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    Agricultural management and pesticide use reduce the functioning of beneficial plant symbionts

    Foley, J. A. et al. Solutions for a cultivated planet. Nature 478, 337–342 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Tilman, D., Balzer, C., Hill, J. & Befort, B. L. Global food demand and the sustainable intensification of agriculture. Proc. Natl Acad. Sci. USA 108, 20260–20264 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bender, S. F., Wagg, C. & van der Heijden, M. G. A. An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends Ecol. Evol. 31, 440–452 (2016).PubMed 
    Article 

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

    Google Scholar 
    Smith, S. & Read, D. Mycorrhizal Symbiosis (Elsevier, 2008).Soudzilovskaia, N. A. et al. Global patterns of plant root colonization intensity by mycorrhizal fungi explained by climate and soil chemistry. Glob. Ecol. Biogeogr. 24, 371–382 (2015).Article 

    Google Scholar 
    Van Der Heijden, M. G. A., Bardgett, R. D. & Van Straalen, N. M. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 11, 296–310 (2008).PubMed 
    Article 

    Google Scholar 
    Bennett, E. M., Carpenter, S. R. & Caraco, N. F. Human impact on erodable phosphorus and eutrophication: a global perspective. Bioscience 51, 227–234 (2001).Article 

    Google Scholar 
    Smith, V. H. & Schindler, D. W. Eutrophication science: where do we go from here? Trends Ecol. Evol. 24, 201–207 (2009).PubMed 
    Article 

    Google Scholar 
    Rillig, M. C. & Mummey, D. L. Mycorrhizas and soil structure. New Phytol. 171, 41–53 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bender, S. F. & van der Heijden, M. G. A. Soil biota enhance agricultural sustainability by improving crop yield, nutrient uptake and reducing nitrogen leaching losses. J. Appl. Ecol. 52, 228–239 (2015).CAS 
    Article 

    Google Scholar 
    Rodriguez, A. & Sanders, I. R. The role of community and population ecology in applying mycorrhizal fungi for improved food security. ISME J. 9, 1053–1061 (2015).PubMed 
    Article 

    Google Scholar 
    Oviatt, P. & Rillig, M. C. Mycorrhizal technologies for an agriculture of the middle. Plants, People, Planet. https://doi.org/10.1002/ppp3.10177 (2020).Ryan, M. H. & Graham, J. H. Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops. New Phytol. 220, 1092–1107 (2018).PubMed 
    Article 

    Google Scholar 
    Rillig, M. C. et al. Why farmers should manage the arbuscular mycorrhizal symbiosis. New Phytol. 222, 1171–1175 (2019).PubMed 
    Article 

    Google Scholar 
    Zhang, S., Lehmann, A., Zheng, W., You, Z. & Rillig, M. C. Arbuscular mycorrhizal fungi increase grain yields: a meta-analysis. New Phytol. 222, 543–555 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Thirkell, T. J., Charters, M. D., Elliott, A. J., Sait, S. M. & Field, K. J. Are mycorrhizal fungi our sustainable saviours? Considerations for achieving food security. J. Ecol. 105, 921–929 (2017).CAS 
    Article 

    Google Scholar 
    Davison, J. et al. Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349, 970–973 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Pringle, A. & Bever, J. D. Analogous effects of arbuscular mycorrhizal fungi in the laboratory and a North Carolina field. New Phytol. 180, 162–175 (2008).PubMed 
    Article 

    Google Scholar 
    Francis, R. & Read, D. J. Mutualism and antagonism in the mycorrhizal symbiosis, with special reference to impacts on plant community structure. Can. J. Bot. 73, 1301–1309 (1995).Article 

    Google Scholar 
    Thirkell, T. J., Pastok, D. & Field, K. J. Carbon for nutrient exchange between arbuscular mycorrhizal fungi and wheat varies according to cultivar and changes in atmospheric carbon dioxide concentration. Glob. Change Biol. 26, 1725–1738 (2020).Article 

    Google Scholar 
    Lehmann, A., Barto, E. K., Powell, J. R. & Rillig, M. C. Mycorrhizal responsiveness trends in annual crop plants and their wild relatives—a meta-analysis on studies from 1981 to 2010. Plant Soil 355, 231–250 (2012).CAS 
    Article 

    Google Scholar 
    Martín-Robles, N. et al. Impacts of domestication on the arbuscular mycorrhizal symbiosis of 27 crop species. New Phytol. 218, 322–334 (2018).PubMed 
    Article 

    Google Scholar 
    Leake, J. et al. Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can. J. Bot. 82, 1016–1045 (2004).Article 

    Google Scholar 
    Oehl, F. et al. Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of central Europe. Appl. Environ. Microbiol. 69, 2816–2824 (2003).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Xiang, D. et al. Land use influences arbuscular mycorrhizal fungal communities in the farming-pastoral ecotone of northern China. New Phytol. 204, 968–978 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bainard, L. D. et al. Plant communities and soil properties mediate agricultural land use impacts on arbuscular mycorrhizal fungi in the Mixed Prairie ecoregion of the North American Great Plains. Agric. Ecosyst. Environ. 249, 187–195 (2017).Article 

    Google Scholar 
    Helgason, T., Daniell, T. J., Husband, R., Fitter, A. H. & Young, J. P. W. Ploughing up the wood-wide web? Nature 394, 431–431 (1998).CAS 
    PubMed 
    Article 

    Google Scholar 
    van der Heijden, M. G. A. et al. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 69–72 (1998).Article 
    CAS 

    Google Scholar 
    Vogelsang, K. M., Reynolds, H. L. & Bever, J. D. Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol. 172, 554–562 (2006).PubMed 
    Article 

    Google Scholar 
    Scheublin, T. R., Ridgway, K. P., Young, J. P. W. & van der Heijden, M. G. A. Nonlegumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. Appl. Environ. Microbiol. 70, 6240–6246 (2004).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Oehl, F. et al. Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol. Biochem. 42, 724–738 (2010).CAS 
    Article 

    Google Scholar 
    De Vries, F. T. et al. Soil food web properties explain ecosystem services across European land use systems. Proc. Natl Acad. Sci. USA 110, 14296–14301 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Verbruggen, E., Xiang, D., Chen, B., Xu, T. & Rillig, M. C. Mycorrhizal fungi associated with high soil N:P ratios are more likely to be lost upon conversion from grasslands to arable agriculture. Soil Biol. Biochem. 86, 1–4 (2015).CAS 
    Article 

    Google Scholar 
    Balami, S., Vašutová, M., Godbold, D., Kotas, P. & Cudlín, P. Soil fungal communities across land use types. iForest 13, 548–558 (2020).Article 

    Google Scholar 
    Öpik, M., Mari, M., Liira, J. & Zobel, M. Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J. Ecol. 94, 778–790 (2006).Article 

    Google Scholar 
    Jansa, J. et al. Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12, 225–234 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    van Groenigen, K. J. et al. Abundance, production and stabilization of microbial biomass under conventional and reduced tillage. Soil Biol. Biochem. 42, 48–55 (2010).Article 
    CAS 

    Google Scholar 
    Sallach, J. B., Thirkell, T. J., Field, K. J. & Carter, L. J. The emerging threat of human‐use antifungals in sustainable and circular agriculture schemes. Plants People Planet 3, 685–693 (2021).Article 

    Google Scholar 
    Meyer, A. et al. Different land use intensities in grassland ecosystems drive ecology of microbial communities involved in nitrogen turnover in soil. PLoS ONE 8, e73536 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Tsiafouli, M. A. et al. Intensive agriculture reduces soil biodiversity across Europe. Glob. Change Biol. 21, 973–985 (2015).Article 

    Google Scholar 
    Tardy, V. et al. Shifts in microbial diversity through land use intensity as drivers of carbon mineralization in soil. Soil Biol. Biochem. 90, 204–213 (2015).CAS 
    Article 

    Google Scholar 
    Sawers, R. J. H. et al. Phosphorus acquisition efficiency in arbuscular mycorrhizal maize is correlated with the abundance of root-external hyphae and the accumulation of transcripts encoding PHT1 phosphate transporters. New Phytol. 214, 632–643 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Svenningsen, N. B. et al. Suppression of the activity of arbuscular mycorrhizal fungi by the soil microbiota. ISME J. 12, 1296–1307 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Schweiger, P. F., Thingstrup, I. & Jakobsen, I. Comparison of two test systems for measuring plant phosphorus uptake via arbuscular mycorrhizal fungi. Mycorrhiza 8, 207–213 (1999).CAS 
    Article 

    Google Scholar 
    Emmett, B. D., Lévesque-Tremblay, V. & Harrison, M. J. Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi. ISME J. 15, 2276–2288 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jiang, F., Zhang, L., Zhou, J., George, T. S. & Feng, G. Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae. New Phytol. 230, 304–315 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Thonar, C., Schnepf, A., Frossard, E., Roose, T. & Jansa, J. Traits related to differences in function among three arbuscular mycorrhizal fungi. Plant Soil 339, 231–245 (2011).CAS 
    Article 

    Google Scholar 
    Cavagnaro, T. R., Smith, F. A., Smith, S. E. & Jakobsen, I. Functional diversity in arbuscular mycorrhizas: exploitation of soil patches with different phosphate enrichment differs among fungal species. Plant Cell Environ. 28, 642–650 (2005).CAS 
    Article 

    Google Scholar 
    Jakobsen, I., Gazey, C. & Abbott, L. K. Phosphate transport by communities of arbuscular mycorrhizal fungi in intact soil cores. New Phytol. 149, 95–103 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Pearson, J. N. & Jakobsen, I. The relative contribution of hyphae and roots to phosphorus uptake by arbuscular mycorrhizal plants, measured by dual labelling with 32P and 33P. New Phytol. 124, 489–494 (1993).CAS 
    Article 

    Google Scholar 
    Nagy, R., Drissner, D., Amrhein, N., Jakobsen, I. & Bucher, M. Erratum: mycorrhizal phosphate uptake pathway in tomato is phosphorus-repressible and transcriptionally regulated. New Phytol. 184, 1029 (2009).Article 

    Google Scholar 
    Smith, S. E., Jakobsen, I., Grønlund, M. & Smith, F. A. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol. 156, 1050–1057 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Williams, A., Manoharan, L., Rosenstock, N. P., Olsson, P. A. & Hedlund, K. Long-term agricultural fertilization alters arbuscular mycorrhizal fungal community composition and barley (Hordeum vulgare) mycorrhizal carbon and phosphorus exchange. New Phytol. 213, 874–885 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Koerselman, W. & Meuleman, A. F. M. The Vegetation N:P Ratio: a new tool to detect the nature of nutrient limitation. J. Appl. Ecol. 33, 1441 (1996).Article 

    Google Scholar 
    Van Aarle, I. M., Olsson, P. A. & Söderström, B. Arbuscular mycorrhizal fungi respond to the substrate pH of their extraradical mycelium by altered growth and root colonization. New Phytol. 155, 173–182 (2002).PubMed 
    Article 

    Google Scholar 
    Staddon, P. L. et al. Mycorrhizal fungal abundance is affected by long-term climatic manipulations in the field. Glob. Change Biol. 9, 186–194 (2003).Article 

    Google Scholar 
    Weber, S. E. et al. Responses of arbuscular mycorrhizal fungi to multiple coinciding global change drivers. Fungal Ecol. 40, 62–71 (2019).Article 

    Google Scholar 
    Peat, H. J. & Fitter, A. H. The distribution of arbuscular mycorrhizas in the British flora. New Phytol. 125, 845–854 (1993).CAS 
    PubMed 
    Article 

    Google Scholar 
    Cruz-Paredes, C. et al. Suppression of arbuscular mycorrhizal fungal activity in a diverse collection of non-cultivated soils. FEMS Microbiol. Ecol. 95, fiz020 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Jansa, J., Erb, A., Oberholzer, H.-R., Šmilauer, P. & Egli, S. Soil and geography are more important determinants of indigenous arbuscular mycorrhizal communities than management practices in Swiss agricultural soils. Mol. Ecol. 23, 2118–2135 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Davison, J. et al. Temperature and pH define the realised niche space of arbuscular mycorrhizal fungi. New Phytol. 231, 763–776 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Yang, H. et al. Changes in soil organic carbon, total nitrogen, and abundance of arbuscular mycorrhizal fungi along a large-scale aridity gradient. Catena 87, 70–77 (2011).CAS 
    Article 

    Google Scholar 
    Riedo, J. et al. Widespread occurrence of pesticides in organically managed agricultural soils—the ghost of a conventional agricultural past? Environ. Sci. Technol. https://doi.org/10.1021/acs.est.0c06405 (2021).Pánková, H., Dostálek, T., Vazačová, K. & Münzbergová, Z. Slow recovery of arbuscular mycorrhizal fungi and plant community after fungicide application: an eight-year experiment. J. Veg. Sci. 29, 695–703 (2018).Article 

    Google Scholar 
    Ipsilantis, I., Samourelis, C. & Karpouzas, D. G. The impact of biological pesticides on arbuscular mycorrhizal fungi. Soil Biol. Biochem. https://doi.org/10.1016/j.soilbio.2011.08.007 (2012).Buysens, C., Dupré de Boulois, H. & Declerck, S. Do fungicides used to control Rhizoctonia solani impact the non-target arbuscular mycorrhizal fungus Rhizophagus irregularis? Mycorrhiza. https://doi.org/10.1007/s00572-014-0610-7 (2015).Lekberg, Y., Wagner, V., Rummel, A., McLeod, M. & Ramsey, P. W. Strong indirect herbicide effects on mycorrhizal associations through plant community shifts and secondary invasions. Ecol. Appl. 27, 2359–2368 (2017).PubMed 
    Article 

    Google Scholar 
    Hage-Ahmed, K., Rosner, K. & Steinkellner, S. Arbuscular mycorrhizal fungi and their response to pesticides. Pest Manag. Sci. 75, 583–590 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kjøller, R. & Rosendahl, S. Effects of fungicides on arbuscular mycorrhizal fungi: differential responses in alkaline phosphatase activity of external and internal hyphae. Biol. Fertil. Soils 31, 361–365 (2000).Article 

    Google Scholar 
    Gange, A. C., Brown, V. K. & Sinclair, G. S. Vesicular-arbuscular mycorrhizal fungi: a determinant of plant community structure in early succession. Funct. Ecol. 7, 616 (1993).Article 

    Google Scholar 
    Hartnett, D. C. & Wilson, G. W. T. The role of mycorrhizas in plant community structure and dynamics: lessons from grasslands. Plant Soil 244, 319–331 (2002).CAS 
    Article 

    Google Scholar 
    Guzman, A. et al. Crop diversity enriches arbuscular mycorrhizal fungal communities in an intensive agricultural landscape. New Phytol. https://doi.org/10.1111/nph.17306 (2021).LUCAS 2018 Technical Reference Document C3 Classification (Land Cover and Land Use) (Eurostat, 2018).Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1‐km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).Article 

    Google Scholar 
    Trabucco, A. & Zomer, R. Global Aridity Index and Potential Evapotranspiration (ET0) Climate Database v.2. figshare https://doi.org/10.6084/m9.figshare.7504448.v3 (2019).García-Palacios, P., Gross, N., Gaitán, J. & Maestre, F. T. Climate mediates the biodiversity-ecosystem stability relationship globally. Proc. Natl Acad. Sci. USA 115, 8400–8405 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Berdugo, M. et al. Global ecosystem thresholds driven by aridity. Science 367, 787–790 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Sinnott, R. W. Virtues of the Haversine. Sky Telescope 68, 158–159 (1984).
    Google Scholar 
    Garland, G. et al. Crop cover is more important than rotational diversity for soil multifunctionality and cereal yields in European cropping systems. Nat. Food 2, 28–37 (2021).Article 

    Google Scholar 
    Boden‐und Substratuntersuchungen zur Düngeberatung (Schweizerische Referenzmethoden der Eidgenössischen Forschungsanstalten, 1996).Berry, D., Mahfoudh, K., Ben, Wagner, M. & Loy, A. Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. Appl. Environ. Microbiol. 77, 7846–7849 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gardes, M., White, T. J., Fortin, J. A., Bruns, T. D. & Taylor, J. W. Identification of indigenous and introduced symbiotic fungi in ectomycorrhizae by amplification of nuclear and mitochondrial ribosomal DNA. Can. J. Bot. 69, 180–190 (1991).CAS 
    Article 

    Google Scholar 
    Gardes, M. & Bruns, T. D. ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol. Ecol. 2, 113–118 (1993).CAS 
    PubMed 
    Article 

    Google Scholar 
    Fiore-Donno, A. M. et al. New barcoded primers for efficient retrieval of cercozoan sequences in high-throughput environmental diversity surveys, with emphasis on worldwide biological soil crusts. Mol. Ecol. Resour. 18, 229–239 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Helfenstein, J., Jegminat, J., McLaren, T. I. & Frossard, E. Soil solution phosphorus turnover: derivation, interpretation, and insights from a global compilation of isotope exchange kinetic studies. Biogeosciences 15, 105–114 (2018).CAS 
    Article 

    Google Scholar 
    Thirkell, T. J. et al. Cultivar‐dependent increases in mycorrhizal nutrient acquisition by barley in response to elevated CO2. Plants People Planet 3, 553–566 (2021).Article 

    Google Scholar 
    Rodushkin, I., Ruth, T. & Huhtasaari, Å. Comparison of two digestion methods for elemental determinations in plant material by ICP techniques. Anal. Chim. Acta 378, 191–200 (1999).CAS 
    Article 

    Google Scholar 
    Ohno, T. & Zibilske, L. M. Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci. Soc. Am. J. 55, 892–895 (1991).CAS 
    Article 

    Google Scholar 
    Frossard, E. et al. in Phosphorus in Action (eds Bünemann, E. et al.) 59–91 (Springer, 2011).Sato, K., Suyama, Y., Saito, M. & Sugawara, K. A new primer for discrimination of arbuscular mycorrhizal fungi with polymerase chain reaction-denature gradient gel electrophoresis. Grassl. Sci. 51, 179–181 (2005).CAS 
    Article 

    Google Scholar 
    Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852–857 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Öpik, M. et al. The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol. 188, 223–241 (2010).PubMed 
    Article 
    CAS 

    Google Scholar 
    Rognes, T., Flouri, T., Nichols, B., Quince, C. & Mahé, F. VSEARCH: a versatile open source tool for metagenomics. PeerJ 4, e2584 (2016).PubMed 
    PubMed Central 
    Article 

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

    Google Scholar 
    McMurdie, P. J. & Holmes, S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    R Core team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).Calcagno, V. glmulti: Model Selection and Multimodel Inference Made Easy. R version 1.0.8 https://CRAN.R-project.org/package=glmulti (2020).Cade, B. S. Model averaging and muddled multimodel inferences. Ecology. https://doi.org/10.1890/14-1639.1 (2015).Barton, K. MuMIn: Multi-Model Inference. R version 1.43.17 https://CRAN.R-project.org/package=MuMIn (2020).Burnham, K. P. & Anderson, D. R. (eds) Model Selection and Multimodel Inference (Springer, 2002).Rosseel, Y. Lavaan: an R package for structural equation modeling. J. Stat. Softw. https://doi.org/10.18637/jss.v048.i02 (2012). More

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    Effects of lime and oxalic acid on antioxidant enzymes and active components of Panax notoginseng under cadmium stress

    Contents of Cd and Ca in Panax notogensing rootsThe Ca content of P. notoginseng roots increased significantly with the increase of lime application rates under the same concentration of oxalic acid sprayed on leaves (Table 2). Compared with no lime application, the Ca content was the highest increased by 212% under 3750 kg hm−2 lime without spraying oxalic acid. The content of Ca slightly increased with the increase of oxalic acid spraying concentrations under the same rate of lime application.Table 2 Effects of foliar spraying of oxalic acid on contents of Cd and Ca in roots of Panax notoginseng under Cd stress.Full size tableThe contents of Cd in roots ranged from 0.22 to 0.70 mg kg−1. The content of 2250 kg hm−2 Cd decreased greatly with the increase of lime application rates under the same spraying concentration of oxalic acid. Compared with the control, the root Cd contents decreased by 68.57% under the application of 2250 kg hm−2 lime and 0.1 mol L−1 oxalic acid spraying. The Cd contents of P. notoginseng roots decreased significantly with the increase of oxalic acid spraying concentrations under application of non-lime and 750 kg hm−2 lime. The root Cd contents decreased at first and then increased with the increase of oxalic acid concentrations under the application of 2250 kg hm−2 lime and 3750 kg hm−2 lime. In addition, the Bivariate analysis showed that the Ca content of P. notoginseng roots was significantly affected by lime (F = 82.84**), and the Cd content of P. notoginseng roots was significantly affected by lime (F = 74.99**) and oxalic acid (F = 7.72*).MDA contents and relative antioxidase activitiesThe content of MDA decreased greatly with the increase of the rates of lime application and oxalic acid spraying concentrations. There was no significant difference in the content of MDA in the roots of P. notoginseng with non-lime and 3750 kg hm−2 lime application. Under 750 kg hm−2, 2250 kg hm−2 lime application, the MDA content with 0.2 mol L−1 oxalic acid spraying concentration treatment decreased by 58.38% and 40.21% comparing with non-oxalic acid spraying application, respectively. The content of MDA (7.57 nmol g−1) was the lowest under 750 kg hm−2 lime application and 0.2 mol L−1 oxalic acid spraying treatment (Fig. 1).Figure 1Effects of foliar spraying of oxalic acid on contents of malondialdehyde in roots of Panax notoginseng under Cd stress. Notes The figure legend showed the spray concentration of oxalic acid (mol L−1), different lowercase letters indicate significant differences between treatments at the same lime application rate (P  Rb1  > R1. The contents of the three saponins had no significant difference with increase of the concentrations of oxalic acid spraying and no application of lime (Table 4).Table 4 Effects of foliar oxalate application on the percentages of three saponins in roots of Panax notoginseng under Cd stress.Full size tableThe contents of R1 with 0.2 mol L−1 oxalic acid spraying was significantly lower than that without oxalic acid spraying and rates of 750 or 3750 kg hm−2 lime application. Under the concentration of 0 or 0.1 mol L−1 oxalic acid spraying, there was no significant difference in contents of R1 with increase of rates of lime application. Under the concentration of 0.2 mol L−1 oxalic acid spraying, the contents of R1 with 3750 kg hm−2 lime was significantly lower 43.84% than that without lime application (Table 4).The contents of Rg1 increased at first and then decreased with the increase of oxalic acid spraying concentrations and 750 kg hm−2 lime application. Under the application rates of 2250 or 3750 kg hm−2 lime, the contents of Rg1 decreased with the increase of oxalic acid spraying concentration. With the same concentration of oxalic acid spraying, the Rg1 content increased at first and then decreased with the increase of lime application rates. Compared with the control, except that the Rg1 content with three concentrations of oxalic acid spraying and 750 kg hm−2 lime was higher than that of the control, the contents of Rg1 in the roots of P. notoginseng under other treatments was lower than that of the control. The Rg1 content was the highest with 750 kg hm−2 lime and 0.1 mol L−1 oxalic acid spraying treatment, which was higher 11.54% than that of the control (Table 4).The contents of Rb1 increased first and then decreased with the increase of oxalic acid spraying concentration and 2250 kg hm−2 lime application. The content of Rb1 with 0.1 mol L−1 oxalic acid spraying reached the maximum value of 3.46%, which was higher 74.75% than that without oxalic acid spraying treatment. Under other lime application treatments, there was no significant difference among different oxalic acid spraying concentrations. With 0.1 and 0.2 mol L−1 oxalic acid spraying treatments, the contents of Rb1 decreased at first and then decreased with the increase of lime application rates (Table 4).Contents of flavonoidsWith the same concentration of oxalic acid spraying, the content of flavonoids increased at first and then decreased with the increase of the amounts of lime application. There was no significant difference in the content of flavonoids under different concentrations of oxalic acid spraying without the application of lime or 3750 kg hm−2 lime. Under 750 and 2250 kg hm−2 lime application, the content of flavonoids increased at first and then decreased with the increase of the concentration of oxalic acid spraying. Under the treatment of 750 kg hm−2 application and 0.1 mol L−1 oxalic acid spraying, the content of flavonoids was the highest, which was 4.38 mg g−1, which was higher 18.38% than that of the same rate of lime application and without spraying oxalic acid. The content of flavonoids with 0.1 mol L−1 oxalic acid spraying treatment increased by 21.74% compared with that without oxalic acid spraying treatment and 2250 kg hm−2 lime application (Fig. 5).Figure 5Effects of foliar spraying of oxalate on the contents of flavonoids in roots of Panax notoginseng under Cd stress.Full size imageBivariate analysis showed that the content of soluble sugar in P. notoginseng root was significantly relationship with the amount of lime application and the concentration of oxalic acid spraying. The content of soluble protein in root was significantly relationship with lime application rates, both of lime and oxalic acid. The contents of free amino acid and proline in roots were significantly relationship with lime application rates, oxalic acid spraying concentrations, both of lime and oxalic acid (Table 5).Table 5 Variance analysis of the effects of oxalic acid, calcium and cadmium on the contents of multiple medicinal ingredients in the roots of Panax notoginseng (F value).Full size tableThe content of R1 in the root of P. notoginseng was significantly relationship with oxalic acid spraying concentrations, lime application rates, both of lime and oxalic acid. The content of flavonoids was significantly relationship with oxalic acid spraying concentrations, lime application rates. More

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    Assessing Asiatic cheetah’s individual diet using metabarcoding and its implication for conservation

    Ceballos, G. & Ehrlich, P. R. Mammal population losses and the extinction crisis. Science 296, 904–907 (2002).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Barnosky, A. D. et al. Has the Earth’s sixth mass extinction already arrived?. Nature 471, 51–57 (2011).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Ripple, W. J. et al. Status and ecological effects of the world’s largest carnivores. Science 343, 1241484 (2014).PubMed 
    Article 
    CAS 

    Google Scholar 
    Carbone, C. & Gittleman, J. L. A common rule for the scaling of carnivore density. Science 295, 2273–2276 (2014).ADS 
    Article 

    Google Scholar 
    Durant, S. M. et al. The global decline of cheetah Acinonyx jubatus and what it means for conservation. Proc. Natl. Acad. Sci. 114, 528–533 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Jowkar, H. et al. Acinonyx jubatus ssp. venaticus. The IUCN Red List of Threatened Species 2008: e.T220A13035342. (2008).Khalatbari, L., Yusefi, G. H., Martínez-Freiría, F., Jowkar, H. & Brito, J. C. Availability of prey and natural habitats are related with temporal dynamics in range and habitat suitability for Asiatic Cheetah. Hystrix 29, 145–151 (2018).
    Google Scholar 
    Asadi, H. The Environmental Limitations and Future of the Asiatic Cheetah in Iran. (1997).CACP. Annual Report. (2014).Khalatbari, L., Jowkar, H., Yusefi, G. H., Brito, J. C. & Ostrowski, S. The current status of Asiatic cheetah in Iran. Cat News 66, 10–13 (2017).
    Google Scholar 
    Marker, L. L. et al. Ecology of free-ranging cheetahs. in Cheetahs: Biology and Conservation (eds. Marker, L. L., Boast, L. K. & Schmidt-Kuntzel, A.) 107–119 (Elsevier, 2017). doi:https://doi.org/10.1016/B978-0-12-804088-1.00008-3Hayward, M. W., Hofmeyr, M., O’Brian, J. & Kerley, G. I. H. Prey preferences of the cheetah (Acinonyx jubatus) (Felidae: Carnivora): morphological limitations or the need to capture rapidly consumable prey before kleptoparasites arrive?. J. Zool. 270, 615–627 (2006).Article 

    Google Scholar 
    Mills, M. G. L., Broomhall, L. S. & Toit, J. T. Cheetah Acinonyx jubatus feeding ecology in the Kruger National Park and a comparison across African savanna habitats: is the cheetah only a successful hunter on open grassland plains?. Wildlife Biol. 10, 177–186 (2004).Article 

    Google Scholar 
    Wachter, B., Jauernig, O. & Breitenmoser, U. Determination of prey hair in faeces of free-ranging Namibian cheetahs with a simple method. Cat News 44, 8–9 (2006).
    Google Scholar 
    Marker, L. L., Muntifering, J. R., Dickman, A. J., Mills, M. G. L. & Macdonald, D. W. Quantifying prey preferences of free-ranging Namibian cheetahs. South Afr. J. Wildl. Res. 33, 43–53 (2003).
    Google Scholar 
    Wacher, T. et al. Sahelo-Saharan Interest Group Wildlife Surveys, Part 4: Ahaggar Mountains, Algeria (March 2005). (2005).Thuo, D. et al. An insight into the prey spectra and livestock predation by cheetahs in Kenya using faecal DNA metabarcoding. Zoology 143, 125853 (2020).PubMed 
    Article 

    Google Scholar 
    Broekhuis, F., Thuo, D. & Hayward, M. W. Feeding ecology of cheetahs in the Maasai Mara, Kenya and the potential for intra- and interspecific competition. J. Zool. 304, 65–72 (2018).Article 

    Google Scholar 
    Cooper, A. B., Pettorelli, N. & Durant, S. M. Large carnivore menus: factors affecting hunting decisions by cheetahs in the Serengeti. Anim. Behav. 73, 651–659 (2007).Article 

    Google Scholar 
    Mills, M. G. L. Living near the edge: A review of the ecological relationships between large carnivores in the arid Kalahari. African J. Wildl. Res. 45, 127–137 (2015).Article 

    Google Scholar 
    Rostro-García, S., Kamler, J. F. & Hunter, L. T. B. To kill, stay or flee: The effects of lions and landscape factors on habitat and kill site selection of cheetahs in South Africa. PLoS ONE 10, e0117743 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Laurenson, M. K. Behavioural costs and constraints of lactation in free-living cheetahs. Anim. Behav. 50, 815–826 (1995).Article 

    Google Scholar 
    Farhadinia, M. S. & Hemami, M.-R. Prey selection by the critically endangered Asiatic cheetah in central Iran. J. Nat. Hist. 44, 1239–1249 (2010).Article 

    Google Scholar 
    Farhadinia, M. S. et al. Feeding ecology of the Asiatic cheetah Acinonyx jubatus venaticus in low prey habitats in northeastern Iran: Implications for effective conservation. J. Arid Environ. 87, 206–211 (2012).ADS 
    Article 

    Google Scholar 
    Zahedian, B. & Nezami, B. Cheetah (Acinonyx jubatus venaticus) (Felidae: Carnivora) feeding ecology in Central Plateau of Iran and effects of prey poor management. J. Wildl. Biodivers. 3, 22–30 (2019).
    Google Scholar 
    Zamani, N. et al. Predation of montane deserts ungulates by Asiatic cheetah Acinonyx jubatus venaticus in Central Iran. Folia Zool. 66, 50–57 (2017).Article 

    Google Scholar 
    Monterroso, P. et al. Factors affecting the (in)accuracy of mammalian mesocarnivore scat identification in South-western Europe. J. Zool. 289, 243–250 (2013).Article 

    Google Scholar 
    Morin, D. J. et al. Bias in carnivore diet analysis resulting from misclassification of predator scats based on field identification. Wildl. Soc. Bull. 40, 669–677 (2016).Article 

    Google Scholar 
    Caro, T. M. Cheetahs of the Serengeti Plains: Group Living in an Asocial Species (University of Chicago Press, 1994).
    Google Scholar 
    Floyd, T. J., Mech, L. D. & Jordan, P. A. Relating wolf scat content to prey consumed. J. Wildl. Manage. 42, 528–532 (1978).Article 

    Google Scholar 
    Jethva, B. D. & Jhala, Y. V. Computing biomass consumption from prey occurrences in Indian wolf scats. Zoo Biol. 23, 513–520 (2004).Article 

    Google Scholar 
    Pompanon, F. et al. Who is eating what: diet assessment using next generation sequencing. Mol. Ecol. 21, 1931–1950 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Taberlet, P., Coissac, E., Pompanon, F., Brochmann, C. & Willerslev, E. Towards next-generation biodiversity assessment using DNA metabarcoding. Mol. Ecol. 21, 2045–2050 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Mata, V. A. et al. How much is enough? Effects of technical and biological replication on metabarcoding dietary analysis. Mol. Ecol. 28, 165–175 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Shehzad, W. et al. Prey preference of Snow Leopard (Panthera uncia) in South Gobi Mongolia. PLoS ONE 7, e32104 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Monterroso, P. et al. Feeding ecological knowledge: the underutilised power of faecal DNA approaches for carnivore diet analysis. Mamm. Rev. 49, 97–112 (2019).Article 

    Google Scholar 
    Shehzad, W. et al. Carnivore diet analysis based on next-generation sequencing: Application to the leopard cat (Prionailurus bengalensis) in Pakistan. Mol. Ecol. 21, 1951–1965 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Thuo, D. et al. Food from faeces: Evaluating the efficacy of scat DNA metabarcoding in dietary analyses. PLoS ONE 14, e0225805 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Araujo, M. S., Bolnick, D. I. & Layman, C. A. The ecological causes of individual specialisation. Ecol. Lett. 14, 948–958 (2011).PubMed 
    Article 

    Google Scholar 
    Balme, G. A., Roex, N., Rogan, M. S. & Hunter, L. T. B. Ecological opportunity drives individual dietary specialization in leopards. J. Anim. Ecol. 89, 589–600 (2020).PubMed 
    Article 

    Google Scholar 
    Bolnick, D. I. et al. The ecology of individuals: incidence and implications of individual specialization. Am. Nat. 161, 1–28 (2003).MathSciNet 
    PubMed 
    Article 

    Google Scholar 
    Harrington, L. A., Harrington, A. L., Hughes, J., Stirling, D. & Macdonald, D. W. The accuracy of scat identification in distribution surveys: American mink, Neovison vison, in the northern highlands of Scotland. Eur. J. Wildl. Res. 56, 377–384 (2010).Article 

    Google Scholar 
    Weiskopf, S. R., Kachel, S. M. & McCarthy, K. P. What are snow leopards really eating? Identifying bias in food-habit studies. Wildl. Soc. Bull. 40, 233–240 (2016).Article 

    Google Scholar 
    Durant, S. M., Caro, T. M., Collins, D. A., Alawi, R. M. & Fitzgibbon, C. D. Migration patterns of Thomson’s gazelles and cheetahs on the Serengeti Plains. Afr. J. Ecol. 26, 257–268 (1988).Article 

    Google Scholar 
    Lindsey, P. A. et al. Minimum prey and area requirements of the vulnerable cheetah Acinonyx jubatus: implications for reintroduction and management of the species in South Africa. Oryx 45, 587–599 (2011).Article 

    Google Scholar 
    Farhadinia, M. S., Akbari, H., Eslami, M. & Adibi, M. A. A review of ecology and conservation status of Asiatic cheetah in Iran. Cat News Spec. Issue 18–26 (2016).Asadi, H. Some Observation on Hunting Behaviours of the Iranian Cheetah in Captivity. (1997).Heptner, V. G. & Sludskii, A. A. Mammals ofthe Soviet Union volume II part 2 Carnivora (hyaenas and cats). (Vysshaya Shkola Publishers, 1974).Ziaie, H. A Field Guide to the Mammals of Iran. (Iran Wildlife Center, 2008).Wilson, J. W. et al. Cheetahs, Acinonyx jubatus, balance turn capacity with pace when chasing prey. Biol. Lett. 9, 20130620 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Grohé, C., Lee, B. & Flynn, J. J. Recent inner ear specialization for high-speed hunting in cheetahs. Sci. Rep. 8, 2301 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Cheraghi, F. et al. Inter-dependent movements of Asiatic Cheetahs Acinonyx jubatus venaticus and a Persian Leopard Panthera pardus saxicolor in a desert environment in Iran (Mammalia: Felidae). Zool. Middle East 65, 283–292 (2019).Article 

    Google Scholar 
    Ghoddousi, A., Soofi, M., Hamidi, A. K. & Lumetsberger, T. Assessing the role of livestock in big cat prey choice using spatiotemporal availability patterns. PLoS ONE 11, e0153439 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Khorozyan, I., Ghoddousi, A., Soofi, M. & Waltert, M. Big cats kill more livestock when wild prey reaches a minimum threshold. Biol. Conserv. 192, 268–275 (2015).Article 

    Google Scholar 
    Zeder, M. A. Domestication and early agriculture in the Mediterranean Basin: Origins, diffusion, and impact. Proc. Natl. Acad. Sci. 105, 11597–11604 (2008).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Daberger, M. Systematic prioritization of livestock grazing rights buyout in the last viable population of Asiatic cheetah (Acinonyx jubatus venaticus) in Iran. (Humboldt University Berlin, 2021).Wolf, C. & Ripple, W. J. Prey depletion as a threat to the world’s large carnivores. R. Soc. Open Sci. 3, 160252 (2016).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Melzheimer, J. et al. Communication hubs of an asocial cat are the source of a human—carnivore conflict and key to its solution. Proc. Natl. Acad. Sci. 117, 33325–33333 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Malakoutikhah, S., Fakheran, S., Tarkesh, M. & Senn, J. Assessing future distribution, suitability of corridors and efficiency of protected areas to conserve vulnerable ungulates under climate change. Divers. Distrib. 26, 1383–1396 (2020).Article 

    Google Scholar 
    Long, R. A., Donovan, T. M., Mackay, P., Zielinski, W. J. & Buzas, J. S. Comparing scat detection dogs, cameras, and hair snares for surveying carnivores. J. Wildl. Manage. 71, 2018–2025 (2007).Article 

    Google Scholar 
    Becker, M. S. et al. Using dogs to find cats: Detection dogs as a survey method for wide-ranging cheetah. J. Zool. 302, 184–192 (2017).Article 

    Google Scholar 
    Johnson, W. E. & O’Brien, S. J. Phylogenetic reconstruction of the Felidae using 16S rRNA and NADH-5 mitochondrial genes. J. Mol. Evol. 44, S98–S116 (1997).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Reese, E. M., Winters, M., Booth, R. K. & Wasser, S. K. Development of a mitochondrial DNA marker that distinguishes domestic dogs from Washington state gray wolves. Conserv. Genet. Resour. 12, 497–501 (2020).Article 

    Google Scholar 
    Ormerod, S. J. Applied issues with predators and predation: Editor’s introduction. J. Appl. Ecol. 39, 181–188 (2002).Article 

    Google Scholar 
    Boast, L. K., Good, K. & Klein, R. Translocation of problem predators: Is it an effective way to mitigate conflict between farmers and cheetahs Acinonyx jubatus in Botswana?. Oryx 50, 537–544 (2016).Article 

    Google Scholar 
    Darvish Sefat, A. A. Atlas of Protected Areas of Iran (University of Tehran, 2006).
    Google Scholar 
    Yusefi, G. H., Faizolahi, K., Darvish, J., Safi, K. & Brito, J. C. The species diversity, distribution, and conservation status of the terrestrial mammals of Iran. J. Mammal. 100, 55–71 (2019).Article 

    Google Scholar 
    Karami, M., Ghadirian, T. & Faizolahi, K. The Atlas of the Mammals of Iran. (Iran Department of the Environment, 2016).Abangah Consulting Engineer Company. Reconvene expanded Livestock Control Committee (LCC) in Touran and establish the LCC for Miandasht with participation of all stakeholders. (2017).Mills, M. G. L. & Hofer, H. Hyaenas. Status Survey and Conservation Action Plan. (IUCN/SSC Hyaena Specualist Group, 1998).Maudet, C., Luikart, G., Dubray, D., Von Hardenberg, A. & Taberlet, P. Low genotyping error rates in wild ungulate faeces sampled in winter. Mol. Ecol. Notes 4, 772–775 (2004).CAS 
    Article 

    Google Scholar 
    Deagle, B. E., Kirkwood, R. & Jarman, S. N. Analysis of Australian fur seal diet by pyrosequencing prey DNA in faeces. Mol. Ecol. 18, 2022–2038 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Frantz, A. C. et al. Reliable microsatellite genotyping of the Eurasian badger (Meles meles) using faecal DNA. Mol. Ecol. 12, 1649–1661 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    Boom, R. et al. Rapid and simple method for purification of nucleic acids. J. Clin. Microbiol. 28, 495–503 (1990).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rosel, P. E. & Kocher, T. D. DNA-based identification of larval cod in stomach contents of predatory fishes. J. Exp. Mar. Bio. Ecol. 267, 75–88 (2002).Article 

    Google Scholar 
    Deagle, B. E. et al. Molecular scatology as a tool to study diet: analysis of prey DNA in scats from captive Steller sea lions. Mol. Ecol. 14, 1831–1842 (2005).CAS 
    PubMed 
    Article 

    Google Scholar 
    Riaz, T. et al. ecoPrimers: inference of new DNA barcode markers from whole genome sequence analysis. Nucleic Acids Res. 39, e145 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Luikart, G. et al. Multiple maternal origins and weak phylogeographic structure in domestic goats. Proc. Natl. Acad. Sci. 98, 5927–5932 (2001).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Menotti-Raymond, M. et al. A genetic linkage map of microsatellites in the domestic cat (Felis catus). Genomics 57, 9–23 (1999).CAS 
    PubMed 
    Article 

    Google Scholar 
    Charruau, P. et al. Phylogeography, genetic structure and population divergence time of cheetahs in Africa and Asia: Evidence for long-term geographic isolates. Mol. Ecol. 20, 706–724 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Driscoll, C. A., Menotti-Raymond, M., Nelson, G., Goldstein, D. & O’Brien, S. J. Genomic microsatellites as evolutionary chronometers: A test in wild cats. Genome Res. 12, 414–423 (2002).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kotze, A., Ehlers, K., Cilliers, D. C. & Grobler, J. P. The power of resolution of microsatellite markers and assignment tests to determine the geographic origin of cheetah (Acinonyx jubatus) in Southern Africa. Mamm. Biol. 73, 457–462 (2008).Article 

    Google Scholar 
    Marker, L. L. et al. Molecular genetic insights on cheetah (Acinonyx jubatus) ecology and conservation in Namibia. J. Hered. 99, 2–13 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Taberlet, P. et al. Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res. 24, 3189–3194 (1996).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Egeter, B. et al. Challenges for assessing vertebrate diversity in turbid Saharan water-bodies using environmental DNA. Genome 61, 807–814 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Magoc, T. & Salzberg, S. L. FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rognes, T., Flouri, T., Nichols, B., Quince, C. & Mahé, F. VSEARCH: A versatile open source tool for metagenomics. PeerJ 4, e2584 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Godinho, R. et al. Real-time assessment of hybridization between wolves and dogs: Combining noninvasive samples with ancestry informative markers. Mol. Ecol. Resour. 15, 317–328 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Valière, N. GIMLET: A computer program for analysing individual identification data. Mol. Ecol. 2, 377–379 (2002).
    Google Scholar 
    Wachter, B. et al. An advanced method to assess the diet of free-ranging large carnivores based on scats. PLoS ONE 7, e38066 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Breuer, T. Diet choice of large carnivores in northern Cameroon. Afr. J. Ecol. 43, 181–190 (2005).Article 

    Google Scholar 
    Wilson, M. F. J., O’Connell, B., Brown, C., Guinan, J. C. & Grehan, A. J. Multiscale terrain analysis of multibeam bathymetry data for habitat mapping on the continental slope. Mar. Geodesy 30, 2 (2007).Article 

    Google Scholar 
    Fick, S. E. & Hijmans, R. J. WorldClim 2: New 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).Article 

    Google Scholar  More

  • in

    Single-cell stable isotope probing in microbial ecology

    Neufeld JD, Wagner M, Murrell JC. Who eats what, where and when? Isotope-labelling experiments are coming of age. ISME J. 2007;1:103–10.CAS 
    PubMed 
    Article 

    Google Scholar 
    Boschker HTS, Nold SC, Wellsbury P, Bos D, de Graaf W, Pel R, et al. Direct linking of microbial populations to specific biogeochemical processes by 13C-labelling of biomarkers. Nature. 1998;392:801–5Jehmlich N, Schmidt F, von Bergen M, Richnow H-H, Vogt C. Protein-based stable isotope probing (Protein-SIP) reveals active species within anoxic mixed cultures. ISME J. 2008;2:1122–33.CAS 
    PubMed 
    Article 

    Google Scholar 
    Radajewski S, Ineson P, Parekh NR, Colin Murrell J. Stable-isotope probing as a tool in microbial ecology. Nature. 2000;403:646–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    Manefield M, Whiteley AS, Griffiths RI, Bailey MJ. RNA stable isotope probing, a novel means of linking microbial community function to phylogeny. Appl Environ Microbiol. 2002;68:5367–73.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Berry D, Mader E, Lee TK, Woebken D, Wang Y, Zhu D, et al. Tracking heavy water (D2O) incorporation for identifying and sorting active microbial cells. Proc Natl Acad Sci USA. 2015;112:E194–203.CAS 
    PubMed 

    Google Scholar 
    Jehmlich N, Vogt C, Lünsmann V, Richnow HH, von Bergen M. Protein-SIP in environmental studies. Curr Opin Biotechnol. 2016;41:26–33.CAS 
    PubMed 
    Article 

    Google Scholar 
    Haichar, FEZ, Achouak W, Christen R, Heulin T, et al. Identification of cellulolytic bacteria in soil by stable isotope probing. Environ Microbiol. 2007;9:625–34Rangel-Castro JI, Ignacio Rangel-Castro J, Killham K, Ostle N, Nicol GW, Anderson IC, et al. Stable isotope probing analysis of the influence of liming on root exudate utilization by soil microorganisms. Environ Microbiol. 2005;7:828–38.CAS 
    PubMed 
    Article 

    Google Scholar 
    Wang Y, Song Y, Tao Y, Muhamadali H, Goodacre R, Zhou N-Y, et al. Reverse and multiple stable isotope probing to study bacterial metabolism and interactions at the single cell level. Anal Chem. 2016;88:9443–50.CAS 
    PubMed 
    Article 

    Google Scholar 
    Sharma K, Palatinszky M, Nikolov G, Berry D, Shank EA. Transparent soil microcosms for live-cell imaging and non-destructive stable isotope probing of soil microorganisms. Elife. 2020;9:e56275.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lee KS, Landry Z, Pereira FC, Wagner M, Berry D, Huang WE, et al. Raman microspectroscopy for microbiology. Nat. Rev. Methods Primers. 2021;1:80.CAS 
    Article 

    Google Scholar 
    Hatzenpichler R, Krukenberg V, Spietz RL, Jay ZJ. Next-generation physiology approaches to study microbiome function at single cell level. Nat Rev Microbiol. 2020;18:241–56.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wagner M. Single-cell ecophysiology of microbes as revealed by raman microspectroscopy or secondary ion mass spectrometry imaging. Ann Rev Microbiol. 2009;63:411–29Lennon JT, Jones SE. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol. 2011;9:119–30.CAS 
    PubMed 
    Article 

    Google Scholar 
    Lewis K. Persister cells, dormancy and infectious disease. Nat Rev Microbiol. 2006;5:48–56.PubMed 
    Article 
    CAS 

    Google Scholar 
    Nielsen KM, Johnsen PJ, Bensasson D, Daffonchio D. Release and persistence of extracellular DNA in the environment. Environ Biosafety Res. 2007;6:37–53.CAS 
    PubMed 
    Article 

    Google Scholar 
    Blazewicz SJ, Barnard RL, Daly RA, Firestone MK. Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses. ISME J. 2013;7:2061–8.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Nocker A, Sossa-Fernandez P, Burr MD, Camper AK. Use of propidium monoazide for live/dead distinction in microbial ecology. Appl Environ Microbiol. 2007;73:5111–7.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Tawakoli PN, Al-Ahmad A, Hoth-Hannig W, Hannig M, Hannig C. Comparison of different live/dead stainings for detection and quantification of adherent microorganisms in the initial oral biofilm. Clin Oral Investig. 2013;17:841–50.CAS 
    PubMed 
    Article 

    Google Scholar 
    Netuschil L, Auschill TM, Sculean A, Arweiler NB. Confusion over live/dead stainings for the detection of vital microorganisms in oral biofilms-which stain is suitable? BMC Oral Health. 2014;14:2.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hatzenpichler R, Connon SA, Goudeau D, Malmstrom RR, Woyke T, Orphan VJ. Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia. Proc Natl Acad Sci USA. 2016;113:E4069–78.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kuru E, Hughes HV, Brown PJ, Hall E, Tekkam S, Cava F, et al. In Situ probing of newly synthesized peptidoglycan in live bacteria with fluorescent D-amino acids. Angew Chem Int Ed Engl. 2012;51:12519–23.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kopf SH, McGlynn SE, Green-Saxena A, Guan Y, Newman DK, Orphan VJ. Heavy water and15N labelling with NanoSIMS analysis reveals growth rate-dependent metabolic heterogeneity in chemostats. Environ Microbiol. 2015;17:2542–56Kopf SH, Sessions AL, Cowley ES, Reyes C, Van Sambeek L, Hu Y, et al. Trace incorporation of heavy water reveals slow and heterogeneous pathogen growth rates in cystic fibrosis sputum. Proc Natl Acad Sci USA. 2016;113:E110–6.CAS 
    PubMed 
    Article 

    Google Scholar 
    Neubauer C, Kasi AS, Grahl N, Sessions AL, Kopf SH, Kato R, et al. Refining the Application of Microbial Lipids as Tracers of Staphylococcus aureus Growth Rates in Cystic Fibrosis Sputum. J Bacteriol. 2018;200:e00365–18.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Haider S, Wagner M, Schmid MC, Sixt BS, Christian JG, Häcker G, et al. Raman microspectroscopy reveals long-term extracellular activity of Chlamydiae. Mol Microbiol. 2010;77:687–700.CAS 
    PubMed 
    Article 

    Google Scholar 
    Kloehn J, Boughton BA, Saunders EC, O’Callaghan S, Binger KJ, McConville MJ. Identification of Metabolically Quiescent Leishmania mexicana Parasites in Peripheral and Cured Dermal Granulomas Using Stable Isotope Tracing Imaging Mass Spectrometry. mBio. 2021;12:e00129–21.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kong L, Setlow P, Li Y-Q. Direct analysis of water content and movement in single dormant bacterial spores using confocal Raman microspectroscopy and Raman imaging. Anal Chem. 2013;85:7094–101.CAS 
    PubMed 
    Article 

    Google Scholar 
    Knudsen SM, Cermak N, Delgado FF, Setlow B, Setlow P, Manalis SR. Water and small-molecule permeation of dormant Bacillus subtilis spores. J Bacteriol. 2016;198:168–77.CAS 
    PubMed 
    Article 

    Google Scholar 
    Chen D, Huang S-S, Li Y-Q. Real-time detection of kinetic germination and heterogeneity of single Bacillus spores by laser tweezers Raman spectroscopy. Anal Chem. 2006;78:6936–41.CAS 
    PubMed 
    Article 

    Google Scholar 
    Devictor V, Clavel J, Julliard R, Lavergne S, Mouillot D, Thuiller W, et al. Defining and measuring ecological specialization. J Appl Ecol. 2010;47:15–25.Article 

    Google Scholar 
    Pereira FC, Berry D. Microbial nutrient niches in the gut. Environ Microbiol. 2017;19:1366–78.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Shakya M, Lo C-C, Chain PSG. Advances and challenges in metatranscriptomic analysis. Front Genet. 2019;10:904.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Berry D, Loy A. Stable-Isotope probing of human and animal microbiome function. Trends Microbiol. 2018;26:999–1007.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Terrado R, Pasulka AL, Lie AA-Y, Orphan VJ, Heidelberg KB, Caron DA. Autotrophic and heterotrophic acquisition of carbon and nitrogen by a mixotrophic chrysophyte established through stable isotope analysis. ISME J. 2017;11:2022–34.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Dekas AE, Parada AE, Mayali X, Fuhrman JA, Wollard J, Weber PK, et al. Characterizing Chemoautotrophy and Heterotrophy in Marine Archaea and Bacteria With Single-Cell Multi-isotope NanoSIP. Front Microbiol. 2019;10:2682.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wegener G, Bausch M, Holler T, Thang NM, Mollar XP, Kellermann MY, et al. Assessing sub-seafloor microbial activity by combined stable isotope probing with deuterated water and 13C-bicarbonate. Environ Microbiol. 2019;14:1517–27Jing X, Gou H, Gong Y, Su X, Xu L, Ji Y, et al. Raman-activated cell sorting and metagenomic sequencing revealing carbon-fixing bacteria in the ocean. Environ Microbiol. 2018;20:2241–55.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Xu J, Zhu D, Ibrahim AD, Allen CCR, Gibson CM, Fowler PW, et al. Raman deuterium isotope probing reveals microbial metabolism at the single-cell level. Anal Chem. 2017;89:13305–12.CAS 
    PubMed 
    Article 

    Google Scholar 
    Zhang M, Hong W, Abutaleb NS, Li J, Dong P-T, Zong C, et al. Rapid determination of antimicrobial susceptibility by stimulated Raman scattering imaging of D2O metabolic incorporation in a single bacterium. Adv Chem Microsc Life Sci Transl Med. 2021.Lima C, Muhamadali H, Xu Y, Kansiz M, Goodacre R. Imaging Isotopically Labeled Bacteria at the Single-Cell Level Using High-Resolution Optical Infrared Photothermal Spectroscopy. Anal Chem. 2021;93:3082–8.CAS 
    PubMed 
    Article 

    Google Scholar 
    Ackermann M. A functional perspective on phenotypic heterogeneity in microorganisms. Nat Rev Microbiol. 2015;13:497–508.CAS 
    PubMed 
    Article 

    Google Scholar 
    Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S. Bacterial persistence as a phenotypic switch. Science. 2004;305:1622–5.CAS 
    PubMed 
    Article 

    Google Scholar 
    Maamar H, Raj A, Dubnau D. Noise in gene expression determines cell fate in Bacillus subtilis. Science. 2007;317:526–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    Emonet T, Cluzel P. Relationship between cellular response and behavioral variability in bacterial chemotaxis. Proc Natl Acad Sci USA. 2008;105:3304–9.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ozbudak EM, Thattai M, Lim HN, Shraiman BI, Van Oudenaarden A. Multistability in the lactose utilization network of Escherichia coli. Nature. 2004;427:737–40.CAS 
    PubMed 
    Article 

    Google Scholar 
    Kiviet DJ, Nghe P, Walker N, Boulineau S, Sunderlikova V, Tans SJ. Stochasticity of metabolism and growth at the single-cell level. Nature. 2014;514:376–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    Kotte O, Volkmer B, Radzikowski JL, Heinemann M. Phenotypic bistability in Escherichia coli’s central carbon metabolism. Mol Syst Biol. 2014;10:736.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    New AM, Cerulus B, Govers SK, Perez-Samper G, Zhu B, Boogmans S, et al. Different levels of catabolite repression optimize growth in stable and variable environments. PLoS Biol. 2014;12:e1001764.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Solopova A, van Gestel J, Weissing FJ, Bachmann H, Teusink B, Kok J, et al. Bet-hedging during bacterial diauxic shift. Proc Natl Acad Sci USA. 2014;111:7427–32.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Schreiber F, Littmann S, Lavik G, Escrig S, Meibom A, Kuypers MMM, et al. Phenotypic heterogeneity driven by nutrient limitation promotes growth in fluctuating environments. Nat Microbiol. 2016;1:16055.CAS 
    PubMed 
    Article 

    Google Scholar 
    Nikolic N, Schreiber F, Dal Co A, Kiviet DJ, Bergmiller T, Littmann S, et al. Cell-to-cell variation and specialization in sugar metabolism in clonal bacterial populations. PLoS Genet. 2017;13:e1007122.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Takhaveev V, Heinemann M. Metabolic heterogeneity in clonal microbial populations. Curr Opin Microbiol. 2018;45:30–8.CAS 
    PubMed 
    Article 

    Google Scholar 
    Altschuler SJ, Wu LF. Cellular heterogeneity: do differences make a difference? Cell. 2010;141:559–63.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Beaumont HJE, Gallie J, Kost C, Ferguson GC, Rainey PB. Experimental evolution of bet hedging. Nature. 2009;462:90–3.CAS 
    PubMed 
    Article 

    Google Scholar 
    Calabrese F, Voloshynovska I, Musat F, Thullner M, Schlömann M, Richnow HH, et al. Quantitation and comparison of phenotypic heterogeneity among single cells of monoclonal microbial populations. Front Microbiol. 2019;10:2814.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zimmermann M, Escrig S, Hübschmann T, Kirf MK, Brand A, Inglis RF, et al. Phenotypic heterogeneity in metabolic traits among single cells of a rare bacterial species in its natural environment quantified with a combination of flow cell sorting and NanoSIMS. Front Microbiol. 2015;6:243.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zimmermann M, Escrig S, Lavik G, Kuypers MMM, Meibom A, Ackermann M, et al. Substrate and electron donor limitation induce phenotypic heterogeneity in different metabolic activities in a green sulphur bacterium. Environ Microbiol Rep. 2018;10:179–83.CAS 
    PubMed 
    Article 

    Google Scholar 
    Sheik AR, Muller EE, Audinot J-N, Lebrun LA, Grysan P, Guignard C, et al. In situ phenotypic heterogeneity among single cells of the filamentous bacterium Candidatus Microthrix parvicella. ISME J. 2016;10:1274–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    Seyedsayamdost MR, Case RJ, Kolter R, Clardy J. The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat Chem. 2011;3:331–5.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ferrier-Pagès C, Leal MC. Stable isotopes as tracers of trophic interactions in marine mutualistic symbioses. Ecol Evol. 2019;9:723–40.PubMed 
    Article 

    Google Scholar 
    Pasulka AL, Thamatrakoln K, Kopf SH, Guan Y, Poulos B, Moradian A, et al. Interrogating marine virus-host interactions and elemental transfer with BONCAT and nanoSIMS-based methods. Environ Microbiol. 2018;20:671–92.CAS 
    PubMed 
    Article 

    Google Scholar 
    Kopp C, Domart-Coulon I, Escrig S, Humbel BM, Hignette M, Meibom A. Subcellular investigation of photosynthesis-driven carbon assimilation in the symbiotic reef coral Pocillopora damicornis. mBio. 2015;6:e02299–14.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rädecker N, Pogoreutz C, Gegner HM, Cárdenas A, Roth F, Bougoure J, et al. Heat stress destabilizes symbiotic nutrient cycling in corals. Proc Natl Acad Sci U S A. 2021;118:e2022653118.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Krueger T, Bodin J, Horwitz N, Loussert-Fonta C, Sakr A, Escrig S, et al. Temperature and feeding induce tissue level changes in autotrophic and heterotrophic nutrient allocation in the coral symbiosis – a NanoSIMS study. Sci Rep. 2018;8:12710.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Gibbin E, Gavish A, Krueger T, Kramarsky-Winter E, Shapiro O, Guiet R, et al. Vibrio coralliilyticus infection triggers a behavioural response and perturbs nutritional exchange and tissue integrity in a symbiotic coral. ISME J. 2019;13:989–1003.CAS 
    PubMed 
    Article 

    Google Scholar 
    Rix L, Ribes M, Coma R, Jahn MT, de Goeij JM, van Oevelen D, et al. Heterotrophy in the earliest gut: a single-cell view of heterotrophic carbon and nitrogen assimilation in sponge-microbe symbioses. ISME J. 2020;14:2554–67.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Thomas T, Moitinho-Silva L, Lurgi M, Björk JR, Easson C, Astudillo-García C, et al. Diversity, structure and convergent evolution of the global sponge microbiome. Nat Commun. 2016;7:11870.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Mills MM, Turk-Kubo KA, van Dijken GL, Henke BA, Harding K, Wilson ST, et al. Unusual marine cyanobacteria/haptophyte symbiosis relies on N2 fixation even in N-rich environments. ISME J. 2020;14:2395–406.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Turk-Kubo KA, Mills MM, Arrigo KR, van Dijken G, Henke BA, Stewart B, et al. UCYN-A/haptophyte symbioses dominate N2 fixation in the Southern California Current System. ISME Commun. 2021;1:1–13.Article 

    Google Scholar 
    Moore CM, Mills MM, Arrigo KR, Berman-Frank I, Bopp L, Boyd PW, et al. Processes and patterns of oceanic nutrient limitation. Nat Geosci. 2013;6:701–10.CAS 
    Article 

    Google Scholar 
    Scheller S, Yu H, Chadwick GL, McGlynn SE, Orphan VJ. Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction. Science. 2016;351:703–7.CAS 
    PubMed 
    Article 

    Google Scholar 
    Pereira FC, Wasmund K, Cobankovic I, Jehmlich N, Herbold CW, Lee KS, et al. Rational design of a microbial consortium of mucosal sugar utilizers reduces Clostridiodes difficile colonization. Nat Commun. 2020;11:5104.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Mooshammer M, Kitzinger K, Schintlmeister A, Ahmerkamp S, Nielsen JL, Nielsen PH, et al. Flow-through stable isotope probing (Flow-SIP) minimizes cross-feeding in complex microbial communities. ISME J. 2021;15:348–53.CAS 
    PubMed 
    Article 

    Google Scholar 
    Drescher K, Nadell CD, Stone HA, Wingreen NS, Bassler BL. Solutions to the public goods dilemma in bacterial biofilms. Curr Biol. 2014;24:50–5.CAS 
    PubMed 
    Article 

    Google Scholar 
    Słomka J, Alcolombri U, Secchi E, Stocker R, Fernandez VI. Encounter rates between bacteria and small sinking particles. New J Phys. 2020;22:043016.Article 

    Google Scholar 
    Alcolombri U, Peaudecerf FJ, Fernandez VI, Behrendt L, Lee KS, Stocker R. Sinking enhances the degradation of organic particles by marine bacteria. Nat Geosci. 2021;14:775–80.CAS 
    Article 

    Google Scholar 
    University of Massachusetts Amherst Massachusetts Lynn Margulis, Margulis L, Fester R. Symbiosis as a source of evolutionary innovation: speciation and morphogenesis. MIT Press; 1991. 454 p.Legin AA, Schintlmeister A, Sommerfeld NS, Eckhard M, Theiner S, Reipert S, et al. Nano-scale imaging of dual stable isotope labeled oxaliplatin in human colon cancer cells reveals the nucleolus as a putative node for therapeutic effect. Nanoscale Adv. 2021;3:249–62.CAS 
    Article 

    Google Scholar 
    Schaible GA, et al. Correlative SIP-FISH-Raman-SEM-NanoSIMS links identity, morphology, biochemistry, and physiology of environmental microbes. ISME COMMUN. 2022;2:52.Article 

    Google Scholar 
    Yu G-H, Chi Z-L, Kappler A, Sun F-S, Liu C-Q, Teng HH, et al. Fungal nanophase particles catalyze iron transformation for oxidative stress removal and iron acquisition. Curr Biol. 2020;30:2943–50.e4.CAS 
    PubMed 
    Article 

    Google Scholar 
    Subirana MA, Riemschneider S, Hause G, Dobritzsch D, Schaumlöffel D, Herzberg M. High spatial resolution imaging of subcellular macro and trace element distribution during phagocytosis. Metallomics. 2022;14:mfac011.PubMed 
    Article 

    Google Scholar 
    Bonnin EA, Fornasiero EF, Lange F, Turck CW, Rizzoli SO. NanoSIMS observations of mouse retinal cells reveal strict metabolic controls on nitrogen turnover. BMC Mol Cell Biol. 2021;22:5.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jo MC, Liu W, Gu L, Dang W, Qin L. High-throughput analysis of yeast replicative aging using a microfluidic system. Proc Natl Acad Sci U S A. 2015;112:9364–9.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Anggraini D, Ota N, Shen Y, Tang T, Tanaka Y, Hosokawa Y, et al. Recent advances in microfluidic devices for single-cell cultivation: methods and applications. Lab Chip. 2022;22:1438–68.CAS 
    PubMed 
    Article 

    Google Scholar 
    Eriksen R, Daria V, Gluckstad J. Fully dynamic multiple-beam optical tweezers. Opt Express. 2002;10:597–602.PubMed 
    Article 

    Google Scholar 
    Dai X, Fu W, Chi H, Mesias VSD, Zhu H, Leung CW, et al. Optical tweezers-controlled hotspot for sensitive and reproducible surface-enhanced Raman spectroscopy characterization of native protein structures. Nat Commun. 2021;12:1292.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Collins DJ, Morahan B, Garcia-Bustos J, Doerig C, Plebanski M, Neild A. Two-dimensional single-cell patterning with one cell per well driven by surface acoustic waves. Nat Commun. 2015;6:8686.CAS 
    PubMed 
    Article 

    Google Scholar 
    Hu F, Shi L, Min W. Biological imaging of chemical bonds by stimulated Raman scattering microscopy. Nat Methods. 2019;16:830–42.CAS 
    PubMed 
    Article 

    Google Scholar 
    Ge X, Pereira FC, Mitteregger M, Berry D, Zhang M, Hausmann B, et al. SRS-FISH: A high-throughput platform linking microbiome metabolism to identity at the single-cell level. Proc Natl Acad Sci U S A. 2022;119:e2203519119.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Vandergrift GW, Kew W, Lukowski JK, Bhattacharjee A, Liyu AV, Shank EA, et al. Imaging and direct sampling capabilities of nanospray desorption electrospray ionization with absorption-mode 21 Tesla Fourier transform ion cyclotron resonance mass spectrometry. Anal Chem. 2022;94:3629–36.CAS 
    PubMed 
    Article 

    Google Scholar 
    Harrison JP, Berry D. Vibrational spectroscopy for imaging single microbial cells in complex biological samples. Front Microbiol. 2017;8:675.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Mayali X. NanoSIMS: microscale quantification of biogeochemical activity with large-scale impacts. Ann Rev Mar Sci. 2020;12:449–67.PubMed 
    Article 

    Google Scholar 
    Alexandrov T. Spatial metabolomics and imaging mass spectrometry in the age of artificial intelligence. Annu Rev Biomed Data Sci. 2020;3:61–87.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Boschker HTS, Middelburg JJ. Stable isotopes and biomarkers in microbial ecology. FEMS Microbiol Ecol. 2002;40:85–95.CAS 
    PubMed 
    Article 

    Google Scholar 
    Mayali X, Weber PK, Nuccio E, Lietard J, Somoza M, Blazewicz SJ, et al. Chip-SIP: Stable Isotope Probing analyzed with rRNA-targeted microarrays and nanoSIMS. Methods Mol Biol. 2019;2046:71–87.PubMed 
    Article 

    Google Scholar 
    Chokkathukalam A, Kim D-H, Barrett MP, Breitling R, Creek DJ. Stable isotope-labeling studies in metabolomics: new insights into structure and dynamics of metabolic networks. Bioanalysis. 2014;6:511–24.CAS 
    PubMed 
    Article 

    Google Scholar 
    Hiller K, Metallo CM, Kelleher JK, Stephanopoulos G. Nontargeted elucidation of metabolic pathways using stable-isotope tracers and mass spectrometry. Anal Chem. 2010;82:6621–8.CAS 
    PubMed 
    Article 

    Google Scholar 
    Rusconi R, Garren M, Stocker R. Microfluidics expanding the frontiers of microbial ecology. Annu Rev Biophys. 2014;43:65–91.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lee KS, Pereira FC, Palatinszky M, Behrendt L, Alcolombri U, Berry D, et al. Optofluidic Raman-activated cell sorting for targeted genome retrieval or cultivation of microbial cells with specific functions. Nat Protoc. 2021;16:634–76.CAS 
    PubMed 
    Article 

    Google Scholar 
    Wagner M, Haider S. New trends in fluorescence in situ hybridization for identification and functional analyses of microbes. Curr Opin Biotechnol. 2012;23:96–102.CAS 
    PubMed 
    Article 

    Google Scholar  More

  • in

    Nonreproductive effects are more important than reproductive effects in a host feeding parasitoid

    Godfray, H. C. Parasitoids: Behavioural and Evolutionary Ecology (Princeton University Press, 1994).Book 

    Google Scholar 
    Jervis, M. A., Ellers, J. & Harvey, J. A. Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annu. Rev. Entomol. 53, 361–385 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Jervis, M. A. & Kidd, N. A. C. Host-feeding strategies in hymenopteran parasitoids. Biol. Rev. 61, 395–434 (1986).Article 

    Google Scholar 
    Cebolla, R., Vanaclocha, P., Urbaneja, A. & Tena, A. Overstinging by hymenopteran parasitoids causes mutilation and surplus killing of hosts. J. Pest Sci. 91, 327–339 (2018).Article 

    Google Scholar 
    Abram, P. K., Brodeur, J., Urbaneja, A. & Tena, A. Nonreproductive effects of insect parasitoids on their hosts. Annu. Rev. Entomol. 64, 259–276 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Münster-Swendsen, M. Population cycles of the spruce needle miner in Denmark driven by interactions with insect parasitoids. In Population Cycles: The Case for Trophic Interactions (ed. Berryman, A. A.) 29–43 (Oxford University Press, 2002).
    Google Scholar 
    Abram, P. K., Brodeur, J., Burte, V. & Boivin, G. Parasitoid-induced host egg abortion: an underappreciated component of biological control services provided by egg parasitoids. Biol. Control 98, 52–60 (2016).Article 

    Google Scholar 
    Vinson, S. B. & Iwantsch, G. F. Host suitability for insect parasitoids. Annu. Rev. Entomol. 25, 397–419 (1980).Article 

    Google Scholar 
    Heimpel, G. E. & Collier, T. R. The evolution of host-feeding behaviour in insect parasitoids. Biol. Rev. 71, 373–400 (1996).Article 

    Google Scholar 
    Heimpel, G. E., Rosenheim, J. A. & Adams, J. M. Behavioral ecology of host feeding in Aphytis melinus parasitoid. Nor. J. Agric. Sci. 6, 101–115 (1994).
    Google Scholar 
    Heimpel, G. E. & Rosenheim, J. A. Dynamic host feeding by the parasitoid Aphytis melinus: the balance between current and future reproduction. J. Anim. Ecol. 64, 153–167 (1995).Article 

    Google Scholar 
    Choi, W. I., Yoon, T. J. & Ryoo, M. I. Host-size-dependent feeding behaviour and progeny sex ratio of Anisopteromalus calandrae (Hym., Pteromalidae). J. Appl. Entomol. 125, 71–77 (2001).Article 

    Google Scholar 
    Burger, J. M. S., Hemerik, L., Leteren, J. C. & Vet, L. E. M. Reproduction now or later: optimal host-handling strategies in the whitefly parasitoid Encasia formosa. Oikos 106, 117–130 (2004).Article 

    Google Scholar 
    Guillemaud, T. et al. The tomato borer, Tuta absoluta, invading the Mediterranean Basin, originates from a single introduction from Central Chile. Sci. Rep. 5, 8371 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Desneux, N., Luna, M. G., Guillemaud, T. & Urbaneja, A. The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. J. Pest Sci. 84, 403–408 (2011).Article 

    Google Scholar 
    Desneux, N. et al. Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J. Pest Sci. 83, 197–215 (2010).Article 

    Google Scholar 
    Biondi, A., Guedes, R. N. C., Wan, F. H. & Desneux, N. Ecology, worldwide spread and management of the invasive South American tomato pinworm, Tuta absoluta: past, present and future. Annu. Rev. Entomol. 63, 239–258 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Campos, M. R., Biondi, A., Adiga, A., Guedes, R. N. C. & Desneux, N. From the Western Palaearctic region to beyond: Tuta absoluta 10 years after invading Europe. J. Pest Sci. 90, 787–796 (2017).Article 

    Google Scholar 
    Han, P. et al. Are we ready for the invasion of Tuta absoluta? Unanswered key questions for elaborating an integrated pest management package in Xinjiang, China. Entomol. Gen. 38, 125 (2018).
    Google Scholar 
    Han, P. et al. Tuta absoluta continues to disperse in Asia: damage, ongoing management and future challenges. J. Pest Sci. 92, 1317–1327 (2019).Article 

    Google Scholar 
    Mansour, R. et al. Occurrence, biology, natural enemies and management of Tuta absoluta in Africa. Entomol. Gen. 38, 83–111 (2018).Article 

    Google Scholar 
    Zhang, G. F. et al. Outbreak of the South American tomato leafminer, Tuta absoluta, in the Chinese mainland: geographic and potential host range expansion. Pest Manag. Sci. 77, 5475–5488 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Desneux, N. et al. Integrated pest management of Tuta absoluta: practical implementations across different world regions. J. Pest Sci. 95, 17–39 (2022).Article 

    Google Scholar 
    Wang, M. H. et al. Polygyny of Tuta absoluta may affect sex pheromone-based control techniques. Entomol. Gen. 41, 357–367 (2021).Article 

    Google Scholar 
    Rostami, E., Madadi, H., Abbasipour, H., Allahyari, H. & Cuthbertson, A. G. S. Pest density influences on tomato pigment contents: the South American tomato pinworm scenario. Entomol. Gen. 40, 195–205 (2020).Article 

    Google Scholar 
    Desneux, N., Decourtye, A. & Delpuech, J. M. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52, 81–106 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Gebiola, M., Bernardo, U., Ribes, A. & Gibson, G. A. P. An integrative study of Necremnus Thomson (Hymenoptera: Eulophidae) associated with invasive pests in Europe and North America: taxonomic and ecological implications. Zool. J. Linn. Soc. 173, 352–423 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Naselli, M. et al. Insights into food webs associated with the South American tomato pinworm. Pest Manag. Sci. 73, 1352–1357 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Campos, M. R. et al. Impact of a shared sugar food source on biological control of Tuta absoluta by the parasitoid Necremnus tutae. J. Pest Sci. 93, 207–218 (2020).Article 

    Google Scholar 
    Zhang, Y. B. et al. Host selection behavior of the host-feeding parasitoid Necremnus tutae on Tuta absoluta. Entomol. Gen. https://doi.org/10.1127/entomologia/2021/1246 (2021).Article 

    Google Scholar 
    Bodino, N., Ferracini, C. & Tavella, L. Is host selection influenced by natal and adult experience in the parasitoid Necremnus tutae (Hymenoptera: Eulophidae)?. Anim. Behav. 112, 221–228 (2016).Article 

    Google Scholar 
    Biondi, A., Desneux, N., Amiens-Desneux, E., Siscaro, G. & Zappalà, L. Biology and developmental strategies of the Palaearctic parasitoid, Bracon nigricans (Hymenoptera: Braconidae) on the Neotropical moth Tuta absoluta (Lepidoptera: Gelechiidae). J. Econ. Entomol. 106, 1638–1647 (2013).PubMed 
    Article 

    Google Scholar 
    Foltyn, S. & Gerling, D. The parasitoids of the aleyrodid Bemisia tabaci in Israel. Development, host preference and discrimination of the aphelinid Eretmocerus mundus. Entomol. Exp. Appl. 38, 255–260 (1985).Article 

    Google Scholar 
    Zhang, Y. B., Yang, N. W., Sun, L. Y. & Wan, F. H. Host instar suitability in two invasive whiteflies for the naturally occurring parasitoid Eretmocerus hayati in China. J. Pest Sci. 88(2), 1612–1618 (2015).
    Google Scholar 
    Lebreton, S., Darrouzet, E. & Chevrier, C. Could hosts considered as low quality for egg-laying be considered as high quality for host-feeding?. J. Insect Physiol. 55, 694–699 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Calvo, F. J., Soriano, J. D., Bolckmans, K. & Belda, J. E. Host instar suitability and life-history parameters under different temperature regimes of Necremnus artynes on Tuta absoluta. Biocontrol Sci. Technol. 23(7), 803–815 (2013).Article 

    Google Scholar 
    Chailleux, A., Desneux, N., Arnó, J. & Gabarra, R. Biology of two key Palaearctic larval ectoparasitoids when parasitizing the invasive pest Tuta absoluta. J. Pest Sci. 87(3), 441–448 (2014).Article 

    Google Scholar 
    Asgari, S. & Rivers, D. B. Venom proteins from endoparasitoid wasps and their role in host-parasite interactions. Annu. Rev. Entomol. 56, 313–335 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Abram, P. K., Gariepy, T. D., Boivin, G. & Brodeur, J. An invasive stink bug as an evolutionary trap for an indigenous egg parasitoid. Biol. Invasions 16, 1387–1395 (2014).Article 

    Google Scholar 
    Schlaepfer, M. A., Sherman, P. W., Blossey, B. & Runge, M. C. Introduced species as evolutionary traps. Ecol. Lett. 8, 241–246 (2005).Article 

    Google Scholar 
    van Driesche, R. G., Bellotti, A., Herrera, C. J. & Castello, J. A. Host feeding and ovipositor insertion as sources of mortality in the mealybug Phenacoccus herreni caused by two encyrtids, Epidinocarsis diversicornis and Acerophagus coccois. Entomol. Exp. Appl. 44, 97–100 (1987).Article 

    Google Scholar 
    Barrett, B. & Brunner, J. Types of parasitoid-induced mortality, host stage preferences, and sex ratios exhibited by Pnigalio flavipes (Hymenoptera: Eulophidae) using Phyllonorycter elmaella (Lepidoptera: Gracillaridae) as a host. Environ. Entomol. 19, 803–807 (1990).Article 

    Google Scholar 
    Huang, Y., Loomans, A. J. M., van Lenteren, J. C. & Xu, R. M. Hyperparasitism behavior of the autoparasitoid Encarsia tricolor on two secondary host species. BioControl 54, 411–424 (2009).Article 

    Google Scholar 
    Patel, K. J., Schuster, D. J. & Smerage, G. H. Density dependent parasitism and host-killing of Liriomyza trifolii (Diptera: Agromyzidae) by Diglyphus intermedius (Hymenoptera: Eulophidae). Fla. Entomol. 86, 8–14 (2003).Article 

    Google Scholar 
    Lauziere, I., Perez-Lachaud, G. & Bordeur, J. Influence of host density on the reproductive strategy of Cephalonomia stephanoderis, a parasitoid of the coffee berry borer. Entomol. Exp. Appl. 92, 21–28 (1999).Article 

    Google Scholar 
    Blanckenhorn, W. U. The evolution of body size: what keeps organisms small?. Quart. Rev. Biol. 75(4), 385–407 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Idriss, G. E. A., Mohamed, S. A., Khamis, F., Plessis, H. D. & Ekesi, S. Biology and performance of two indigenous larval parasitoids on Tuta absoluta (Lepidoptera: Gelechiidae) in Sudan. Biocontrol Sci. Technol. 28(6), 614–628 (2018).Article 

    Google Scholar 
    Blanckenhorn, W. U., Preziosi, R. F. & Fairbairn, D. J. Time and energy constraints and the evolution of sexual size dimorphism-to eat or to mate?. Evol. Ecol. 9, 369–381 (1995).Article 

    Google Scholar 
    Blomqvist, D., Johansson, O. C., Unger, U., Larsson, M. & Flodin, L. A. Male aerial display and reversed sexual size dimorphism in the dunlin. Anim. Behav. 54, 1291–1299 (1997).CAS 
    PubMed 
    Article 

    Google Scholar 
    Simmons, L. W., Tomkins, J. L. & Hunt, J. Sperm competition games played by dimorphic male beetles. Proc. R. Soc. Lond. B 266, 145–150 (1999).Article 

    Google Scholar 
    Madsen, T. & Shine, R. Costs of reproduction influence the evolution of sexual size dimorphism in snakes. Evolution 48, 1389–1397 (1994).PubMed 
    Article 

    Google Scholar 
    Blanckenhorn, W. U., Morf, C., Mühlhäuser, C. & Reusch, T. Spatiotemporal variation in selection on body size in the dung fly Sepsis cynipsea. J. Evol. Biol. 9, 369–381 (1999).
    Google Scholar  More

  • in

    Short-term mercury exposure disrupts muscular and hepatic lipid metabolism in a migrant songbird

    Bowler, D. E. et al. Mapping human pressures on biodiversity across the planet uncovers anthropogenic threat complexes. People Nat. 2, 380–394 (2020).Article 

    Google Scholar 
    Persson, L. et al. Outside the safe operating space of the planetary boundary for novel entities. Environ. Sci. Technol. https://doi.org/10.1021/acs.est.1c04158 (2022).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    United Nations Environment Programme (UNEP). 2019. Global Mercury Assessment 2018. UN Environment Programme, Chemicals and Health Branch Geneva, Switzerland. https://www.unep.org/resources/publication/global-mercury-assessment-2018Rimmer, C. C., Miller, E. K., McFarland, K. P., Taylor, R. J. & Faccio, S. D. Mercury bioaccumulation and trophic transfer in the terrestrial food web of a montane forest. Ecotoxicology 19, 697–709 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Cristol, D. A. et al. The movement of aquatic mercury through terrestrial food webs. Science 320, 335 (2008).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Evers, D. The effects of methylmercury on wildlife: A comprehensive review and approach for interpretation. Encycl. Anthropocene 5, 181–194 (2018).Article 

    Google Scholar 
    Whitney, M. C. & Cristol, D. A. Impacts of sublethal mercury exposure on birds: a detailed review. Rev. Environ. Contam. Toxicol. 244, 113–163 (2017).
    Google Scholar 
    Seewagen, C. L. Threats of environmental mercury to birds: Knowledge gaps and priorities for future research. Bird Conserv. Int. 20, 112–123 (2010).Article 

    Google Scholar 
    Seewagen, C. L. The threat of global mercury pollution to bird migration: Potential mechanisms and current evidence. Ecotoxicology 29, 1254–1267 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ma, Y., Branfireun, B. A., Hobson, K. A. & Guglielmo, C. G. Evidence of negative seasonal carry-over effects of breeding ground mercury exposure on survival of migratory songbirds. J. Avian Biol. 49, jav-01656 (2018).Article 

    Google Scholar 
    Newton, I. Can conditions experienced during migration limit the population levels of birds?. J. Ornithol. 147, 146–166 (2006).Article 

    Google Scholar 
    Klaassen, M., Hoye, B. J., Nolet, B. A. & Buttemer, W. A. Ecophysiology of avian migration in the face of current global hazards. Philos. Trans. R. Soc. B 367, 1719–1732 (2020).Article 

    Google Scholar 
    Zurell, D., Graham, C. H., Gallien, L., Thuiller, W. & Zimmermann, N. E. Long-distance migratory birds threatened by multiple independent risks from global change. Nat. Clim. Chang. 8, 992–996 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Seewagen, C. L., Ma, Y., Morbey, Y. E. & Guglielmo, C. G. Stopover departure behavior and flight orientation of spring-migrant Yellow-rumped Warblers (Setophaga coronata) experimentally exposed to methylmercury. J. Ornithol. 160, 617–624 (2019).Article 

    Google Scholar 
    Seewagen, C. L. Blood mercury levels and the stopover refueling performance of a long-distance migratory songbird. Can. J. Zool. 91, 41–45 (2013).CAS 
    Article 

    Google Scholar 
    Adams, E. M., Williams, K. A., Olsen, B. J. & Evers, D. C. Mercury exposure in migrating songbirds: Correlations with physical condition. Ecotoxicology 29, 1240–1253 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ma, Y., Perez, C. R., Branfireun, B. A. & Guglielmo, C. G. Dietary exposure to methylmercury affects flight endurance in a migratory songbird. Environ. Pollut. 234, 894–901 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Gerson, A. R., Cristol, D. A. & Seewagen, C. L. Environmentally relevant methylmercury exposure reduces the metabolic scope of a model songbird. Environ. Pollut. 246, 790–796 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Jenni, L. & Jenni-Eiermann, S. Fuel supply and metabolic constraints in migrating birds. J. Avian Biol. 29, 521–552 (1998).Article 

    Google Scholar 
    McWilliams, S. R., Guglielmo, C., Pierce, B. & Klaassen, M. Flying, fasting, and feeding in birds during migration: A nutritional and physiological ecology perspective. J. Avian Biol. 35, 377–393 (2004).Article 

    Google Scholar 
    Guglielmo, C. G. Move that fatty acid: Fuel selection and transport in migratory birds and bats. Integr. Comp. Biol. 50, 336–345 (2010).PubMed 
    Article 

    Google Scholar 
    Guglielmo, C. G. Obese super athletes: Fat-fueled migration in birds and bats. J. Exp. Biol. 221(Suppl_1), 165753 (2018).Article 

    Google Scholar 
    Kawakami, T. et al. Differential effects of cobalt and mercury on lipid metabolism in the white adipose tissue of high-fat diet-induced obesity mice. Toxicol. Appl. Pharmacol. 258, 32–42 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Yadetie, F. et al. Global transcriptome analysis of Atlantic cod (Gadus morhua) liver after in vivo methylmercury exposure suggests effects on energy metabolism pathways. Aquat. Toxicol. 126, 314–325 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Park, K. & Seo, E. Association between toenail mercury and metabolic syndrome is modified by selenium. Nutrients 8, 424 (2016).PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Caito, S. W., Newell-Caito, J., Martell, M., Crawford, N. & Aschner, M. Methylmercury induces metabolic alterations in Caenorhabditis elegans: Role for C/EBP transcription factor. Toxicol. Sci. 174, 112–123 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Edmonds, S. T., O’Driscoll, N. J., Hillier, N. K., Atwood, J. L. & Evers, D. C. Factors regulating the bioavailability of methylmercury to breeding rusty blackbirds in northeastern wetlands. Environ. Pollut. 171, 148–154 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Rowse, L. M., Rodewald, A. D., Mažeika, S. & Sullivan, P. Pathways and consequences of contaminant flux to Acadian flycatchers (Empidonax virescens) in urbanizing landscapes of Ohio, USA. Sci. Total Environ. 485, 461–467 (2014).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    Marsh, R. L. Catabolic enzyme activities in relation to premigratory fattening and muscle hypertrophy in the gray catbird (Dumetella carolinensis). J. Comp. Physiol. 141, 417–423 (1981).CAS 
    Article 

    Google Scholar 
    Guglielmo, C. G., Haunerland, N. H., Hochachka, P. W. & Williams, T. D. Seasonal dynamics of flight muscle fatty acid binding protein and catabolic enzymes in a migratory shorebird. Am. J. Physiol.-Regul. Integr. Comp. Physiol. 282(5), R1405–R1413 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    Maillet, D. & Weber, J. M. Relationship between n-3 PUFA content and energy metabolism in the flight muscles of a migrating shorebird: Evidence for natural doping. J. Exp. Biol. 210, 413–420 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Weber, J. M. Metabolic fuels: Regulating fluxes to select mix. J. Exp. Biol. 214, 286–294 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Feige, J. N., Gelman, L., Michalik, L., Desvergne, B. & Wahli, W. From molecular action to physiological outputs: Peroxisome proliferator-activated receptors are nuclear receptors at the crossroads of key cellular functions. Prog. Lipid. Res. 45, 120–159 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bensinger, S. J. & Tontonoz, P. Integration of metabolism and inflammation by lipid-activated nuclear receptors. Nature 454, 470–477. https://doi.org/10.1038/nature07202 (2008).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Ynalvez, R., Gutierrez, J. & Gonzalez-Cantu, H. Mini-review: Toxicity of mercury as a consequence of enzyme alteration. Biometals 29, 781–788 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Gerson, A. R. & Guglielmo, C. G. Energetics and metabolite profiles during early flight in American robins (Turdus Migratorius). J. Comp. Physiol. B. 183, 983–991 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Price, E. R., McFarlan, J. T. & Guglielmo, C. G. Preparing for migration? The effects of photoperiod and exercise on muscle oxidative enzymes, lipid transporters, and phospholipids in white-crowned sparrows. Physiol. Biochem. Zool. 83, 252–262 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bradley, S. S., Dick, M. F., Guglielmo, C. G. & Timoshenko, A. V. Seasonal and flight-related variation of galectin expression in heart, liver and flight muscles of yellow-rumped warblers (Setophaga coronata). Glycoconj. J. 34, 603–611 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    McFarlan, J. T., Bonen, A. & Guglielmo, C. G. Seasonal upregulation of fatty acid transporters in flight muscles of migratory white-throated sparrows (Zonotrichia albicollis). J. Exp. Biol. 212, 2934–2940 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Zhang, Y., King, M. O., Harmon, E., Eyster, K. & Swanson, D. L. Migration-induced variation of fatty acid transporters and cellular metabolic intensity in passerine birds. J. Comp. Physiol. B. 185, 797–810 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Dick, M. F. & Guglielmo, C. G. Dietary polyunsaturated fatty acids influence flight muscle oxidative capacity but not endurance flight performance in a migratory songbird. Am. J. Physiol.-Regul. Integr. Compar. Physiol. 316(4), R362–R375 (2019).CAS 
    Article 

    Google Scholar 
    Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101–1108 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bittencourt, L. O. et al. Oxidative biochemistry disbalance and changes on proteomic profile in salivary glands of rats induced by chronic exposure to methylmercury. Oxid. Med. Cell. Longev. https://doi.org/10.1155/2017/5653291 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Shi, Q., Sun, N., Kou, H., Wang, H. & Zhao, H. Chronic effects of mercury on Bufo gargarizans larvae: Thyroid disruption, liver damage, oxidative stress and lipid metabolism disorder. Ecotoxicol. Environ. Saf. 164, 500–509 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Nøstbakken, O. J. et al. Dietary methylmercury alters the proteome in Atlantic salmon (Salmo salar) kidney. Aquat. Toxicol. 108, 70–77 (2012).PubMed 
    Article 
    CAS 

    Google Scholar 
    Zink, E. M. Comparison of the mercury induced proteomes of Escherichia coli MG1655 with and without the NR1 plasmid. MSc thesis, Washington State University, Pullman, WA (2009).Lundgren, B. O. & Kiessling, K. H. Seasonal variation in catabolic enzyme activities in breast muscle of some migratory birds. Oecologia 66, 468–471 (1985).ADS 
    PubMed 
    Article 

    Google Scholar 
    Banerjee, S. & Chaturvedi, C. M. Migratory preparation associated alterations in pectoralis muscle biochemistry and proteome in Palearctic-Indian emberizid migratory finch, red-headed bunting, Emberiza bruniceps. Comp. Biochem. Physiol. D Genom. Proteom. 17, 9–25 (2016).CAS 

    Google Scholar 
    Dick, M. F. The long haul: migratory flight preparation and performance in songbirds. Ph.D. dissertation, University of Western Ontario, London, Canada (2017).Driedzic, W. R., Crowe, H. L., Hicklin, P. W. & Sephton, D. H. Adaptations in pectoralis muscle, heart mass, and energy metabolism during premigratory fattening in semipalmated sandpipers (Calidris pusilla). Can. J. Zool. 71, 1602–1608 (1993).Article 

    Google Scholar 
    De Moranville, K. J. et al. PPAR expression, muscle size and metabolic rates across the gray catbird’s annual cycle are greatest in preparation for fall migration. J. Exper. Biol. 222, 198028 (2019).Article 

    Google Scholar 
    Zajac, D. M., Cerasale, D. J., Landman, S. & Guglielmo, C. G. Behavioral and physiological effects of photoperiod-induced migratory state and leptin on Zonotrichia albicollis: II. Effects on fatty acid metabolism. Gen. Comp. Endocrinol. 174, 269–275 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Tinant, G. et al. Methylmercury displays pro-adipogenic properties in rainbow trout preadipocytes. Chemosphere 263, 127917 (2021).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Cambier, S. et al. At environmental doses, dietary methylmercury inhibits mitochondrial energy metabolism in skeletal muscles of the zebra fish (Danio rerio). Int. J. Biochem. Cell Biol. 41, 791–799 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ferain, A. et al. Transcriptional effects of phospholipid fatty acid profile on rainbow trout liver cells exposed to methylmercury. Aquat. Toxicol. 199, 174–187 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Börchers, T., Højrup, P., Nielsen, S. U., Roepstorff, P., Spener, F., Knudsen, J. Revision of the amino acid sequence of human heart fatty acid-binding protein. In Cellular Fatty Acid-binding Proteins 127–133 (Springer, Boston, 1990).Dörmann, P. et al. Amino acid exchange and covalent modification by cysteine and glutathione explain isoforms of fatty acid-binding protein occurring in bovine liver. J. Biol. Chem. 268, 16286–16292 (1993).PubMed 
    Article 

    Google Scholar 
    Su, X. & Abumrad, N. A. Cellular fatty acid uptake: A pathway under construction. Trends Endocrinol. Metab. 20(2), 72–77 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    van Oort, M. M. et al. Each of the four intracellular cysteines of CD36 is essential for insulin-or AMP-activated protein kinase-induced CD36 translocation. Arch. Physiol. Biochem. 120, 40–49 (2014).PubMed 
    Article 
    CAS 

    Google Scholar 
    Wang, G., Bonkovsky, H. L., de Lemos, A. & Burczynski, F. J. Recent insights into the biological functions of liver fatty acid binding protein 1. J. Lipid Res. 56, 2238–2247 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Vallee, B. L. & Ulmer, D. D. Biochemical effects of mercury, cadmium, and lead. Annu. Rev. Biochem. 41, 91–128 (1972).CAS 
    PubMed 
    Article 

    Google Scholar 
    Aschner, M. & Syversen, T. Methylmercury: Recent advances in the understanding of its neurotoxicity. Ther. Drug Monit. 27, 278–283 (2005).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kenow, K. P., Meyer, M. W., Hines, R. K. & Karasov, W. H. Distribution and accumulation of mercury in tissues of captive-reared common loon (Gavia immer) chicks. Environ. Toxicol. Chem. 26, 1047–1055 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Varian-Ramos, C. W., Whitney, M., Rice, G. W. & Cristol, D. A. Form of dietary methylmercury does not affect total mercury accumulation in the tissues of zebra finch. Bull. Environ. Contam. Toxicol. 99, 1–8 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Rizzetti, D. A. et al. Chronic mercury at low doses impairs white adipose tissue plasticity. Toxicology 418, 41–50 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Richter, C. A. et al. Methylmercury-induced changes in gene transcription associated with neuroendocrine disruption in largemouth bass (Micropterus salmoides). Gen. Comp. Endocrinol. 203, 215–224 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Barnes, D. M., Hanlon, P. R. & Kircher, E. A. Effects of inorganic HgCl2 on adipogenesis. Toxicol. Sci. 75(2), 368–377 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    Corder, K. R., DeMoranville, K. J., Russell, D. E., Huss, J. M. & Schaeffer, P. J. Annual life-stage regulation of lipid metabolism and storage and association with PPARs in a migrant species: the gray catbird (Dumetella carolinensis). J. Exp. Biol. 219, 3391–3398 (2016).PubMed 

    Google Scholar 
    DeMoranville, K. J., Carter, W. A., Pierce, B. J. & McWilliams, S. R. Flight training in a migratory bird drives metabolic gene expression in the flight muscle but not liver, and dietary fat quality influences select genes. Am. J. Physiol.-Regul. Integr. Compar. Physiol. 319(6), R637–R652 (2020).CAS 
    Article 

    Google Scholar 
    Gavrilova, O. et al. Liver peroxisome proliferator-activated receptor γ contributes to hepatic steatosis, triglyceride clearance, and regulation of body fat mass. J. Biol. Chem. 278(36), 34268–34276 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bedoucha, M., Atzpodien, E. & Boelsterli, U. A. Diabetic KKAy mice exhibit increased hepatic PPARγ1 gene expression and develop hepatic steatosis upon chronic treatment with antidiabetic thiazolidinediones. J. Hepatol. 35, 17–23 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Egeler, O., Williams, T. D. & Guglielmo, C. G. Modulation of lipogenic enzymes, fatty acid synthase and Δ 9-desaturase, in relation to migration in the western sandpiper (Calidris mauri). J. Comp. Physiol. B 170, 169–174 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Klaper, R. et al. Use of a 15k gene microarray to determine gene expression changes in response to acute and chronic methylmercury exposure in the fathead minnow (Pimephales promelas). J. Fish Biol. 72, 2207–2280 (2008).CAS 
    Article 

    Google Scholar 
    Calow, P. Physiological costs of combating chemical toxicants: Ecological implications. Comp. Biochem. Physiol. C 100, 3–6 (1991).CAS 
    PubMed 
    Article 

    Google Scholar 
    Spalding, M. G. et al. Histologic, neurologic, and immunologic effects of methylmercury in captive great egrets. J. Wildl. Dis. 36, 423–435 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Carlson, J. R., Cristol, D. & Swaddle, J. P. Dietary mercury exposure causes decreased escape takeoff flight performance and increased molt rate in European starlings (Sturnus vulgaris). Ecotoxicology 23, 1464–1473 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Faaborg, J. et al. Conserving migratory land birds in the New World: Do we know enough?. Ecol. Appl. 20, 398–418 (2010).PubMed 
    Article 

    Google Scholar 
    Duijns, S. et al. Body condition explains migratory performance of a long-distance migrant. Proc. R. Soc. B https://doi.org/10.1098/rspb.2017.1374 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    Life table construction for crapemyrtle bark scale (Acanthococcus lagerstroemiae): the effect of different plant nutrient conditions on insect performance

    USDA, N. Census of Horticultural Specialties (USDA, 2014).
    Google Scholar 
    USDA, N. Census of Horticultural Specialties (USDA, 2019).
    Google Scholar 
    Soliman, A. S. & Shanan, N. T. The role of natural exogenous foliar applications in alleviating salinity stress in Lagerstroemia indica L. seedlings. J. Appl. Hortic. 19, 35–45 (2017).Article 

    Google Scholar 
    Chappell, M. R., Braman, S. K., Williams-Woodward, J. & Knox, G. J. J. o. E. H. Optimizing plant health and pest management of Lagerstroemia spp. in commercial production and landscape situations in the southeastern United States: A review. 30, 161–172 (2012).Gu, M., Merchant, M., Robbins, J. & Hopkins, J. Crape Myrtle Bark Scale: A New Exotic Pest. Texas A&M AgriLife Ext. Service. EHT 49 (2014).Kondo, T., Gullan, P. J. & Williams, D. J. Coccidology. The study of scale insects (Hemiptera: Sternorrhyncha: Coccoidea). Ciencia y Tecnología Agropecuaria 9, 55–61 (2008).Article 

    Google Scholar 
    Jiang, N. & Xu, H. Observertion on Eriococcus lagerostroemiae Kuwana. J. Anhui Agric. Coll. 25, 142–144 (1998).
    Google Scholar 
    He, D., Cheng, J., Zhao, H. & Chen, S. Biological characteristic and control efficacy of Eriococcus lagerstroemiae. Chin. Bull. Entomol. 45, 812–814 (2008).
    Google Scholar 
    Harcourt, D. The development and use of life tables in the study of natural insect populations. Annu. Rev. Entomol. 14, 175–196 (1969).Article 

    Google Scholar 
    Leslie, P. H. On the use of matrices in certain population mathematics. Biometrika 33, 183–212 (1945).MathSciNet 
    CAS 
    PubMed 
    MATH 
    Article 

    Google Scholar 
    Birch, L. The intrinsic rate of natural increase of an insect population. J. Anim. Ecol., 15–26 (1948).Chi, H. Life-table analysis incorporating both sexes and variable development rates among individuals. Environ. Entomol. 17, 26–34 (1988).Article 

    Google Scholar 
    Chi, H. & Liu, H. Two new methods for the study of insect population ecology. Bull. Inst. Zool. Acad. Sin 24, 225–240 (1985).
    Google Scholar 
    Fathipour, Y. & Maleknia, B. in Ecofriendly Pest Management for Food Security (ed Omkar) 329–366 (Academic Press, 2016).Auad, A. et al. The impact of temperature on biological aspects and life table of Rhopalosiphum padi (Hemiptera: Aphididae) fed with signal grass. Fla. Entomol. 569–577 (2009).Qu, Y. et al. Sublethal and hormesis effects of beta-cypermethrin on the biology, life table parameters and reproductive potential of soybean aphid Aphis glycines. Ecotoxicology 26, 1002–1009 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Araujo, E. S., Benatto, A., Mogor, A. F., Penteado, S. C. & Zawadneak, M. A. Biological parameters and fertility life table of Aphis forbesi Weed, 1889 (Hemiptera: Aphididae) on strawberry. Braz. J. Biol. 76, 937–941. https://doi.org/10.1590/1519-6984.04715 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    Krishnamoorthy, S. V. & Mahadevan, N. R. Life table studies of sugarcane scale, Melanaspis glomerata G. J. Entomol. Res. 27, 203–212 (2003).
    Google Scholar 
    Uematsu, H. Studies on life table for an armored scale insect, Aonidiella taxus Leonardi (Homoptera: Diaspididae). J. Fac. Agric. Kyushu Univ. (1979).Hill, M. G., Mauchline, N. A., Hall, A. J. & Stannard, K. A. Life table parameters of two armoured scale insect (Hemiptera: Diaspididae) species on resistant and susceptible kiwifruit (Actinidia spp.) germplasm. N. Z. J. Crop Hortic. Sci. 37, 335–343 (2009).Article 

    Google Scholar 
    Yong, C. X. W. Z. C. & Shaoyun, Z. J. Y. S. W. Age-specific life table of chinese white wax scale (Ericerus pela) natural population and analysis of death key factors. Scientia Silvae Sinica 9 (2008).Rosado, J. F. et al. Natural biological control of green scale (Hemiptera: Coccidae): a field life-table study. Biocontrol. Sci. Technol. 24, 190–202 (2014).Article 

    Google Scholar 
    Fand, B. B., Gautam, R. D., Chander, S. & Suroshe, S. S. Life table analysis of the mealybug, Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae) under laboratory conditions. J. Entomol. Res. 34, 175–179 (2010).
    Google Scholar 
    Vargas-Madríz, H. et al. Life and fertility table of Bactericera cockerelli (Hemiptera: Triozidae), under different fertilization treatments in the 7705 tomato hybrid. Rev. Chil. entomol. 39 (2014).Huang, Y. B. & Chi, H. Age-stage, two-sex life tables of Bactrocera cucurbitae (Coquillett)(Diptera: Tephritidae) with a discussion on the problem of applying female age-specific life tables to insect populations. Insect Sci. 19, 263–273 (2012).Article 

    Google Scholar 
    Saska, P. et al. Leaf structural traits rather than drought resistance determine aphid performance on spring wheat. J. Pest. Sci. 94, 423–434 (2021).Article 

    Google Scholar 
    Ma, K., Tang, Q., Xia, J., Lv, N. & Gao, X. Fitness costs of sulfoxaflor resistance in the cotton aphid, Aphis gossypii Glover. Pestic. Biochem. Physiol. 158, 40–46 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ullah, F. et al. Fitness costs in clothianidin-resistant population of the melon aphid, Aphis gossypii. PLoS ONE 15, e0238707 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Güncan, A. & Gümüş, E. Influence of different hazelnut cultivars on some demographic characteristics of the filbert aphid (Hemiptera: Aphididae). J. Econ. Entomol. 110, 1856–1862 (2017).PubMed 
    Article 

    Google Scholar 
    Bailey, R., Chang, N.-T., Lai, P.-Y. & Hsu, T.-C. Life table of cycad scale, Aulacaspis yasumatsui (Hemiptera: Diaspididae), reared on Cycas in Taiwan. J. Asia Pac. Entomol. 13, 183–187 (2010).Article 

    Google Scholar 
    Wang, Z., Chen, Y. & Diaz, R. Temperature-dependent development and host range of crapemyrtle bark scale, Acanthococcus lagerstroemiae (Kuwana)(Hemiptera: Eriococcidae). Fla. Entomol. 102, 181–186 (2019).Article 

    Google Scholar 
    Zhang, Z.-J. et al. A determining factor for insect feeding preference in the silkworm, Bombyx mori. PLoS Biol. 17, e3000162 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wang, Z., Chen, Y., Diaz, R. & Laine, R. A. Physiology of crapemyrtle bark scale, Acanthococcus lagerstroemiae (Kuwana), associated with seasonally altered cold tolerance. J. Insect Physiol. 112, 1–8 (2019).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Suh, S.-J. Notes on some parasitoids (Hymenoptera: Chalcidoidea) associated with Acanthococcus lagerstroemiae (Kuwana)(Hemiptera: Eriococcidae) in the Republic of Korea. Insecta mundi 0690, 1–5 (2019).
    Google Scholar 
    Meindl, G. A., Bain, D. J. & Ashman, T.-L. Edaphic factors and plant–insect interactions: Direct and indirect effects of serpentine soil on florivores and pollinators. Oecologia 173, 1355–1366 (2013).ADS 
    PubMed 
    Article 

    Google Scholar 
    Wielgolaski, F. E. Phenological modifications in plants by various edaphic factors. Int. J. Biometeorol. 45, 196–202 (2001).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Uchida, R. in Plant nutrient management in Hawaii’s soils (ed Raymond S. Uchida James A. Silva) 31–55 (University of Hawaii at Manoa, College of Agriculture & Tropical Resources, 2000).Flanders, S. E. Observations on host plant induced behavior of scale insects and their endoparasites. Can. Entomol. 102, 913–926 (1970).Article 

    Google Scholar 
    Yang, T.-C. & Chi, H. Life tables and development of Bemisia argentifolii (Homoptera: Aleyrodidae) at different temperatures. J. Econ. Entomol. 99, 691–698 (2006).PubMed 
    Article 

    Google Scholar 
    Tuan, S. J., Lee, C. C. & Chi, H. Population and damage projection of Spodoptera litura (F.) on peanuts (Arachis hypogaea L.) under different conditions using the age-stage, two-sex life table. Pest Manag. Sci. 70, 805–813 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Vafaie, E. et al. Seasonal population patterns of a new scale pest, Acanthococcus lagerstroemiae Kuwana (Hemiptera: Sternorrhynca: Eriococcidae), of Crapemyrtles in Texas, Louisiana, and Arkansas. J. Environ. Hortic. 38, 8–14 (2020).Article 

    Google Scholar 
    Vafaie, E. K. Bark and systemic insecticidal control of Acanthococcus (= Eriococcus) lagerstroemiae (Hemiptera: Eriococcidae) on Potted Crapemyrtles, 2017. Arthropod manag. tests 44, tsy109 (2019).Vafaie, E. K. & Knight, C. M. J. A. M. T. Bark and systemic insecticidal control of Acanthococcus (= Eriococcus) lagerstroemiae (Crapemyrtle Bark Scale) on Landscape Crapemyrtles, 2016. 42, tsx130 (2017).Vafaie, E. & Gu, M. Insecticidal control of crapemyrtle bark scale on potted crapemyrtles, Fall 2018. Arthropod. Manag. Tests 44, tsz061 (2019).Article 

    Google Scholar 
    Aktar, M. W., Sengupta, D. & Chowdhury, A. J. I. t. Impact of pesticides use in agriculture: their benefits and hazards. 2, 1 (2009).Grafton-Cardwell, E. & Vehrs, S. Monitoring for organophosphate-and carbamate-resistant armored scale (Homoptera: Diaspididae) in San Joaquin valley citrus. J. Econ. Entomol. 88, 495–504 (1995).CAS 
    Article 

    Google Scholar 
    Almarinez, B. J. M. et al. Biological control: A major component of the pest management program for the invasive coconut scale insect, Aspidiotus rigidus Reyne, in the Philippines. Insects 11, 745 (2020).PubMed Central 
    Article 

    Google Scholar 
    Grout, T. & Richards, G. Value of pheromone traps for predicting infestations of red scale, Aonidiella aurantii (Maskell)(Hom., Diaspididae), limited by natural enemy activity and insecticides used to control citrus thrips, Scirtothrips aurantii Faure (Thys., Thripidae). J. Appl. Entomol. 111, 20–27 (1991).Article 

    Google Scholar 
    Grafton-Cardwell, E., Millar, J., O’Connell, N. & Hanks, L. Sex pheromone of yellow scale, Aonidiella citrina (Homoptera: Diaspididae): Evaluation as an IPM tactic. J. Agric. Urban. Entomol. 17, 75–88 (2000).CAS 

    Google Scholar 
    Jactel, H., Menassieu, P., Lettere, M., Mori, K. & Einhorn, J. Field response of maritime pine scale, Matsucoccus feytaudi Duc. (Homoptera: Margarodidae), to synthetic sex pheromone stereoisomers. J. Chem. Ecol. 20, 2159–2170 (1994).CAS 
    PubMed 
    Article 

    Google Scholar 
    Mendel, Z. et al. Outdoor attractancy of males of Matsucoccus josephi (Homoptera: Matsucoccidae) and Elatophilus hebraicus (Hemiptera: Anthocoridae) to synthetic female sex pheromone of Matsucoccus josephi. J. Chem. Ecol. 21, 331–341 (1995).CAS 
    PubMed 
    Article 

    Google Scholar 
    Zada, A. et al. Sex pheromone of the citrus mealybug Planococcus citri: Synthesis and optimization of trap parameters. J. Econ. Entomol. 97, 361–368 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    Zhang, Z. & Shi, Y. Studies on the Morphology and Biology of Eriococcus Lagerstroemiae Kuwana. J. Shandong Agri. Univ. 2 (1986).Savopoulou-Soultani, M., Papadopoulos, N. T., Milonas, P. & Moyal, P. Abiotic factors and insect abundance. PSYCHE 2012 (2012).Vandegehuchte, M. L., de la Pena, E. & Bonte, D. Relative importance of biotic and abiotic soil components to plant growth and insect herbivore population dynamics. PLoS ONE 5, e12937 (2010).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Clavijo McCormick, A. Can plant–natural enemy communication withstand disruption by biotic and abiotic factors?. Ecol. Evol. 6, 8569–8582 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Nebapure, S. M. & Sagar, D. Insect-plant interaction: A road map from knowledge to novel technology. Karnataka J. Agric. Sci. 28, 1–7 (2015).
    Google Scholar 
    Murashige, T. & Skoog, F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15, 473–497 (1962).CAS 
    Article 

    Google Scholar 
    Hogendorp, B. K., Cloyd, R. A. & Swiader, J. M. Effect of nitrogen fertility on reproduction and development of citrus mealybug, Planococcus citri Risso (Homoptera: Pseudococcidae), feeding on two colors of coleus Solenostemon scutellarioides L. Codd. Environ. Entomol. 35, 201–211 (2006).Article 

    Google Scholar 
    Lema, K. & Mahungu, N. in Tropical root crops: Production and uses in Africa: proceedings of the Second Triennial Symposium of the International Society for Tropical Root Crops-Africa Branch held in Douala, Cameroon, 14-19 Aug. 1983. (IDRC, Ottawa, ON, CA).McClure, M. S. Dispersal of the scale Fiorinia externa (Homoptera: Diaspididae) and effects of edaphic factors on its establishment on hemlock. Environ. Entomol. 6, 539–544 (1977).Article 

    Google Scholar 
    Salama, H., Amin, A. & Hawash, M. Effect of nutrients supplied to citrus seedlings on their susceptibility to infestation with the scale insects Aonidiella aurantii (Maskell) and Lepidosaphes beckii (Newman)(Coccoidea). Zeitschrift für Angewandte Entomologie 71, 395–405 (1972).Article 

    Google Scholar 
    Rasmann, S. & Pellissier, L. in Climate Change and Insect Pests Vol. 8 (ed P. Niemelä C. Björkman) 38–53 (Wallingford, UK: CAB Int., 2015).Wang, Z. & Li, S. Effects of nitrogen and phosphorus fertilization on plant growth and nitrate accumulation in vegetables. J. Plant Nutr. 27, 539–556 (2004).CAS 
    Article 

    Google Scholar 
    Da Costa, P. B. et al. The effects of different fertilization conditions on bacterial plant growth promoting traits: Guidelines for directed bacterial prospection and testing. Plant Soil. 368, 267–280 (2013).Article 

    Google Scholar 
    Dong, H., Kong, X., Li, W., Tang, W. & Zhang, D. Effects of plant density and nitrogen and potassium fertilization on cotton yield and uptake of major nutrients in two fields with varying fertility. Field Crops Res. 119, 106–113 (2010).Article 

    Google Scholar 
    Aulakh, M., Dev, G. & Arora, B. Effect of sulphur fertilization on the nitrogen–sulphur relationships in alfalfa (Medicago sativa L. Pers.). Plant Soil. 45, 75–80 (1976).CAS 
    Article 

    Google Scholar 
    Powell, G., Tosh, C. R. & Hardie, J. Host plant selection by aphids: Behavioral, evolutionary, and applied perspectives. Annu. Rev. Entomol. 51, 309–330 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Sauge, M. H., Grechi, I. & Poëssel, J. L. Nitrogen fertilization effects on Myzus persicae aphid dynamics on peach: Vegetative growth allocation or chemical defence?. Entomol. Exp. Appl. 136, 123–133 (2010).CAS 
    Article 

    Google Scholar 
    Chen, Y., Serteyn, L., Wang, Z., He, K. & Francis, F. Reduction of plant suitability for corn leaf aphid (Hemiptera: Aphididae) under elevated carbon dioxide condition. Environ. Entomol. (2019).Miller, D. R. & Kosztarab, M. Recent advances in the study of scale insects. Annu. Rev. Entomol. 24, 1–27 (1979).CAS 
    Article 

    Google Scholar 
    Hardy, N. B., Peterson, D. A. & Normark, B. B. Scale insect host ranges are broader in the tropics. Biol. Lett. 11, 20150924 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Chen, Q. et al. Age-stage, two-sex life table of Parapoynx crisonalis (Lepidoptera: Pyralidae) at different temperatures. PLoS ONE 12, e0173380 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Li, X. et al. Density-dependent demography and mass-rearing of Carposina sasakii (Lepidoptera: Carposinidae) incorporating life table variability. J. Econ. Entomol. 112, 255–265 (2019).PubMed 
    Article 

    Google Scholar 
    Ning, S., Zhang, W., Sun, Y. & Feng, J. Development of insect life tables: comparison of two demographic methods of Delia antiqua (Diptera: Anthomyiidae) on different hosts. Sci. Rep. 7, 1–10 (2017).ADS 
    Article 

    Google Scholar 
    TWOSEX-MSChart: A computer program for the age-stage, two-sex life table analysis (2020).Goodman, D. Optimal life histories, optimal notation, and the value of reproductive value. Am. Nat. 119, 803–823 (1982).MathSciNet 
    Article 

    Google Scholar 
    Efron, B. & Tibshirani, R. J. An Introduction to the Bootstrap (CRC Press, 1994).MATH 
    Book 

    Google Scholar  More

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    Anisogamy explains why males benefit more from additional matings

    Lehtonen12 presents three simple models with the same broad structure: a single mutant individual with divergent mating behaviour arises in a population of ‘residents’ that all play the same strategy, and the success of that mutant is then followed (Figs. 1, 2). Specifically, Lehtonen investigates the fitness benefits of increased mating for mutant males in comparison to mutant females. Two important parameters can be varied: (i) the degree of anisogamy (defined here as the ratio of sperm number to egg number), which captures how divergent males and females are in the size (and thus number) of gametes they produce, and (ii) the efficiency of fertilisation, which determines how easily gametes can find and fuse with each other. If fertilisation is highly efficient, then gametes of the less numerous type will achieve nearly full fertilisation; on the other hand, inefficient fertilisation can result in gametes of both sexes going unfertilised.Fig. 2: Structure of the three models of Lehtonen12, showing differences in mating behaviour between resident males (green), resident females (blue) and mutant males and females (both yellow).For illustration, we suppose that females produce four eggs each and males produce eight sperm (the anisogamy ratio in nature is typically much higher). In Model 1, resident individuals spawn monogamously in a ‘nest’ (black outline), whereas mutant males and females can bring additional partners to their nest to spawn in a group. In Model 2, resident individuals divide their gametes equally among m spawning groups, each consisting of m individuals of each sex (shown here with m = 2). Mutant males and females instead divide their gametes among a larger or smaller number of groups, mmutant (shown here with mmutant = 4). In Model 3, there is a further sex asymmetry in addition to anisogamy: Fertilisation takes place inside the female’s body. Resident individuals mate with m partners (shown here with m = 2), whereas mutant males and females mate with a larger or smaller number of partners, mmutant (shown here with mmutant = 4).Full size imageIn the first two models, fertilisation is external and no assumptions are made about pre-existing differences between the sexes apart from the number of gametes they produce. In other words, males and females are identical except that males produce sperm in greater numbers than females produce eggs. In Model 1, resident individuals are assumed to mate monogamously, whereas a mutant can monopolise multiple partners of the opposite sex (Fig. 2). Importantly, both male and female mutants can bring additional partners back to their ‘nest’ to spawn in a group. When fertilisation is highly efficient, females can fertilise all of their eggs by bringing back a single male, and there is simply no benefit (in this model) of seeking further partners (Fig. 1A). In contrast, anisogamy means that males always produce at least some gametes in excess, and thus can benefit from seeking additional mates. When fertilisation is inefficient, however, both sexes benefit from increasing the concentration of opposite-sex gametes at their ‘nest’ (Fig. 1B). This latter benefit is sex-symmetric, whereas the former continues to apply only to males. As a consequence, the Bateman gradients are always steeper for males than for females (Fig. 1A, B), confirming Bateman’s argument.Model 2 similarly assumes external fertilisation, but in this case the resident males and females meet in groups consisting of m individuals of each sex (Fig. 2). Fertilisation occurs via group spawning. It is assumed that each resident individual divides its gametes evenly across M groups, whereas mutant individuals can instead spread their gametes over a larger or smaller number of groups (note that the author assumes that M = m, but this assumption could be relaxed without undermining the core argument). Spreading gametes out across a larger number of spawning groups does not increase the concentration of opposite-sex gametes they encounter (Fig. 2). However, a mutant that spreads its gametes more widely reduces the density of its own gametes across those groups in which it spawns. This in turn results in there being more opposite-sex gametes for each gamete of the mutant’s sex in those groups. For example, in Fig. 2, mutant males spawn in twice as many groups as resident males and thereby halve the density of their own sperm in each group. The resulting egg-to-sperm ratio of (frac{4}{6}=frac{2}{3}) is more favourable than the ratio of (frac{4}{8}=frac{1}{2}) that the resident males experience. Mutant females can similarly increase local sperm-to-egg ratios by spreading their eggs over more groups. However, in contrast to males, this only leads to fitness benefit if fertilisation is inefficient, and even then the benefit to females is very modest (scarcely perceptible in Fig. 1D). Gamete spreading reduces wasteful competition among the mutants’ own gametes for fertilisation. Such ‘local’ gamete competition, like gamete competition more generally, is stronger among sperm than among eggs because sperm are more numerous under anisogamy13,14. Consequently, as in Model 1, Bateman gradients are always steeper in males (Fig. 1C, D). Recall that the results of the above models emerge in the absence of any assumptions beyond the sex difference in the number of gametes produced.The third and final model allows for a further pre-existing difference between the sexes in addition to anisogamy: internal fertilisation, which is common and widespread in animals (Fig. 2)15. Each female is assumed to mate with m males, while each male divides his gametes evenly among m females. As in the previous two models, males benefit more than females from additional matings under most conditions. However, in the particular case where fertilisation is highly inefficient and the ratio of sperm to eggs is not too large, the pattern can theoretically reverse, such that female Bateman gradients exceed their male counterparts (Fig. 1F). The reason is that the effects of gamete concentration are asymmetric under internal fertilisation: Multiple mating by a female increases the local concentration of sperm its eggs experience, whereas a male’s multiple mating does not increase the concentration of eggs around its sperm (Fig. 2). Under conditions of severe sperm limitation—due to both weak anisogamy and highly inefficient fertilisation—this can lead to females benefitting more from additional matings than males (Fig. 1F). Although intriguing, it is unclear whether this finding has any empirical relevance, as sperm limitation is probably rarely severe in internal fertilisers. Under more realistic conditions of moderate to high fertilisation rates, sex differences in the degree of local gamete competition once again become decisive, and male Bateman gradients exceed their female counterparts (Fig. 1E). More