More stories

  • in

    Combining socioeconomic and biophysical data to identify people-centric restoration opportunities

    Chazdon, R. L. et al. Carbon sequestration potential of second-growth forest regeneration in the Latin American tropics. Sci. Adv. 2, e1501639 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    IKI. The Bonn Challenge. https://www.bonnchallenge.org/ (2022).UNCCD. Land Degradation Neutrality. https://www.unccd.int/land-and-life/land-degradation-neutrality/overview (2022).Bastin, J.-F. et al. The global tree restoration potential. Science 365, 76–79 (2019).Article 
    CAS 
    PubMed 

    Google Scholar 
    Brancalion, P. H. S. et al. Global restoration opportunities in tropical rainforest landscapes. Sci. Adv. 5, eaav3223 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Strassburg, B. B. N. et al. Global priority areas for ecosystem restoration. Nature 586, 724–729 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Erbaugh, J. T. et al. Global forest restoration and the importance of prioritizing local communities. Nat. Ecol. Evol. 4, 1472–1476 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Fleischman, F. et al. Restoration prioritization must be informed by marginalized people. Nature 607, E5–E6 (2022).Article 
    CAS 
    PubMed 

    Google Scholar 
    Chaturvedi, R. et al. Restoration Opportunities Atlas of India. www.india.restorationatlas.org/methodology (2022).McLain, R., Lawry, S., Guariguata, M. R. & Reed, J. Toward a tenure-responsive approach to forest landscape restoration: a proposed tenure diagnostic for assessing restoration opportunities. Land Use Policy 104, 103748 (2021).Article 

    Google Scholar 
    Binod, B., Bhattarcharjee, A. & Ishwar, N. M. Bonn Challenge and India: Progress on Restoration Efforts Across States and Landscapes (IUCN, 2018).Government of India. Aspirational Districts Phase 1 (vikaspedia, 2018).Government of India. Census of India. https://censusindia.gov.in/2011census/dchb/DCHB.html (2011).DeFries, R. et al. Land management can contribute to net zero. Science 376, 1163–1165 (2022).Article 
    CAS 
    PubMed 

    Google Scholar 
    Borah, B., Bhattacharya, A. & Ishwar, N. M. Bonn Challenge and India. Progress On Restoration Efforts Across States and Landscapes. https://www.bonnchallenge.org/pledges/india (2018).Gopalakrishna, T. et al. Existing land uses constrain climate change mitigation potential of forest restoration in India. Conserv. Lett. https://doi.org/10.1111/conl.12867 (2022).Dhyani, S. et al. Agroforestry to achieve global climate adaptation and mitigation targets: are South Asian countries sufficiently prepared? Forests 12, 303 (2021).Article 

    Google Scholar 
    Nerlekar, A. N. et al. Removal or utilization? Testing alternative approaches to the management of an invasive woody legume in an arid Indian grassland. Restor. Ecol. https://doi.org/10.1111/rec.13477 (2022).Coleman, E. A. et al. Limited effects of tree planting on forest canopy cover and rural livelihoods in Northern India. Nat Sustain 4, 997–1004 (2021).Article 

    Google Scholar 
    Ramprasad, V., Joglekar, A. & Fleischman, F. Plantations and pastoralists: afforestation activities make pastoralists in the Indian Himalaya vulnerable. Ecol. Soci. https://doi.org/10.5751/ES-11810-250401 (2020).DeFries, R. et al. Improved household living standards can restore dry tropical forests. Biotropica https://doi.org/10.1111/btp.12978 (2021).Lele, S., Khare, A. & Mokashi, S. Estimating and Mapping CFR Potential (ATREE, 2020).Agarwala, M. et al. Impact of biogas interventions on forest biomass and regeneration in southern India. Global Ecol. Conservation 11, 213–223 (2017).Article 

    Google Scholar 
    Menon, A. & Schmidt-Vogt, D. Effects of the COVID-19 pandemic on farmers and their responses: a study of three farming systems in Kerala. South India. Land 11, 144 (2022).
    Google Scholar 
    Fremout, T. et al. Diversity for Restoration (D4R): Guiding the selection of tree species and seed sources for climate‐resilient restoration of tropical forest landscapes. J. Appl. Ecol. 59, 664–679 (2022).Article 

    Google Scholar 
    Hughes, K. A. et al. Can restoration of the commons reduce rural vulnerability? A Quasi-experimental comparison of COVID-19 livelihood-based coping strategies among rural households in three Indian States. Int. J. Common. 16, 189 (2022).Article 

    Google Scholar 
    Madhusudan, M. D. & Vanak, A. Mapping the Distribution and Extent of India’s Semi-arid Open Natural Ecosystems. https://doi.org/10.1002/essoar.10507612.1 (2021).Vanak, A. T., Hiremath, A. J., Ganesh, T. & Rai, N. D. Filling in the (Forest) Blanks: the Past, Present and Future of India’s Savanna Grasslands (ATREE, 2017).Oxford Poverty & Human Development Initiative. Global Multidimensional Poverty Index 2018. The Most Detailed Picture to Date of the World’s Poorest People. https://ophi.org.uk/wp-content/uploads/G-MPI_2018_2ed_web.pdf (2018).Hijmans, R. J. et al. raster: Geographic Data Analysis and Modeling. https://rspatial.org/raster (2023).Bivand, R. et al. rgdal: Bindings for the ‘Geospatial’ Data Abstraction Library. https://cran.r-project.org/web/packages/rgdal/index.html (2023).QGIS Development Team. QGIS Geographic Information System (Open Source Geospatial Foundation Project, 2022). More

  • in

    Coastal algal blooms have intensified over the past 20 years

    RESEARCH BRIEFINGS
    01 March 2023

    Global spatial and temporal patterns of coastal phytoplankton blooms were characterized using daily satellite imaging between 2003 and 2020. These blooms were identified on the coast of 126 of the 153 ocean-bordering countries examined. The extent and frequency of blooms have increased globally over the past two decades. More

  • in

    Untitled public forestlands threat Amazon conservation

    There is a recent change in the modus operandi of Brazilian Amazon deforestation. The proportion of illegal deforestation in public land increased from ~43–44% (2015–2018) to ~49–52% (2019–2021)10. Land grabbers occupy public lands (deforesting or raising cattle) in a high-risk expectation of receiving title to the land and/or trading the land with significant returns (land speculation)6,7. Therefore, we argue that it is crucial to rapidly assign most of the Amazon’s UPFs to land tenure regimes associated with conservation. Land-tenure security will bring greater governance and protection to these areas. Achieving this goal requires a combination of three measures: (1) careful attention to the choice of land tenure categories for UPFs, (2) technological improvements, and (3) law enforcement.Choice of land tenure category for UPFsPublic lands in Brazil include several categories, such as conservation areas (with several subcategories under law number 9985/2000), Indigenous lands, and rural settlements, among others. Therefore, the category choice for each undesignated public land area requires studies to determine those lands’ social, environmental, or productive suitability, taking note of their histories of occupation, cultural importance, and potential uses. The unpopulated forest is a myth. Most of the areas in the Amazon have been occupied by human populations—traditional communities, indigenous villages, uncontacted tribes, “riverside” (ribeirinho) peoples, or small farmers—for generations. Ancestral occupation of land without proof or associated studies, however, does not guarantee land rights. Therefore, to avoid unfair competition for land and unilateral political decisions, the best choice of land category for a given UPF to meet social, ecological and economic demands would benefit from active social participation, multidisciplinary scientific studies, in situ observations, and innovative technologies (e.g., remote sensing, data processing capabilities, machine learning, cloud computing) to provide fast, scalable, and quality information.Final allocation decisions, however, must be preceded by participatory and transparent consultation processes to avoid conflicts and safeguard land rights. The measure of assigning tenure categories to the UPFs has a high level of complexity in itself and may benefit from the support of multi-actors (e.g., governments, academia, civil society, private sector) at multi-levels (e.g., studies, participation processes, decision-making processes) and multi-scales (local, regional and national). Despite the complexity, there are examples in the early 2000s of joint efforts to allocate land (“Terra Legal” Program) and create protected areas on a large scale and in a short period of time in the Brazilian Amazon. We emphasize, however, that the tenure categories selected for the UPFs need to maintain forest cover, remain in the public domain in compliance with national laws, and enhance long-term Amazon conservation, respecting the rights of resident populations.Technological improvements to control land grabbing in UPFLasting conservation of the Amazon rainforest depends on ending land-grabbing and illegal deforestation in public forests (designated or undesignated). However, land grabbers are using a self-declaratory tool to declare illegally invaded public lands as private properties, which demands immediate technological improvements to the system.The Rural Environmental Registry (CAR is the Portuguese acronym) is a mechanism of environmental oversight of private lands under the Brazilian Forest Code (Law 12,651/2012). CARs are registered on a web-based platform (Rural Environmental Registry System – SICAR). By law, landowners must self-declare their property boundaries and land use types (e.g., residential, agricultural, protection) in SICAR, respecting legally required protection of certain forest areas and watercourses. Then, a state environmental agency must validate the information. Unfortunately, the validation process has been extremely slow (e.g., More

  • in

    Phototrophy by antenna-containing rhodopsin pumps in aquatic environments

    Balashov, S. P. et al. Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna. Science 309, 2061–2064 (2005).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Imasheva, E. S., Balashov, S. P., Choi, A. R., Jung, K.-H. & Lanyi, J. K. Reconstitution of Gloeobacter violaceus rhodopsin with a light-harvesting carotenoid antenna. Biochemistry 48, 10948–10955 (2009).Article 
    CAS 
    PubMed 

    Google Scholar 
    Fuhrman, J. A., Schwalbach, M. S. & Stingl, U. Proteorhodopsins: an array of physiological roles? Nat. Rev. Microbiol. 6, 488–494 (2008).Article 
    CAS 
    PubMed 

    Google Scholar 
    Vollmers, J. et al. Poles apart: Arctic and Antarctic Octadecabacter strains share high genome plasticity and a new type of xanthorhodopsin. PLoS ONE 8, e63422 (2013).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bertsova, Y. V., Arutyunyan, A. M. & Bogachev, A. V. Na+-translocating rhodopsin from Dokdonia sp. PRO95 does not contain carotenoid antenna. Biochem. Mosc. 81, 414–419 (2016).Article 
    CAS 

    Google Scholar 
    Misra, R., Eliash, T., Sudo, Y. & Sheves, M. Retinal–salinixanthin interactions in a thermophilic rhodopsin. J. Phys. Chem. B 123, 10–20 (2019).Article 
    CAS 
    PubMed 

    Google Scholar 
    Béjà, O. et al. Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289, 1902–1906 (2000).Article 
    ADS 
    PubMed 

    Google Scholar 
    Béjà, O., Spudich, E. N., Spudich, J. L., Leclerc, M. & DeLong, E. F. Proteorhodopsin phototrophy in the ocean. Nature 411, 786–789 (2001).Article 
    ADS 
    PubMed 

    Google Scholar 
    Atamna-Ismaeel, N. et al. Widespread distribution of proteorhodopsins in freshwater and brackish ecosystems. ISME J. 2, 656–662 (2008).Article 
    CAS 
    PubMed 

    Google Scholar 
    Frigaard, N.-U., Martinez, A., Mincer, T. J. & DeLong, E. F. Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea. Nature 439, 847–850 (2006).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Finkel, O. M., Béjà, O. & Belkin, S. Global abundance of microbial rhodopsins. ISME J. 7, 448–451 (2013).Article 
    CAS 
    PubMed 

    Google Scholar 
    Gómez-Consarnau, L. et al. Microbial rhodopsins are major contributors to the solar energy captured in the sea. Sci. Adv. 5, eaaw8855 (2019).Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    DeLong, E. F. & Béjà, O. The light-driven proton pump proteorhodopsin enhances bacterial survival during tough times. PLoS Biol. 8, e1000359 (2010).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Munson-McGee, J. H. et al. Decoupling of respiration rates and abundance in marine prokaryoplankton. Nature 612, 764–770 (2022).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wang, W.-W., Sineshchekov, O. A., Spudich, E. N. & Spudich, J. L. Spectroscopic and photochemical characterization of a deep ocean proteorhodopsin. J. Biol. Chem. 278, 33985–33991 (2003).Article 
    CAS 
    PubMed 

    Google Scholar 
    Man, D. Diversification and spectral tuning in marine proteorhodopsins. EMBO J. 22, 1725–1731 (2003).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lanyi, J. K. & Balashov, S. P. in Halophiles and Hypersaline Environments (eds. Ventosa, A., Oren, A. & Ma, Y.) 319–340 (Springer, 2011).Balashov, S. P. et al. Reconstitution of Gloeobacter rhodopsin with echinenone: role of the 4-keto group. Biochemistry 49, 9792–9799 (2010).Article 
    CAS 
    PubMed 

    Google Scholar 
    Kopejtka, K. et al. A bacterium from a mountain lake harvests light using both proton-pumping xanthorhodopsins and bacteriochlorophyll-based photosystems. Proc. Natl Acad. Sci. USA 119, e2211018119 (2022).Article 
    CAS 
    PubMed 

    Google Scholar 
    Pushkarev, A. & Béjà, O. Functional metagenomic screen reveals new and diverse microbial rhodopsins. ISME J. 10, 2331–2335 (2016).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pushkarev, A. et al. A distinct abundant group of microbial rhodopsins discovered using functional metagenomics. Nature 558, 595–599 (2018).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Chazan, A. et al. Diverse heliorhodopsins detected via functional metagenomics in freshwater Actinobacteria, Chloroflexi and Archaea. Environ. Microbiol. 24, 110–121 (2022).Article 
    CAS 
    PubMed 

    Google Scholar 
    Inoue, K. et al. A light-driven sodium ion pump in marine bacteria. Nat. Commun. 4, 1678 (2013).Article 
    ADS 
    PubMed 

    Google Scholar 
    Bhosale, P. & Bernstein, P. S. Microbial xanthophylls. Appl. Microbiol. Biotechnol. 68, 445–455 (2005).Article 
    CAS 
    PubMed 

    Google Scholar 
    Demmig-Adams, B., Polutchko, S. K. & Adams, W. W. Structure–function–environment relationship of the isomers zeaxanthin and lutein. Photochem 2, 308–325 (2022).Article 

    Google Scholar 
    Barreiro C. & Barredo J. L. Microbial Carotenoids: Methods and Protocols (Humana Press, 2018).Ram, S., Mitra, M., Shah, F., Tirkey, S. R. & Mishra, S. Bacteria as an alternate biofactory for carotenoid production: a review of its applications, opportunities and challenges. J. Funct. Foods 67, 103867 (2020).Article 
    CAS 

    Google Scholar 
    Shibata, M. et al. Oligomeric states of microbial rhodopsins determined by high-speed atomic force microscopy and circular dichroic spectroscopy. Sci. Rep. 8, 8262 (2018).Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Luecke, H. et al. Crystallographic structure of xanthorhodopsin, the light-driven proton pump with a dual chromophore. Proc. Natl Acad. Sci. USA 105, 16561–16565 (2008).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Chuon, K. et al. Assembly of natively synthesized dual chromophores into functional actinorhodopsin. Front. Microbiol. 12, 652328 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Yoshizawa, S., Kawanabe, A., Ito, H., Kandori, H. & Kogure, K. Diversity and functional analysis of proteorhodopsin in marine Flavobacteria. Environ. Microbiol. 14, 1240–1248 (2012).Article 
    CAS 
    PubMed 

    Google Scholar 
    Ahmed, F. et al. Profiling of carotenoids and antioxidant capacity of microalgae from subtropical coastal and brackish waters. Food Chem. 165, 300–306 (2014).Article 
    CAS 
    PubMed 

    Google Scholar 
    Shihoya, W. et al. Crystal structure of heliorhodopsin. Nature 574, 132–136 (2019).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Kishi, K. E. et al. Structural basis for channel conduction in the pump-like channelrhodopsin ChRmine. Cell 185, 672–689.e23 (2022).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Balashov, S. P., Imasheva, E. S., Wang, J. M. & Lanyi, J. K. Excitation energy-transfer and the relative orientation of retinal and carotenoid in xanthorhodopsin. Biophys. J. 95, 2402–2414 (2008).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lakowicz, J. R. (ed.) in Principles of Fluorescence Spectroscopy 27–61 (Springer, 2006).Dana, J. et al. Testing the fate of nascent holes in CdSe nanocrystals with sub-10 fs pump–probe spectroscopy. Nanoscale 13, 1982–1987 (2021).Article 
    CAS 
    PubMed 

    Google Scholar 
    Polívka, T. et al. Femtosecond carotenoid to retinal energy transfer in xanthorhodopsin. Biophys. J. 96, 2268–2277 (2009).Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Iyer, E. S. S., Gdor, I., Eliash, T., Sheves, M. & Ruhman, S. Efficient femtosecond energy transfer from carotenoid to retinal in Gloeobacter rhodopsin–salinixanthin complex. J. Phys. Chem. B 119, 2345–2349 (2015).Article 
    CAS 
    PubMed 

    Google Scholar 
    Doi, S., Tsukamoto, T., Yoshizawa, S. & Sudo, Y. An inhibitory role of Arg-84 in anion channelrhodopsin-2 expressed in Escherichia coli. Sci. Rep. 7, 41879 (2017).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Nagiri, C. et al. Crystal structure of human endothelin ETB receptor in complex with peptide inverse agonist IRL2500. Commun. Biol. 2, 236 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Yamashita, K., Hirata, K. & Yamamoto, M. KAMO: towards automated data processing for microcrystals. Acta Crystallogr. D Struct. Biol. 74, 441–449 (2018).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kabsch, W. XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125–132 (2010).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486–501 (2010).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Afonine, P. V. et al. Towards automated crystallographic structure refinement with phenix.refine.Acta Crystallogr. D Biol. Crystallogr. 68, 352–367 (2012).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Zivanov, J. et al. New tools for automated high-resolution cryo-EM structure determination in RELION-3.eLife 7, e42166 (2018).Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).Punjani, A., Zhang, H. & Fleet, D. J. Non-uniform refinement: adaptive regularization improves single-particle cryo-EM reconstruction. Nat. Methods 17, 1214–1221 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Rosenthal, P. B. & Henderson, R. Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J. Mol. Biol. 333, 721–745 (2003).Article 
    CAS 
    PubMed 

    Google Scholar 
    Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126–2132 (2004).Article 
    PubMed 

    Google Scholar 
    Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213–221 (2010).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Yamashita, K., Palmer, C. M., Burnley, T. & Murshudov, G. N. Cryo-EM single-particle structure refinement and map calculation using Servalcat. Acta Crystallogr. D Struct. Biol. 77, 1282–1291 (2021).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).Article 
    CAS 
    PubMed 

    Google Scholar 
    Inoue, K. et al. Exploration of natural red-shifted rhodopsins using a machine learning-based Bayesian experimental design. Commun. Biol. 4, 362 (2021).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Salazar, G. et al. Gene expression changes and community turnover differentially shape the global ocean metatranscriptome. Cell 179, 1068–1083.e21 (2019).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Chen, I.-M. A. et al. The IMG/M data management and analysis system v.6.0: new tools and advanced capabilities. Nucleic Acids Res. 49, D751–D763 (2021).Article 
    CAS 
    PubMed 

    Google Scholar 
    Nayfach, S. et al. A genomic catalog of Earth’s microbiomes. Nat. Biotechnol. 39, 499–509 (2021).Article 
    CAS 
    PubMed 

    Google Scholar 
    Sunagawa, S. et al. Metagenomic species profiling using universal phylogenetic marker genes. Nat. Methods 10, 1196–1199 (2013).Article 
    CAS 
    PubMed 

    Google Scholar 
    Wickham, H. in ggplot2 (eds Gentleman, R., Hornik, K. & Parmigiani, G.) 189–201 (Springer, 2016).Katoh, K., Misawa, K., Kuma, K. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066 (2002).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).Article 
    CAS 
    PubMed 

    Google Scholar 
    Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518–522 (2018).Article 
    CAS 
    PubMed 

    Google Scholar  More

  • in

    Coastal phytoplankton blooms expand and intensify in the 21st century

    Data sourcesMODIS on the Aqua satellite provides a global coverage within 1–2 days. All images acquired by this satellite mission from January 2003 to December 2020 were used in our study to detect global coastal phytoplankton blooms, with a total of 0.76 million images. MODIS Level-1A images were downloaded from the Ocean Biology Distributed Active Archive Center (OB.DAAC) at NASA Goddard Space Flight Center (GSFC), and were subsequently processed with SeaDAS software (version 7.5) to obtain Rayleigh-corrected reflectance (Rrc (dimensionless), which was converted using the rhos (in sr−1) product (rhos × π) from SeaDAS)41, remote sensing reflectance (Rrs (sr−1)) and quality control flags (l2_flags). If a pixel was flagged by any of the following, it was then removed from phytoplankton bloom detection: straylight, cloud, land, high sunglint, high solar zenith angle and high sensor zenith angle (https://oceancolor.gsfc.nasa.gov/atbd/ocl2flags/). MODIS level-3 product for aerosol optical thicknesses (AOT) at 869 nm was also obtained from OB.DAAC NASA GSFC (version R2018.0), which was used to examine the impacts of aerosols on bloom trends.We examined the algal blooms in the EEZs of 153 ocean-bordering countries (excluding the EEZs in the Caspian Sea or around the Antarctic), 126 of which were found with at least one bloom in the past two decades. The EEZ dataset is available at https://www.marineregions.org/download_file.php?name=World_EEZ_v11_20191118.zip. The EEZs are up to 200 nautical miles (or 370 km) away from coastlines, which include all continental shelf areas and offer the majority of marine resources available for human use. Regional statistics of algal blooms were also performed for LMEs. LMEs encompass global coastal oceans and outer edges of coastal currents areas, which are defined by various distinct features of the oceans, including hydrology, productivity, bathymetry and trophically dependent populations42. Of the 66 LMEs identified globally, we excluded the Arctic and Antarctic regions and examined 54 LMEs. The boundaries of LMEs were obtained from https://www.sciencebase.gov/catalog/item/55c77722e4b08400b1fd8244.We used HAEDAT to validate our satellite-detected phytoplankton blooms in terms of presence or absence. The HAEDAT dataset (http://haedat.iode.org) is a collection of records of HAB events, maintained under the UNESCO Intergovernmental Oceanographic Commission and with data archives since 1985. For each HAB event, the HAEDAT records its bloom period (ranging from days to months) and geolocation. We merged duplicate entries when both the recorded locations and times of the HAEDAT events were very similar to one another, and a total number of 2,609 HAEDAT events were ultimately selected between 2003 and 2020.We used the ¼° resolution National Oceanic and Atmospheric Administration Optimum Interpolated SST (v. 2.1) data to examine the potential simulating effects of warming on the global phytoplankton trends. We also estimated the SST gradients following the method of Martínez-Moreno33. As detailed in ref. 33, the SST gradient can be used as a proxy for the magnitude of oceanic mesoscale currents (EKE). We used the SST gradient to explore the effects of ocean circulation dynamics on algal blooms.Fertilizer uses and aquaculture production for different countries was used to examine the potential effects of nutrient enrichment from humans on global phytoplankton bloom trends. Annual data between 2003 and 2019 on synthetic fertilizer use, including nitrogen and phosphorus, are available from https://ourworldindata.org/fertilizers. Annual aquaculture production includes cultivated fish and crustaceans in marine and inland waters, and sea tanks, and the data between 2003 and 2018 are available from https://ourworldindata.org/grapher/aquaculture-farmed-fish-production.The MEI, which combines various oceanic and atmospheric variables36, was used to examine the connections between El Niño–Southern Oscillation activities and marine phytoplankton blooms. The dataset is available from https://psl.noaa.gov/enso/mei/.Development of an automated bloom detection methodA recent study by the UNESCO Intergovernmental Oceanographic Commission revealed that globally reported HAB events have increased6. However, such an overall increasing trend was found to be highly correlated with recently intensified sampling efforts6. Once this potential bias was accounted for by examining the ratio between HAB events to the number of samplings5, there was no significant global trend in HAB incidence, though there were increases in certain regions. With synoptic, frequent, and large-scale observations, satellite remote sensing has been extensively used to monitor algal blooms in oceanic environments17,18,19. For example, chlorophyll a (Chla) concentrations, a proxy for phytoplankton biomass, has been provided as a standard product by NASA since the proof-of-concept Coastal Zone Color Scanner (1978–1986) era43,44. The current default algorithm used to retrieve Chla products is based on the high absorption of Chla at the blue band45,46, which often shows high accuracy in the clear open oceans but high uncertainties in coastal waters. This is because, in productive and dynamic coastal oceans, the absorption of Chla in the blue band can be obscured by the presence of suspended sediments and/or coloured dissolved organic matter (CDOM)47. To address this problem, various regionalized Chla algorithms have been developed48. Unfortunately, the concentrations of the water constituents (CDOM, sediment and Chla) can vary substantially across different coastal oceans. As a result, a universal Chla algorithm that can accurately estimate Chla concentrations in global coastal oceans is not currently available.Alternatively, many spectral indices have been developed to identify phytoplankton blooms instead of quantifying their bloom biomass, including the normalized fluorescence line height21 (nFLH), red tide index49 (RI), algal bloom index47 (ABI), red–blue difference (RBD)50, Karenia brevis bloom index50 (KBBI) and red tide detection index51 (RDI). In practice, the most important task for these index-based algorithms is to determine their optimal thresholds for bloom classification. However, such optimal thresholds can be regional-or image-specific20, due to the complexity of optical features in coastal waters and/or the contamination of unfavourable observational conditions (such as thick aerosols, thin clouds, and so on), making it difficult to apply spectral-index-based algorithms at a global scale.To circumvent the difficulty in determining unified thresholds for various spectral indices across global coastal oceans, an approach from a recent study to classify algal blooms in freshwater lakes52 was adopted and modified here. In that study, the remotely sensed reflectance data in three visible bands (red, green and blue) were converted into two-dimensional colour space created by the Commission Internationale del’éclairage (CIE), in which the position on the CIE chromaticity diagram represented the colour perceived by human eyes (Extended Data Fig. 1a). As the algal blooms in freshwater lakes were manifested as greenish colours, the reflectance of bloom-containing pixels was expected to be distributed in the green gamut of the CIE chromaticity diagram; the stronger the bloom, the closer the distance to the upper border of the diagram (the greener the water).Here, the colour of phytoplankton blooms in the coastal oceans can be greenish, yellowish, brownish, or even reddish53, owing to the compositions of bloom species (diatoms or dinoflagellates) and the concentrations of different water constituents. Furthermore, the Chla concentrations of the coastal blooms are typically lower than those in inland waters, thus demanding more accurate classification algorithms. Thus, the algorithm proposed by Hou et al.52 was modified when using the CIE chromaticity space for bloom detection in marine environments. Specifically, we used the following coordinate conversion formulas to obtain the xy coordinate values in the CIE colour space:$$begin{array}{c}x=X/(X+Y+Z)\ y=Y/(X+Y+Z)\ X=2.7689R+1.7517G+1.1302B\ Y=1.0000R+4.5907G+0.0601B\ Z=0.0000R+0.0565G+5.5943Bend{array}$$
    (1)
    where R, G and B represent the Rrc at 748 nm, 678 nm (fluorescence band) and 667 nm in the MODIS Aqua data, respectively. By contrast, the R, G and B channels used in Hou et al.52 were the red, green and blue bands. We used the fluorescence band for the G channel because, for a given region, the 678 nm signal increases monotonically with the Chla concentration for blooms of moderate intensity21, which is similar to the response of greenness to freshwater algal blooms. Thus, the converted y value in the CIE coordinate system represents the strength of the fluorescence. In practice, for pixels with phytoplankton blooms, the converted colours in the chromaticity diagram will be located within the green, yellow or orange–red gamut (see Extended Data Fig. 1a); the stronger the fluorescence signal is, the closer the distance to the upper border of the CIE diagram (larger y value). By contrast, for bloom-free pixels without a fluorescence signal, their converted xy coordinates will be located in the blue or purple gamut. Therefore, we can determine a lower boundary in the CIE two-dimensional coordinate system to separate bloom and non-bloom pixels, similar to the method proposed by Hou et al.52.We selected 53,820 bloom-containing pixels from the MODIS Rrc data as training samples to determine the boundary of the CIE colour space. These sample points were selected from nearshore waters worldwide where frequent phytoplankton blooms have been reported (Extended Data Fig. 2); the algal species included various species of dinoflagellates and diatoms20. A total of 80 images was used, which were acquired from different seasons and across various bloom magnitudes, to ensure that the samples used could almost exhaustively represent the different bloom conditions in the coastal oceans.We combined the MODIS FLHRrc (fluorescence line height based on Rrc) and enhanced red–green–blue composite (ERGB) to delineate bloom pixels manually. The FLHRrc image was calculated as:$$begin{array}{c}{{rm{FLH}}}_{{rm{Rrc}}}={R}_{{rm{rc}}678}times {F}_{678}-[{R}_{{rm{rc}}667}times {F}_{667}+({R}_{{rm{rc}}748}times {F}_{748}\ ,,-,{R}_{{rm{rc}}667}times {F}_{667})times (678-667)/(748-667)]end{array}$$
    (2)
    where Rrc667, Rrc678 and Rrc748 are the Rrc at 667, 678 and 748 nm, respectively, and F667, F678 and F748 are the corresponding extraterrestrial solar irradiance. ERGB composite images were generated using Rrc of three bands at 555 (R), 488 (G) and 443 nm (B). Although phytoplankton-rich and sediment-rich waters have high FLHRrc values, they appear as darkish and bright features in the ERGB images (Extended Data Fig. 3), respectively21. In fact, visual examination with fluorescence signals and ERGB has been widely accepted as a practical way to delineate coastal algal blooms on a limited number of images21,54,55. Note that the FLHRrc here was slightly different from the NASA standard nFLH product56, as the latter is generated using Rrs (corrected for both Rayleigh and aerosol scattering) instead of Rrc (with residual effects of aerosols). However, when using the NASA standard algorithm to further perform aerosol scattering correction over Rrc, 20.7% of our selected bloom-containing pixels failed to obtain valid Rrs (without retrievals or flagged as low quality), especially for those with strong blooms (see examples in Extended Data Fig. 4). Likewise, we also found various nearshore regions with invalid Rrs retrievals. By contrast, Rrc had valid data for all selected samples and showed more coverage in nearshore coastal waters. The differences between Rrs and Rrc were because the assumptions for the standard atmospheric correction algorithm do not hold for bloom pixels or nearshore waters with complex optical properties57. In fact, Rrc has been used as an alternative to Rrs in various applications in complex waters58,59.We converted the Rrc data of 53,820 selected sample pixels into the xy coordinates in the CIE colour space (Extended Data Fig. 1a). As expected, these samples of bloom-containing pixels were located in the upper half of the chromaticity diagram (the green, yellow and orange–red gamut) (Extended Data Fig. 1a). We determined the lower boundary of these sample points in the chromaticity diagram, which represents the lightest colour and thus the weakest phytoplankton blooms; any point that falls above this boundary represents stronger blooms. The method to determine the boundary was similar to Hou et al.52: we first binned the sample points according to the x value in the chromaticity diagram and estimated the 1st percentile (Q1%) of the corresponding Y for each bin; then, we fit the Q1% using two-order polynomial regression. Sensitivity analysis with Q0.3% (the three-sigma value) resulted in minor changes ( 1/3 AND y  > y2), it is classified as a ‘bloom’ pixel.Depending on the local region and application purpose, the meaning of ‘phytoplankton bloom’ may differ. Here, for a global application, the pixelwise bloom classification is based on the relationship (represented using the CIE colour space) between Rrc in the 667-, 678- and 754-nm bands derived from visual interpretation of the 80 pairs of FLHRrc and ERGB imagery. Instead of a simple threshold, we used a lower boundary of the sample points in the chromaticity diagram to define a bloom. In simple words, a pixel is classified as a bloom if its fluorescence signal is detectable (the associated xy coordinate in the CIE colour space located above the lower boundary). Histogram of the nFLH values from the 53,820 training pixels demonstrated the minimum value of ~0.02 mW cm−2 μm−1 (Extended Data Fig. 1a), which is in line with the lower-bound signal of K. brevis blooms on the West Florida shelf21,47. Note that, such a minimum nFLH is determined from the global training pixels, and it does not necessarily represent a unified lower bound for phytoplankton blooms across the entire globe, especially considering that fluorescence efficiency may be a large variable across different regions. Different regions may have different lower bounds of nFLH to define a bloom, and such variability is represented by the predefined boundary in the CIE chromaticity diagram in our study. Correspondingly, although the accuracy of Chla retrievals may have large uncertainties in coastal waters, the histogram of the 53,820 training pixels shows a lower bound of ~1 mg m−3 (Extended Data Fig. 1a). Similarly to nFLH, such a lower bound may not be applicable to all coastal regions, as different regions may have different lower bounds of Chla for bloom definition.Although the MODIS cloud (generated by SeaDAS with Rrc869 0.12) and Index2 ( More

  • in

    Carbon stocks of billions of individual African dryland trees estimated

    Tucker, C. et al. Nature 615, 80–86 (2023).Article 

    Google Scholar 
    Bayala, J. et al. Agric. Ecosyst. Environ. 205, 25–35 (2015).Article 

    Google Scholar 
    Keesstra, S. D. et al. Soil 2, 111–128 (2016).Article 

    Google Scholar 
    Dewi, S. et al. Int. J. Biodivers. Sci. Ecosyst. Serv. Mgmt 13, 312–329 (2017).Article 

    Google Scholar 
    Ahlström, A. et al. Science 348, 895–899 (2015).Article 
    PubMed 

    Google Scholar 
    Poulter, B. et al. Nature 509, 600–603 (2014).Article 
    PubMed 

    Google Scholar 
    Prăvălie, R. et al. Environ. Res. 201, 111580 (2021).Article 
    PubMed 

    Google Scholar 
    Reij, C. P. & Smaling, E. M. A. Land Use Policy 25, 410–420 (2008).Article 

    Google Scholar 
    Zomer, R. J., Bossio, D. A., Trabucco, A., van Noordwijk, M. & Xu, J. Circ. Agric. Syst. 2, 3 (2022).Article 

    Google Scholar 
    Chomba, S., Sinclair, F., Savadogo, P., Bourne, M. & Lohbeck, M. Front. For. Glob. Change 3, 571679 (2020).Article 

    Google Scholar 
    Dakpogan, A., Bayala, J., Ouattara, I. & Ellington, E. in United for Lands: From National Coalitions to a Pipeline of Bankable Projects for the Great Green Wall 54–56 (United Nations, 2022).
    Google Scholar 
    Garrity, D. P. & Bayala, J. in Sustainable Development Through Trees on Farms: Agroforestry in its Fifth Decade (ed. van Noordwijk, M.) 153–175 (World Agroforestry, 2019).
    Google Scholar 
    Schnell, S., Kleinn, C. & Ståhl, G. Environ. Monit. Assess. 187, 600 (2015).Article 
    PubMed 

    Google Scholar  More

  • in

    Regardless of personality, males show similar levels of plasticity in territory defense in a Neotropical poison frog

    Bell, A. M. Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J. Evol. Biol. 18, 464–473 (2005).Article 
    CAS 
    PubMed 

    Google Scholar 
    Dochtermann, N. A. & Jenkins, S. H. Behavioural syndromes in Merriam’s kangaroo rats (Dipodomys merriami): A test of competing hypotheses. Proc. R. Soc. Lond. B 274, 2343–2349 (2007).
    Google Scholar 
    Tremmel, M. & Müller, C. Insect personality depends on environmental conditions. Behav. Ecol. 24, 386–392 (2013).Article 

    Google Scholar 
    Zidar, J. et al. A comparison of animal personality and coping styles in the red junglefowl. Anim. Behav. 130, 209–220 (2017).Article 

    Google Scholar 
    Sih, A., Bell, A. & Johnson, J. C. Behavioral syndromes: An ecological and evolutionary overview. Trends Ecol. Evol. 19, 372–378 (2004).Article 
    PubMed 

    Google Scholar 
    Réale, D. & Dingemanse, N. J. Personality and individual social specialization. In Social behaviour: Genes, ecology and evolution (eds Székely, T. et al.) 417–441 (Cambridge University Press, 2010).Chapter 

    Google Scholar 
    Dingemanse, N. J. & Dochtermann, N. A. Quantifying individual variation in behaviour. Mixed-effect modelling approaches. J. Anim. Ecol. 82, 39–54 (2013).Article 
    PubMed 

    Google Scholar 
    Dingemanse, N. J., Kazem, A. J. N., Reale, D. & Wright, J. Behavioural reaction norms: Animal personality meets individual plasticity. Trends Ecol. Evol. 25, 81–89 (2010).Article 
    PubMed 

    Google Scholar 
    Wolf, M., van Doorn, G. S. & Weissing, F. J. Evolutionary emergence of responsive and unresponsive personalities. Proc. Natl. Acad. Sci. USA 105, 15825–15830 (2008).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ólafsdóttir, G. Á. & Magellan, K. Interactions between boldness, foraging performance and behavioural plasticity across social contexts. Behav. Ecol. Sociobiol. 70, 1879–1889 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Mathot, K. J., Wright, J., Kempenaers, B. & Dingemanse, N. J. Adaptive strategies for managing uncertainty may explain personality-related differences in behavioural plasticity. Oikos 121(7), 1009–1020 (2012).Article 

    Google Scholar 
    Réale, D., Reader, S. M., Sol, D., McDougall, P. T. & Dingemanse, N. J. Integrating animal temperament within ecology and evolution. Biol. Rev. 82, 291–318 (2007).Article 
    PubMed 

    Google Scholar 
    Coppens, C. M., de Boer, S. F. & Koolhaas, J. M. Coping styles and behavioural flexibility: Towards underlying mechanisms. Philos. Trans. R. Soc. B Biol. Sci. 365, 4021–4028 (2010).Article 

    Google Scholar 
    Benus, R. F., Daas, S. D., Koolhaas, J. M. & van Oortmerssen, G. A. Routine formation and flexibility in social and non-social behaviour of aggressive and non-aggressive male mice. Behaviour 112, 176–193 (1990).Article 

    Google Scholar 
    Dall, S. R., Houston, A. I. & McNamara, J. M. The behavioural ecology of personality: Consistent individual differences from an adaptive perspective. Ecol. Lett. 7, 734–739 (2004).Article 

    Google Scholar 
    Mitchell, D. J. & Biro, P. A. Is behavioural plasticity consistent across different environmental gradients and through time?. Proc. R. Soc. B. 284(1860), 20170893 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Stamps, J. A. Individual differences in behavioural plasticities. Biol. Rev. 91, 534–567 (2016).Article 
    PubMed 

    Google Scholar 
    Stamps, J. A. & Biro, P. A. Personality and individual differences in plasticity. Curr. Opin. Behav. Sci. 12, 18–23 (2016).Article 

    Google Scholar 
    Dingemanse, N. J., Both, C., Drent, P. J. & Tinbergen, J. M. Fitness consequences of avian personalities in a fluctuating environment. Proc. R. Soc. Lond. B 271, 847 (2004).Article 

    Google Scholar 
    Smith, B. R. & Blumstein, D. T. Fitness consequences of personality: a meta-analysis. Behav. Ecol. 19, 448–455 (2008).Article 

    Google Scholar 
    Dingemanse, N. J. & Réale, D. Natural selection and animal personality. Behaviour 142, 1159–1184 (2005).Article 

    Google Scholar 
    Duque-Wilckens, N., Trainor, B. C. & Marler, C. A. Aggression and territoriality. In Encyclopedia of animal behavior (ed. Choe, J. C.) 539–546 (Elsevier, 2019).Chapter 

    Google Scholar 
    AmphibiaWeb. AmphibiaWeb: Information on amphibian biology and conservation. Available at https://amphibiaweb.org (2022).Ringler, M. et al. Acoustic ranging in poison frogs—It is not about signal amplitude alone. Behav. Ecol. Sociobiol. 71, 114 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ringler, M., Ursprung, E. & Hödl, W. Site fidelity and patterns of short- and long-term movement in the brilliant-thighed poison frog Allobates femoralis (Aromobatidae). Behav. Ecol. Sociobiol. 63, 1281–1293 (2009).Article 

    Google Scholar 
    Ringler, M., Ringler, E., Magaña Mendoza, D. & Hödl, W. Intrusion experiments to measure territory size: Development of the method, tests through simulations, and application in the frog Allobates femoralis. PLoS ONE 6, e25844 (2011).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ringler, E., Ringler, M., Jehle, R. & Hödl, W. The female perspective of mating in A. femoralis, a territorial frog with paternal care—A spatial and genetic analysis. PLoS ONE 7, e40237 (2012).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ursprung, E., Ringler, M., Jehle, R. & Hödl, W. Strong male/male competition allows for nonchoosy females: High levels of polygynandry in a territorial frog with paternal care. Mol. Ecol. 20, 1759–1771 (2011).Article 
    PubMed 

    Google Scholar 
    Pröhl, H. Territorial behavior in dendrobatid frogs. J Herpetol 39, 354–365 (2005).Article 

    Google Scholar 
    Peignier, M. et al. Exploring links between personality traits and their social and non-social environments in wild poison frogs. Behav. Ecol. Sociobiol. 76, 93 (2022).Article 

    Google Scholar 
    Chaloupka, S. et al. Repeatable territorial aggression in a Neotropical poison frog. Front. Ecol. Evol. 10, 398 (2022).Article 

    Google Scholar 
    Amézquita Torres, A. et al. Masking interference and the evolution of the acoustic communication system in the Amazonian dendrobatid frog Allobates femoralis. Evolution 60, 1874–1887 (2006).
    Google Scholar 
    Rodríguez López, C., Amézquita Torres, A., Ringler, M., Pašukonis, A. & Hödl, W. Calling amplitude flexibility and acoustic spacing in the territorial frog Allobates femoralis. Behav. Ecol. Sociobiol. 74, 1–10 (2020).
    Google Scholar 
    Asab. Guidelines for the treatment of animals in behavioural research and teaching. Anim. Behav. 159, 1–11 (2020).
    Google Scholar 
    Du Percie Sert, N. et al. The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biol 18, e3000410 (2020).Article 

    Google Scholar 
    Ringler, E., Mangione, R. & Ringler, M. Where have all the tadpoles gone? Individual genetic tracking of amphibian larvae until adulthood. Mol. Ecol. Resour. 15, 737–746 (2015).Article 
    PubMed 

    Google Scholar 
    Ringler, M. et al. High-resolution forest mapping for behavioural studies in the Nature Reserve ‘Les Nouragues’, French Guiana. J. Maps 12, 26–32 (2016).Article 

    Google Scholar 
    Keith, D. A. et al. A function-based typology for Earth’s ecosystems. Nature 610, 513–518 (2022).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kaefer, I. L., Montanarin, A., da Costa, R. S. & Lima, P. A. Temporal patterns of reproductive activity and site attachment of the brilliant-thighed frog Allobates femoralis from central Amazonia. J. Herpetol. 46, 549–554 (2012).Article 

    Google Scholar 
    Rasband, W. S. ImageJ (U. S. National Institutes of Health, 1997–2021).Bolger, D. T., Morrison, T. A., Vance, B., Lee, D. & Farid, H. A computer-assisted system for photographic mark–recapture analysis. Methods Ecol. Evol. 3, 813–822 (2012).Article 

    Google Scholar 
    Narins, P. M., Hödl, W. & Grabul, D. S. Bimodal signal requisite for agonistic behavior in a dart-poison frog, Epipedobates femoralis. Proc. Natl. Acad. Sci. USA 100, 577–580 (2003).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gasser, H., Amézquita Torres, A. & Hödl, W. Who is calling? Intraspecific call variation in the aromobatid frog Allobates femoralis. Ethology 115, 596–607 (2009).Article 

    Google Scholar 
    Hödl, W. Dendrobates femoralis (Dendrobatidae): a handy fellow for frog bioacoustics in Proceedings of the 4th Ordinary General meeting of the Societas Europaea Herpetologica, (ed.van Gelder, J. J., Strijbosch, H. & Bergers, P.) (1987).Ursprung, E., Ringler, M. & Hödl, W. Phonotactic approach pattern in the neotropical frog Allobates femoralis: A spatial and temporal analysis. Behaviour 146, 153–170 (2009).Article 

    Google Scholar 
    Sonnleitner, R., Ringler, M., Loretto, M.-C. & Ringler, E. Experience shapes accuracy in territorial decision-making in a poison frog. Biol. Lett. 16, 20200094 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hödl, W. Phyllobates femoralis (Dendrobatidae): Rufverhalten und akustische Orientierung der Männchen (Freilandaufnahmen) in Bundesstaatliche Hauptstelle für Wissenschaftliche Kinematographie (1983).Tumulty, J. P. et al. Brilliant-thighed poison frogs do not use acoustic identity information to treat territorial neighbours as dear enemies. Anim. Behav. 141, 203–220 (2018).Article 

    Google Scholar 
    Fernandes, I. Y. et al. Unlinking the speciation steps: Geographical factors drive changes in sexual signals of an Amazonian Nurse-Frog through body size variation. Evol. Biol. 48, 81–93 (2021).Article 

    Google Scholar 
    Garcia, M. J. et al. Dueling frogs: do male green tree frogs (Hyla cinerea) eavesdrop on and assess nearby calling competitors?. Behav. Ecol. Sociobiol. 73(2), 1041 (2019).Article 

    Google Scholar 
    Gingras, B., Böckle, M., Herbst, C. T. & Fitch, W. T. Call acoustics reflect body size across four clades of anurans. J Zool 289(2), 143–150 (2013).Article 

    Google Scholar 
    Stoffel, M. A., Nakagawa, S. & Schielzeth, H. rptR: Repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods Ecol. Evol. 8, 1639–1644 (2017).Article 

    Google Scholar 
    Fox, J. et al. Package ‘sem’: Structural Equation Models. https://CRAN.R-project.org/package=sem (2022).Burnham, K. P. & Anderson, D. R. Model selection and multimodel inference: A practical information-theoretic approach 2nd edn. (Springer, 2002).MATH 

    Google Scholar 
    Hertel, A. G., Niemelä, P. T., Dingemanse, N. J. & Mueller, T. A guide for studying among-individual behavioral variation from movement data in the wild. Mov. Ecol. 8, 30 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: The MCMCglmmR package. J. Stat. Softw. 33, 1–22 (2010).Article 

    Google Scholar 
    Bürkner, P.-C. brms: An R package for Bayesian multilevel models using stan. J. Stat. Softw. 80, 1–28 (2017).Article 

    Google Scholar 
    Gelman, A., Hwang, J. & Vehtari, A. Understanding predictive information criteria for Bayesian models. Stat. Comput. 24, 997–1016 (2014).Article 
    MathSciNet 
    MATH 

    Google Scholar 
    Whalen, A. & Hoppitt, W. J. E. Bayesian model selection with network based diffusion analysis. Front. Psychol. 7, 409 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    R Core Team. R: A language and environment for statistical computing (R Foundation for Statistical Computing, 2019).
    Google Scholar 
    Ryan, M. J., Bartholomew, G. A. & Rand, A. S. Energetics of reproduction in a neotropical frog, Physalaemus pustulosus. Ecology 64, 1456–1462 (1983).Article 

    Google Scholar 
    Taigen, T. L. & Wells, K. D. Energetics of vocalization by an anuran amphibian (Hyla versicolor). J. Comp. Physiol. 155, 163–170 (1985).Article 

    Google Scholar 
    Pough, F. H. & Taigen, T. L. Metabolic correlates of the foraging and social behaviour of dart-poison frogs. Anim. Behav. 39, 145–155 (1990).Article 

    Google Scholar 
    Bell, A. M., Hankison, S. J. & Laskowski, K. L. The repeatability of behaviour: A meta-analysis. Anim. Behav. 77, 771–783 (2009).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kelleher, S. R., Silla, A. J. & Byrne, P. G. Animal personality and behavioral syndromes in amphibians: A review of the evidence, experimental approaches, and implications for conservation. Behav. Ecol. Sociobiol. 72, 10539 (2018).Article 

    Google Scholar 
    Moser-Purdy, C., MacDougall-Shackleton, E. A. & Mennill, D. J. Enemies are not always dear: Male song sparrows adjust dear enemy effect expression in response to female fertility. Anim. Behav. 126, 17–22 (2017).Article 

    Google Scholar  More

  • in

    Freeze-thaw cycles alter the growth sprouting strategy of wetland plants by promoting denitrification

    Campbell, J. L. & Laudon, H. Carbon response to changing winter conditions in northern regions: current understanding and emerging research needs. Environ. Rev. 27, 545–566 (2019).Article 

    Google Scholar 
    Groffman, P. M. et al. Effects of mild winter freezing on soil nitrogen and carbon dynamics in a northern hardwood forest. Biogeochemistry 56, 191–213 (2001).Article 
    CAS 

    Google Scholar 
    Song, C. et al. Large methane emission upon spring thaw from natural wetlands in the northern permafrost region. Environ. Res. Lett. 7, 034009 (2012).Article 

    Google Scholar 
    Chen, H. et al. Methane emissions during different freezing-thawing periods from a fen on the Qinghai-Tibetan Plateau: Four years of measurements. Agric. Ecosyst. Environ. 297, 108279 (2021).
    Google Scholar 
    Bao, T., Xu, X., Jia, G., Billesbach, D. P. & Sullivan, R. C. Much stronger tundra methane emissions during autumn freeze than spring thaw. Glob. Chang. Biol. 27, 376–387 (2021).Article 
    CAS 

    Google Scholar 
    Yu, J. et al. Enhanced net formations of nitrous oxide and methane underneath the frozen soil in Sanjiang wetland, northeastern China. J. Geophys. Res 112, D07111 (2007).Article 

    Google Scholar 
    Kreyling, J., Peršoh, D., Werner, S., Benzenberg, M. & Wöllecke, J. Short-term impacts of soil freeze-thaw cycles on roots and root-associated fungi of Holcus lanatus and Calluna vulgaris. Plant Soil 353, 19–31 (2012).Article 
    CAS 

    Google Scholar 
    Min, K., Chen, K. & Arora, R. Effect of short-term versus prolonged freezing on freeze–thaw injury and post-thaw recovery in spinach: Importance in laboratory freeze–thaw protocols. Environ. Exp. Bot. 106, 124–131 (2014).Article 
    CAS 

    Google Scholar 
    Kennedy, A. Photosynthetic response of the Antarctic moss Polytrichum alpestre Hoppe to low temperatures and freeze-thaw stress. Polar Biol. 13, 271–279 (1993).Article 

    Google Scholar 
    Sanders-DeMott, R., Sorensen, P. O., Reinmann, A. B. & Templer, P. H. Growing season warming and winter freeze–thaw cycles reduce root nitrogen uptake capacity and increase soil solution nitrogen in a northern forest ecosystem. Biogeochemistry 137, 337–349 (2018).Article 
    CAS 

    Google Scholar 
    Vankoughnett, M. R. & Henry, H. A. L. Soil freezing and N deposition: transient vs. multi-year effects on extractable C and N, potential trace gas losses and microbial biomass. Soil Biol. Biochem. 77, 170–178 (2014).Article 
    CAS 

    Google Scholar 
    Kreyling, J., Beierkuhnlein, C., Pritsch, K., Schloter, M. & Jentsch, A. Recurrent soil freeze-thaw cycles enhance grassland productivity. New Phytol. 177, 938–945 (2008).Article 

    Google Scholar 
    Song, Y., Zou, Y., Wang, G. & Yu, X. Altered soil carbon and nitrogen cycles due to the freeze-thaw effect: a meta-analysis. Soil Biol. Biochem. 109, 35–49 (2017).Article 
    CAS 

    Google Scholar 
    Vankoughnett, M. R. & Henry, H. A. L. Soil freezing and N deposition: transient vs multi-year effects on plant productivity and relative species abundance. New Phytol. 202, 1277–1285 (2014).Article 
    CAS 

    Google Scholar 
    Luan, Z. & Cao, H. Response of fine root growth and nitrogen and phosphorus contents to soil freezing in Calamagrostis angustifolia wetland, Sanjiang Plain, Northeast China. J. Food Agric. Environ. 10, 1495–1499 (2012).
    Google Scholar 
    Garcia, M. O. et al. Soil microbes trade-off biogeochemical cycling for stress tolerance traits in response to year-round climate change. Front. Microbiol. 11, 616 (2020).Article 

    Google Scholar 
    Tang, H., Bai, J., Chen, F., Liu, Y. & Lou, Y. Effects of salinity and temperature on tuber sprouting and growth of Schoenoplectus nipponicus. Ecosphere 12, e03448 (2021).Article 

    Google Scholar 
    Satyanti, A., Guja, L. K. & Nicotra, A. B. Temperature variability drives within-species variation in germination strategy and establishment characteristics of an alpine herb. Oecologia 189, 407–419 (2019).Article 

    Google Scholar 
    Harrison, J. L., Schultz, K., Blagden, M., Sanders-DeMott, R. & Templer, P. H. Growing season soil warming may counteract trend of nitrogen oligotrophication in a northern hardwood forest. Biogeochemistry 151, 139–152 (2020).Article 
    CAS 

    Google Scholar 
    Semenchuk, P. R. et al. Deeper snow alters soil nutrient availability and leaf nutrient status in high Arctic tundra. Biogeochemistry 124, 81–94 (2015).Article 

    Google Scholar 
    Song, Y., Zou, Y., Wang, G. & Yu, X. Stimulation of nitrogen turnover due to nutrients release from aggregates affected by freeze-thaw in wetland soils. Phys. Chem. Earth 97, 3–11 (2017).Article 

    Google Scholar 
    Keith, D. A., Rodoreda, S. & Bedward, M. Decadal change in wetland-woodland boundaries during the late 20th century reflects climatic trends. Glob. Chang. Biol. 16, 2300–2306 (2010).Article 

    Google Scholar 
    Wang, J., Song, C., Hou, A. & Xi, F. Methane emission potential from freshwater marsh soils of Northeast China: response to simulated freezing-thawing cycles. Wetlands 37, 437–445 (2017).Article 

    Google Scholar 
    Yu, X. et al. Wetland plant litter decomposition occurring during the freeze season under disparate flooded conditions. Sci. Total Environ. 706, 136091 (2020).Article 
    CAS 

    Google Scholar 
    Dong, X. et al. Variations in active layer soil hydrothermal dynamics of typical wetlands in permafrost region in the Great Hing’an Mountains, northeast China. Ecol. Indic. 129, 107880 (2021).Article 

    Google Scholar 
    Li, Y. et al. Freeze-thaw cycles increase the mobility of phosphorus fractions based on soil aggregate in restored wetlands. CATENA 209, 105846 (2022).Article 
    CAS 

    Google Scholar 
    Song, C., Zhang, J., Wang, Y., Wang, Y. & Zhao, Z. Emission of CO2, CH4 and N2O from freshwater marsh in northeast of China. J. Environ. Manage. 88, 428–436 (2008).Article 
    CAS 

    Google Scholar 
    Wang, G., Liu, J., Zhao, H., Wang, J. & Yu, J. Phosphorus sorption by freeze–thaw treated wetland soils derived from a winter-cold zone (Sanjiang Plain, Northeast China). Geoderma 138, 153–161 (2007).Article 
    CAS 

    Google Scholar 
    Ji, X., Liu, M., Yang, J. & Feng, F. Meta-analysis of the impact of freeze–thaw cycles on soil microbial diversity and C and N dynamics. Soil Biol. Biochem. 168, 108608 (2022).Article 
    CAS 

    Google Scholar 
    Ren, J. et al. Shifts in soil bacterial and archaeal communities during freeze-thaw cycles in a seasonal frozen marsh, Northeast China. Sci. Total. Environ. 625, 782–791 (2018).Article 
    CAS 

    Google Scholar 
    Mitsch, W. J. & Gosselink, J. G. Wetlands. 5th edn (Wiley, Hoboken, New Jersey, 2015).Yu, X., Zou, Y., Jiang, M., Lu, X. & Wang, G. Response of soil constituents to freeze–thaw cycles in wetland soil solution. Soil Biol. Biochem. 43, 1308–1320 (2011).Article 
    CAS 

    Google Scholar 
    Sawicka, J. E., Robador, A., Hubert, C., Jørgensen, B. B. & Bruchert, V. Effects of freeze-thaw cycles on anaerobic microbial processes in an Arctic intertidal mud flat. ISME J 4, 585–594 (2010).Article 
    CAS 

    Google Scholar 
    Song, Y. The Freeze-thaw Effect On Soil Mineralization Between Various Moisture States Of Wetlands. Master of Natural Science thesis (Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, 2017).Mason, R. E. et al. Evidence, causes, and consequences of declining nitrogen availability in terrestrial ecosystems. Science 376, eabh3767 (2022).Article 
    CAS 

    Google Scholar 
    Koerselman, W. & Meuleman, A. F. M. The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J. Appl. Ecol. 33, 1441–1450 (1996).Article 

    Google Scholar 
    Yang, K. et al. Immediate and carry-over effects of increased soil frost on soil respiration and microbial activity in a spruce forest. Soil Biol. Biochem. 135, 51–59 (2019).Article 
    CAS 

    Google Scholar 
    Lambers, H., Chapin, F. S. I. & Pons, T. L. Plant Physiological Ecology. 2nd edn (Springer, 2008).Ott, J. P., Klimešová, J. & Hartnett, D. C. The ecology and significance of below-ground bud banks in plants. Ann. Bot. 123, 1099–1118 (2019).Article 

    Google Scholar 
    Pedersen, E. P., Elberling, B. & Michelsen, A. Foraging deeply: depth‐specific plant nitrogen uptake in response to climate‐induced N‐release and permafrost thaw in the High Arctic. Glob. Chang. Biol. 26, 6523–6536 (2020).Article 

    Google Scholar 
    Dyer, A.R. Maternal and sibling factors induce dormancy in dimorphic seed pairs of Aegilops triuncialis. Plant Ecol. 172, 211–218 (2004).Article 

    Google Scholar 
    Renne, I. J. et al. Eavesdropping in plants: delayed germination via biochemical recognition. J. Ecol. 102, 86–94 (2014).Article 

    Google Scholar 
    Li, H. Eco-physiological Responding Characteristics of Scirpus Planiculmis on Coupling of Water Table Depths and Salinity in Momoge Wetland. Master Dissertation thesis, University of Chinese Academy of Sciences (Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, 2013).Yu, D. Responses of Sprouting and Growth to Environmental Factors in Bolboschoenus Planiculmis. Master Dissertation thesis (Harbin Normal University, 2022).Zhang, C., Willis, C. G., Donohue, K., Ma, Z. & Du, G. Effects of environment, life-history and phylogeny on germination strategy of 789 angiosperms species on the eastern Tibetan Plateau. Ecol. Indic. 129, 107974 (2021).Article 

    Google Scholar 
    Hoyle, G. L. et al. Seed germination strategies: an evolutionary trajectory independent of vegetative functional traits. Front. Plant Sci. 6, 731 (2015).Article 

    Google Scholar 
    Mercer, K. L., Alexander, H. M. & Snow, A. A. Selection on seedling emergence timing and size in an annual plant, Helianthus annuus (common sunflower, Asteraceae). Am. J. Bot. 98, 975–985 (2011).Article 

    Google Scholar 
    Cui, Y. et al. Ecoenzymatic stoichiometry reveals microbial phosphorus limitation decreases the nitrogen cycling potential of soils in semi-arid agricultural ecosystems. Soil Tillage. Res. 197, 104463 (2020).Article 

    Google Scholar 
    Ye, Z. et al. Ecoenzymatic stoichiometry reflects the regulation of microbial carbon and nitrogen limitation on soil nitrogen cycling potential in arid agriculture ecosystems. J. Soils Sediments 22, 1228–1241 (2022).Article 
    CAS 

    Google Scholar 
    Pan, Y. et al. Drivers of plant traits that allow survival in wetlands. Funct. Ecol. 34, 956–967 (2020).Article 

    Google Scholar 
    Pezeshki, S. R. Wetland plant responses to soil flooding. Environ. Exp. Bot. 46, 299–312 (2001).Article 

    Google Scholar 
    Zheng, S. Soil Water-heat Process and Nitrogen Transformation During Freezing and Thawing Period in Wetland of Momoge. Master Dissertation thesis (Jilin Agricultural University, 2019).An, Y., Gao, Y., Zhang, Y., Tong, S. & Liu, X. Early establishment of Suaeda salsa population as affected by soil moisture and salinity: implications for pioneer species introduction in saline-sodic wetlands in Songnen Plain, China. Ecol. Indic. 107, 105654 (2019).Article 
    CAS 

    Google Scholar 
    FAO/IIASA/ISRIC/ISS-CAS/JRC. Harmonized World Soil Database (version 1.2). (FAO, Rome, Italy and IIASA, Laxenburg, Austria, 2012).Jiang, M., Lu, X., Xu, L. & Yang, Q. Estimation on benefit of latent soil nutrient in melmeg reserve wetlands. J. Nat. Resour 20, 279–285 (2005).
    Google Scholar 
    Wang, Y. & Zhang, S. The pH distribution and soil nutrient characteristic at different habitats-a case study of Momoge Wetland. J. Anhui Agric. Sci. 50, 135–139 (2022).
    Google Scholar 
    Hao, M. The Ecological Restoration Research on Momoge Scripus Planiculmis Wetland. Master Dissertation thesis, University of Chinese Academy of Sciences (Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, 2016).Ma, H. et al. Effect of nitrate supply on the facilitation between two salt-marsh plants (Suaeda salsa and Scirpus planiculmis). J. Plant. Ecol. 13, 204–212 (2020).Article 

    Google Scholar 
    Liu, B. et al. Effects of burial depth and water depth on seedling emergence and early growth of Scirpus planiculmis Fr. Schmidt. Ecol. Eng. 87, 30–33 (2016).Article 

    Google Scholar 
    Zhang, L., Zhang, G., Li, H. & Sun, G. Eco-physiological responses of Scirpus planiculmis to different water-salt conditions in Momoge wetland. Pol. J. Environ. Stud. 23, 1813–1820 (2014).
    Google Scholar 
    Sosnová, M., van Diggelen, R. & Klimešová, J. Distribution of clonal growth forms in wetlands. Aquat. Bot. 92, 33–39 (2010).Article 

    Google Scholar 
    Lu, R. Analytical Methods of Soil Agrochemistry (China Agricultural Science and Technology Press, 2000).Bao, S. Soil and Agricultural Chemistry Analysis. 3 edn. (China Agriculture Press, 2000).Magoc, T. & Salzberg, S. L. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963 (2011).Article 
    CAS 

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

    Google Scholar 
    Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011).Article 
    CAS 

    Google Scholar 
    Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998 (2013).Article 
    CAS 

    Google Scholar 
    Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013).Article 
    CAS 

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

    Google Scholar 
    Li, D., Liu, C. M., Luo, R., Sadakane, K. & Lam, T. W. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31, 1674–1676 (2015).Article 
    CAS 

    Google Scholar 
    Gurevich, A., Saveliev, V., Vyahhi, N. & Tesler, G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 29, 1072–1075 (2013).Article 
    CAS 

    Google Scholar 
    Zhu, W., Lomsadze, A. & Borodovsky, M. Ab initio gene identification in metagenomic sequences. Nucleic Acids Res. 38, e132 (2010).Article 

    Google Scholar 
    Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150–3152 (2012).Article 
    CAS 

    Google Scholar 
    Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59–60 (2015).Article 
    CAS 

    Google Scholar 
    Lauro, F. M. et al. An integrative study of a meromictic lake ecosystem in Antarctica. ISME J 5, 879–895 (2011).Article 
    CAS 

    Google Scholar 
    Shen, M. et al. Trophic status is associated with community structure and metabolic potential of planktonic microbiota in Plateau lakes. Front. Microbiol. 10, 2560 (2019).Article 

    Google Scholar 
    Kieft, B. et al. Microbial community structure-function relationships in Yaquina Bay estuary reveal spatially distinct carbon and nitrogen cycling capacities. Front. Microbiol. 9, 1282 (2018).Article 

    Google Scholar 
    Kay, M. Effect Sizes with ART (2021).Mangiafico, S. S. Summary and Analysis of Extension Program Evaluation in R, version 1.18.8 https://rcompanion.org/handbook/ (2016).R Core Team R: A Language and Environment for Statistical Computing (2020).Fox, J. & Weisberg, S. An R Companion to Applied Regression. 3rd edn (Thousand Oaks, Sage, CA, 2019).Kay, M., Elkin, L. A., Higgins, J. J. & Wobbrock, J. O. ARTool: Aligned Rank Transform for Nonparametric Factorial ANOVAs. R package version 0.11.1. https://doi.org/10.5281/zenodo.594511 (2021).Wobbrock, J. O., Findlate, L., Gergle, D. & Higgins, J. J. The aligned rank transform for nonparametric factorial analyses using only anova procedures. 29th Annual Chi Conference on Human Factors in Computing Systems (CHI 2011), p. 143-146. https://doi.org/10.1145/1978942.1978963 (2011).Elkin, L. A., Kay, M., Higgins, J. J. & Wobbrock, J. O. An aligned rank transform procedure for multifactor contrast Tests. Proceedings of the ACM Symposium on User Interface Software and Technology (UIST 2021), p. 754-768. https://doi.org/10.1145/3472749.3474784 (2021).Lenth, R. V. emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.6.3. (2021).Wickham, H. ggplot2: Elegant Graphics for Data Analysis (2016).Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.5-7 (2020).Revelle, W. psych: Procedures for Psychological, Psychometric, and Personality Research, Northwestern University, Evanston, Illinois, USA, R package version 2.2.9 (2022).Wei, T. & Simko, V. R package ‘corrplot’: Visualization of a Correlation Matrix (Version 0.90) (2021). More