More stories

  • in

    Climate change disturbs wildlife microbiomes

    1.
    Baquero, F. & Nombela, C. Clin. Microbiol. Infec. 18(Suppl. 4), 2–4 (2012).
    2.
    Roughgarden, J., Gilbert, S. F., Rosenberg, E., Zilber-Rosenberg, I. & Lloyd, E. A. Biol. Theory 13, 44–65 (2018).
    Article  Google Scholar 

    3.
    Greenspan, S. E. et al. Nat. Clim. Change https://doi.org/10.1038/s41558-020-0899-5 (2020).

    4.
    Caporaso, J. G. et al. Proc. Natl Acad. Sci. USA 108, 4516–4522 (2011).
    CAS  Article  Google Scholar 

    5.
    Cho, I. & Blaser, M. J. Nat. Rev. Genet. 13, 260–270 (2012).
    CAS  Article  Google Scholar 

    6.
    Walke, J. B. et al. ISME J. 8, 2207–2217 (2014).
    CAS  Article  Google Scholar 

    7.
    Antwis, R. E. et al. PLoS ONE 9, e85563 (2014).
    Article  Google Scholar 

    8.
    Heiman, M. L. & Greenway, F. L. Mol. Metab. 5, 317–320 (2016).
    CAS  Article  Google Scholar 

    9.
    Romero, G. Q. et al. Nat. Commun. 11, 3215 (2020).
    CAS  Article  Google Scholar 

    10.
    Sabagh, L. T. et al. Copeia 2012, 683–689 (2012).
    Article  Google Scholar  More

  • in

    Winter in a warming Arctic

    1.
    Cooper, E. J. Annu. Rev. Ecol. Evol. S. 45, 271–295 (2014).
    Article  Google Scholar 
    2.
    Rapacz, M. et al. Plant Sci. 225, 34–44 (2014).
    CAS  Article  Google Scholar 

    3.
    Bokhorst, S., Bjerke, J. W., Tømmervik, H., Preece, C. & Phoenix, G. K. Ambio 41, 246–255 (2012).
    Article  Google Scholar 

    4.
    Niitynen, P. et al. Nat. Clim. Change https://doi.org/10.1038/s41558-020-00916-4 (2020).

    5.
    Blok, D. et al. Environ. Res. Lett. 6, 035502 (2011).
    Article  Google Scholar 

    6.
    Elmendorf, S. C. et al. Nat. Clim. Change 2, 453–457 (2012).
    Article  Google Scholar 

    7.
    Myers-Smith, I. H. et al. Nat. Clim. Change 5, 887–891 (2015).
    Article  Google Scholar 

    8.
    Snow, Water, Ice and Permafrost in the Arctic (SWIPA) (Arctic Monitoring and Assessment Programme (AMAP), 2017).

    9.
    Zhu, L. K., Ives, A. R., Zhang, C., Guo, Y. Y. & Radeloff, V. C. Nat. Clim. Change 9, 886–893 (2019).
    Article  Google Scholar  More

  • in

    A framework for in situ molecular characterization of coral holobionts using nanopore sequencing

    1.
    Hughes, T. P. et al. Global warming and recurrent mass bleaching of corals. Nature 543, 373–377. https://doi.org/10.1038/nature21707 (2017).
    ADS  CAS  Article  PubMed  Google Scholar 
    2.
    LaJeunesse, T. C. et al. Systematic revision of symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28, 2570–2580. https://doi.org/10.1016/j.cub.2018.07.008 (2018).
    CAS  Article  PubMed  Google Scholar 

    3.
    Bourne, D. G., Morrow, K. M. & Webster, N. S. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu. Rev. Microbiol. 70, 317–340. https://doi.org/10.1146/annurev-micro-102215-095440 (2016).
    CAS  Article  PubMed  Google Scholar 

    4.
    Peixoto, R. S., Rosado, P. M., Leite, D. C. D., Rosado, A. S. & Bourne, D. G. Beneficial microorganisms for corals (BMC): proposed mechanisms for coral health and resilience. Front. Microbiol. https://doi.org/10.3389/Fmicb.2017.00341 (2017).
    Article  PubMed  PubMed Central  Google Scholar 

    5.
    Reshef, L., Koren, O., Loya, Y., Zilber-Rosenberg, I. & Rosenberg, E. The coral probiotic hypothesis. Environ. Microbiol. 8, 2068–2073. https://doi.org/10.1111/j.1462-2920.2006.01148.x (2006).
    CAS  Article  PubMed  Google Scholar 

    6.
    Lesser, M. P. et al. Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar. Ecol. Prog. Ser. 346, 143–152. https://doi.org/10.3354/meps07008 (2007).
    ADS  CAS  Article  Google Scholar 

    7.
    Ben-Haim, Y. et al. Vibrio coralliilyticus sp. nov., a temperature-dependent pathogen of the coral Pocillopora damicornis. Int. J. System. Evol. Microbiol. 53, 309–315. https://doi.org/10.1099/ijs.0.02402-0 (2003).
    CAS  Article  Google Scholar 

    8.
    Johnston, E. C. et al. A genomic glance through the fog of plasticity and diversification in Pocillopora. Sci. Rep. https://doi.org/10.1038/S41598-017-06085-3 (2017).
    Article  PubMed  PubMed Central  Google Scholar 

    9.
    Shearer, T. L., Van Oppen, M. J., Romano, S. L. & Worheide, G. Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol. Ecol. 11, 2475–2487 (2002).
    CAS  Article  Google Scholar 

    10.
    Hellberg, M. E. No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evol. Biol. 6, 24. https://doi.org/10.1186/1471-2148-6-24 (2006).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    11.
    Wares, J. P. Mitochondrial cytochrome b sequence data are not an improvement for species identification in scleractinian corals. PeerJ 2, e564. https://doi.org/10.7717/peerj.564 (2014).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    12.
    Arrigoni, R. et al. A new sequence data set of SSU rRNA gene for Scleractinia and its phylogenetic and ecological applications. Mol. Ecol. Resour. 17, 1054–1071. https://doi.org/10.1111/1755-0998.12640 (2017).
    CAS  Article  PubMed  Google Scholar 

    13.
    Suzuki, G. & Nomura, K. Species boundaries of Astreopora corals (Scleractinia, Acroporidae) inferred by mitochondrial and nuclear molecular markers. Zool. Sci. 30, 626–632. https://doi.org/10.2108/zsj.30.626 (2013).
    CAS  Article  PubMed  Google Scholar 

    14.
    Gelin, P., Postaire, B., Fauvelot, C. & Magalon, H. Reevaluating species number, distribution and endemism of the coral genus Pocillopora Lamarck, 1816 using species delimitation methods and microsatellites. Mol. Phylogenet. Evol. 109, 430–446. https://doi.org/10.1016/j.ympev.2017.01.018 (2017).
    CAS  Article  PubMed  Google Scholar 

    15.
    LaJeunesse, T. C. Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the its region: In search of a “species” level marker. J. Phycol. 37, 866–880. https://doi.org/10.1046/j.1529-8817.2001.01031.x (2001).
    CAS  Article  Google Scholar 

    16.
    Hume, B. C. C. et al. An improved primer set and amplification protocol with increased specificity and sensitivity targeting the Symbiodinium ITS2 region. PeerJ 6, e4816. https://doi.org/10.7717/peerj.4816 (2018).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    17.
    Hume, B. C. C. et al. SymPortal: A novel analytical framework and platform for coral algal symbiont next-generation sequencing ITS2 profiling. Mol. Ecol. Resour. 19, 1063–1080. https://doi.org/10.1111/1755-0998.13004 (2019).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    18.
    Arif, C. et al. Assessing Symbiodinium diversity in scleractinian corals via next-generation sequencing-based genotyping of the ITS2 rDNA region. Mol. Ecol. 23, 4418–4433. https://doi.org/10.1111/mec.12869 (2014).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    19.
    Smith, E. G., Ketchum, R. N. & Burt, J. A. Host specificity of Symbiodinium variants revealed by an ITS2 metahaplotype approach. Isme J. 11, 1500–1503. https://doi.org/10.1038/ismej.2016.206 (2017).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    20.
    Ziegler, M. et al. Biogeography and molecular diversity of coral symbionts in the genus Symbiodinium around the Arabian Peninsula. J. Biogeogr. 44, 674–686. https://doi.org/10.1111/jbi.12913 (2017).
    Article  PubMed  PubMed Central  Google Scholar 

    21.
    Mouchka, M. E., Hewson, I. & Harvell, C. D. Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. Integr. Comp. Biol. 50, 662–674. https://doi.org/10.1093/icb/icq061 (2010).
    Article  PubMed  Google Scholar 

    22.
    Hernandez-Agreda, A., Leggat, W., Bongaerts, P. & Ainsworth, T. D. The microbial signature provides insight into the mechanistic basis of coral success across reef habitats. mBio https://doi.org/10.1128/mBio.00560-16 (2016).
    Article  PubMed  PubMed Central  Google Scholar 

    23.
    Neave, M. J., Apprill, A., Ferrier-Pages, C. & Voolstra, C. R. Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas. Appl. Microbiol. Biotechnol. 100, 8315–8324. https://doi.org/10.1007/s00253-016-7777-0 (2016).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    24.
    Hernandez-Agreda, A., Gates, R. D. & Ainsworth, T. D. Defining the Core Microbiome in Corals’ Microbial Soup. Trends Microbiol. 25, 125–140. https://doi.org/10.1016/j.tim.2016.11.003 (2017).
    CAS  Article  PubMed  Google Scholar 

    25.
    Roder, C., Bayer, T., Aranda, M., Kruse, M. & Voolstra, C. R. Microbiome structure of the fungid coral Ctenactis echinata aligns with environmental differences. Mol. Ecol. 24, 3501–3511. https://doi.org/10.1111/mec.13251 (2015).
    Article  PubMed  PubMed Central  Google Scholar 

    26.
    Pogoreutz, C. et al. Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome. Ecol. Evol. 8, 2240–2252. https://doi.org/10.1002/ece3.3830 (2018).
    Article  PubMed  PubMed Central  Google Scholar 

    27.
    Neave, M. J. et al. Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales. Isme J. 11, 186–200. https://doi.org/10.1038/ismej.2016.95 (2017).
    Article  PubMed  Google Scholar 

    28.
    Menegon, M. et al. On site DNA barcoding by nanopore sequencing. PLoS ONE 12, e0184741. https://doi.org/10.1371/journal.pone.0184741 (2017).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    29.
    Parker, J., Helmstetter, A. J., Devey, D., Wilkinson, T. & Papadopulos, A. S. T. Field-based species identification of closely-related plants using real-time nanopore sequencing. Sci. Rep. 7, 8345. https://doi.org/10.1038/s41598-017-08461-5 (2017).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    30.
    Pomerantz, A. et al. Real-time DNA barcoding in a rainforest using nanopore sequencing: opportunities for rapid biodiversity assessments and local capacity building. Gigascience https://doi.org/10.1093/gigascience/giy033 (2018).
    Article  PubMed  PubMed Central  Google Scholar 

    31.
    Santos, A., van Aerle, R., Barrientos, L. & Martinez-Urtaza, J. Computational methods for 16S metabarcoding studies using Nanopore sequencing data. Comput. Struct. Biotechnol. J. 18, 296–305. https://doi.org/10.1016/j.csbj.2020.01.005 (2020).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    32.
    Berntson, E. A., Bayer, F. M., McArthur, A. G. & France, S. C. Phylogenetic relationships within the Octocorallia (Cnidaria:Anthozoa) based on nuclear 18S rRNA sequences. Mar. Biol. 138, 235–246. https://doi.org/10.1007/s002270000457 (2001).
    CAS  Article  Google Scholar 

    33.
    Pootakham, W. et al. High resolution profiling of coral-associated bacterial communities using full-length 16S rRNA sequence data from PacBio SMRT sequencing system. Sci. Rep. 7, 2774. https://doi.org/10.1038/s41598-017-03139-4 (2017).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    34.
    Hume, B. et al. Corals from the Persian/Arabian Gulf as models for thermotolerant reef-builders: prevalence of clade C3 Symbiodinium, host fluorescence and ex situ temperature tolerance. Mar. Pollut. Bull. 72, 313–322. https://doi.org/10.1016/j.marpolbul.2012.11.032 (2013).
    CAS  Article  PubMed  Google Scholar 

    35.
    Hume, B. C. et al. Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world’s hottest sea, the Persian/Arabian Gulf. Sci. Rep. 5, 8562. https://doi.org/10.1038/srep08562 (2015).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    36.
    Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100. https://doi.org/10.1093/bioinformatics/bty191 (2018).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    37.
    Noonan, S. H. C., Fabricius, K. E. & Humphrey, C. Symbiodinium community composition in scleractinian corals is not affected by life-long exposure to elevated carbon dioxide. PLoS ONE https://doi.org/10.1371/journal.pone.0063985 (2013).
    Article  PubMed  PubMed Central  Google Scholar 

    38.
    Bayer, T. et al. Bacteria of the genus Endozoicomonas dominate the microbiome of the Mediterranean gorgonian coral Eunicella cavolini. Mar. Ecol. Prog. Ser. https://doi.org/10.3354/meps10197 (2013).
    Article  Google Scholar 

    39.
    Glasl, B., Herndl, G. J. & Frade, P. R. The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. Isme J. 10, 2280–2292. https://doi.org/10.1038/ismej.2016.9 (2016).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    40.
    Morrow, K. M. et al. Natural volcanic CO2 seeps reveal future trajectories for host-microbial associations in corals and sponges. Isme J. 9, 894–908. https://doi.org/10.1038/ismej.2014.188 (2015).
    CAS  Article  PubMed  Google Scholar 

    41.
    Morrow, K. M., Bromhall, K., Motti, C. A., Munn, C. B. & Bourne, D. G. Allelochemicals produced by brown macroalgae of the lobophora genus are active against coral larvae and associated bacteria, supporting pathogenic shifts to vibrio dominance. Appl. Environ. Microb. https://doi.org/10.1128/AEM.02391-16 (2017).
    Article  Google Scholar 

    42.
    Neave, M. J., Michell, C. T., Apprill, A. & Voolstra, C. R. Endozoicomonas genomes reveal functional adaptation and plasticity in bacterial strains symbiotically associated with diverse marine hosts. Sci. Rep. 7, 40579. https://doi.org/10.1038/srep40579 (2017).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    43.
    Cardenas, A. et al. Excess labile carbon promotes the expression of virulence factors in coral reef bacterioplankton. Isme J. 12, 59–76. https://doi.org/10.1038/ismej.2017.142 (2018).
    CAS  Article  PubMed  Google Scholar 

    44.
    Pollock, F. J. et al. Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny. Nat. Commun. https://doi.org/10.1038/S41467-018-07275-X (2018).
    Article  PubMed  PubMed Central  Google Scholar 

    45.
    Cardenas, A., Rodriguez, L. M., Pizarro, V., Cadavid, L. F. & Arevalo-Ferro, C. Shifts in bacterial communities of two caribbean reef-building coral species affected by white plague disease. Isme J. 6, 502–512. https://doi.org/10.1038/ismej.2011.123 (2012).
    CAS  Article  PubMed  Google Scholar 

    46.
    Gajigan, A. P., Diaz, L. A. & Conaco, C. Resilience of the prokaryotic microbial community of Acropora digitifera to elevated temperature. Microbiologyopen https://doi.org/10.1002/mbo3.478 (2017).
    Article  PubMed  PubMed Central  Google Scholar 

    47.
    Shnit-Orland, M., Sivan, A. & Kushmaro, A. Shewanella corallii sp. nov., a marine bacterium isolated from a Red Sea coral. Int. J. System. Evol. Microbiol. 60, 2293–2297. https://doi.org/10.1099/ijs.0.015768-0 (2010).
    CAS  Article  Google Scholar 

    48.
    Ziegler, M. et al. Coral microbial community dynamics in response to anthropogenic impacts near a major city in the central Red Sea. Mar. Pollut. Bull. 105, 629–640. https://doi.org/10.1016/j.marpolbul.2015.12.045 (2016).
    CAS  Article  PubMed  Google Scholar 

    49.
    Paramasivam, N. et al. Bacterial Consortium of Millepora dichotoma exhibiting unusual multifocal lesion event in the gulf of Eilat Red Sea. Microb Ecol 65, 50–59. https://doi.org/10.1007/s00248-012-0097-8 (2013).
    Article  PubMed  Google Scholar 

    50.
    Paramasivam, N., Ben-Dov, E., Arotsker, L. & Kushmaro, A. Eilatimonas milleporae gen. nov., sp. nov., a marine bacterium isolated from the hydrocoral Millepora dichotoma. Int. J. Syst. Evol. Microbiol. 63, 1880–1884. https://doi.org/10.1099/ijs.0.043976-0 (2013).
    CAS  Article  PubMed  Google Scholar 

    51.
    Spring, S., Lunsdorf, H., Fuchs, B. M. & Tindall, B. J. The photosynthetic apparatus and its regulation in the aerobic Gammaproteobacterium Congregibacter litoralis gen. nov., sp nov. PLoS ONE https://doi.org/10.1371/journal.pone.0004866 (2009).
    Article  PubMed  PubMed Central  Google Scholar 

    52.
    Roder, C. et al. Bacterial profiling of White Plague Disease in a comparative coral species framework. Isme J. 8, 31–39. https://doi.org/10.1038/ismej.2013.127 (2014).
    CAS  Article  PubMed  Google Scholar 

    53.
    Sekar, R., Mills, D. K., Remily, E. R., Voss, J. D. & Richardson, L. L. Microbial communities in the surface mucopolysaccharide layer and the black band microbial mat of black band-diseased Siderastrea siderea. Appl. Environ. Microbiol. 72, 5963–5973. https://doi.org/10.1128/AEM.00843-06 (2006).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    54.
    Blackall, L. L., Wilson, B. & van Oppen, M. J. Coral-the world’s most diverse symbiotic ecosystem. Mol. Ecol. 24, 5330–5347. https://doi.org/10.1111/mec.13400 (2015).
    Article  PubMed  Google Scholar 

    55.
    LaJeunesse, T. C. “Species” radiations of symbiotic Dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition (vol 22, pg 570, 2005). Mol. Biol. Evol. 22, 1158–1158. https://doi.org/10.1093/molbev/msi042 (2005).
    CAS  Article  Google Scholar 

    56.
    Hume, B. C. et al. Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change. Proc. Natl. Acad. Sci. USA 113, 4416–4421. https://doi.org/10.1073/pnas.1601910113 (2016).
    ADS  CAS  Article  PubMed  Google Scholar 

    57.
    Thornhill, D. J., Lewis, A. M., Wham, D. C. & LaJeunesse, T. C. Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evolution 68, 352–367. https://doi.org/10.1111/evo.12270 (2014).
    CAS  Article  PubMed  Google Scholar  More

  • in

    Revealing soil legacy phosphorus to promote sustainable agriculture in Brazil

    1.
    Godfray, H. C. J. et al. Food security: the challenge of feeding 9 billion people. Science 327, 812–818. https://doi.org/10.1126/science.1185383 (2010).
    ADS  CAS  Article  PubMed  Google Scholar 
    2.
    OECD/FAO. Agricultural Outlook 2018–2027, OECD Publishing, Paris/Food and Agriculture Organization of the United Nations, Rome. https://doi.org/10.1787/agr_outlook-2018-en (2018).

    3.
    FAO. The future of food and agriculture – Trends and challenges. Rome. (2017).

    4.
    Strassburg, B. B. N. et al. When enough should be enough: improving the use of current agricultural lands could meet production demands and spare natural habitats in Brazil. Glob. Environ. Chang. 28, 84–97 (2014).
    Article  Google Scholar 

    5.
    Bowman, M. S. et al. Persistence of cattle ranching in the Brazilian Amazon: a spatial analysis of the rationale for beef production. Land Use Policy 29, 558–568 (2012).
    Article  Google Scholar 

    6.
    Bustamante, M. M. C. et al. Estimating greenhouse gas emissions from cattle raising in Brazil. Clim. Chang. 115, 559–577 (2012).
    ADS  CAS  Article  Google Scholar 

    7.
    Oliveira, D. M. S. et al. Is the expansion of sugarcane over pasturelands a sustainable strategy for Brazil’s bioenergy industry?. Renew. Sust. Energy Rev. 102, 346–355 (2019).
    Article  Google Scholar 

    8.
    Roy, E. D. et al. Soil phosphorus sorption capacity after three decades of intensive fertilization in Mato Grosso, Brazil. Agric. Ecos. Environ. 249, 206–214 (2017).
    CAS  Article  Google Scholar 

    9.
    Jarvie, H. P. et al. The pivotal role of phosphorus in a resilient water–energy–food security nexus. J. Environ. Qual. 44, 1049–1062 (2015).
    CAS  Article  Google Scholar 

    10.
    ANDA – Associação Nacional para Difusão de Adubos. Indicadores – Fertilizantes entregues ao mercado. https://anda.org.br/index.php?mpg=03.00.00 (2017).

    11.
    U.S. Geological Survey. Mineral commodity summaries 2016. https://doi.org/10.3133/70140094 (2016).

    12.
    MacDonald, G. K., Bennett, E. M., Potter, P. A. & Ramankutty, N. Agronomic phosphorus imbalances across the world’s croplands. Proc. Nat. Acad. Sci. 108(7), 3086–3091. https://doi.org/10.1073/pnas.1010808108 (2011).
    ADS  Article  PubMed  Google Scholar 

    13.
    Lun, F. et al. Global and regional phosphorus budgets in agricultural systems and their implications for phosphorus-use efficiency. Earth Syst. Sci. Data 10, 1–18. https://doi.org/10.5194/essd-10-1-2018 (2018).
    ADS  Article  Google Scholar 

    14.
    Rodrigues, M., Pavinato, P. S., Withers, P. J. A., Teles, A. P. B. & Herrera, W. F. B. Legacy phosphorus and no tillage agriculture in tropical oxisols of the Brazilian savanna. Sci. Total Environ. 542, 1050–1061 (2016).
    ADS  CAS  Article  Google Scholar 

    15.
    Sattari, S. Z., Bouwman, A. F., Giller, K. E. & van Ittersum, M. K. Residual soil phosphorus as the missing piece in the global phosphorus crisis puzzle. Proc. Nat. Acad. Sci. 109, 6348–6353 (2012).
    ADS  CAS  Article  Google Scholar 

    16.
    Rowe, H. et al. Integrating legacy soil phosphorus into sustainable nutrient management practices on farms. Nutr. Cycl. Agroec. 104, 393–412 (2016).
    CAS  Article  Google Scholar 

    17.
    Shen, J. et al. Phosphorus dynamics: from soil to plant. Plant Phys. 156, 997–1005 (2011).
    CAS  Article  Google Scholar 

    18.
    IBGE – Instituto Brasileiro de Geografia e Estatística. Sistema IBGE de Recuperação Automática – SIDRA. Brasil. https://sidra.ibge.gov.br (2018).

    19.
    Projeto MapBiomas. Coleção 4.0 da Série Anual de Mapas de Cobertura e Uso de Solo do Brasil. https://mapbiomas.org (2019).

    20.
    Dias, L. C. P., Pimenta, F. M., Santos, A. B., Costa, M. H. & Ladle, R. J. Patterns of land use, extensification, and intensification of Brazilian agriculture. Glob. Chang. Biol. 22, 2887–2903 (2016).
    ADS  Article  Google Scholar 

    21.
    Du, E. et al. Global patterns of terrestrial nitrogen and phosphorus limitation. Nat. Geosci. 13, 221–226. https://doi.org/10.1038/s41561-019-0530-4 (2020).
    ADS  CAS  Article  Google Scholar 

    22.
    Withers, P. J. A. et al. Transitions to sustainable management of phosphorus in Brazilian agriculture. Sci. Rep. 8, 2537. https://doi.org/10.1038/s41598-018-20887-z (2018).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    23.
    FAO. World fertiliser trends and outlook to 2018. Rome. 53p. (2015).

    24.
    Kassam, A., Friedrich, T. & Derpsch, R. Global spread of conservation agriculture. Int. J. Environ. Studies. 76, 29–51. https://doi.org/10.1080/00207233.2018.1494927 (2018).
    CAS  Article  Google Scholar 

    25.
    Franchini, J. C. et al. Evolution of crop yields in different tillage and cropping systems over two decades in southern Brazil. Field Crops Res. 137, 178–185 (2012).
    Article  Google Scholar 

    26.
    Roy, E. D. et al. The phosphorus cost of agricultural intensification in the tropics. Nat. Plants 2, 16043. https://doi.org/10.1038/nplants.2016.43 (2016).
    CAS  Article  PubMed  Google Scholar 

    27.
    Schoumans, O. F., Bouraoui, F., Kabbe, C., Oenema, O. & van Dijk, K. C. Phosphorus management in Europe in a changing world. Ambio 44(Suppl. 2), S180–S192. https://doi.org/10.1007/s13280-014-0613-9 (2015).
    CAS  Article  PubMed  Google Scholar 

    28.
    Antoniadis, V., Hatzis, F., Bachtsevanidis, D. & Koutroubas, S. D. Phosphorus availability in low-P and acidic soils as affected by liming and P addition. Commun. Soil Sci. Plant Anal. 46, 1288–1298. https://doi.org/10.1080/00103624.2015.1033539 (2015).
    CAS  Article  Google Scholar 

    29.
    Bouwman, A. F., Beusen, A. H. W. & Billen, G. Human alteration of the global nitrogen and phosphorus soil balances for the period 1970–2050, Global Biogeoc. Cyc. 23, GB0A04. https://doi.org/10.1029/2009GB003576 (2009).

    30.
    Withers, P. J. A. et al. Stewardship to tackle global phosphorus inefficiency: the case of Europe. Ambio 44(2), 193–206 (2015).
    CAS  Article  Google Scholar 

    31.
    Soltangheisi, A. et al. Improving phosphorus sustainability of sugarcane production in Brazil. GCB Bioenergy 11, 1444–1455. https://doi.org/10.1111/gcbb.12650 (2019).
    CAS  Article  PubMed  Google Scholar 

    32.
    MacDonald, G. K. et al. Guiding phosphorus stewardship for multiple ecosystem services. Ecos. Health Sust. 2(12), e01251. https://doi.org/10.1002/ehs2.1251 (2016).
    Article  Google Scholar 

    33.
    Schipanski, M. E. et al. Realizing resilient food systems. Bioscience 66(7), 600–610. https://doi.org/10.1093/biosci/biw052 (2016).
    Article  Google Scholar 

    34.
    MAPA – Ministério da Agricultura, Pecuária e Abastecimento. Projeções do Agronegócio. Brasil 2015/16 a 2025/26. Projeções de Longo Prazo. 138p. (2016).

    35.
    Forest Act. Federal Law # 12,651. https://www.planalto.gov.br/ccivil_03/Ato2011-2014/2012/Lei/L12651compilado.htm (2012).

    36.
    Dias-Filho, M. B. Diagnóstico das Pastagens no Brasil. Embrapa Amazônia Oriental. Série Documentos 402. Belém-PA, 36p. (2014).

    37.
    Bouwman, A. F. et al. Lessons from temporal and spatial patterns in global use of N and P fertiliser on cropland. Sci. Rep. 7, 40366. https://doi.org/10.1038/srep40366 (2017).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    38.
    MacDonald, G. K., Bennett, E. M. & Carpenter, S. R. Embodied phosphorus and the global connections of United States agriculture. Environ. Res. Letters 7, 044024. https://doi.org/10.1088/1748-9326/7/4/044024 (2012).
    ADS  CAS  Article  Google Scholar 

    39.
    Novais, R.F., Smyth, T.J. & Nunes, F.N. Fósforo. In: Novais, R.F. et al. Fertilidade do solo. Viçosa, MG, Sociedade Brasileira de Ciência do Solo, p. 471–537 (2007).

    40.
    Negassa, W. & Leinweber, P. How does the Hedley sequential phosphorus fractionation reflect impacts of land use and management on soil phosphorus: a review. J. Plant Nutr. Soil Sci. 172, 305–325 (2009).
    CAS  Article  Google Scholar 

    41.
    CONAB – Companhia Nacional de Abastecimento. Acompanhamento da safra brasileira de grãos. Brasília. https://www.conab.gov.br/info-agro/safras/graos (2018).

    42.
    Dong, W. Y. et al. Responses of soil microbial communities and enzyme activities to nitrogen and phosphorus additions in Chinese fir plantations of subtropical China. Biogeosci. 12, 5537–5546. https://doi.org/10.5194/bg-12-5537-2015 (2015).
    ADS  Article  Google Scholar 

    43.
    Cherubin, M. R. et al. Sugarcane straw removal: Implications to soil fertility and fertiliser demand in Brazil. Bioeng. Res. 12, 888–900. https://doi.org/10.1007/s12155-019-10021-w (2019).
    CAS  Article  Google Scholar 

    44.
    Balemi, T. & Negisho, K. Management of soil phosphorus and plant adaptation mechanisms to phosphorus stress for sustainable crop production: a review. J. Soil Sci. Plant Nutr. 12(3), 547–562. https://doi.org/10.4067/S0718-95162012005000015 (2012).
    Article  Google Scholar 

    45.
    Khan, M. S., Zaidi, A. & Wani, P. A. Role of phosphate-solubilizing microorganisms in sustainable agriculture – a review. Agron. Sust. Develop. 27, 29–43. https://doi.org/10.1051/agro:2006011 (2007).
    Article  Google Scholar 

    46.
    Kalayu, G. Phosphate solubilizing microorganisms: promising approach as biofertilisers. Int. J. Agron. 2019, 4917256. https://doi.org/10.1155/2019/4917256 (2019).
    CAS  Article  Google Scholar 

    47.
    Simpson, R. J. et al. Strategies and agronomic interventions to improve the phosphorus-use efficiency of farming systems. Plant Soil 349, 89–120. https://doi.org/10.1007/s11104-011-0880-1 (2011).
    CAS  Article  Google Scholar 

    48.
    Almeida, D. S., Penn, C. J. & Rosolem, C. A. Assessment of phosphorus availability in soil cultivated with ruzigrass. Geoderma 312, 64–73 (2018).
    ADS  CAS  Article  Google Scholar 

    49.
    Bindraban, P. S., Dimkpa, C., Nagarajan, L., Roy, A. & Rabbinge, R. Revisiting fertilisers and fertilisation strategies for improved nutrient uptake by plants. Biol. Fert. Soils 51, 897–911. https://doi.org/10.1007/s00374-015-1039-7 (2015).
    CAS  Article  Google Scholar 

    50.
    Johnston, A. M. & Bruulsema, T. W. 4R nutrient stewardship for improved nutrient use efficiency. Procedia Eng. 83, 365–370. https://doi.org/10.1016/j.proeng.2014.09.029 (2014).
    Article  Google Scholar 

    51.
    Shigaki, F., Sharpley, A. & Prochnow, L. I. Animal-based agriculture, phosphorus management and water quality in Brazil: options for the future. Sci. Agric. 63(2), 194–209. https://doi.org/10.1590/S0103-90162006000200013 (2006).
    CAS  Article  Google Scholar 

    52.
    Almagro, A., Oliveira, P. T. S., Nearing, M. A. & Hagemann, S. Projected climate change impacts in rainfall erosivity over Brazil. Sci. Rep. 7, 8130. https://doi.org/10.1038/s41598-017-08298-y (2017).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    53.
    FAO – Food and agriculture organization. The world agricultural production. https://faostat.fao.org/site/339/default.aspx (2006).

    54.
    Nunes, S. P. O campo político da agricultura familiar e a idéia de “Projeto alternativo de desenvolvimento”. Master dissertation. Federal University of Paraná – UFPR. Curitiba. 152p. (2007).

    55.
    Alves, E., Teixeira Filho, A. & Tolloni, H. Demographic aspects of agricultural development: Brazil, 1950–74. In: Yeganiantz, L. (Ed.). Brazilian agriculture and agricultural research. Brasília: Embrapa, p. 9–60 (1984).

    56.
    IFA – International Fertiliser Association. Ifadata. https://ifadata.fertiliser.org/ucResult.aspx?temp=20160502093015 (2016).

    57.
    Marin, F. R., Pilau, F. G., Spolador, H. F. S., Otto, O. & Pedreira, C. G. S. Intensificação sustentável da agricultura brasileira, cenários para 2050. Rev. Pol. Agríc. XXV(3), 108–124 (2016).
    Google Scholar 

    58.
    Nicolella, A. C., Dragone, D. S. & Bacha, C. J. C. Determinantes da demanda de fertilizantes no Brasil no período de 1970 a 2002. Rev. Econ. Sociol. Rural 43(1), 81–100. https://doi.org/10.1590/S0103-20032005000100005 (2005).
    Article  Google Scholar 

    59.
    QGIS Development Team. QGIS Geographic Information System. Open Source Geospatial Foundation Project. https://qgis.osgeo.org (2018).

    60.
    CNA Brasil – Confederação Nacional da Agricultura. https://www.cnabrasil.org.br/noticias/assocon-divulga-crescimento-de-5-no-numero-de-bovinos-confinados-em-2017 (2017).

    61.
    Costa-Junior, C., Cerri, C. E., Pires, A. V. & Cerri, C. C. Net greenhouse gas emissions from manure management using anaerobic digestion technology in a beef cattle feedlot in Brazil. Sci. Total Environ. 505, 1018–1025 (2015).
    ADS  CAS  Article  Google Scholar 

    62.
    Prado, R. M., Caione, G. & Campos, C. N. S. Filter Cake and Vinasse as fertilisers contributing to conservation agriculture. Appl. Environ. Soil Sci. https://doi.org/10.1155/2013/581984 (2013).
    Article  Google Scholar 

    63.
    Francisco, E. A. B., Câmara, G. M. S. & Segatelli, C. R. Estado nutricional e produção do capim-pé-de-galinha e da soja cultivada em sucessão em sistema antecipado de adubação. Bragantia 66(2), 259–266 (2007).
    Article  Google Scholar 

    64.
    Pauletti, V. Nutrientes: teor e interpretação. Campinas: Fundação ABC/Fundação Cargill, 59p. (1998).

    65.
    Broch, D. L. & Ranno, S. K. Fertilidade do solo, Adubação e Nutrição da Cultura da Soja. In: Fundação MS, Tecnologia de Produção: Soja e Milho 2012/2013. Maracaju: Fundação MS, p. 2–38 (2012).

    66.
    Corrêa, J. C., Nicoloso, R. S., Menezes, J. F. S. & Benites, V. M. Critérios Técnicos para Recomendação de Biofertilizante de Origem Animal em Sistemas de Produção Agrícolas e Florestais. https://pt.engormix.com/suinocultura/artigos/biofertilizante-producao-agricolas-florestais-t37769.htm (2012).

    67.
    Rosseto, R., Dias, F. L. F., Vitti, A. C., Cantarella, H. & Landell, M. G. A. Manejo conservacionista e reciclagem de nutrientes em cana-de-açúcar tendo em vista a colheita mecânica. Inf. Agron. 124, 8–13 (2008).
    Google Scholar 

    68.
    Malavolta, E. Manual de Nutrição Mineral de Plantas (Agronômica Ceres, São Paulo, 2006).
    Google Scholar  More

  • in

    Urban resources limit pair coordination over offspring provisioning

    1.
    Royle, N. J., Smiseth, P. T. & Kölliker, M. The Evolution of Parental Care (Oxford University Press, Oxford, 2012).
    Google Scholar 
    2.
    Williams, G. C. Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am. Nat. 100, 687–690 (1966).
    Article  Google Scholar 

    3.
    Trivers, R. L. Sexual Selection and the Descent of Man 136–179 (Aldine Press, Chicago, 1972).
    Google Scholar 

    4.
    Lessells, C. M. The Evolution of Parental Care (Oxford Univeristy Press, Oxford, 2012).
    Google Scholar 

    5.
    Houston, A. I., Székely, T. & McNamara, J. M. Conflict between parents over care. Trends Ecol. Evol. 20, 33–38 (2005).
    Article  Google Scholar 

    6.
    Lessells, C. M. The evolutionary outcome of sexual conflict. Philos. Trans. R. Soc. B Biol. Sci. 361, 301–317 (2006).
    CAS  Article  Google Scholar 

    7.
    Houston, A. I. & Davies, N. B. The evolution of cooperation and life history in the dunnock, Prunella modularis. Behav. Ecol. Ecol. Conseq. Adapt. Behav. 20, 471–487 (1985).
    Google Scholar 

    8.
    McNamara, J. M., Gasson, C. E. & Houston, A. I. Incorporating rules for responding into evolutionary games. Nature 401, 368–371 (1999).
    ADS  CAS  PubMed  Google Scholar 

    9.
    McNamara, J. M., Houston, A. I., Barta, Z. & Osorno, J. L. Should young ever be better off with one parent than with two?. Behav. Ecol. 14, 301–310 (2003).
    Article  Google Scholar 

    10.
    Lessells, C. M. & McNamara, J. M. Sexual conflict over parental investment in repeated bouts: Negotiation reduces overall care. Proc. R. Soc. B Biol. Sci. 279, 1506–1514 (2012).
    CAS  Article  Google Scholar 

    11.
    Johnstone, R. A. & Hinde, C. A. Negotiation over offspring care – how should parents respond to each other’s efforts?. Behav. Ecol. 17, 818–827 (2006).
    Article  Google Scholar 

    12.
    Royle, N. J., Hartley, I. R. & Parker, G. A. Sexual conflict reduces offspring fitness in zebra finches. Nature 416, 733–736 (2002).
    ADS  CAS  Article  Google Scholar 

    13.
    Johnstone, R. A. et al. Reciprocity and conditional cooperation between great tit parents. Behav. Ecol. 25, 216–222 (2014).
    Article  Google Scholar 

    14.
    Savage, J. L., Browning, L. E., Manica, A., Russell, A. F. & Johnstone, R. A. Turn-taking in cooperative offspring care: By-product of individual provisioning behavior or active response rule?. Behav. Ecol. Sociobiol. 71, 162 (2017).
    Article  Google Scholar 

    15.
    Raihani, N. J., Nelson-Flower, M. J., Moyes, K., Browning, L. E. & Ridley, A. R. Synchronous provisioning increases brood survival in cooperatively breeding pied babblers. J. Anim. Ecol. 79, 44–52 (2010).
    Article  Google Scholar 

    16.
    Mariette, M. M. & Griffith, C. S. The adaptive significance of provisioning and foraging coordination between breeding partners. Am. Nat. 185, 270–280 (2015).
    Article  Google Scholar 

    17.
    Bebbington, K. & Hatchwell, B. J. Coordinated parental provisioning is related to feeding rate and reproductive success in a songbird. Behav. Ecol. 27, 652–659 (2016).
    Article  Google Scholar 

    18.
    Leniowski, K. & Węgrzyn, E. Synchronisation of parental behaviours reduces the risk of nest predation in a socially monogamous passerine bird. Sci. Rep. 8, 7385 (2018).
    ADS  CAS  Article  Google Scholar 

    19.
    Shen, S. F., Chen, H. C., Vehrencamp, S. L. & Yuan, H. W. Group provisioning limits sharing conflict among nestlings in joint-nesting Taiwan yuhinas. Biol. Lett. 6, 318–321 (2010).
    Article  Google Scholar 

    20.
    Savage, J. L. & Hinde, C. A. What can we quantify about carer behavior?. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00418 (2019).
    Article  Google Scholar 

    21.
    Baldan, D., Curk, T., Hinde, C. A. & Lessells, C. M. Alternation of nest visits varies with experimentally manipulated workload in brood-provisioning great tits. Anim. Behav. 156, 139–146. https://doi.org/10.1016/j.anbehav.2019.08.004 (2019).
    Article  Google Scholar 

    22.
    Griffioen, M., Müller, W. & Iserbyt, A. A fixed agreement—consequences of brood size manipulation on alternation in blue tits. PeerJ 7, e6826. https://doi.org/10.7717/peerj.6826 (2019).
    Article  PubMed  PubMed Central  Google Scholar 

    23.
    Iserbyt, A., Fresneau, N., Kortenhoff, T., Eens, M. & Muller, W. Decreasing parental task specialization promotes conditional cooperation. Sci. Rep. 7, 20 (2017).
    Article  Google Scholar 

    24.
    Baldan, D., Hinde, C. A. & Lessells, C. M. Turn-taking between provisioning parents: Partitioning alternation. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00448 (2019).
    Article  Google Scholar 

    25.
    Lejeune, L. et al. Environmental effects on parental care visitation patterns in blue tits Cyanistes caeruleus. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00356 (2019).
    Article  Google Scholar 

    26.
    Longcore, T. & Rich, C. Ecological light pollution. Front. Ecol. Environ. 2, 191–198. https://doi.org/10.1890/1540-9295(2004)002[0191:Elp]2.0.Co;2 (2004).
    Article  Google Scholar 

    27.
    Warren, P. S., Katti, M., Ermann, M. & Brazel, A. Urban bioacoustics: It’s not just noise. Anim. Behav. 71, 491–502. https://doi.org/10.1016/j.anbehav.2005.07.014 (2006).
    Article  Google Scholar 

    28.
    McCarthy, M. P., Best, M. J. & Betts, R. A. Climate change in cities due to global warming and urban effects. Geophys. Res. Lett. https://doi.org/10.1029/2010gl042845 (2010).
    Article  Google Scholar 

    29.
    Chamberlain, D. E. et al. Avian productivity in urban landscapes: A review and meta-analysis. Ibis 151, 1–18. https://doi.org/10.1111/j.1474-919X.2008.00899.x (2009).
    Article  Google Scholar 

    30.
    Pollock, C. J., Capilla-Lasheras, P., McGill, R. A. R., Helm, B. & Dominoni, D. M. Integrated behavioural and stable isotope data reveal altered diet linked to low breeding success in urban-dwelling blue tits (Cyanistes caeruleus). Sci. Rep. 7, 5014. https://doi.org/10.1038/s41598-017-04575-y (2017).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    31.
    Seress, G. et al. Impact of urbanization on abundance and phenology of caterpillars and consequences for breeding in an insectivorous bird. Ecol. Appl. 28, 1143–1156. https://doi.org/10.1002/eap.1730 (2018).
    Article  PubMed  Google Scholar 

    32.
    Seress, G., Sándor, K., Evans, K. L. & Liker, A. Food availability limits avian reproduction in the city: An experimental study on great tits Parus major. J. Anim. Ecol. 00, 1–11. https://doi.org/10.1111/1365-2656.13211 (2020).
    Article  Google Scholar 

    33.
    Wilkin, T. A., King, L. E. & Sheldon, B. C. Habitat quality, nestling diet, and provisioning behaviour in great tits Parus major. J. Avian Biol. 40, 135–145. https://doi.org/10.1111/j.1600-048X.2009.04362.x (2009).
    Article  Google Scholar 

    34.
    Peach, W. J., Mallord, J. W., Ockendon, N., Orsman, C. J. & Haines, W. G. Depleted suburban house sparrow Passer domesticus population not limited by food availability. Urban Ecosyst. 21, 1053–1065. https://doi.org/10.1007/s11252-018-0784-4 (2018).
    Article  Google Scholar 

    35.
    Schoech, S. J. et al. Food supplementation: A tool to increase reproductive output? A case study in the threatened Florida Scrub-Jay. Biol. Cons. 141, 162–173. https://doi.org/10.1016/j.biocon.2007.09.009 (2008).
    Article  Google Scholar 

    36.
    Sol, D., Lapiedra, O. & González-Lagos, C. Behavioural adjustments for a life in the city. Anim. Behav. 85, 1101–1112. https://doi.org/10.1016/j.anbehav.2013.01.023 (2013).
    Article  Google Scholar 

    37.
    Isaksson, C. & Andersson, S. Carotenoid diet and nestling provisioning in urban and rural great tits Parus major. J. Avian Biol. 38, 564–572. https://doi.org/10.1111/j.2007.0908-8857.04030.x (2007).
    Article  Google Scholar 

    38.
    New, T. R. Insect Conservation and Urban Environments (Springer, Berlin, 2015).
    Google Scholar 

    39.
    Helden, A., Stamp, G. & Leather, S. Urban biodiversity: Comparison of insect assemblages on native and non-native trees. Urban Ecosyst. 15, 611–624. https://doi.org/10.1007/s11252-012-0231-x (2012).
    Article  Google Scholar 

    40.
    Tallamy, D. W. & Shropshire, K. J. Ranking lepidopteran use of native versus introduced plants. Conserv. Biol. 23, 941–947 (2009).
    Article  Google Scholar 

    41.
    Burghardt, K. T., Tallamy, D. W., Philips, C. & Shropshire, K. J. Non-native plants reduce abundance, richness, and host specialization in lepidopteran communities. Ecosphere 1, art11. https://doi.org/10.1890/es10-00032.1 (2010).
    Article  Google Scholar 

    42.
    Marciniak, B., Nadolski, J., Nowakowska, M., Loga, B. & Bańbura, J. Habitat and annual variation in arthropod abundance affects blue tit Cyanistes caeruleus reproduction. Acta Ornithol. 42, 53–62 (2007).
    Article  Google Scholar 

    43.
    Neil, K. & Wu, J. Effects of urbanization on plant flowering phenology: A review. Urban Ecosyst. 9, 243–257. https://doi.org/10.1007/s11252-006-9354-2 (2006).
    Article  Google Scholar 

    44.
    Lessells, C. M. & Stephens, D. W. Central place foraging: Single-prey loaders again. Anim. Behav. 31, 238–243 (1983).
    Article  Google Scholar 

    45.
    Orians, G. H. & Pearson, N. E. On the Theory of Central Place Foraging. Analysis of Ecological Systems 155–177 (Ohio State University Press, Columbus, 1979).
    Google Scholar 

    46.
    Arnold, K. E., Ramsay, S. L., Henderson, L. & Larcombe, S. D. Seasonal variation in diet quality: Antioxidants, invertebrates and blue tits Cyanistes caeruleus. Biol. J. Lin. Soc. 99, 708–717. https://doi.org/10.1111/j.1095-8312.2010.01377.x (2010).
    Article  Google Scholar 

    47.
    Ouyang, J. Q., Baldan, D., Munguia, C. & Davies, S. Genetic inheritance and environment determine endocrine plasticity to urban living. Proc. R. Soc. B Biol. Sci. 286, 20191215. https://doi.org/10.1098/rspb.2019.1215 (2019).
    CAS  Article  Google Scholar 

    48.
    Newhouse, M. J., Marra, P. P. & Johnson, L. S. Reproductive success of house wrens in suburban and rural landscapes. Wilson J. Ornithol. 120, 99–104 (2008).
    Article  Google Scholar 

    49.
    Potti, J., Dávila, J. A., Tella, J. L., Frías, Ó & Villar, S. Gender and viability selection on morphology in fledgling pied flycatchers. Mol. Ecol. 11, 1317–1326. https://doi.org/10.1046/j.1365-294X.2002.01545.x (2002).
    CAS  Article  PubMed  Google Scholar 

    50.
    Balogh, A. L., Ryder, T. B. & Marra, P. P. Population demography of Gray Catbirds in the suburban matrix: Sources, sinks and domestic cats. J. Ornithol. 152, 717–726. https://doi.org/10.1007/s10336-011-0648-7 (2011).
    Article  Google Scholar 

    51.
    Stillfried, M. et al. Do cities represent sources, sinks or isolated islands for urban wild boar population structure?. J. Appl. Ecol. 54, 272–281. https://doi.org/10.1111/1365-2664.12756 (2017).
    Article  Google Scholar 

    52.
    Holmes, R. T. Foraging patterns of forest birds: Male–female differences. Wilson Bull. 98, 196–213 (1986).
    Google Scholar 

    53.
    Chaves, F. G., Vecchi, M. B. & Alves, M. A. S. Intersexual differences in the foraging behavior of Formicivora littoralis (Thamnophilidae), an endangered Neotropical bird. Stud. Neotrop. Fauna Environ. 52, 179–186. https://doi.org/10.1080/01650521.2017.1335275 (2017).
    Article  Google Scholar 

    54.
    Mänd, R., Rasmann, E. & Mägi, M. When a male changes his ways: Sex differences in feeding behavior in the pied flycatcher. Behav. Ecol. 24, 853–858. https://doi.org/10.1093/beheco/art025 (2013).
    Article  Google Scholar 

    55.
    Kölliker, M., Brinkhof, M. W. G., Heeb, P., Fitze, P. S. & Richner, H. The quantitative genetic basis of offspring solicitation and parental response in a passerine bird with biparental care. Proc. R. Soc. Lond. Ser. B Biol. Sci. 267, 2127–2132 (2000).
    Article  Google Scholar 

    56.
    Naef-Daenzer, B. Patch time allocation and patch sampling by foraging great and blue tits. Anim. Behav. 59, 989–999 (2000).
    CAS  Article  Google Scholar 

    57.
    Jarrett, C., Powell, L. L., McDevitt, H., Helm, B. & Welch, A. J. Bitter fruits of hard labour: Diet metabarcoding and telemetry reveal that urban songbirds travel further for lower-quality food. Oecologia 193, 377–388. https://doi.org/10.1007/s00442-020-04678-w (2020).
    ADS  Article  PubMed  PubMed Central  Google Scholar 

    58.
    Gering, J. C. & Blair, R. B. Predation on artificial bird nests along an urban gradient: Predatory risk or relaxation in urban environments?. Ecography 22, 532–541. https://doi.org/10.1111/j.1600-0587.1999.tb01283.x (1999).
    Article  Google Scholar 

    59.
    Fischer, J. D., Cleeton, S. H., Lyons, T. P. & Miller, J. R. Urbanization and the predation paradox: The role of trophic dynamics in structuring vertebrate communities. Bioscience 62, 809–818. https://doi.org/10.1525/bio.2012.62.9.6 (2012).
    Article  Google Scholar 

    60.
    Vincze, E. et al. Does urbanization affect predation of bird nests? A meta-analysis. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2017.00029 (2017).
    Article  Google Scholar 

    61.
    Griggio, M. & Hoi, H. An experiment on the function of the long-term pair bond period in the socially monogamous bearded reedling. Anim. Behav. 82, 1329–1335. https://doi.org/10.1016/j.anbehav.2011.09.016 (2011).
    Article  Google Scholar 

    62.
    Griffith, S. C. Cooperation and coordination in socially monogamous birds: Moving away from a focus on sexual conflict. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00455 (2019).
    Article  Google Scholar 

    63.
    Alberti, M. Eco-evolutionary dynamics in an urbanizing planet. Trends Ecol. Evol. 30, 114–126. https://doi.org/10.1016/j.tree.2014.11.007 (2015).
    Article  PubMed  Google Scholar 

    64.
    Liebl, A. L. & Martin, L. B. Exploratory behaviour and stressor hyper-responsiveness facilitate range expansion of an introduced songbird. Proc. Biol. Sci. 279, 4375–4381. https://doi.org/10.1098/rspb.2012.1606 (2012).
    Article  PubMed  PubMed Central  Google Scholar 

    65.
    Sepp, T., McGraw, K. J., Kaasik, A. & Giraudeau, M. A review of urban impacts on avian life-history evolution: Does city living lead to slower pace of life?. Glob. Change Biol. 24, 1452–1469. https://doi.org/10.1111/gcb.13969 (2018).
    ADS  Article  Google Scholar 

    66.
    Patricelli, G. L. & Blickley, J. L. Avian communication in urban noise: Causes and consequences of vocal adjustment. Auk 123, 639–649. https://doi.org/10.1093/auk/123.3.639 (2006).
    Article  Google Scholar 

    67.
    Grabarczyk, E. E. & Gill, S. A. Anthropogenic noise affects male house wren response to but not detection of territorial intruders. PLoS One 14, e0220576. https://doi.org/10.1371/journal.pone.0220576 (2019).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    68.
    Schroeder, J., Nakagawa, S., Cleasby, I. R. & Burke, T. Passerine birds breeding under chronic noise experience reduced fitness. PLoS One 7, e39200. https://doi.org/10.1371/journal.pone.0039200 (2012).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    69.
    Halfwerk, W. et al. Low-frequency songs lose their potency in noisy urban conditions. Proc. Natl. Acad. Sci. 108, 14549–14554. https://doi.org/10.1073/pnas.1109091108 (2011).
    ADS  Article  PubMed  Google Scholar 

    70.
    Mariette, M. M. Acoustic cooperation: Acoustic communication regulates conflict and cooperation within the family. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00445 (2019).
    Article  Google Scholar 

    71.
    Johnstone, R. A. & Savage, J. L. Conditional cooperation and turn-taking in parental care. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00335 (2019).
    Article  Google Scholar 

    72.
    Ihle, M., Pick, J. L., Winney, I. S., Nakagawa, S. & Burke, T. Measuring up to reality: Null models and analysis simulations to study parental coordination over provisioning offspring. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00142 (2019).
    Article  Google Scholar 

    73.
    Ihle, M. et al. Rearing success does not improve with apparent pair coordination in offspring provisioning. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2019.00405 (2019).
    Article  Google Scholar 

    74.
    Seress, G., Lipovits, A., Bokony, V. & Czuni, L. Quantifying the urban gradient: A practical method for broad measurements. Landsc. Urban Plan. 131, 42–50. https://doi.org/10.1016/j.landurbplan.2014.07.010 (2014).
    Article  Google Scholar 

    75.
    75Johnson, L. S. in The Birds of North America (ed Editor A. F. Poole) (2014).

    76.
    Pearse, A. T., Cavitt, J. F. & Cully, J. F. effects of food supplementation on female nest attentiveness and incubation mate feeding in two sympatric wren species. Wilson Bull. 116, 23–30 (2004).
    Article  Google Scholar 

    77.
    Greenewalt, C. H. & Jones, F. M. Photographic studies of the feeding of nestling house wrens. Proc. Am. Philos. Soc. 99, 200–204 (1955).
    Google Scholar 

    78.
    Welbers, A. A. M. H. et al. Artificial light at night reduces daily energy expenditure in breeding great tits (Parus major). Front. Ecol. Evol. https://doi.org/10.3389/fevo.2017.00055 (2017).
    Article  Google Scholar 

    79.
    Baldan, D. & Griggio, M. Pair coordination is related to later brood desertion in a provisioning songbird. Anim. Behav. 156, 147–152. https://doi.org/10.1016/j.anbehav.2019.08.002 (2019).
    Article  Google Scholar 

    80.
    Pinheiro J, Bates D, DebRoy S, Sarkar D & Team, R. C. nlme: Linear and nonlinear mixed effects models. (2019).

    81.
    Rolinski, S., Horn, H., Petzoldt, T. & Paul, L. Identifying cardinal dates in phytoplankton time series to enable the analysis of long-term trends. Oecologia 153, 997–1008 (2007).
    ADS  Article  Google Scholar 

    82.
    Douma, J. C. & Weedon, J. T. Analysing continuous proportions in ecology and evolution: A practical introduction to beta and Dirichlet regression. Methods Ecol. Evol. 10, 1412–1430. https://doi.org/10.1111/2041-210x.13234 (2019).
    Article  Google Scholar 

    83.
    Martin, E. mclogit: Multinomial logit models, with or without random effects or overdispersion (2020).

    84.
    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 48 (2015).
    Article  Google Scholar 

    85.
    Cohen, J. Statistical Power Analysis for the Behavioral Sciences (Lawrence Erlbaum Associates, Hillsdale, 1988).
    Google Scholar 

    86.
    Lakens, D. Calculating and reporting effect sizes to facilitate cumulative science: A practical primer for t-tests and ANOVAs. Front. Psychol. https://doi.org/10.3389/fpsyg.2013.00863 (2013).
    Article  PubMed  PubMed Central  Google Scholar 

    87.
    Lenth, R. emmeans: Estimated marginal means, aka least-squares means. (2020). More

  • in

    Coupled changes in soil organic carbon fractions and microbial community composition in urban and suburban forests

    1.
    Hui, D., Deng, Q., Tian, H. & Luo, Y. Climate Change and Carbon Sequestration in Forest Ecosystems 555–594 (Springer, New York, 2017).
    Google Scholar 
    2.
    Lal, R. & Augustin, B. Carbon Sequestration in Urban Ecosystems (Springer, Dordrecht, 2012).
    Google Scholar 

    3.
    Zhang, J. & Sta, P. Effects of urbanization on forest vegetation, soil and landscape. Acta Ecol. Sin. 19, 654–658 (1999).
    Google Scholar 

    4.
    George, K., Ziska, L. H., Bunce, J. A. & Quebedeaux, B. Elevated atmospheric CO2 concentration and temperature across an urban–rural transect. Atmos. Environ. 41, 7654–7665. https://doi.org/10.1016/j.atmosenv.2007.08.018 (2007).
    ADS  CAS  Article  Google Scholar 

    5.
    Pouyat, R. V. et al. Soil Carbon in Urban Forest Ecosystems (CRC Press, Cambridge, 2003).
    Google Scholar 

    6.
    Zhang, W. et al. Methane uptake in forest soils along an urban-to-rural gradient in Pearl River Delta, South China. Sci. Rep. 4, 5120. https://doi.org/10.1038/srep05120 (2014).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    7.
    Zhou, D. et al. Spatiotemporal trends of urban heat island effect along the urban development intensity gradient in China. Sci. Total Environ. 544, 617–626. https://doi.org/10.1016/j.scitotenv.2015.11.168 (2016).
    ADS  CAS  Article  PubMed  Google Scholar 

    8.
    Norman, J., MacLean, H. L. & Kennedy, C. A. Comparing high and low residential density: Life-cycle analysis of energy use and greenhouse gas emissions. J. Urban Plan. Dev. 132, 10–21. https://doi.org/10.1061//ASCE/0733-9488/2006/132:1/10 (2006).
    Article  Google Scholar 

    9.
    Carreiro, M. M. & Tripler, C. E. Forest remnants along urban-rural gradients: Examining their potential for global change research. Ecosystems 8, 568–582. https://doi.org/10.1007/s10021-003-0172-6 (2005).
    Article  Google Scholar 

    10.
    Meng, L. et al. Responses of ecosystem carbon cycle to experimental warming: A meta-analysis. Ecology 94, 726. https://doi.org/10.1890/12-0279.1 (2013).
    Article  Google Scholar 

    11.
    Lukac, M. et al. Forest soil carbon cycle under elevated CO2—A case of increased throughput?. Forestry 82, 75–86. https://doi.org/10.1093/forestry/cpn041 (2009).
    Article  Google Scholar 

    12.
    Luo, Y. & Weng, E. Dynamic disequilibrium of the terrestrial carbon cycle under global change. Trends Ecol. Evol. 26, 96–104. https://doi.org/10.1016/j.tree.2010.11.003 (2011).
    Article  PubMed  Google Scholar 

    13.
    Deng, Q. et al. Effects of CO2 enrichment, high nitrogen deposition and high precipitation on a model forest ecosystem in southern China. Chin. J. Plant Ecol. 33, 1023–1033 (2009).
    Google Scholar 

    14.
    De Graaff, M., Van Groenigen, K., Six, J. & Hungate, B. K. C. Interactions between plant growth and soil nutrient cycling under elevated CO2: A meta-analysis. Glob. Change Biol. 12, 2077–2091. https://doi.org/10.1111/j.1365-2486.2006.01240.x (2010).
    Article  Google Scholar 

    15.
    Chen, X., Deng, Q., Lin, G., Lin, M. & Wei, H. Changing rainfall frequency affects soil organic carbon concentrations by altering non-labile soil organic carbon concentrations in a tropical monsoon forest. Sci. Total Environ. 644, 762–769. https://doi.org/10.1016/j.scitotenv.2018.07.035 (2018).
    ADS  CAS  Article  PubMed  Google Scholar 

    16.
    Stockmann, U. et al. The knowns, known unknowns and unknowns of sequestration of soil organic carbon. Agric. Ecosyst. Environ. 164, 80–99. https://doi.org/10.1016/j.agee.2012.10.001 (2013).
    CAS  Article  Google Scholar 

    17.
    von Lützow, M. et al. SOM fractionation methods: Relevance to functional pools and to stabilization mechanisms. Soil Biol. Biochem. 39, 2183–2207. https://doi.org/10.1016/j.soilbio.2007.03.007 (2007).
    CAS  Article  Google Scholar 

    18.
    Garten, C. T. Comparison of forest soil carbon dynamics at five sites along a latitudinal gradient. Geoderma 167–168, 30–40. https://doi.org/10.1016/j.geoderma.2011.08.007 (2011).
    ADS  CAS  Article  Google Scholar 

    19.
    Mclauchlan, K. K. & Hobbie, S. E. Comparison of labile soil organic matter fractionation techniques. Soil Sci. Soc. Am. J. 68, S34–S34. https://doi.org/10.2136/sssaj2004.1616 (2004).
    Article  Google Scholar 

    20.
    von Lützow, M. et al. Stabilization of organic matter in temperate soils: Mechanisms and their relevance under different soil conditions—A review. Eur. J. Soil Sci. 57, 426–445. https://doi.org/10.1111/j.1365-2389.2006.00809.x (2006).
    CAS  Article  Google Scholar 

    21.
    Schmidt, M. W. et al. Persistence of soil organic matter as an ecosystem property. Nature 478, 49–56. https://doi.org/10.1038/nature10386 (2011).
    ADS  CAS  Article  PubMed  Google Scholar 

    22.
    Pan, G. et al. Soil carbon sequestration with bioactivity: A new emerging frontier for sustainable soil management. Adv. Earth Sci. 30, 940–951 (2015).
    CAS  Google Scholar 

    23.
    You, Y. et al. Relating microbial community structure to functioning in forest soil organic carbon transformation and turnover. Ecol. Evol. 4, 633–647. https://doi.org/10.1002/ece3.969 (2014).
    Article  PubMed  PubMed Central  Google Scholar 

    24.
    Shao, S. et al. Linkage of microbial residue dynamics with soil organic carbon accumulation during subtropical forest succession. Soil Biol. Biochem. 114, 114–120. https://doi.org/10.1016/j.soilbio.2017.07.007 (2017).
    CAS  Article  Google Scholar 

    25.
    Cotrufo, M. F., Wallenstein, M. D., Boot, C. M., Denef, K. & Paul, E. The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: Do labile plant inputs form stable soil organic matter?. Glob. Change Biol. 19, 988–995. https://doi.org/10.1111/gcb.12113 (2013).
    ADS  Article  Google Scholar 

    26.
    Newbound, M., Bennett, L. T., Tibbits, J. & Kasel, S. Soil chemical properties, rather than landscape context, influence woodland fungal communities along an urban-rural gradient. Austral. Ecol. 37, 236–247. https://doi.org/10.1111/j.1442-9993.2011.02269.x (2012).
    Article  Google Scholar 

    27.
    Chai, L. et al. Urbanization altered regional soil organic matter quantity and quality: Insight from excitation emission matrix (EEM) and parallel factor analysis (PARAFAC). Chemosphere 220, 249–258. https://doi.org/10.1016/j.chemosphere.2018.12.132 (2019).
    ADS  CAS  Article  PubMed  Google Scholar 

    28.
    Wang, Y. D., Wang, H. M., Xu, M. J., Ma, Z. Q. & Wang, Z. L. Soil organic carbon stocks and CO2 effluxes of native and exotic pine plantations in subtropical China. CATENA 128, 167–173. https://doi.org/10.1016/j.catena.2015.02.003 (2015).
    CAS  Article  Google Scholar 

    29.
    Zhou, G. et al. Old-growth forests can accumulate carbon in soils. Science 314, 1417. https://doi.org/10.1126/science.1130168 (2006).
    ADS  CAS  Article  PubMed  Google Scholar 

    30.
    Chen, H. et al. Changes in soil carbon sequestration in Pinus massoniana forests along an urban-to-rural gradient of southern China. Biogeosciences 10, 6609–6616. https://doi.org/10.5194/bg-10-6609-2013 (2013).
    ADS  CAS  Article  Google Scholar 

    31.
    Fang, Y. T., Gundersen, P., Mo, J. M. & Zhu, W. X. Input and output of dissolved organic and inorganic nitrogen in subtropical forests of South China under high air pollution. Biogeosciences 5, 339–352 (2008).
    ADS  CAS  Article  Google Scholar 

    32.
    Hou, E., Xiang, H., Li, J., Li, J. & Wen, D. Heavy metal contamination in soils of remnant natural and plantation forests in an urbanized region of the Pearl River Delta, China. Forests 5, 885–900. https://doi.org/10.3390/f5050885 (2014).
    Article  Google Scholar 

    33.
    Huang, L. The Characteristics of Remnant Lower Subtropical Evergreen Broad-Leaved Forests and Their Relationships with Environmental Factors in Urbanized Areas (South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, 2012).
    Google Scholar 

    34.
    Song, P. et al. Effects of historical logging on soil microbial communities in a subtropical forest in southern China. Plant Soil 397, 115–126. https://doi.org/10.1007/s11104-015-2553-y (2015).
    CAS  Article  Google Scholar 

    35.
    Sun, F. F., da Wen, Z., Kuang, Y. W., Li, J. & Zhang, J. G. Concentrations of sulphur and heavy metals in needles and rooting soils of Masson pine (Pinus massoniana L.) trees growing along an urban-rural gradient in Guangzhou, China. Environ. Monit. Assess. 154, 263–274. https://doi.org/10.1007/s10661-008-0394-3 (2009).
    CAS  Article  PubMed  Google Scholar 

    36.
    Groffman, P. M., Pouyat, R. V., McDonnell, M. J., Pickett, S. T. & Zipperer, W. C. Carbon pools and trace gas fluxes in urban forest soils. In Soil Management and Greenhouse Effect: Advances in Soil Science (eds Kimble, J. M. et al.) 147–158 (CRC Press, Amsterdam, 1995).
    Google Scholar 

    37.
    Koerner, B. A. & Klopatek, J. M. Carbon fluxes and nitrogen availability along an urban–rural gradient in a desert landscape. Urban Ecosyst. 13, 1–21. https://doi.org/10.1007/s11252-009-0105-z (2009).
    Article  Google Scholar 

    38.
    Dungait, J. A. J., Hopkins, D. W., Gregory, A. S. & Whitmore, A. P. Soil organic matter turnover is governed by accessibility not recalcitrance. Glob. Change Biol. 18, 1781–1796. https://doi.org/10.1111/j.1365-2486.2012.02665.x (2012).
    ADS  Article  Google Scholar 

    39.
    Leifeld, J. & Kögel-Knabner, I. Soil organic matter fractions as early indicators for carbon stock changes under different land-use?. Geoderma 124, 143–155. https://doi.org/10.1016/j.geoderma.2004.04.009 (2005).
    ADS  CAS  Article  Google Scholar 

    40.
    Pouyat, R., Groffman, P., Yesilonis, I. & Hernandez, L. Soil carbon pools and fluxes in urban ecosystems. Environ. Pollut. 116, S107–S118. https://doi.org/10.1016/s0269-7491(01)00263-9 (2002).
    CAS  Article  PubMed  Google Scholar 

    41.
    Nadelhoffer, K. J. & Raich, J. W. Fine root production estimates and belowground carbon allocation in forest ecosystems. Ecology 73, 1139–1147. https://doi.org/10.2307/1940664 (1992).
    Article  Google Scholar 

    42.
    Luo, Z., Feng, W., Luo, Y., Baldock, J. & Wang, E. Soil organic carbon dynamics jointly controlled by climate, carbon inputs, soil properties and soil carbon fractions. Glob. Change Biol. 23, 4430–4439. https://doi.org/10.1111/gcb.13767 (2017).
    ADS  Article  Google Scholar 

    43.
    Urbanová, M., Šnajdr, J. & Baldrian, P. Composition of fungal and bacterial communities in forest litter and soil is largely determined by dominant trees. Soil Biol. Biochem. 84, 53–64. https://doi.org/10.1016/j.soilbio.2015.02.011 (2015).
    CAS  Article  Google Scholar 

    44.
    Bowden, R. D. et al. litter input controls on soil carbon in a temperate deciduous forest. Soil Sci. Soc. Am. J. 78, S66–S75. https://doi.org/10.2136/sssaj2013.09.0413nafsc (2014).
    Article  Google Scholar 

    45.
    Carreiro, M. M., Howe, K., Parkhurst, D. F. & Pouyat, R. V. Variation in quality and decomposability of red oak leaf litter along an urban-rural gradient. Biol. Fertil. Soils 30, 258–268. https://doi.org/10.1007/s003740050617 (1999).
    Article  Google Scholar 

    46.
    Xu, X. & Hirata, E. Decomposition patterns of leaf litter of seven common canopy species in a subtropical forest: N and P dynamics. Plant Soil 273, 279–289. https://doi.org/10.1007/s11104-004-8069-5 (2005).
    CAS  Article  Google Scholar 

    47.
    Wang, Q., Wang, S., Feng, Z. & Huang, Y. Active soil organic matter and its relationship with soil quality. Acta Ecol. Sin. 25, 513–519 (2005).
    CAS  Google Scholar 

    48.
    Hu, S., Coleman, D. C., Carroll, C. R., Hendrix, P. F. & Beare, M. H. Labile soil carbon pools in subtropical forest and agricultural ecosystems as influenced by management practices and vegetation types. Agric. Ecosyst. Environ. 65, 69–78. https://doi.org/10.1016/s0167-8809(97)00049-2 (1997).
    CAS  Article  Google Scholar 

    49.
    Blair, G. J., Lefroy, R. & Lisle, L. Soil carbon fractions based on their degree of oxidation, and the development of a carbon management index for agricultural systems. Aust. J. Agric. Res. 46, 393–406. https://doi.org/10.1071/AR9951459 (1995).
    Article  Google Scholar 

    50.
    Chen, X. et al. Effects of precipitation on soil organic carbon fractions in three subtropical forests in southern China. J. Plant Ecol. 9(1), 10–19. https://doi.org/10.1093/jpe/rtv027 (2015).
    Article  Google Scholar 

    51.
    Culman, S. W. et al. Permanganate oxidizable carbon reflects a processed soil fraction that is sensitive to management. Soil Sci. Soc. Am. J. 76, 494. https://doi.org/10.2136/sssaj2011.0286 (2012).
    ADS  CAS  Article  Google Scholar 

    52.
    Chen, S., Wang, X. & Lu, F. Research on forest microbial community function variations in urban and suburban forests. Chin. J. Soil Sci. 1, 614–620. https://doi.org/10.1001/archophthalmol.2012.1393 (2012).
    Article  Google Scholar 

    53.
    Zhao, Z. & Guo, H. Effects of urbanization on the quantity changes of microbes in urban-to-rural gradient forest soil. J. Anhui Agric. Sci. 38, 5188–5190 (2010).
    Google Scholar 

    54.
    Hackl, E., Pfeffer, M., Donat, C., Bachmann, G. & Zechmeister-Boltenstern, S. Composition of the microbial communities in the mineral soil under different types of natural forest. Soil Biol. Biochem. 37, 661–671. https://doi.org/10.1016/j.soilbio.2004.08.023 (2005).
    CAS  Article  Google Scholar 

    55.
    Brant, J. B., Myrold, D. D. & Sulzman, E. W. Root controls on soil microbial community structure in forest soils. Oecologia 148, 650–659. https://doi.org/10.1007/s00442-006-0402-7 (2006).
    ADS  Article  PubMed  Google Scholar 

    56.
    Wang, H. et al. Stable soil organic carbon is positively linked to microbial-derived compounds in four plantations of subtropical China. Biogeosci. Discuss. 10, 18093–18119. https://doi.org/10.5194/bgd-10-18093-2013 (2013).
    ADS  Article  Google Scholar 

    57.
    Six, J., Frey, S. D., Thiet, R. K. & Batten, K. M. Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci. Soc. Am. J. 70, 555–569. https://doi.org/10.2136/sssaj2004.0347 (2006).
    ADS  CAS  Article  Google Scholar 

    58.
    Ziegler, S. E., Billings, S. A., Lane, C. S., Li, J. & Fogel, M. L. Warming alters routing of labile and slower-turnover carbon through distinct microbial groups in boreal forest organic soils. Soil Biol. Biochem. 60, 23–32. https://doi.org/10.1016/j.soilbio.2013.01.001 (2013).
    CAS  Article  Google Scholar 

    59.
    Baum, C., Fienemann, M., Glatzel, S. & Gleixner, G. Overstory-specific effects of litter fall on the microbial carbon turnover in a mature deciduous forest. For. Ecol. Manage. 258, 109–114. https://doi.org/10.1016/j.foreco.2009.03.047 (2009).
    Article  Google Scholar 

    60.
    Creamer, C. A. et al. Microbial community structure mediates response of soil C decomposition to litter addition and warming. Soil Biol. Biochem. 80, 175–188. https://doi.org/10.1016/j.soilbio.2014.10.008 (2015).
    CAS  Article  Google Scholar 

    61.
    Kramer, C. & Gleixner, G. Variable use of plant- and soil-derived carbon by microorganisms in agricultural soils. Soil Biol. Biochem. 38, 3267–3278. https://doi.org/10.1016/j.soilbio.2006.04.006 (2006).
    CAS  Article  Google Scholar 

    62.
    Brabcová, V., Štursová, M. & Baldrian, P. Nutrient content affects the turnover of fungal biomass in forest topsoil and the composition of associated microbial communities. Soil Biol. Biochem. 118, 187–198. https://doi.org/10.1016/j.soilbio.2017.12.012 (2018).
    CAS  Article  Google Scholar 

    63.
    Kaur, A., Chaudhary, A., Kaur, A., Choudhary, R. & Kaushik, R. Phospholipid fatty acid—A bioindicator of environment monitoring and assessment in soil ecosystem. Curr. Sci. 89, 1103–1112 (2005).
    CAS  Google Scholar 

    64.
    Hanson, C. A., Allison, S. D., Bradford, M. A., Wallenstein, M. D. & Treseder, K. K. Fungal taxa target different carbon sources in forest soil. Ecosystems 11, 1157–1167. https://doi.org/10.1007/s10021-008-9186-4 (2008).
    CAS  Article  Google Scholar 

    65.
    Liu, M., Hu, F. & Chen, X. A review on mechanisms of soil organic carbon stabilization. Acta Ecol. Sin. 27, 2642–2650 (2007).
    CAS  Article  Google Scholar 

    66.
    Fang, Y. et al. Nitrogen deposition and forest nitrogen cycling along an urban-rural transect in southern China. Glob. Change Biol. 17, 872–885. https://doi.org/10.1111/j.1365-2486.2010.02283.x (2011).
    ADS  Article  Google Scholar 

    67.
    Huang, L., Zhu, W., Ren, H., Chen, H. & Wang, J. Impact of atmospheric nitrogen deposition on soil properties and herb-layer diversity in remnant forests along an urban–rural gradient in Guangzhou, southern China. Plant Ecol. 213, 1187–1202. https://doi.org/10.1007/s11258-012-0080-y (2012).
    Article  Google Scholar 

    68.
    He, J. et al. Stoichiometric characteristics of soil C, N and P in subtropical forests along an urban-to-suburb gradient. Chin. J. Ecol. 35, 591–596 (2016).
    Google Scholar 

    69.
    Wu, J. et al. Prolonged acid rain facilitates soil organic carbon accumulation in a mature forest in Southern China. Sci. Total Environ. 544, 94–102. https://doi.org/10.1016/j.scitotenv.2015.11.025 (2016).
    ADS  CAS  Article  PubMed  Google Scholar 

    70.
    Duan, H., Liu, J., Deng, Q., Chen, X. & Zhang, D. Effects of elevated CO2 and N deposition on plant biomass accumulation and allocation in subtropical forest ecosystems: A mesocosm study. Chin. J. Plant Ecol. 33, 570–579. https://doi.org/10.1080/01443610410001685646 (2009).
    CAS  Article  Google Scholar 

    71.
    Chen, X., Liu, J., Deng, Q., Yan, J. & Zhang, D. Effects of elevated CO2 and nitrogen addition on soil organic carbon fractions in a subtropical forest. Plant Soil 357, 25–34. https://doi.org/10.1007/s11104-012-1145-3 (2012).
    CAS  Article  Google Scholar 

    72.
    Bird, J. A., Herman, D. J. & Firestone, M. K. Rhizosphere priming of soil organic matter by bacterial groups in a grassland soil. Soil Biol. Biochem. 43, 718–725. https://doi.org/10.1016/j.soilbio.2010.08.010 (2011).
    CAS  Article  Google Scholar 

    73.
    Hopkins, F. M. et al. Increased belowground carbon inputs and warming promote loss of soil organic carbon through complementary microbial responses. Soil Biol. Biochem. 76, 57–69. https://doi.org/10.1016/j.soilbio.2014.04.028 (2014).
    CAS  Article  Google Scholar 

    74.
    Curlevski, N. J. A., Drigo, B., Cairney, J. W. G. & Anderson, I. C. Influence of elevated atmospheric CO2 and water availability on soil fungal communities under Eucalyptus saligna. Soil Biol. Biochem. 70, 263–271. https://doi.org/10.1016/j.soilbio.2013.12.010 (2014).
    CAS  Article  Google Scholar 

    75.
    Crow, S. E. et al. Sources of plant-derived carbon and stability of organic matter in soil: Implications for global change. Glob. Change Biol. 15, 2003–2019. https://doi.org/10.1111/j.1365-2486.2009.01850.x (2009).
    ADS  Article  Google Scholar 

    76.
    Fontaine, S., Mariotti, A. & Abbadie, L. The priming effect of organic matter: A question of microbial competition?. Soil Biol. Biochem. 35, 837–843. https://doi.org/10.1016/s0038-0717(03)00123-8 (2003).
    CAS  Article  Google Scholar 

    77.
    Zhou, D., Zhao, S., Liu, S. & Zhang, L. Spatiotemporal trends of terrestrial vegetation activity along the urban development intensity gradient in China’s 32 major cities. Sci. Total Environ. 488–489, 136–145. https://doi.org/10.1016/j.scitotenv.2014.04.080 (2014).
    ADS  CAS  Article  PubMed  Google Scholar 

    78.
    Liu, L. et al. Interactive effects of nitrogen and phosphorus on soil microbial communities in a tropical forest. PLoS ONE 8, e61188. https://doi.org/10.1371/journal.pone.0061188 (2013).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    79.
    Saetre, P. & Bååth, E. Spatial variation and patterns of soil microbial community structure in a mixed spruce–birch stand. Soil Biol. Biochem. 32, 909–917. https://doi.org/10.1016/s0038-0717(99)00215-1 (2000).
    CAS  Article  Google Scholar 

    80.
    Bossio, D. A., Scow, K. M., Gunapala, N. & Graham, K. J. Determinants of soil microbial communities: Effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microb. Ecol. 36, 1–12. https://doi.org/10.1007/s002489900087 (1998).
    CAS  Article  PubMed  Google Scholar 

    81.
    Wei, H., Chen, X., He, J., Zhang, J. & Shen, W. Exogenous nitrogen addition reduced the temperature sensitivity of microbial respiration without altering the microbial community composition. Front. Microbiol. 8, 2382. https://doi.org/10.3389/fmicb.2017.02382 (2017).
    Article  PubMed  PubMed Central  Google Scholar  More

  • in

    Temporal tracking of quantum-dot apatite across in vitro mycorrhizal networks shows how host demand can influence fungal nutrient transfer strategies

    1.
    Wipf D, Krajinski F, van Tuinen D, Recorbet G, Courty P. Trading on the arbuscular mycorrhiza market: from arbuscules to common mycorrhizal networks. N Phytol. 2019;223:1–11.
    Article  CAS  Google Scholar 
    2.
    Miller RM, Jastrow JD, Reinhardt DR. External hyphal production of vesicular-arbuscular mycorrhizal fungi in pasture and tallgrass prairie communities. Oecologia. 1995;103:17–23.
    CAS  PubMed  Article  Google Scholar 

    3.
    Leake J, Johnson D, Donnelly D, Muckle G, Boddy L, Read DJ. Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Bot. 2004;82:1016–45.
    Article  Google Scholar 

    4.
    Bago B, Pfeffer PE, Shachar-Hill Y. Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol. 2000;124:949–58.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    5.
    Drigo B, Pijl AS, Duyts H, Kielak AM, Gamper HA, Houtekamer MJ, et al. Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc Natl Acad Sci. 2010;107:10938–42.
    CAS  PubMed  Article  Google Scholar 

    6.
    Giri B, Saxena B. Response of arbuscular mycorrhizal fungi to global climate change and their role in terrestrial ecosystem C and N cycling. In: Varma A, Prasad R, Tuteja N editors. Mycorrhiza—function, diversity, state of the art. Cham: Springer International Publishing; 2017. p. 305–27.

    7.
    Field KJ, Pressel S, Duckett JG, Rimington WR, Bidartondo MI. Symbiotic options for the conquest of land. Trends Ecol Evol. 2015;30:477–86.
    PubMed  Article  Google Scholar 

    8.
    Martin FM, Uroz S, Barker DG. Ancestral alliances: plant mutualistic symbioses with fungi and bacteria. Science. 2017;356:eaad4501.
    PubMed  Article  CAS  Google Scholar 

    9.
    Brundrett MC. Coevolution of roots and mycorrhizas of land plants. N Phytol. 2002;154:275–304.
    Article  Google Scholar 

    10.
    Werner GDA, Cornelissen JHC, Cornwell WK, Soudzilovskaia NA, Kattge J, West SA, et al. Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown. Proc Natl Acad Sci. 2018;115:5229–34.
    CAS  PubMed  Article  Google Scholar 

    11.
    Gange AC, Stagg PG, Ward LK. Arbuscular mycorrhizal fungi affect phytophagous insect specialism. Ecol Lett. 2002;5:11–5.
    Article  Google Scholar 

    12.
    Koricheva J, Gange AC, Jones T. Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology. 2009;90:2088–97.
    PubMed  Article  Google Scholar 

    13.
    Hart MM, Reader RJ, Klironomos JN. Plant coexistence mediated by arbuscular mycorrhizal fungi. Trends Ecol Evol. 2003;18:418–23.
    Article  Google Scholar 

    14.
    Hiiesalu I, Pärtel M, Davison J, Gerhold P, Metsis M, Moora M, et al. Species richness of arbuscular mycorrhizal fungi: associations with grassland plant richness and biomass. N Phytol. 2014;203:233–44.
    CAS  Article  Google Scholar 

    15.
    Gerz M, Bueno CG, Zobel M, Moora M. Plant community mycorrhization in temperate forests and grasslands: relations with edaphic properties and plant diversity. J Veg Sci. 2016;27:89–99.
    Article  Google Scholar 

    16.
    He X, Critchley C, Bledsoe C. Nitrogen transfer within and between plants through common mycorrhizal networks (CMNs). CRC Crit Rev Plant Sci. 2003;22:531–67.
    Article  Google Scholar 

    17.
    Smith, Sally E., and David J. Read. Mycorrhizal symbiosis. 3rd edn. (Academic press, London, 2008).

    18.
    Luginbuehl LH, Menard GN, Kurup S, Van Erp H, Radhakrishnan GV, Breakspear A, et al. Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science. 2017;356:1175–8.
    CAS  PubMed  Article  Google Scholar 

    19.
    Liu A, Hamel C, Hamilton RI, Ma BL, Smith DL. Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza. 2000;9:331–6.
    CAS  Article  Google Scholar 

    20.
    Azcón R, Ambrosano E, Charest C. Nutrient acquisition in mycorrhizal lettuce plants under different phosphorus and nitrogen concentration. Plant Sci. 2003;165:1137–45.
    Article  CAS  Google Scholar 

    21.
    Ramírez-Viga TK, Aguilar R, Castillo-Argüero S, Chiappa-Carrara X, Guadarrama P, Ramos-Zapata J. Wetland plant species improve performance when inoculated with arbuscular mycorrhizal fungi: a meta-analysis of experimental pot studies. Mycorrhiza. 2018;28:477–93.
    PubMed  Article  Google Scholar 

    22.
    Weremijewicz J, Janos DP. Common mycorrhizal networks amplify size inequality in Andropogon gerardii monocultures. N Phytol. 2013;198:203–13.
    CAS  Article  Google Scholar 

    23.
    Bücking H, Shachar-Hill Y. Phosphate uptake, transport and transfer by the arbuscular mycorrhizal fungus Glomus intraradices is stimulated by increased carbohydrate availability. N Phytol. 2005;165:899–912.
    Article  CAS  Google Scholar 

    24.
    Fellbaum CR, Gachomo EW, Beesetty Y, Choudhari S, Strahan GD, Pfeffer PE, et al. Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci. 2012;109:2666–71.
    CAS  PubMed  Article  Google Scholar 

    25.
    Fellbaum CR, Mensah JA, Cloos AJ, Strahan GE, Pfeffer PE, Kiers ET, et al. Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. N Phytol. 2014;203:646–56.
    CAS  Article  Google Scholar 

    26.
    Konvalinková T, Püschel D, Janoušková M, Gryndler M, Jansa J. Duration and intensity of shade differentially affects mycorrhizal growth- and phosphorus uptake responses of Medicago truncatula. Front Plant Sci. 2015;6:1–11.
    Article  Google Scholar 

    27.
    Zheng C, Ji B, Zhang J, Zhang F, Bever JD. Shading decreases plant carbon preferential allocation towards the most beneficial mycorrhizal mutualist. N Phytol. 2015;205:361–8.
    CAS  Article  Google Scholar 

    28.
    Varga S, Kytöviita M. Mycorrhizal benefit differs among the sexes in a gynodioecious species. Ecology. 2010;91:2583–93.
    PubMed  Article  Google Scholar 

    29.
    Merrild MP, Ambus P, Rosendahl S, Jakobsen I. Common arbuscular mycorrhizal networks amplify competition for phosphorus between seedlings and established plants. N Phytol. 2013;200:229–40.
    CAS  Article  Google Scholar 

    30.
    Walder F, Brulé D, Koegel S, Wiemken A, Boller T, Courty PE. Plant phosphorus acquisition in a common mycorrhizal network: regulation of phosphate transporter genes of the Pht1 family in sorghum and flax. N Phytol. 2015;205:1632–45.
    CAS  Article  Google Scholar 

    31.
    Weremijewicz J, Sternberg L, da SLO, Janos DP. Common mycorrhizal networks amplify competition by preferential mineral nutrient allocation to large host plants. N Phytol. 2016;212:461–71.
    CAS  Article  Google Scholar 

    32.
    Werner GDA, Kiers ET. Partner selection in the mycorrhizal mutualism. N Phytol. 2015;205:1437–42.
    Article  Google Scholar 

    33.
    Bachelot B, Lee CT. Dynamic preferential allocation to arbuscular mycorrhizal fungi explains fungal succession and coexistence. Ecology. 2018;99:372–84.
    PubMed  Article  Google Scholar 

    34.
    Wyatt GAK, Kiers ET, Gardner A, West SA. A biological market analysis of the plant-mycorrhizal symbiosis. Evolution. 2014;68:2603–18.
    PubMed  Article  Google Scholar 

    35.
    Noë R, Kiers ET. Mycorrhizal markets, firms, and co-ops. Trends Ecol Evol. 2018;33:777–89.
    PubMed  Article  Google Scholar 

    36.
    Bender SF, Wagg C, van der Heijden MGA. An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends Ecol Evol. 2016;31:440–52.
    PubMed  Article  Google Scholar 

    37.
    Konvalinková T, Jansa J. Lights off for arbuscular mycorrhiza: on its symbiotic functioning under light deprivation. Front Plant Sci. 2016;7:1–11.
    Article  Google Scholar 

    38.
    Whiteside MD, Werner GDAA, Caldas VEA, van’t Padje A, Dupin SE, Elbers B, et al. Mycorrhizal fungi respond to resource inequality by moving phosphorus from rich to poor patches across networks. Curr Biol. 2019;29:2043–50.e8.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    39.
    Bailey RE, Nie S. Alloyed semiconductor quantum dots: tuning the optical properties without changing the particle size. J Am Chem Soc. 2003;125:7100–6.
    CAS  PubMed  Article  Google Scholar 

    40.
    Jang E, Jun S, Pu L. High quality CdSeS nanocrystals synthesized by facile single injection process and their electroluminescence. Chem Commun. 2003;24:2964–5.

    41.
    Declerck S, Fortin JA, Strullu DG (eds). In vitro culture of mycorrhizas. Berlin, Heidelberg: Springer; 2005.

    42.
    Engelmoer DJP, Behm JE, Kiers ET. Intense competition between arbuscular mycorrhizal mutualists in an in vitro root microbiome negatively affects total fungal abundance. Mol Ecol. 2014;23:1584–93.
    CAS  PubMed  Article  Google Scholar 

    43.
    Ness RLL, Vlek PLG. Mechanism of calcium and phosphate release from hydroxy-apatite by mycorrhizal hyphae. Soil Sci Soc Am J. 2000;64:949–55.
    CAS  Article  Google Scholar 

    44.
    Tang I-M, Krishnamra N, Charoenphandhu N, Hoonsawat R, Pon-On W. Biomagnetic of apatite-coated cobalt ferrite: a core–shell particle for protein adsorption and pH-controlled release. Nanoscale Res Lett. 2010;6:19.
    PubMed  PubMed Central  Google Scholar 

    45.
    Kawashita M, Taninai K, Li Z, Ishikawa K, Yoshida Y. Preparation of low-crystalline apatite nanoparticles and their coating onto quartz substrates. J Mater Sci Mater Med. 2012;23:1355–62.
    CAS  PubMed  Article  Google Scholar 

    46.
    Sun S, Chan LS, Li Y-L. Flower-like apatite recording microbial processes through deep geological time and its implication to the search for mineral records of life on Mars. Am Miner. 2014;99:2116–25.
    Article  Google Scholar 

    47.
    Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, et al. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science. 2011;333:880–2.
    CAS  PubMed  Article  Google Scholar 

    48.
    R core team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2018. https://www.r-project.org/.

    49.
    Walker C. A simple blue staining technique for arbuscular mycorrhizal and other root-inhabiting fung. Inoculum. 2005;56:68–9.
    Google Scholar 

    50.
    Rossow MJ, Sasaki JM, Digman MA, Gratton E. Raster image correlation spectroscopy in live cells. Nat Protoc. 2010;5:1761–74.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    51.
    Whiteside MD, Digman MA, Gratton E, Treseder KK. Organic nitrogen uptake by arbuscular mycorrhizal fungi in a boreal forest. Soil Biol Biochem. 2012;55:7–13.
    CAS  Article  Google Scholar 

    52.
    Bates D, Mächler M, Bolker B, Walker S. “Fitting Linear Mixed-Effects Models Using lme4.” Journal of Statistical Software. 2015. 67;1:1–48.

    53.
    Kuznetsova A, Brockhoff PB, Christensen RHB (2017). “lmerTest Package: Tests in Linear Mixed Effects Models.” Journal of Statistical Software. 2017. 82;13:1–26.

    54.
    Fox J, Weisberg S. An R companion to applied regression. 2nd edn (Sage Publications, Inc, Thousand Oaks CA, 2016).

    55.
    Javot H, Pumplin N, Harrison MJ. Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ. 2007;30:310–22.
    CAS  PubMed  Article  Google Scholar 

    56.
    Konečný J, Hršelová H, Bukovská P, Hujslová M, Jansa J. Correlative evidence for co-regulation of phosphorus and carbon exchanges with symbiotic fungus in the arbuscular mycorrhizal Medicago truncatula. PLoS ONE. 2019;14:1–24.
    Article  CAS  Google Scholar 

    57.
    Keymer A, Pimprikar P, Wewer V, Huber C, Brands M, Bucerius SL, et al. Lipid transfer from plants to arbuscular mycorrhiza fungi. Elife. 2017;6:1–33.
    Article  Google Scholar 

    58.
    Burleigh SH, Cavagnaro T, Jakobsen I. Functional diversity of arbuscular mycorrhizas extends to the expression of plant genes involved in P nutrition. J Exp Bot. 2002;53:1593–601.
    CAS  PubMed  Article  Google Scholar 

    59.
    Smith SE. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol. 2003;133:16–20.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    60.
    Grønlund M, Albrechtsen M, Johansen IE, Hammer EC, Nielsen TH, Jakobsen I. The interplay between P uptake pathways in mycorrhizal peas: a combined physiological and gene-silencing approach. Physiol Plant. 2013;149:234–48.
    PubMed  Article  CAS  Google Scholar 

    61.
    Smith SE, Smith FA, Jakobsen I. Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. N Phytol. 2004;162:511–24.
    Article  Google Scholar 

    62.
    Watts-Williams SJ, Jakobsen I, Cavagnaro TR, Grønlund M. Local and distal effects of arbuscular mycorrhizal colonization on direct pathway Pi uptake and root growth in Medicago truncatula. J Exp Bot. 2015;66:4061–73.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    63.
    Pel R, Dupin S, Schat H, Ellers J, Kiers ET, van Straalen NM. Growth benefits provided by different arbuscular mycorrhizal fungi to Plantago lanceolata depend on the form of available phosphorus. Eur J Soil Biol. 2018;88:89–96.
    CAS  Article  Google Scholar 

    64.
    Reynolds HL, Vogelsang KM, Hartley AE, Bever JD, Schultz PA. Variable responses of old-field perennials to arbuscular mycorrhizal fungi and phosphorus source. Oecologia. 2006;147:348–58.
    PubMed  Article  Google Scholar 

    65.
    Lu R, Drubin DG, Sun Y. Clathrin-mediated endocytosis in budding yeast at a glance. J Cell Sci. 2016;129:1531–6.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    66.
    Fischer-Parton S, Parton RM, Hickey PC, Dijksterhuis J, Atkinson HA, Read ND. Confocal microscopy of FM4-64 as a tool for analysing endocytosis and vesicle trafficking in living fungal hyphae. J Microsc. 2000;198:246–59.
    CAS  PubMed  Article  Google Scholar 

    67.
    Read ND, Kalkman ER. Does endocytosis occur in fungal hyphae? Fungal Genet Biol. 2003;39:199–203.
    CAS  PubMed  Article  Google Scholar 

    68.
    Epp E, Nazarova E, Regan H, Douglas LM, Konopka JB, Vogel J, et al. Clathrin- and arp2/3-independent endocytosis in the fungal pathogen Candida albicans. MBio. 2013;4:e00476–13.
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    69.
    Colin Y, Nicolitch O, Turpault MP, Uroz S. Mineral types and tree species determine the functional and taxonomic structures of forest soil bacterial communities. Appl Environ Microbiol. 2017;83:1–23.
    Article  Google Scholar 

    70.
    Fontaine L, Thiffault N, Paré D, Fortin J-A, Piché Y. Phosphate-solubilizing bacteria isolated from ectomycorrhizal mycelium of Picea glauca are highly efficient at fluorapatite weathering. Botany. 2016;94:1183–93.
    CAS  Article  Google Scholar 

    71.
    Alloush GA, Clark RB. Maize response to phosphate rock and arbuscular mycorrhizal fungi in acidic soil. Commun Soil Sci Plant Anal. 2001;32:231–54.
    CAS  Article  Google Scholar 

    72.
    Powell CL, Daniel J. Mycorrhizal fungi stimulate uptake of soluble and insoluble phosphate fertilizer from a phosphate‐deficient soil. N Phytol. 1978;80:351–8.
    CAS  Article  Google Scholar 

    73.
    Jakobsen I, Hammer EC. Nutrient dynamics in arbuscular mycorrhizal networks. In: Horton TR, editor. Mycorrhizal networks. Dordrecht: Springer Netherlands; 2015. p. 91–131.

    74.
    Marler MJ, Zabinski CA, Callaway RM. Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology. 1999;80:1180–6.
    Article  Google Scholar 

    75.
    Carey EV, Marler MJ, Callaway RM. Mycorrhizae transfer carbon from a native grass to an invasive weed: evidence from stable isotopes and physiology. Plant Ecol. 2004;172:133–41.
    Article  Google Scholar 

    76.
    van der Heijden MGA. Arbuscular mycorrhizal fungi as support systems for seedling establishment in grassland. Ecol Lett. 2004;7:293–303.
    Article  Google Scholar 

    77.
    van der Heijden MGA, Horton TR. Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J Ecol. 2009;97:1139–50.
    Article  Google Scholar 

    78.
    Digman MA, Brown CM, Sengupta P, Wiseman PW, Horwitz AR, Gratton E. Measuring fast dynamics in solutions and cells with a laser scanning microscope. Biophys J. 2005;89:1317–27.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    79.
    Nieves DJ, Li Y, Fernig DG, Levy R. Photothermal raster image correlation spectroscopy of gold nanoparticles in solution and on live cells. R Soc Open Sci. 2015;2:140454.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    80.
    Johnson NC, Graham JH, Smith FA. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. N Phytol. 1997;135:575–85.
    Article  Google Scholar 

    81.
    Johnson NC, Wilson JA, Bowker MA, Wilson JA, Miller RM. Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc Natl Acad Sci. 2010;107:2093–8.
    CAS  PubMed  Article  Google Scholar 

    82.
    Argüello A, O’Brien MJ, van der Heijden MGA, Wiemken A, Schmid B, Niklaus PA. Options of partners improve carbon for phosphorus trade in the arbuscular mycorrhizal mutualism. Ecol Lett. 2016;19:648–56.
    PubMed  Article  Google Scholar 

    83.
    Noë R, Hammerstein P. Biological markets: supply and demand determine the effect of partner choice in cooperation, mutualism and mating. Behav Ecol Sociobiol. 1994;35:1–11.
    Article  Google Scholar 

    84.
    Werner GDA, Strassmann JE, Ivens ABF, Engelmoer DJP, Verbruggen E, Queller DC, et al. Evolution of microbial markets. Proc Natl Acad Sci. 2014;111:1237–44.
    CAS  PubMed  Article  Google Scholar 

    85.
    Musat N, Musat F, Weber PK, Pett-Ridge J. Tracking microbial interactions with NanoSIMS. Curr Opin Biotechnol. 2016;41:114–21.
    CAS  PubMed  Article  Google Scholar 

    86.
    Bücking H, Mensah JA, Fellbaum CR. Common mycorrhizal networks and their effect on the bargaining power of the fungal partner in the arbuscular mycorrhizal symbiosis. Commun Integr Biol. 2016;9:1–4.
    Article  CAS  Google Scholar 

    87.
    Roger A, Colard A, Angelard C, Sanders IR. Relatedness among arbuscular mycorrhizal fungi drives plant growth and intraspecific fungal coexistence. ISME J. 2013;7:2137–46.
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    88.
    Wagg C, Jansa J, Schmid B, van der Heijden MGA. Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol Lett. 2011;14:1001–9.
    PubMed  Article  Google Scholar 

    89.
    Douglas AE. Conflict, cheats and the persistence of symbioses. N Phytol. 2008;177:849–58.
    Article  Google Scholar  More

  • in

    Fine-scale tundra vegetation patterns are strongly related to winter thermal conditions

    1.
    Natali, S. M. et al. Large loss of CO2 in winter observed across the northern permafrost region. Nat. Clim. Change 9, 852–857 (2019).
    CAS  Google Scholar 
    2.
    Myers-Smith, I. H. et al. Shrub expansion in tundra ecosystems: dynamics, impacts and research priorities. Environ. Res. Lett. 6, 15 (2011).
    Google Scholar 

    3.
    Elmendorf, S. C. et al. Plot-scale evidence of tundra vegetation change and links to recent summer warming. Nat. Clim. Change 2, 453–457 (2012).
    Google Scholar 

    4.
    Bjorkman, A. D. et al. Plant functional trait change across a warming tundra biome. Nature 562, 57–62 (2018).
    CAS  Google Scholar 

    5.
    Niittynen, P., Heikkinen, R. K. & Luoto, M. Snow cover is a neglected driver of Arctic biodiversity loss. Nat. Clim. Change 8, 997–1001 (2018).
    Google Scholar 

    6.
    Snow, Water, Ice and Permafrost in the Arctic (SWIPA) 2017 (Arctic Monitoring and Assessment Programme (AMAP), 2017).

    7.
    Box, J. E. et al. Key indicators of Arctic climate change: 1971–2017. Environ. Res. Lett. 14, 045010 (2019).
    CAS  Google Scholar 

    8.
    Bintanja, R. & Andry, O. Towards a rain-dominated Arctic. Nat. Clim. Change 7, 263–267 (2017).
    Google Scholar 

    9.
    Post, E. et al. Ecological dynamics across the Arctic associated with recent climate change. Science 325, 1355–1358 (2009).
    CAS  Google Scholar 

    10.
    Blok, D. et al. The response of Arctic vegetation to the summer climate: relation between shrub cover, NDVI, surface albedo and temperature. Environ. Res. Lett. 6, 9 (2011).
    Google Scholar 

    11.
    Cooper, E. J. Warmer shorter winters disrupt Arctic terrestrial ecosystems. Annu. Rev. Ecol. Evol. Syst. 45, 271–295 (2014).
    Google Scholar 

    12.
    Sanders-DeMott, R. & Templer, P. H. What about winter? Integrating the missing season into climate change experiments in seasonally snow covered ecosystems. Methods Ecol. Evol. 8, 1183–1191 (2017).
    Google Scholar 

    13.
    Bokhorst, S., Bjerke, J. W., Tommervik, H., Preece, C. & Phoenix, G. K. Ecosystem response to climatic change: the importance of the cold season. Ambio 41, 246–255 (2012).
    Google Scholar 

    14.
    Williams, C. M., Henry, H. A. L. & Sinclair, B. J. Cold truths: how winter drives responses of terrestrial organisms to climate change. Biol. Rev. 90, 214–235 (2015).
    Google Scholar 

    15.
    Wipf, S., Stoeckli, V. & Bebi, P. Winter climate change in alpine tundra: plant responses to changes in snow depth and snowmelt timing. Climatic Change 94, 105–121 (2009).
    Google Scholar 

    16.
    Bokhorst, S. F., Bjerke, J. W., Tommervik, H., Callaghan, T. V. & Phoenix, G. K. Winter warming events damage sub-Arctic vegetation: consistent evidence from an experimental manipulation and a natural event. J. Ecol. 97, 1408–1415 (2009).
    Google Scholar 

    17.
    Rapacz, M. et al. Overwintering of herbaceous plants in a changing climate: still more questions than answers. Plant Sci. 225, 34–44 (2014).
    CAS  Google Scholar 

    18.
    Loffler, J. & Pape, R. Thermal niche predictors of alpine plant species. Ecology 101, e02891 (2020).
    Google Scholar 

    19.
    Choler, P. Winter soil temperature dependence of alpine plant distribution: implications for anticipating vegetation changes under a warming climate. Perspect. Plant Ecol. Evol. Syst. 30, 6–15 (2018).
    Google Scholar 

    20.
    Billings, W. D. & Mooney, H. A. Ecology of Arctic and alpine plants. Biol. Rev. Camb. Phil. Soc. 43, 481–529 (1968).
    Google Scholar 

    21.
    Cornelissen, J. H. C. & Makoto, K. Winter climate change, plant traits and nutrient and carbon cycling in cold biomes. Ecol. Res. 29, 517–527 (2014).
    CAS  Google Scholar 

    22.
    Groffman, P. M. et al. Colder soils in a warmer world: a snow manipulation study in a northern hardwood forest ecosystem. Biogeochemistry 56, 135–150 (2001).
    CAS  Google Scholar 

    23.
    Deems, J. S., Fassnacht, S. R. & Elder, K. J. Interannual consistency in fractal snow depth patterns at two Colorado mountain sites. J. Hydrometeorol. 9, 977–988 (2008).
    Google Scholar 

    24.
    Wahren, C. H. A., Walker, M. D. & Bret-Harte, M. S. Vegetation responses in Alaskan Arctic tundra after 8 years of a summer warming and winter snow manipulation experiment. Glob. Change Biol. 11, 537–552 (2005).
    Google Scholar 

    25.
    Darrouzet-Nardi, A. et al. Limited effects of early snowmelt on plants, decomposers, and soil nutrients in Arctic tundra soils. Ecol. Evol. 9, 1820–1844 (2019).
    Google Scholar 

    26.
    Nobrega, S. & Grogan, P. Deeper snow enhances winter respiration from both plant-associated and bulk soil carbon pools in birch hummock tundra. Ecosystems 10, 419–431 (2007).
    CAS  Google Scholar 

    27.
    Niittynen, P. & Luoto, M. The importance of snow in species distribution models of Arctic vegetation. Ecography 41, 1024–1037 (2018).
    Google Scholar 

    28.
    Blankinship, J. C., Meadows, M. W., Lucas, R. G. & Hart, S. C. Snowmelt timing alters shallow but not deep soil moisture in the Sierra Nevada. Water Resour. Res. 50, 1448–1456 (2014).
    Google Scholar 

    29.
    Kranner, I., Beckett, R., Hochman, A. & Nash, T. H. Desiccation-tolerance in lichens: a review. Bryologist 111, 576–593 (2008).
    Google Scholar 

    30.
    Cornelissen, J. H. C., Lang, S. I., Soudzilovskaia, N. A. & During, H. J. Comparative cryptogam ecology: a review of bryophyte and lichen traits that drive biogeochemistry. Ann. Bot. 99, 987–1001 (2007).
    CAS  Google Scholar 

    31.
    Sonesson, M. & Callaghan, T. V. Strategies of survival in plants of the Fennoscandian tundra. Arctic 44, 95–105 (1991).
    Google Scholar 

    32.
    Bjerke, J. W. et al. Contrasting sensitivity to extreme winter warming events of dominant sub-Arctic heathland bryophyte and lichen species. J. Ecol. 99, 1481–1488 (2011).
    Google Scholar 

    33.
    Pannewitz, S., Schlensog, M., Green, T. G. A., Sancho, L. G. & Schroeter, B. Are lichens active under snow in continental Antarctica? Oecologia 135, 30–38 (2003).
    Google Scholar 

    34.
    Natali, S. M., Schuur, E. A. G. & Rubin, R. L. Increased plant productivity in Alaskan tundra as a result of experimental warming of soil and permafrost. J. Ecol. 100, 488–498 (2012).
    Google Scholar 

    35.
    Weijers, S., Buchwal, A., Blok, D., Loffler, J. & Elberling, B. High Arctic summer warming tracked by increased Cassiope tetragona growth in the world’s northernmost polar desert. Glob. Change Biol. 23, 5006–5020 (2017).
    Google Scholar 

    36.
    Morris, W. F. et al. Longevity can buffer plant and animal populations against changing climatic variability. Ecology 89, 19–25 (2008).
    Google Scholar 

    37.
    Strimbeck, G. R., Schaberg, P. G., Fossdal, C. G., Schroder, W. P. & Kjellsen, T. D. Extreme low temperature tolerance in woody plants. Front. Plant Sci. 6, 15 (2015).
    Google Scholar 

    38.
    Gonzalez, V. T. et al. High resistance to climatic variability in a dominant tundra shrub species. PeerJ 7, e6967 (2019).
    Google Scholar 

    39.
    Thomas, H. J. D. et al. Traditional plant functional groups explain variation in economic but not size-related traits across the tundra biome. Glob. Ecol. Biogeogr. 28, 78–95 (2019).
    CAS  Google Scholar 

    40.
    Shipley, B., Lechowicz, M. J., Wright, I. & Reich, P. B. Fundamental trade-offs generating the worldwide leaf economics spectrum. Ecology 87, 535–541 (2006).
    Google Scholar 

    41.
    Good, M., Morgan, J. W., Venn, S. & Green, P. Timing of snowmelt affects species composition via plant strategy filtering. Basic Appl. Ecol. 35, 54–62 (2019).
    Google Scholar 

    42.
    Cornelissen, J. H. C. et al. Global change and Arctic ecosystems: is lichen decline a function of increases in vascular plant biomass? J. Ecol. 89, 984–994 (2001).
    Google Scholar 

    43.
    Zhu, L. K., Ives, A. R., Zhang, C., Guo, Y. Y. & Radeloff, V. C. Climate change causes functionally colder winters for snow cover-dependent organisms. Nat. Clim. Change 9, 886–893 (2019).
    Google Scholar 

    44.
    Williams, J. W. & Jackson, S. T. Novel climates, no-analog communities, and ecological surprises. Front. Ecol. Environ. 5, 475–482 (2007).
    Google Scholar 

    45.
    Medlyn, B. E. et al. Using ecosystem experiments to improve vegetation models. Nat. Clim. Change 5, 528–534 (2015).
    Google Scholar 

    46.
    Myers-Smith, I. H. et al. Climate sensitivity of shrub growth across the tundra biome. Nat. Clim. Change 5, 887–891 (2015).
    Google Scholar 

    47.
    Potter, K. A., Woods, H. A. & Pincebourde, S. Microclimatic challenges in global change biology. Glob. Change Biol. 19, 2932–2939 (2013).
    Google Scholar 

    48.
    Alsos, I. G. et al. Frequent long-distance plant colonization in the changing Arctic. Science 316, 1606–1609 (2007).
    CAS  Google Scholar 

    49.
    Kemppinen, J., Niittynen, P., Aalto, J., le Roux, P. C. & Luoto, M. Water as a resource, stress and disturbance shaping tundra vegetation. Oikos 128, 811–822 (2019).
    Google Scholar 

    50.
    Robinson, S. A. et al. Rapid change in east Antarctic terrestrial vegetation in response to regional drying. Nat. Clim. Change 8, 879–884 (2018).
    CAS  Google Scholar 

    51.
    Chamberlain, S. A. & Szocs, E. taxize: taxonomic search and retrieval in R. F1000Res 2, 191 (2013).
    Google Scholar 

    52.
    McCune, B. & Keon, D. Equations for potential annual direct incident radiation and heat load. J. Veg. Sci. 13, 603–606 (2002).
    Google Scholar 

    53.
    R Core Team R: A language and environment for statistical computing (R Foundation for Statistical Computing, 2019); https://www.r-project.org/

    54.
    Minchin, P. R. An evaluation of the relative robustness of techniques for ecological ordination. Vegetatio 69, 89–107 (1987).
    Google Scholar 

    55.
    Oksanen, J. et al. vegan: community ecology package. R package version 2.3-3 (2016).

    56.
    Franklin, J. Mapping Species Distributions: Spatial Inference and Prediction (Cambridge Univ. Press, 2009).

    57.
    Elith, J., Leathwick, J. R. & Hastie, T. A working guide to boosted regression trees. J. Anim. Ecol. 77, 802–813 (2008).
    CAS  Google Scholar 

    58.
    Thuiller, W., Georges, D., Engler, R. & Breiner, F. biomod2: ensemble platform for species distribution modeling. R package version 3.3-7 (2016).

    59.
    Pedersen, E. J., Miller, D. L., Simpson, G. L. & Ross, N. Hierarchical generalized additive models in ecology: an introduction with mgcv. PeerJ 7, e6876 (2019).
    Google Scholar 

    60.
    Wood, S. N. Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J. R. Stat. Soc. B 73, 3–36 (2011).
    Google Scholar 

    61.
    Ridgeway, G. gbm: generalized boosted regression models. R package version 2.1.1 (2015).

    62.
    Thuiller, W., Lafourcade, B., Engler, R. & Araujo, M. B. BIOMOD—a platform for ensemble forecasting of species distributions. Ecography 32, 369–373 (2009).
    Google Scholar  More