomical traits. Plant Biol. 20, 848–856 (2018).CAS 
    PubMed 

    Google Scholar 
    57.Fah, N. A. Plant Anatomy. 2nd ed, Oxford,USA, Butterworth Heinemann (1990).58.Holbrook, N.M. Water Balance of Plants. In: Taiz L, Zeiger E eds. Plant Physiology, 5th ed. Sunderland, Sinauer Associates Inc (2010).59.Glover, B. Differentiation in plant epidermal cells. J. Exp. Bot. 51, 497–505 (2000).CAS 
    PubMed 

    Google Scholar 
    60.Vogelman, T., Nishio, J. & Smith, W. Leaves and light capture: light propagation and gradients of carbon fixation within leaves. Trends Plant Sci. 1, 65–70 (1996).
    Google Scholar 
    61.Fini, A. M. et al. Mesophyll conductance plays a central role in leaf functioning of Oleaceae species exposed to contrasting sunlight irradiance. Physiol. Plant. 157, 54–68 (2016).CAS 
    PubMed 

    Google Scholar 
    62.Oguchi, R., Hikosaka, K. & Hirose, T. Leaf anatomy as a constraint for photosynthetic acclimation: Differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. Plant, Cell Environ. 28, 916–927 (2005).
    Google Scholar 
    63.Pollastrini, M. et al. Interaction and competition processes among tree species in young experimental mixed forests, assessed with chlorophyll fluorescence and leaf morphology. Plant Biol. 16, 323–331 (2014).CAS 
    PubMed 

    Google Scholar 
    64.Sevillano, I., Short, I., Grant, J. & O’Reilly, C. Effects of light availability on morphology, growth and biomass allocation of Fagus sylvatica and Quercus robur seedlings. For. Ecol. Manag. 374, 11–19 (2016).
    Google Scholar 
    65.Nguyen, H. T., Radacsi, P., Gosztola, B. & Nemeth, E. Effects of temperature and light intensity on morphological and phytochemical characters and antioxidant potential of wormwood (Artemisia absinthium L.). Biochem. Syst. Ecol. 79, 1–7 (2018).CAS 

    Google Scholar 
    66.Boardman, N. K. Comparative photosynthesis of sun and shade plants. Ann. Rev. Plant Physiol. 28, 355–377 (1977).CAS 

    Google Scholar 
    67.Bejaoui, F. et al. Changes in chloroplast lipid contents and chloroplast ultrastructure in Sulla carnosa and Sulla coronaria leaves under salt stress. J. Plant Physiol. 198, 32–38 (2016).CAS 
    PubMed 

    Google Scholar 
    68.Van Rensburg, L., Krüger, G. H. J. & Krüger, H. Proline accumulation as drought-tolerance selection criterion: Its relationship to membrane integrity and chloroplast ultrastructure in Nicotiana tabacum L. J. Plant Physiol. 141, 188–194 (1993).
    Google Scholar 
    69.Westoby, M. & Wright, I. The leaf size – twig size spectrum and its relationship to other important spectra of variation among species. Oecologia 135, 621–628 (2003).ADS 
    PubMed 

    Google Scholar 
    70.Scoffoni, C. et al. Leaf vein xylem conduit diameter influences susceptibility to embolism and hydraulic decline. New Phytol. 213, 1076–1092 (2017).CAS 
    PubMed 

    Google Scholar 
    71.Sack, L. & Scoffoni, C. Leaf venation: Structure, function, development, evolution, ecology andapplications in the past, present and future. New Phytol. 198, 983–1000 (2013).PubMed 

    Google Scholar 
    72.Brodribb, T., Holbrook, N., Edwards, E. & Gutierrez, M. Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees. Plant Cell Environ. 26, 443–450 (2003).
    Google Scholar 
    73.Scoffoni, C. et al. Light-induced plasticity in leaf hydraulics, venation, anatomy, and gas exchange in ecologically diverse Hawaiian lobeliads. New Phytol. 207, 43–58 (2015).CAS 
    PubMed 

    Google Scholar 
    74.Mendes, K. R. & Marenco, R. A. Leaf traits and gas exchange in saplings of native tree species in the Central Amazon. Scientia Agricola 67, 624–632 (2010).
    Google Scholar 
    75.Puglielli, G., Varone, L., Gratani, L. & Catoni, R. Specific leaf area variations drive acclimation of Cistus salvifolius in different light environments. Photosynthetica 55, 31–40 (2017).CAS 

    Google Scholar 
    76.O’Brien, T., Feder, N. & McCully, M. Polychromatic staining of plant cell walls by toluidine blue. Protoplasma 59, 368–373 (1965).
    Google Scholar 
    77.Karnovsky, M. J. A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J. Cell Biol. 27, 137–138 (1965).
    Google Scholar 
    78.Spurr, A. R. A low viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26, 31–43 (1969).CAS 
    PubMed 

    Google Scholar 
    79.Reynolds, E. S. The use of load citrate at a high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    80.Hardoon, D. R., Szedmak, S. & Shawe-Taylor, J. Canonical correlation analysis: an overview with application to learning methods. Neural Comput. 16, 2639–2664 (2004).PubMed 
    MATH 

    Google Scholar  More

  • in

    Biodiversity faces its make-or-break year, and research will be key

    EDITORIAL
    19 January 2022

    Biodiversity faces its make-or-break year, and research will be key

    A new action plan to halt biodiversity loss needs scientific specialists to work with those who study how governments function.

    Twitter

    Facebook

    Email

    Download PDF

    Targeted measures can help to stop extinctions, including of Père David’s deer (Elaphurus davidianus), but conserving biodiversity will also require combating climate change, cutting pollution and enhancing sustainable food systems.Credit: Staffan Widstrand/Wild Wonders of China/Nature Picture Library

    Biodiversity is being lost at a rate not seen since the last mass extinction. But the United Nations decade-old plan to slow down and eventually stop the decline of species and ecosystems by 2020 has failed. Most of the plan’s 20 targets — known as the Aichi Biodiversity Targets — have not been met.The Aichi targets are part of an international agreement called the UN Convention on Biological Diversity, and member states are now finalizing replacements for them. Currently referred to as the post-2020 global biodiversity framework (GBF), the new targets are expected to be agreed this summer at the second part of the convention’s Conference of the Parties (COP15) in Kunming, China. The meeting was due to be held in May, but is likely to be delayed by a few months. Finalizing the framework will be down to government representatives working with the world’s leading biodiversity specialists. But input from social-science researchers, especially those who study how organizations and governments work, would improve its chances of success.A draft of the GBF was published last July. It aims to slow down the rate of biodiversity loss by 2030. And by 2050, biodiversity will be “valued, conserved, restored and wisely used, maintaining ecosystem services, sustaining a healthy planet and delivering benefits essential for all people”. The plan comprises 4 broad goals and 21 associated targets. The headline targets include conserving 30% of land and sea areas by 2030, and reducing government subsidies that harm biodiversity by US$500 billion per year. Overall, the goals and targets are designed to tackle each of the main contributors to biodiversity loss, which include agriculture and food systems, climate change, invasive species, pollution and unsustainable production and consumption.
    Fewer than 20 extinctions a year: does the world need a single target for biodiversity?
    The biodiversity convention’s science advisory body is reviewing the GBF and helping governments to decide how the targets are to be monitored. But researchers and policymakers have been writing biodiversity action plans since the 1990s, and most of these strategies have failed to make a lasting impact on two of the three key demands: that global biodiversity be conserved and that natural resources be used sustainably.Some of these failures are to do with governance, which is why it is important to involve not just researchers in the biological sciences, but also people who study organizations and how governments work. This knowledge, when allied to conservation science, will help policymakers to obtain a fuller picture of both the science gaps and the organizational challenges in implementing biodiversity plans.The GBF is a comprehensive plan. But success will require systemic change across public policy. That is both a strength and a weakness. If systemic change can be implemented, it will lead to real change. But if it cannot, there’s no plan B. This has led some researchers to argue that one target or number should be prioritized, and defined in a way that is clear to the public and to policymakers. It would be biodiversity’s equivalent of the 2 °C climate target. The researchers’ “rallying point for policy action and agreements” is to keep species extinction to well below 20 per year across all major groups (M. D. A. Rounsevell et al. Science 368, 1193–1195; 2020). Such focus does yield results. A study published in Conservation Letters found a high probability that targeted action has prevented 21–32 bird and 7–16 mammal extinctions since 1993 (F. C. Bolam et al. Conserv. Lett. 14, e12762; 2021). Extinction rates would have been around three to four times greater without conservation action, the researchers found.But not all agree that just one target should be given priority. A group of more than 50 biodiversity researchers from 23 countries point out in a policy report this week (see go.nature.com/3fv8oiv) that data on species are distributed unequally: 10, mostly high-income, countries account for 82% of records.
    The United Nations must get its new biodiversity targets right
    The researchers also modelled how different scenarios would affect the GBF’s 21 targets. They found that achieving the targets would require action in all of the target areas — not just a few. Focusing strongly on just one or two targets — such as expanding protected areas — will have, at best, a modest impact on achieving the UN convention’s goals and targets.The difficulty in getting governments to adopt such an integrated approach is that they (as well as non-governmental organizations and businesses) tend to tackle sustainability challenges piecemeal. Actions from last November’s climate COP in Glasgow, UK, will be implemented separately from those decided at the biodiversity COP because, in most countries, different government departments deal with climate change and biodiversity.The science advisers for the biodiversity convention will meet in Geneva, Switzerland, in March to finalize their advice. They are not advocating reform of how governments organize themselves to implement policies in sustainable development — partly (and rightly) because this is generally beyond their fields of expertise. But it’s not too late to consult those with the relevant knowledge.In the past, the UN has commissioned social scientists, for example in the UN Intellectual History Project, a series of 17 studies summarizing the experience of UN agencies spanning gender equality, diplomacy, development, trade and official statistics. However, this work, which ended in 2010, did not assess what has and hasn’t worked in science and environmental policy. Unless these perspectives are incorporated into biodiversity-research advice, any future plans risk going the way of their predecessors.

    Nature 601, 298 (2022)
    doi: https://doi.org/10.1038/d41586-022-00110-w

    Related Articles

    China takes centre stage in global biodiversity push

    Fewer than 20 extinctions a year: does the world need a single target for biodiversity?

    The biodiversity leader who is fighting for nature amid a pandemic

    The United Nations must get its new biodiversity targets right

    Subjects

    Biodiversity

    Climate change

    Economics

    Policy

    Latest on:

    Biodiversity

    Wind power versus wildlife: root mitigation in evidence
    Correspondence 11 JAN 22

    Two million species catalogued by 500 experts
    Correspondence 11 JAN 22

    Landmark Colombian bird study repeated to right colonial-era wrongs
    News 11 JAN 22

    Climate change

    Countries should boycott Brazil over export-driven deforestation
    Correspondence 18 JAN 22

    Put defence money into planetary emergencies, urge Nobel winners
    Correspondence 18 JAN 22

    Message to mayors: cities need nature
    World View 17 JAN 22

    Economics

    Tackling the crisis of care for older people: lessons from India and Japan
    Outlook 19 JAN 22

    Extreme rainfall slows the global economy
    News & Views 12 JAN 22

    There is no silver bullet against climate change
    Correspondence 02 NOV 21

    Jobs

    Molecular Biologist/Plant Pathologist

    Forest Research
    Farnham, United Kingdom

    Research Fellow

    The University of Warwick
    Coventry, United Kingdom

    Scientist I / Scientist II

    OMass Technologies Limited
    Oxford, United Kingdom

    MSCA COFUND Doctoral Programme “UNIPhD – Training the next-generation talents”

    University of Padova (UNIPD)
    Padua, Italy More

  • in

    Experimental inoculation trial to determine the effects of temperature and humidity on White-nose Syndrome in hibernating bats

    All methods in this study were approved by the Institutional Animal Care and Use Committee at Texas Tech University (protocol 18032-12). All procedures were performed in accordance with relevant guidelines in the manuscript and the ARRIVE (Animal Research: Reporting of In Vivo Experiments) guidelines (https://arriveguidelines.org/).Experimental design for testing effects of temperature and humidity on Pd infection severity on Perimyotis subflavus
    We randomly assigned bats to seven environmental chambers (Caron, Model 7000-33-1, Marietta, Ohio, USA) in a blocked experimental design, controlling temperature and humidity in each chamber (Fig. 1). In each environmental chamber, we divided bats into two cages (23 × 38 × 50 cm) constructed from mesh fabric (Part FMLF, Seattle Fabrics, Inc., Seattle, Washington, USA), PVC pipe, and plastic sheeting. We stratified random assignment to ensure even distribution of initial body mass and sex across microclimate treatments. In addition to the seven treatments with fixed temperature and humidity conditions, we had two treatments that allowed bats to freely move among temperature or humidity conditions (Fig. 1). One group of bats (n = 14) was free to move among three chambers with a common temperature (8 °C) but different humidity (water vapor pressure deficit (VPD) = 0.05 kPa, 0.10 kPa, or 0.15 kPa, corresponding to 95, 90, and 85% relative humidity (RH))36. A second group of bats (n = 14) was free to move among three chambers with a common VPD condition (0.10 kPa, medium humidity) but different temperatures (5, 8, or 11 °C) (Fig. 1). Because our research questions were focused on comparing the effect of temperature and humidity conditions on disease severity, we did not include sham-inoculated control animals in the experiment. We made this decision to reduce the total number of animals used in the experiment and to maximize replication to test the effects of temperature and humidity on disease.Figure 1Schematic of the experimental design and sample sizes with 7 environmental chambers with fixed temperature and humidity conditions and two sets of connected chambers allowing bats to behaviorally select temperature (left) or humidity conditions (bottom) for the infection trial on tri-colored bats (Perimyotis subflavus). Water loss conditions were based on water vapor pressure deficit (VPD) levels set to 0.05 kPA to produce low potential evaporative water loss (pEWL) for high humidity, 0.10 kPa for medium pEWL and humidity, or 0.15 kPA for high pEWL and low humidity. Numbers are sample sizes of bats assigned to separate cages within each chamber. Bats in the low temperature and high humidity chamber were combined into a single cage after a camera failed at the start of the experiment (top right).Full size imageWe inoculated each bat by spreading 20 µL of Pd solution (5 × 105 conidia µL−1) evenly across both wings, following established protocols8,9,32,37; treatments were conducted blind without knowledge of which bat was being assigned to what group and bats were inoculated in no particular order to reduce the confounding influence on the order of treatment. We used a Pd strain collected by Karen J. Vanderwolf at Trent University from naturally infected Myotis lucifugus. We cultured Pd on Sabouraud Dextrose Agar with chloramphenicol and gentamicin (SabDex) (Part L96359, Fisher Scientific, Houston, Texas, USA) and incubated subcultured plates at 10 °C for 60 days to allow the formation of conidia. We then harvested conidia by flooding plates with phosphate buffered saline solution containing 0.5% Tween20 (PBST). Conidia were resuspended in PBST, enumerated, and diluted to the inoculum concentration8.Microclimate treatment conditionsWe used three temperatures 5, 8, or 11 °C to represent a range of roosting temperatures of P. subflavus in natural hibernacula24,29. We set humidity in environmental chambers to achieve specific levels of water vapor pressure deficit (VPD) between the surface of the bat and the environment because relative humidity varies by temperature36. Higher VPD corresponds to drier air resulting in higher potential evaporative water loss (pEWL). We used three levels of VPD: 0.05, 0.10, or 0.15 kPa corresponding to low pEWL (high humidity), medium pEWL (medium humidity), and high pEWL (low humidity) levels (Fig. 1). We verified the ambient temperature and relative humidity in each chamber at 10-min intervals (Hobo Model U23-001, Onset Computer Corporation, Bourne, Massachussetts, USA). For bats in the connected chambers that could behaviorally select their temperature and humidity conditions, we quantified the number of days bats spent in each condition38.Animal handling and data collectionWe used 98 (42 females, 56 males) tricolored bats collected on 10 December 2018 from culverts in Mississippi and transported directly to Texas Tech University39. We took morphometric measurements (body mass ± 0.1 g, forearm length ± 0.1 mm) and used quantitative magnetic resonance (QMR; Echo-MRI-B, Echo Medical Systems, Houston, Texas, USA) to determine pre-hibernation fat at the start of the experiment39,40. As an indicator of pre-hibernation stress, we collected a fur sample from the dorsal intrascapular region to quantify fur cortisol concentration with a commercial ELISA kit, following the manufacturer’s protocol (Arbor Assays, Michigan, USA) (see Supplemental Methods). Fur is moulted once per year in the late summer period41 and therefore fur cortisol reflects the level of circulating cortisol during the period of fur growth prior to hibernation. We attached a uniquely marked, modified datalogger42 (DS1925L iButton, Maxim Integrated, San Jose, California, USA) to the back of each bat using ostomy cement to record skin temperature39. Prior to inoculation, we swabbed bats with a sterile polyester swab (Fisherbrand synthetic tipped applicators 23-400-116) five times on forearm and five times on muzzle to determine if any bats were naturally infected with Pd at time of collection. Swabs were stored in RNAlater at  − 20 °C until testing using quantitative polymerase chain reaction (qPCR) at Northern Arizona University43.During the experiment, we provided ad libitum drinking water in each cage but did not provide food. We secured a motion-activated infrared camera (Model HT5940T, Speco Technologies, New York, New York, USA) above each cage to monitor bats throughout the experiment. Because one camera failed at the start of the experiment, we combined bats in that treatment chamber into a single cage (Fig. 1) and replicated this disturbance among all chambers. We monitored bats without disturbance by reviewing video recordings daily. Three bats died of unknown cause before the end of the experiment and were removed from analyses.After 83 days of hibernation, we terminated the experiment and bats were removed from cages and processed to determine body condition using QMR39. We took respirometry measurements on a subset of animals38, and swabbed for Pd as described above. We photographed the left ventral wing using ultraviolet (UV) transillumination (368-nm wavelength and 2-s exposure) to detect and measure florescence associated with Pd infection37,44. For histology, we removed the wing section from the fifth digit and the body and rolled wing tissue around dental wax dowels and 10% neutral buffered formalin. We collected a 90–110 µL blood sample in lithium-heparin-treated capillary tubes for immediate analysis of blood chemistry with a handheld analyzer (i-STAT1 Vet Scan, Abaxis, Union City, California, USA). Using an EC8+ cartridge, we measured sodium, potassium, chloride, anion gap, glucose, BUN (urea nitrogen), hematocrit, hemoglobin, pH, pCO2, TCO2, HCO3, and base excess (Table S1). We quantified arousals from torpor as reported by McGuire et al.39. All bats were handled and euthanized under Animal Care and Use Committee permit 18032-12 at Texas Tech University.Infection and disease metricsWe used several metrics to determine pathogen and disease presence and severity37: presence and amount of the pathogen, Pd, on a bat were determined by qPCR43, and presence of the disease, WNS, was determined via detection of orange-yellow florescence under UV light characteristic of Pd infection44 and histological presence of characteristic lesions and pustules with fungal hyphae45,46. Three types of cutaneous infection were described histologically, including characteristic cupping erosions with fungal hyphae, neutrophilic pustules with fungal hyphae, and fungal hyphae in the stratum corneum with dermal necrosis. Any bats with any of these three conditions noted were scored as WNS positive by histology. Presence and quantity of DNA of Pd was tested by qPCR at Northern Arizona University. All samples were run in duplicate and considered positive if at least one run was positive below a cycle threshold (Ct) of 40 and quantified using a quantification curve from serial dilutions (nanograms of Pd using the equation load = 10((22.049-Ct value)/3.34789), r2 = 0.986)47. Load values were averaged across multiple runs and then converted to attograms by multiplying loads in nanograms by 109.Statistical analysesWe used three different response variables (Pd prevalence, Pd loads, and WNS prevalence by histology) to determine whether infection status varied by microclimate treatment conditions. Low sample sizes of positive infection status by UV detection (n = 4) precluded use in statistical analyses (Table 1). We used generalized linear models with binomial distribution for analyses of Pd prevalence and WNS prevalence and a linear mixed effects model with Gaussian errors for Pd loads. Although the experiment was designed with replication at the cage level to account for cage effects, we were unable to include cage as a random effect because of the low numbers of bats that had signs of Pd or WNS infection. We analyzed whether infection status (i.e., Pd prevalence, Pd load, or WNS prevalence) varied by sex and cortisol separately from an a priori candidate model set (Table 2) to cope efficiently with small sample sizes. We first asked whether infection response varied by sex to determine if bats could be pooled in subsequent analyses. We analyzed separately whether infection response varied by pre-hibernation cortisol at the start of the experiment on the subset of animals for which we had cortisol measurements (n = 83). We then used an information-theoretic approach comparing a candidate set of models with Akaike Information Criterion (AIC)48 using initial fat mass as an individual covariate and temperature and humidity treatment conditions as categorical treatment groups to assess the effect of microclimate on infection response (Table 2). Bats behaviorally selecting their temperature and humidity conditions were assigned to a temperature or humidity treatment level if a bat spent  > 89% of captive days at that condition or was otherwise placed in an ‘inconstant condition’ treatment group. For WNS prevalence, we used the bias reduction method implemented in package brglm49 to deal with complete separation present in the data (in some treatments all bats were scored as negative for WNS) (Table 1; Fig. 2).Table 1 Signs of Pd infection or WNS disease for tri-colored bats (Perimyotis subflavus) exposed to different temperature and humidity regimes.Full size tableTable 2 Model selection results for model comparisons of humidity and temperature and pre-hibernation fat mass on Pd prevalence, Pd load, and WNS prevalence.Full size tableFigure 2Signs of Pseudogymnoascus destructans (Pd) infection or white-nose syndrome (WNS) disease for tri-colored bats (Perimyotis subflavus) exposed to different temperature and humidity regimes. (A) Fraction of bats with Pd detected by qPCR; (B) Fraction of bats with signs of WNS disease by histology, and (C) Mean quantity of Pd on bats at the end of the experiment. There was no statistical support for differences between temperature or humidity treatments for any response metrics. Points are estimated means and vertical lines show binomial standard error for prevalence and standard errors for Pd load.Full size imageBecause this was the first captive hibernation experiment with P. subflavus, we investigated the effects of temperature and humidity on the hibernation physiology of the species38,39 and how physiological markers (e.g., blood chemistry) may be associated with disease. To determine if physiological indicators were related to infection status at the end of the experiment, we compared total number of torpor arousal bouts during the experiment and 13 different blood chemistry metrics from blood samples taken at the end of the experiment and used t-test comparisons (at α = 0.05) for each metric between Pd/WNS positive and negative bats. We designated bats as Pd/WNS positive if a bat tested positive for either Pd or WNS by qPCR, UV, or histology. We used Program R version 3.6.2 to conduct all analyses.Experimental design for testing effects of temperature and humidity on Pd growth on substratesWe used five environmental chambers (CARON, Model 7000-33-1, Marietta, Ohio, USA) to test for the effects of temperature and humidity on fungal growth on natural and artificial substrates (Fig. S1). Our experimental design comprised a reduced temperature series and humidity gradient than what we used for the experiment on bats. In the humidity gradient, temperature was held constant at 8 °C, with 85%, 90%, and 95% RH representing our low, medium, and high humidity treatments, respectively. In the temperature series, vapor pressure deficit (VPD) was held constant across the low (5 °C), medium (8 °C), and high (11 °C) temperatures (VPD = nominally 0.01 kPa, range (0.105–0.107). The chamber set to 8 °C and 90% humidity (VPD = 0.107 kPa) was common to both series.Media plate inoculation and fungal growth measurementWe constructed modified plate lids to prevent contamination while allowing humidity to equilibrate across the plate lid. We drilled 14 equidistant holes (5.5 mm diameter) into each plate lid and hot glued a piece of circular filter paper to the top of the lid. Lids were then disinfected thoroughly with a hydrogen peroxide wipe before being placed in a disinfected, sealed storage container.We prepared Pd inoculum as described above for the infection trial on bats. We inoculated 30 SabDex plates with 100 µL of inoculum at a concentration of 20 conidia µL−1 by serial dilution with a starting concentration of 2.0 × 104 conidia µL−1 diluted four times by a factor of 10. We used sterile, individually wrapped 1-µL plastic inoculation loops to spread the inoculum evenly across the surface of the plates, added the modified plate lids, and immediately transferred plates into environmental chambers. We included six replicate plates in each of the five microclimate conditions.We took weekly digital photographs (Nikon, Model 26524, Tokyo, Japan) of each plate for the 5-week duration of the experiment (Fig. 3A). Our camera was mounted on a tripod to ensure consistent placement of plates relative to the camera. Each photo included a ruler, which was used to calibrate measurements made in ImageJ (Version 2.0.0-rc-69/1.52p, National Institutes of Health, Bethesda, Maryland, USA). One observer made all measurements for consistency. We used the freehand selection tool to trace the boundary of each fungal colony using a drawing tablet (Wacom, Model CTL-490, Kazo, Saitama, Japan). From these selections, we obtained the total surface area growth as the sum of all area selection (in cm2).Figure 3Examples demonstrate the process of measuring and estimating fungal growth of Pseudogymnoascus destructans (Pd) on media plates in temperature and humidity treatment conditions. (A) Examples of fungal growth on media plates measured at days 7, 14, 21, 28, and 34 from two of the treatment conditions (11 °C, 92% RH and 5 °C, 88% RH). (B) Examples of estimating maximum growth rate and latency variables from fungal growth measurements in panel A. We fit a sigmoidal curve to describe fungal growth (thick solid black line) to estimate the inflection point of the curve (vertical solid line). We calculated the slope (solid red line) at the inflection point of the curve to estimate maximum growth rate, and the days until total growth area reached 2.5 cm2 (dashed red lines) as an estimate of latency.Full size imageWe modelled the growth of Pd on each plate as a sigmoidal curve (Fig. 3B), which we fit using the SSlogis and nls functions in Program R v. 3.6.350. The model fitting function provides an estimate of the inflection point of the curve, and we calculated the slope at the inflection point to estimate the maximum growth rate. We also estimated the latency to rapid fungal growth on the plates by determining the date at which the total area of fungus on the plate reached 2.5 cm2 as an arbitrary threshold.We also quantified growth of individual colonies. To avoid biasing growth rate estimates, we excluded colonies that intercepted another colony by choosing independent colonies at the final time point and tracking them backwards through time. If there were fewer than 10 independent colonies at the final time point, we added additional unimpeded colonies with each earlier time point until the total number of colonies reached 10. We modelled growth of individual colonies following the same procedure as for total area of growth on the plate, with an arbitrary threshold of 0.05 cm2 for latency calculations. We used linear mixed models to test for the effects of temperature and humidity on maximum growth rate or latency, including plate as a random factor to account for measuring multiple colonies per plate.Rock inoculation and fungal growth measurementTo evaluate fungal growth and persistence on a natural substrate, we inoculated pieces of sandstone flagstone. We etched a 4 × 6 sampling grid, composed of 5 × 5 cm squares, onto the surface of each sandstone rock (Texas Rock and Flagstone, Lubbock, Texas, USA), where each square served as a sampling unit (Fig. S2). Each row represented a time series for a single replicate, while each column was composed of replicates for the respective time point. Rocks were then autoclaved at 121 °C for 40 min and stored individually in a disinfected, sealed container until inoculation. At the time of inoculation, we evenly spread 200 µL of inoculum (2.5 × 104 conidia µL−1) across each sampling square and immediately transferred the rock to an environmental chamber.We measured fungal growth at days 0, 14, 28, and 56. We used a sterile cotton swab to collect fungal DNA from each sampling square. Swabs were moistened with RNAlater and rolled horizontally, vertically, and diagonally across the surface of the sampling square to ensure contact with the total surface area. One researcher collected all swabs to maximize consistency among swabs collected throughout the experiment. Swabs were placed in RNAlater and stored at − 20 °C until shipped to Northern Arizona University for qPCR analysis43. We quantified fungal loads for each swab sample from qPCR using the quantification curve provided above and normalized fungal loads to the value at day zero for each rock respectively. We then used linear models to test for effects of temperature and humidity on changes in fungal load (log transformed) over time.To evaluate viability of Pd, we swabbed the entire inoculated surface of each rock at the end of the experiment and vortexed the swabs in RNAlater for one minute to release fungal DNA from the swab. We then applied 100 µL of RNAlater fungal solution from each rock to a respective SabDex media plate, using a sterile inoculation loop. After 2 weeks of incubation at 11 °C and 92% RH, we visually assessed plates for presence of fungal growth to determine viability of Pd collected from rocks at the end of the growth experiment. More