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    Big dino, little dino: how T. rex’s relatives changed their size

    Theropod dinosaurs such as Tarbosaurus bataar grew large or small in a range of ways.Credit: Marco Ansaloni/SPL

    A sweeping analysis of shin bones has given researchers a glimpse into how some dinosaurs evolved into mega-beasts such as Tyrannosaurus, and others into smaller, bird-like creatures. The work, published this week in Science1, reveals that dinosaurs used more than one evolutionary trick to become larger — or smaller — over time.Prevailing wisdom held that large-bodied animals are bigger than their smaller-bodied relatives because they grow faster during their most rapid period of growth. That trend holds true for modern animals including birds and mammals — elephants and ostriches grow faster than chihuahuas and sparrows, for example.It’s not the case for all animals. Crocodiles and alligators, for instance, become large because they grow for a long time. But palaeontologists had assumed that for theropod dinosaurs — a group that includes the iconic T. rex and which spawned modern birds — large species got big through rapid growth spurts. “It’s kind of become the established idea in dinosaurs,” says palaeontologist Michael D’Emic at Adelphi University in Garden City, New York.But that’s not what D’Emic found when he sawed into the bones of Majungasaurus, a 7-metre-long T. rex relative that lived 66 million years ago on what is now Madagascar. The speed of growth in dinosaurs is recorded in rings laid down each year in their bones. Instead of seeing wide rings corresponding to a rapid adolescent growth spurt, D’Emic found lots of narrow growth rings, suggesting that Majungasaurus had become large over a prolonged period.“I was very surprised,” he says. The next dinosaur he examined, a similar-sized beast called Ceratasaurus, was the opposite — a big dinosaur that grew fast during its growth spurt, says D’Emic.Bone growth ringsOver a decade, D’Emic and his colleagues amassed bone growth-ring measurements from 42 theropod species to see which strategies led to large and small bodies. They found that 31% of theropod species were larger than their ancestors because of faster growth and 28% because of prolonged growth. Meanwhile, 21% became smaller than their ancestors by shortening their growth spurts, and 19% by slowing growth.The study covered theropod species that lived between 230 million years ago and the end of the Cretaceous period 66 million years ago, when a mass-extinction event wiped out the non-avian dinosaurs. It’s “a huge evolutionary timescale”, to include in an analysis, says Vera Weisbecker, an evolutionary biologist at Flinders University in Adelaide, Australia. “That is really impressive,” she says. “It’s just fascinating that there are so many developmental ways to become big or small.”Palaeontologist Kevin Padian at the University of California, Berkeley, says the analysis is the kind of work that needs to be done, animal group by animal group, to understand how body size evolves.Drivers of changeBut Meike Köhler, an evolutionary palaeobiologist at the Catalan Institution for Research and Advanced Studies in Barcelona, Spain, says the findings are not surprising because previous work has shown a range of growth strategies across animal species. Köhler would like to see an analysis that considers what ecological circumstances influenced how animals changed in size over time.Weisbecker says that the growth strategy used might be related to evolutionary pressures. “If you looked at all the ones with explosive early growth, you might be able to test if they happen to be the ones that are more likely to be predated on, for example,” she says.For each species, the growth strategy that led to its individual body size probably related to its unique environment, says Padian. “It’s not a one-size-fits-all, which is a good thing for us to learn,” he says. “We might have thought that, but they’ve documented it.”D’Emic says he and his team are conducting similar analyses on other groups, including mammals — a group that contains many more species to sample — to see whether the diversity is found in other branches of the evolutionary tree. More

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    Seasonal activities of the phyllosphere microbiome of perennial crops

    Robertson, G. P. et al. Cellulosic biofuel contributions to a sustainable energy future: Choices and outcomes. Sci. (80-.) 356, 1–9 (2017).Article 

    Google Scholar 
    Ma, L. et al. The impact of stand age and fertilization on the soil microbiome of Miscanthus × giganteus. Phytobiomes J. 5, 51–59 (2021).Article 

    Google Scholar 
    Hestrin, R., Lee, M. R., Whitaker, B. K. & Pett-Ridge, J. The switchgrass microbiome: a review of structure, function, and taxonomic distribution. Phytobiomes J. 5, 14–28 (2021).Article 

    Google Scholar 
    Heaton, E. A., Dohleman, F. G. & Long, S. P. Meeting US biofuel goals with less land: The potential of Miscanthus. Glob. Chang. Biol. 14, 2000–2014 (2008).Article 
    ADS 

    Google Scholar 
    Langholtz, M., Stokes, B. & Eaton, L. 2016 billion-ton report: Advancing domestic resources for a thriving bioeconomy (Executive Summary). Ind. Biotechnol. 12, 282–289 (2016).Article 

    Google Scholar 
    Roley, S. S. et al. Associative nitrogen fixation (ANF) across a nitrogen input gradient. PLoS One 13, 1–19 (2018).Article 

    Google Scholar 
    Toju, H. et al. Core microbiomes for sustainable agroecosystems. Nat. Plants 4, 247–257 (2018).Article 
    PubMed 

    Google Scholar 
    Busby, P. E. et al. Research priorities for harnessing plant microbiomes in sustainable agriculture. PLoS Biol. 15, 1–14 (2017).Article 

    Google Scholar 
    Wang, N. R. & Haney, C. H. Harnessing the genetic potential of the plant microbiome. Biochem. (Lond.) 42, 20–25 (2020).Article 
    CAS 

    Google Scholar 
    Haskett, T. L., Tkacz, A. & Poole, P. S. Engineering rhizobacteria for sustainable agriculture. ISME J. 15, 949–964 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hacquard, S. et al. Microbiota and host nutrition across plant and animal kingdoms. Cell Host Microbe 17, 603–616 (2015).Article 
    CAS 
    PubMed 

    Google Scholar 
    Gopal, M. & Gupta, A. Microbiome selection could spur next-generation plant breeding strategies. Front. Microbiol. 7, 1971 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hardoim, P. R. et al. The hidden world within plants: Ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol. Mol. Biol. Rev. 79, 293–320 (2015).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Andrews, J. H. & Harris, R. F. The ecology and biogeography of microorganisms on plant surfaces. Annu. Rev. Phytopathol. 38, 145–180 (2000).Article 
    PubMed 

    Google Scholar 
    Bulgarelli, D., Schlaeppi, K., Spaepen, S., van Themaat, E. V. L. & Schulze-Lefert, P. Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64, 807–838 (2013).Article 
    CAS 
    PubMed 

    Google Scholar 
    Müller, D. B., Vogel, C., Bai, Y. & Vorholt, J. A. The Plant Microbiota: Systems-Level Insights and Perspectives. Annu. Rev. Genet. 50, 120215–034952 (2016).Article 

    Google Scholar 
    Kuzyakov, Y. & Razavi, B. S. Rhizosphere size and shape: Temporal dynamics and spatial stationarity. Soil Biol. Biochem. 135, 343–360 (2019).Article 
    CAS 

    Google Scholar 
    Bell, T. H. et al. Manipulating wild and tamed phytobiomes: Challenges and opportunities. Phytobiomes J. 3, 3–21 (2019).Article 

    Google Scholar 
    Chen, T. et al. A plant genetic network for preventing dysbiosis in the phyllosphere. Nature 580, 653–657 (2020).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Vorholt, J. A. Microbial life in the phyllosphere. Nat. Rev. Microbiol. 10, 828–840 (2012).Article 
    CAS 
    PubMed 

    Google Scholar 
    Koskella, B. The phyllosphere. Curr. Biol. 30, R1143–R1146 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Lindow, S. E. & Brandl, M. T. Microbiology of the phyllosphere. Appl. Environ. Microbiol. 69, 1875–1883 (2003).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bringel, F. & Couée, I. Pivotal roles of phyllosphere microorganisms at the interface between plant functioning and atmospheric trace gas dynamics. Front. Microbiol. 6, 486 (2015).Dorokhov, Y. L., Sheshukova, E. V. & Komarova, T. V. Methanol in plant life. Front. Plant Sci. 871, 1–6 (2018).
    Google Scholar 
    Cavicchioli, R. et al. Scientists’ warning to humanity: microorganisms and climate change. Nat. Rev. Microbiol. 17, 569–586 (2019).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Peñuelas, J. & Terradas, J. The foliar microbiome. Trends Plant Sci. 19, 278–280 (2014).Article 
    PubMed 

    Google Scholar 
    Edwards, J. et al. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc. Natl Acad. Sci. USA. 112, E911–E920 (2015).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Zhalnina, K. et al. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat. Microbiol. 3, 470 (2018).Article 
    CAS 
    PubMed 

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

    Google Scholar 
    Shade, A. & Stopnisek, N. Abundance-occupancy distributions to prioritize plant core microbiome membership. Curr. Opin. Microbiol. 49, 50–58 (2019).Article 
    PubMed 

    Google Scholar 
    Stopnisek, N. & Shade, A. Persistent microbiome members in the common bean rhizosphere: an integrated analysis of space, time, and plant genotype. ISME J. 15, 2708–2722 (2021).Grady, K. L., Sorensen, J. W., Stopnisek, N., Guittar, J. & Shade, A. Assembly and seasonality of core phyllosphere microbiota on perennial biofuel crops. Nat. Commun. 10, 4135 (2019).Singer, E., Bonnette, J., Kenaley, S. C., Woyke, T. & Juenger, T. E. Plant compartment and genetic variation drive microbiome composition in switchgrass roots. Environ. Microbiol. Rep. 11, 185–195 (2019).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lundberg, D. S. et al. Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86–90 (2012).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bulgarelli, D. et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91–95 (2012).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Bahulikar, R. A., Torres-Jerez, I., Worley, E., Craven, K. & Udvardi, M. K. Diversity of nitrogen-fixing bacteria associated with switchgrass in the native tallgrass prairie of Northern Oklahoma. Appl. Environ. Microbiol. 80, 5636–5643 (2014).Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Roley, S. S., Xue, C., Hamilton, S. K., Tiedje, J. M. & Robertson, G. P. Isotopic evidence for episodic nitrogen fixation in switchgrass (Panicum virgatum L.). Soil Biol. Biochem. 129, 90–98 (2019).Article 
    CAS 

    Google Scholar 
    Bowers, R. M. et al. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat. Biotechnol. 35, 725–731 (2017).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Yoon, S. H., Ha, S. M., Lim, J., Kwon, S. & Chun, J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van. Leeuwenhoek, Int. J. Gen. Mol. Microbiol. 110, 1281–1286 (2017).Article 
    CAS 

    Google Scholar 
    Julsing, M. K., Rijpkema, M., Woerdenbag, H. J., Quax, W. J. & Kayser, O. Functional analysis of genes involved in the biosynthesis of isoprene in Bacillus subtilis. Appl. Microbiol. Biotechnol. 75, 1377–1384 (2007).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Carlström, C. I. et al. Synthetic microbiota reveal priority effects and keystone strains in the Arabidopsis phyllosphere. Nat. Ecol. Evol. 3, 1445–1454 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Laskowska, E. & Kuczyńska-Wiśnik, D. New insight into the mechanisms protecting bacteria during desiccation. Curr. Genet. 66, 313–318 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Zou, H. et al. The metabolism and biotechnological application of betaine in microorganism. Appl. Microbiol. Biotechnol. 100, 3865–3876 (2016).Article 
    CAS 
    PubMed 

    Google Scholar 
    Rastogi, G., Coaker, G. L. & Leveau, J. H. J. New insights into the structure and function of phyllosphere microbiota through high-throughput molecular approaches. FEMS Microbiol. Lett. 348, 1–10 (2013).Article 
    CAS 
    PubMed 

    Google Scholar 
    Urrejola, C. et al. Genomic features for desiccation tolerance and sugar biosynthesis in the extremophile gloeocapsopsis sp. UTEX B3054. Front. Microbiol. 10, 1–11 (2019).Article 

    Google Scholar 
    Lacerda-Júnior, G. V. et al. Land use and seasonal effects on the soil microbiome of a Brazilian dry forest. Front. Microbiol. 10, 1–14 (2019).Article 

    Google Scholar 
    Dai, J. et al. Unraveling adaptation of Pontibacter korlensis to radiation and infertility in desert through complete genome and comparative transcriptomic analysis. Sci. Rep. 5, 1–9 (2015).Article 

    Google Scholar 
    Harty, C. E. et al. Ethanol stimulates trehalose production through a SpoT-DksA-AlgU-dependent pathway in Pseudomonas aeruginosa. J. Bacteriol. 201, 1–21 (2019).Kimmerer, T. W. & MacDonald, R. C. Acetaldehyde and ethanol biosynthesis in leaves of plants. Plant Physiol. 84, 1204–1209 (1987).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ferner, E., Rennenberg, H. & Kreuzwieser, J. Effect of flooding on C metabolism of flood-tolerant (Quercus robur) and non-tolerant (Fagus sylvatica) tree species. Tree Physiol. 32, 135–145 (2012).Article 
    CAS 
    PubMed 

    Google Scholar 
    Kimmerer, T. W. & Kozlowski, T. T. Ethylene, ethane, acetaldehyde, and ethanol production by plants under stress. Plant Physiol. 69, 840–847 (1982).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Liu, Y. et al. Assessment of drought tolerance of 49 switchgrass (Panicum virgatum) genotypes using physiological and morphological parameters. Biotechnol. Biofuels 8, 1–18 (2015).Article 

    Google Scholar 
    Wingler, A. et al. Trehalose 6-phosphate is required for the onset of leaf senescence associated with high carbon availability. Plant Physiol. 158, 1241–1251 (2012).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gottschlich, L., Geiser, P., Bortfeld-Miller, M., Field, C. M. & Vorholt, J. A. Complex general stress response regulation in Sphingomonas melonis Fr1 revealed by transcriptional analyses. Sci. Rep. 9, 1–13 (2019).Article 
    CAS 

    Google Scholar 
    Chen, C., Li, S., McKeever, D. R. & Beattie, G. A. The widespread plant-colonizing bacterial species Pseudomonas syringae detects and exploits an extracellular pool of choline in hosts. Plant J. 75, 891–902 (2013).Article 
    CAS 
    PubMed 

    Google Scholar 
    Valenzuela-Soto, E. M. & Figueroa-Soto, C. G. Biosynthesis and degradation of glycine betaine and its potential to control plant growth and development. in Osmoprotectant-Mediated Abiotic Stress Tolerance in Plants (eds. Anwar Hossain, M., Kumar, V., Burritt, D. J., Fujita, M. & Makela, P. S. A.) 241–256 (Springer, 2019). https://doi.org/10.1007/978-3-030-27423-8_5.Kerchev, P., De Smet, B., Waszczak, C., Messens, J. & Van Breusegem, F. Redox strategies for crop improvement. Antioxid. Redox Signal 23, 1186–1205 (2015).Article 
    CAS 
    PubMed 

    Google Scholar 
    Considine, M. J. & Foyer, C. H. Redox regulation of plant development. Antioxid. Redox Signal. 21, 1305–1326 (2014).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Spaepen, S., Vanderleyden, J. & Remans, R. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. Rev. 31, 425–448 (2007).Article 
    CAS 
    PubMed 

    Google Scholar 
    Egamberdieva, D., Wirth, S. J., Alqarawi, A. A., Abd-Allah, E. F. & Hashem, A. Phytohormones and beneficial microbes: Essential components for plants to balance stress and fitness. Front. Microbiol. 8, 1–14 (2017).Article 

    Google Scholar 
    Lajoie, G., Maglione, R. & Kembel, S. W. Adaptive matching between phyllosphere bacteria and their tree hosts in a neotropical forest. Microbiome 8, 1–10 (2020).Article 

    Google Scholar 
    McGenity, T. J., Crombie, A. T. & Murrell, J. C. Microbial cycling of isoprene, the most abundantly produced biological volatile organic compound on Earth. ISME J. 12, 931–941 (2018).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sharkey, T. D., Wiberley, A. E. & Donohue, A. R. Isoprene emission from plants: Why and how. Ann. Bot. 101, 5–18 (2008).Article 
    CAS 
    PubMed 

    Google Scholar 
    Zuo, Z. et al. Isoprene acts as a signaling molecule in gene networks important for stress responses and plant growth. Plant Physiol. 180, 124–152 (2019).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sharkey, T. D. & Yeh, S. Isoprene emission from plants. Plant Mol. Biol. 52, 407–436 (2001).CAS 

    Google Scholar 
    Sharkey, T. D., Loreto, F. & Delwiche, C. High carbon dioxide and sun/shade effects on isoprene emission from oak and aspen tree leaves. Plant, Cell Environ. 14, 333–338 (1991).Article 
    CAS 

    Google Scholar 
    Eller, A. S. D. et al. Volatile organic compound emissions from switchgrass cultivars used as biofuel crops. Atmos. Environ. 45, 3333–3337 (2011).Article 
    ADS 
    CAS 

    Google Scholar 
    Morrison, E. C., Drewer, J. & Heal, M. R. A comparison of isoprene and monoterpene emission rates from the perennial bioenergy crops short-rotation coppice willow and Miscanthus and the annual arable crops wheat and oilseed rape. GCB Bioenergy 8, 211–225 (2016).Article 
    CAS 

    Google Scholar 
    Sivy, T. L., Shirk, M. C. & Fall, R. Isoprene synthase activity parallels fluctuations of isoprene release during growth of Bacillus subtilis. Biochem. Biophys. Res. Commun. 294, 71–75 (2002).Article 
    CAS 
    PubMed 

    Google Scholar 
    Crombie, A. T. et al. Poplar phyllosphere harbors disparate isoprene-degrading bacteria. Proc. Natl Acad. Sci. USA. 115, 13081–13086 (2018).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    El Khawand, M. et al. Isolation of isoprene degrading bacteria from soils, development of isoA gene probes and identification of the active isoprene-degrading soil community using DNA-stable isotope probing. Environ. Microbiol. 18, 2743–2753 (2016).Article 
    CAS 
    PubMed 

    Google Scholar 
    Nowicka, B. & Kruk, J. Occurrence, biosynthesis and function of isoprenoid quinones. Biochim. Biophys. Acta – Bioenerg. 1797, 1587–1605 (2010).Article 
    CAS 

    Google Scholar 
    Kałużna, M. et al. Pseudomonas cerasi sp. nov. (non Griffin, 1911) isolated from diseased tissue of cherry. Syst. Appl. Microbiol. 39, 370–377 (2016).Article 
    PubMed 

    Google Scholar 
    El-Tarabily, K. A., Nassar, A. H., Hardy, G. E. S. J. & Sivasithamparam, K. Plant growth promotion and biological control of Pythium aphanidermatum, a pathogen of cucumber, by endophytic actinomycetes. J. Appl. Microbiol 106, 13–26 (2009).Article 
    CAS 
    PubMed 

    Google Scholar 
    Javed, Z., Tripathi, G. D., Mishra, M. & Dashora, K. Actinomycetes – the microbial machinery for the organic-cycling, plant growth, and sustainable soil health. Biocatal. Agric. Biotechnol. 31, 101893 (2021).Article 
    CAS 

    Google Scholar 
    Anwar, S., Ali, B. & Sajid, I. Screening of rhizospheric actinomycetes for various in-vitro and in-vivo plant growth promoting (PGP) traits and for agroactive compounds. Front. Microbiol. 7, 1–11 (2016).Article 

    Google Scholar 
    Bao, L. et al. Microbial community overlap between the phyllosphere and rhizosphere of three plants from Yongxing Island, South China Sea. Microbiologyopen 9, 1–18 (2020).Article 

    Google Scholar 
    Remus-Emsermann, M. N. P. & Schlechter, R. O. Phyllosphere microbiology: at the interface between microbial individuals and the plant host. N. Phytol. 218, 1327–1333 (2018).Article 

    Google Scholar 
    Beilsmith, K. et al. Genome-wide association studies on the phyllosphere microbiome: embracing complexity in host–microbe interactions. Plant J. 97, 164–181 (2019).Article 
    CAS 
    PubMed 

    Google Scholar 
    Levy, A., Conway, J. M., Dangl, J. L. & Woyke, T. Elucidating bacterial gene functions in the plant microbiome. Cell Host Microbe 24, 475–485 (2018).Article 
    CAS 
    PubMed 

    Google Scholar 
    Trivedi, P., Leach, J. E., Tringe, S. G., Sa, T. & Singh, B. K. Plant–microbiome interactions: from community assembly to plant health. Nat. Rev. Microbiol. 18, 607–621 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Choi, H. et al. Identification of viruses and viroids infecting tomato and pepper plants in vietnam by metatranscriptomics. Int. J. Mol. Sci. 21, 1–16 (2020).Article 
    ADS 

    Google Scholar 
    Marzano, S. Y. L. & Domier, L. L. Novel mycoviruses discovered from metatranscriptomics survey of soybean phyllosphere phytobiomes. Virus Res 213, 332–342 (2016).Article 
    CAS 
    PubMed 

    Google Scholar 
    Chao S, et al. Metatranscriptomic sequencing suggests the presence of novel RNA viruses in rice rransmitted by brown planthopper. Viruses. 13, 2464 (2021).Delmotte, N. et al. Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc. Natl Acad. Sci. 106, 16428–16433 (2009).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Suzuki, Y., Makino, A. & Mae, T. An efficient method for extraction of RNA from rice leaves at different ages using benzyl chloride. J. Exp. Bot. 52, 1575–1579 (2001).Article 
    CAS 
    PubMed 

    Google Scholar 
    Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl Acad. Sci. 108, 4516–4522 (2011).Article 
    ADS 
    CAS 
    PubMed 

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

    Google Scholar 
    Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Druzhinina, I. S. et al. Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts. PLoS Genet. 14, e1007322 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Haridas, S. et al. 101 Dothideomycetes genomes: A test case for predicting lifestyles and emergence of pathogens. Stud. Mycol. 96, 141–153 (2020).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gostinčar, C. et al. Genome sequencing of four Aureobasidium pullulans varieties: Biotechnological potential, stress tolerance, and description of new species. BMC Genomics 15, 549 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gill, U. S. et al. Draft genome sequence resource of switchgrass rust pathogen, puccinia novopanici isolate ard-01. Phytopathology 109, 1513–1515 (2019).Article 
    CAS 
    PubMed 

    Google Scholar 
    Bowsher, A. W., Benucci, G. M. N., Bonito, G. & Shade, A. Seasonal dynamics of core fungi in the switchgrass phyllosphere, and co-occurrence with leaf bacteria. Phytobiomes J. 5, 60–68 (2021).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 
    PubMed 

    Google Scholar 
    Kang, D. D. et al. MetaBAT 2: An adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ 2019, 1–13 (2019).
    Google Scholar 
    Nayfach, S., Shi, Z. J., Seshadri, R., Pollard, K. S. & Kyrpides, N. C. New insights from uncultivated genomes of the global human gut microbiome. Nature 568, 505–510 (2019).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Swan, B. K. et al. Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean. Proc. Natl Acad. Sci. USA. 110, 11463–11468 (2013).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Eren, A. M. et al. Anvi’o: an advanced analysis and visualization platform for’omics data. PeerJ. 2015, 1–29 (2015).
    Google Scholar 
    Lee, M. D. GToTree: a user-friendly workflow for phylogenomics. Bioinformatics 35, 4162–4164 (2019).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Shaffer, M. et al. DRAM for distilling microbial metabolism to automate the curation of microbiome function. Nucleic Acids Res. 48, 8883–8900 (2020).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Parks, D. H. et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat. Biotechnol. 36, 996 (2018).Article 
    CAS 
    PubMed 

    Google Scholar 
    Suzuki, R. & Shimodaira, H. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22, 1540–1542 (2006).Article 
    CAS 
    PubMed 

    Google Scholar 
    Blin, K. et al. AntiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res. 49, W29–W35 (2021).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Navarro-Muñoz, J. C. et al. A computational framework to explore large-scale biosynthetic diversity. Nat. Chem. Biol. 16, 60–68 (2020).Article 
    PubMed 

    Google Scholar 
    Zimmermann, J., Kaleta, C. & Waschina, S. Gapseq: informed prediction of bacterial metabolic pathways and reconstruction of accurate metabolic models. Genome Biol. 22, 1–35 (2021).Article 

    Google Scholar 
    Tseng, T. T., Tyler, B. M. & Setubal, J. C. Protein secretion systems in bacterial-host associations, and their description in the Gene Ontology. BMC Microbiol 9, 1–9 (2009).Article 

    Google Scholar 
    Lucke, M., Correa, M. G. & Levy, A. The role of secretion systems, effectors, and secondary metabolites of beneficial rhizobia in interactions with plants and microbes. Front. Plant Sci. 11, 589416 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Palmer, J. L., Hilton, S., Picot, E., Bending, G. D. & Schäfer, H. Tree phyllospheres are a habitat for diverse populations of CO-oxidizing bacteria. Environ. Microbiol. 23, 6309–6327 (2021).Article 
    CAS 
    PubMed 

    Google Scholar 
    Bay, S. K. et al. Trace gas oxidizers are widespread and active members of soil microbial communities. Nat. Microbiol. 6, 246–256 (2021).Article 
    CAS 
    PubMed 

    Google Scholar  More

  • in

    The spatio-temporal distribution of alkaline phosphatase activity and phoD gene abundance and diversity in sediment of Sancha Lake

    Smith, V. H. Eutrophication of freshwater and coastal marine ecosystems: A global problem. Environ. Sc. Pollut. R. Int. 10, 126–139 (2003).Article 
    CAS 

    Google Scholar 
    Jeppesen, E., Sondergaard, M. & Jensen, J. P. Lake responses to reduced nutrient loading an analysis of contemporary long term data from 35 case studies. Freshw. Biol. 50, 1747–1771 (2005).Article 
    CAS 

    Google Scholar 
    Kim, L. H., Choi, E. & Michal, K. S. Sediment characteristics, phosphorus types and phosphorus release rates between river and lake sediments. Chemosphere 50, 53–61 (2003).Article 
    ADS 
    CAS 

    Google Scholar 
    Jiang, X. J., Xiang, C. & Yao, Y. Effects of biological activity, light, temperature and oxygen on phosphorus release processes at the sediment and water interface of Taihu Lake, China. Water Res. 42, 2251–2259 (2008).Article 
    CAS 

    Google Scholar 
    Wang, S. R., Jin, X. C. & Bu, Q. Y. Effects of dissolved oxygen supply level on phosphorus release from lake sediments. Colloids Surf. A 316, 245–252 (2008).Article 
    CAS 

    Google Scholar 
    Miao, S. Y., De-Laune, R. D. & Jug-Sujinda, A. Influence of sediment redox conditions on release/solubility of metals and nutrients in a Louisiana Mississippi River deltaic plain freshwater lake. Sci. Total Environ. 371, 334–343 (2006).Article 
    ADS 
    CAS 

    Google Scholar 
    Smits, J. G. C. & Van Beek, J. K. L. ECO: A generic eutrophication model including comprehensive sediment-water interaction. PLoS ONE 8, e68104 (2013).Article 
    ADS 
    CAS 

    Google Scholar 
    Topcu, A. & Pulatsu, S. Phosphorus fractions and cycling in the sediment of a shallow eutrophic pond. Tarim Bilim. Derg. 20, 63–70 (2014).Article 

    Google Scholar 
    Jeppesen, E., Sondergaard, M. & Jensen, J. P. Lake responses to reduced nutrient loading-an analysis of contemporary long-term data from 35 case studies. Freshw. Biol. 50, 1747–1771 (2005).Article 
    CAS 

    Google Scholar 
    Song, C. L., Cao, X. Y. & Liu, Y. B. Seasonal variations in chlorophyll a concentrations in relation to potentials of sediment phosphate release by different mechanisms in a large chinese shallow eutrophic lake (Lake Taihu). Geomicrobiol. J. 26, 508–515 (2009).Article 
    CAS 

    Google Scholar 
    Pop, O., Martin, U., Abel, C. & Müller, J. P. The twin-arginine signal peptide of PhoD and the TatAd/Cd proteins of Bacillus subtilis form an autonomous tat translocation system. J. Biol. Chem. 277, 3268–3273 (2002).Article 
    CAS 

    Google Scholar 
    Luo, H. W., Zhang, H. M. & Long, R. A. Depth distributions of alkaline phosphatase and phosphonate utilization genes in the North Pacific Subtropical Gyre. Aquat. Microb. Ecol. 62, 61–69 (2011).Article 

    Google Scholar 
    Tan, H. et al. Long-term phosphorus fertilisation increased the diversity of the total bacterial community and the phoD phosphorus mineraliser group in pasture soils. Biol. Fertil. Soils 49, 661–672 (2012).Article 

    Google Scholar 
    Wan, W. J. et al. Spatial differences in soil microbial diversity caused by pH-driven organic phosphorus mineralization. Land Degrad. Dev. 32, 766–776 (2021).Article 

    Google Scholar 
    Chen, X. et al. Response of soil phoD phosphatase gene to long-term combined applications of chemical fertilizers and organic materials. Appl. Soil Ecol. 119, 197–204 (2017).Article 
    ADS 

    Google Scholar 
    Sagnon, A. et al. Amendment with Burkina Faso phosphate rock-enriched composts alters soil chemical properties and microbial structure, and enhances sorghum agronomic performance. Sci. Rep. 12, 13945 (2022).Article 
    ADS 
    CAS 

    Google Scholar 
    Chhabra, S. et al. Fertilization management affects the alkaline phosphatase bacterial community in barley rhizosphere soil. Biol. Fertil. Soils 49, 31–39 (2012).Article 

    Google Scholar 
    Luo, H. W., Benner, R., Long, R. A. & Hu, J. J. Subcellular localization of marine bacterial alkaline phosphatases. Proc. Natl. Acad. Sci. 106, 212–219 (2009).Article 

    Google Scholar 
    Zhang, T. X. et al. Suspended particles phoD alkaline phosphatase gene diversity in large shallow eutrophic Lake Taihu. Sci. Total Environ. 728, 138615 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    Li, H. et al. Nutrients regeneration pathway, release potential, transformation pattern and algal utilization strategies jointly drove cyanobacterial growth and their succession. J. Environ. Sci. 103, 255–267 (2021).Article 
    CAS 

    Google Scholar 
    Sun, T. T., Huang, T. & Liu, Y. X. Effects of cyanobacterial growth and decline on the phoD-harboring bacterial community structure in sediments of Lake Chaohu. J. Lake Sci. 34, 32 (2022).ADS 

    Google Scholar 
    Li, Y., Ai, M. J., Sun, Y., Zhang, Y. Q. & Zhang, J. Q. Spirosoma lacussanchae sp. nov., a phosphate-solubilizing bacterium isolated from a freshwater reservoir. Int. J. Syst. Evol. Microbiol. 67, 3144–3149 (2017).Article 
    CAS 

    Google Scholar 
    Li, Y., Zhang, J. J., Xu, W. L. & Mou, Z. S. Microbial community structure in the sediments and its relation to environmental factors in eutrophicated Sancha Lake. Int. J. Environ. Res. Public Health 16, 1931–1946 (2019).Article 
    CAS 

    Google Scholar 
    Jia, B. Y., Tang, Y. & Fu, W. L. Relationship among sediment characteristics, eutrophication process and human activities in the Sancha Lake. China Environ. Sci. 33, 1638–1644 (2013).CAS 

    Google Scholar 
    Li, Y., Zhang, J. J., Zhang, J. Q., Xu, W. L. & Mou, Z. S. Characteristics of inorganic phosphate-solubilizing bacteria from the sediments of a Eutrophic Lake. Int. J. Environ. Res. Public Health 16, 2141 (2019).Article 
    CAS 

    Google Scholar 
    Ruban, V., Brigault, S., Demare, D. & Philippe, A. M. An investigation of the origin and mobility of phosphorus in freshwater sediments from Bort-Les-Orgues reservoir, France. J. Environ. Monit. 1, 403–407 (1999).Article 
    CAS 

    Google Scholar 
    Ruban, V., López-Sánchez, J. F. & Pardo, P. Harmonized protocol and certified reference material for the determination of extractable contents of phosphorus in freshwater sediments: A synthesis of recent works. Fresenius J. Anal. Chem. 370, 224–228 (2001).Article 
    CAS 

    Google Scholar 
    Li, Y., Zhang, J. Q., Gong, Z. L., Fu, W. L. & Wu, D. M. Fractions and temporal and spatial distribution of phosphorus in the sediments of Sancha lake. Appl. Ecol. Environ. Res. 17, 11731–11743 (2019).Article 

    Google Scholar 
    Li, Y., Zhang, J. Q., Gong, Z. L., Xu, W. L. & Mou, Z. S. Gcd gene diversity of quinoprotein glucose dehydrogenase in the sediment of Sancha lake and its response to the environment. Int. J. Environ. Res. Public Health 16, 1–10 (2019).Article 

    Google Scholar 
    Luo, G. W. et al. Long-term fertilisation regimes affect the composition of the alkaline phosphomonoesterase encoding microbial community of a vertisol and its derivative soil fractions. Biol. Fertil. Soils 53, 375–388 (2017).Article 
    CAS 

    Google Scholar 
    Lagos, L. et al. Effect of phosphorus addition on total and alkaline phosphomonoesterase-harboring bacterial populations in ryegrass rhizosphere microsites. Biol. Fertil. Soils 52, 1007–1019 (2016).Article 
    CAS 

    Google Scholar 
    Acuña, J. et al. Bacterial alkaline phosphomono-esterase in the rhizospheres of plants grown in chilean extreme environments. Biol. Fertil. Soils 52, 763–773 (2016).Article 

    Google Scholar 
    Nicholas, A. B. et al. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Methods. 10, 57–59 (2013).Article 

    Google Scholar 
    Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree: Computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26, 1641–1650 (2009).Article 
    CAS 

    Google Scholar 
    Fan, X. F. & Xing, P. The vertical distribution of sediment archaeal community in the (black bloom) disturbing Zhushan Bay of Lake Taihu. Archaea 2016, 201–208 (2016).Article 

    Google Scholar 
    White, J. R., Nagarajan, N. & Pop, M. O. Statistical methods for detecting differentially abundant features in clinical metagenomic samples (differential abundance in clinical metagenomics). PLoS Comput. Biol. 5, 1–11 (2009).Article 

    Google Scholar 
    Hu, H., Chen, X. J., Hou, F. J., Wu, Y. P. & Cheng, Y. X. Bacterial and fungal community structures in loess plateau grasslands with different grazing intensities. Front. Microbiol. 8, 606 (2017).Article 

    Google Scholar 
    Dai, J. Y. et al. Bacterial alkaline phosphatases and affiliated encoding genes in natural waters: A review. J. Lake Sci. 28, 1153–1166 (2016).Article 

    Google Scholar 
    Chróst, R. J. & Overbeck, J. Kinetics of alkaline phosphatase activity and phosphorus availability for phytoplankton and bacterio-plankton in lake plusee (North German Eutrophic Lake). Microb. Ecol. 13, 229–248 (1987).Article 

    Google Scholar 
    Margalef, O. et al. Global patterns of phosphatase activity in natural soils. Sci. Rep. 7, 1337 (2017).Article 
    ADS 
    CAS 

    Google Scholar 
    Zhao, D. D., Luo, J. F., Huang, X. Y. & Lin, W. T. Diversity of bacterial APase phoD gene in the Pearl River water. Acta Sci. Circum. 35, 722–728 (2015).CAS 

    Google Scholar 
    Valdespino-Castillo, P. M. et al. Alkaline phosphatases in microbialites and bacterioplankton from Alchichica soda lake, Mexico. FEMS Microbiol. Ecol. 90, 504–519 (2014).CAS 

    Google Scholar 
    Ni, Z. K., Li, Y. & Wang, S. R. Cognizing and characterizing the organic phosphorus in lake sediments: Advances and challenges. Water Res. 220, 118663 (2022).Article 
    CAS 

    Google Scholar 
    Han, S. S. & Wen, T. M. Phosphorus release and affecting factors in the sediments of eutrophic water. J. Ecol. 23, 98–101 (2004).
    Google Scholar 
    Wang, F. F., Qu, J. H. & Hu, Y. S. Spatio-temporal characteristics and correlation of phosphate, pH and alkaline phosphatase on water-sediment interface of Lake Taihu. Ecol. Environ. Sci. 21, 907–912 (2012).
    Google Scholar 
    Lu, Y. M. et al. Bioavailability of organic phosphorus in Lake Chaohu sediments. J. Environ. Eng. Technol. 10, 197–204 (2020).
    Google Scholar 
    LeBrun, E. S., King, R. S., Back, J. A. & Kang, S. Microbial community structure and function decoupling across a phosphorus gradient in streams. Microb. Ecol. 75, 64–73 (2018).Article 
    CAS 

    Google Scholar 
    Zhang, J. et al. Connecting sources, fractions and algal availability of sediment phosphorus in shallow lakes: An approach to the criteria for sediment phosphorus concentrations. J. Environ. Sci. 25, 798–810 (2023).Article 

    Google Scholar 
    Hu, Y. J. et al. Effects of long-term fertilization on phoD-harboring bacterial community in Karst soils. Sci. Total Environ. 628–629, 53–63 (2018).Article 
    ADS 

    Google Scholar  More

  • in

    Public interest in individual study animals can bolster wildlife conservation

    Benson, E. S. Sci. Context 29, 107–128 (2016).Article 
    PubMed 

    Google Scholar 
    Buckmaster, C. A. Lab Anim. 44, 237 (2015).Article 

    Google Scholar 
    Kelly, M. J. et al. J. Zool. 244, 473–488 (1998).Article 

    Google Scholar 
    Spagnuolo, O. S. B., Lemerle, M. A., Holekamp, K. E. & Wiesel, I. Mamm. Biol. https://doi.org/10.1007/s42991-022-00309-4 (2022).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    California Department of Fish and Wildlife. Mountain lion P-22 compassionately euthanized following complete health evaluation results. wildlife.ca.gov, https://wildlife.ca.gov/News/mountain-lion-p-22-compassionately-euthanized-following-complete-health-evaluation-results (17 December 2022).Road Ecology Center, UC Davis. California roadkill observation system, https://www.wildlifecrossing.net/california/ (accessed 19 December 2022).Wong-Parodi, G. & Feygina, I. Environ. Commun. 15, 571–593 (2021).Article 

    Google Scholar 
    Carmi, N., Arnon, S. & Orion, N. J. Environ. Educ. 46, 183–201 (2015).Article 

    Google Scholar 
    Manfredo, M. J., Urquiza-Haas, E. G., Don Carlos, A. W., Bruskotter, J. T. & Dietsch, A. M. Biol. Conserv. 241, 108297 (2020).Article 

    Google Scholar 
    Schueler, D. S. & Newberry, M. G. III Appl. Environ. Educ. Commun. 19, 259–273 (2020).Article 

    Google Scholar 
    Jennings, L. Public gets to name Dallas Zoo’s baby giraffe. Dallas Zoo https://zoohoo.dallaszoo.com/2014/11/05/public-gets-to-name-dallas-zoos-baby-giraffe/ (5 November 2014).Verma, A., van der Wal, R. & Fischer, A. Ambio 44(Suppl 4), 648–660 (2015).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Macdonald, D. W., Jacobsen, K. S., Burnham, D., Johnson, P. J. & Loveridge, A. J. Animals 6, 26 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Jones, M. D., Shanahan, E. A. & McBeth, M. K. The Science of Stories: Applications of the Narrative Policy Framework in Public Policy Analysis (Palgrave MacMillan, 2014). More

  • in

    Diagnosing destabilization risk in global land carbon sinks

    Fernández-Martínez, M. et al. Global trends in carbon sinks and their relationships with CO2 and temperature. Nat. Clim. Change 9, 73–79 (2019).Article 
    ADS 

    Google Scholar 
    Scheffer, M. et al. Early-warning signals for critical transitions. Nature 461, 53–59 (2009).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Dakos, V. et al. Slowing down as an early warning signal for abrupt climate change. Proc. Natl Acad. Sci. USA 105, 14308–14312 (2008).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gasser, T. et al. Path-dependent reductions in CO2 emission budgets caused by permafrost carbon release. Nat. Geosci. 11, 830–835 (2018).Article 
    ADS 
    CAS 

    Google Scholar 
    Zhu, Z. et al. Greening of the Earth and its drivers. Nat. Clim. Change 6, 791–795 (2016).Article 
    ADS 
    CAS 

    Google Scholar 
    Bastos, A. et al. Contrasting effects of CO2 fertilization, land-use change and warming on seasonal amplitude of Northern Hemisphere CO2 exchange. Atmos. Chem. Phys. 19, 12361–12375 (2019).Article 
    ADS 
    CAS 

    Google Scholar 
    Pugh, T. A. M. et al. Role of forest regrowth in global carbon sink dynamics. Proc. Natl Acad. Sci. USA 116, 4382–4387 (2019).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wang, S. et al. Recent global decline of CO2 fertilization effects on vegetation photosynthesis. Science 370, 1295–1300 (2020).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Peñuelas, J. et al. Assessment of the impacts of climate change on Mediterranean terrestrial ecosystems based on data from field experiments and long-term monitored field gradients in Catalonia. Environ. Exp. Bot. 152, 49–59 (2018).Article 

    Google Scholar 
    Terrer, C. et al. Nitrogen and phosphorus constrain the CO2 fertilization of global plant biomass. Nat. Clim. Change 9, 684–689 (2019).Article 
    ADS 
    CAS 

    Google Scholar 
    Gatti, L. V. et al. Amazonia as a carbon source linked to deforestation and climate change. Nature 595, 388–393 (2021).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Carpenter, S. R. & Brock, W. A. Rising variance: a leading indicator of ecological transition. Ecol. Lett. 9, 311–318 (2006).Article 
    CAS 
    PubMed 

    Google Scholar 
    Dakos, V., Nes, E. H. & Scheffer, M. Flickering as an early warning signal. Theor. Ecol. 6, 309–317 (2013).Article 

    Google Scholar 
    Sillmann, J., Daloz, A. S., Schaller, N. & Schwingshackl, C. in Climate Change 3rd edn (ed. Letcher, T. M.) 359–372 (Elsevier, 2021).Reichstein, M. et al. Climate extremes and the carbon cycle. Nature 500, 287–295 (2013).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Wang, X. et al. A two-fold increase of carbon cycle sensitivity to tropical temperature variations. Nature 506, 212–215 (2014).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Barnosky, A. D. et al. Approaching a state shift in Earth’s biosphere. Nature 486, 52–58 (2012).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Buermann, W. et al. Climate-driven shifts in continental net primary production implicated as a driver of a recent abrupt increase in the land carbon sink. Biogeosciences 13, 1597–1607 (2016).Article 
    ADS 
    CAS 

    Google Scholar 
    Luyssaert, S. et al. CO2 balance of boreal, temperate, and tropical forests derived from a global database. Glob. Change Biol. 13, 2509–2537 (2007).Article 
    ADS 

    Google Scholar 
    Peñuelas, J. et al. Shifting from a fertilization-dominated to a warming-dominated period. Nat. Ecol. Evol. 1, 1438–1445 (2017).Article 
    PubMed 

    Google Scholar 
    Fernández-Martínez, M. et al. Nutrient availability as the key regulator of global forest carbon balance. Nat. Clim. Change 4, 471–476 (2014).Article 
    ADS 

    Google Scholar 
    Fernández-Martínez, M. et al. Spatial variability and controls over biomass stocks, carbon fluxes and resource-use efficiencies in forest ecosystems. Trees Struct. Funct. 28, 597–611 (2014).Article 

    Google Scholar 
    Ciais, P. et al. Five decades of northern land carbon uptake revealed by the interhemispheric CO2 gradient. Nature 568, 221–225 (2019).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Tilman, D., Lehman, C. L. & Thomson, K. T. Plant diversity and ecosystem productivity: theoretical considerations. Proc. Natl Acad. Sci. USA 94, 1857–1861 (1997).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    de Mazancourt, C. et al. Predicting ecosystem stability from community composition and biodiversity. Ecol. Lett. 16, 617–625 (2013).Article 
    PubMed 

    Google Scholar 
    Sakschewski, B. et al. Resilience of Amazon forests emerges from plant trait diversity. Nat. Clim. Change 6, 1032–1036 (2016).Article 
    ADS 

    Google Scholar 
    Fernández‐Martínez, M. et al. The role of climate, foliar stoichiometry and plant diversity on ecosystem carbon balance. Glob. Change Biol. 26, 7067–7078 (2020).Article 
    ADS 

    Google Scholar 
    Musavi, T. et al. Stand age and species richness dampen interannual variation of ecosystem-level photosynthetic capacity. Nat. Ecol. Evol. 1, 0048 (2017).Article 

    Google Scholar 
    Anderegg, W. R. L. et al. Hydraulic diversity of forests regulates ecosystem resilience during drought. Nature 561, 538–541 (2018).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    IPBES: Summary for Policymakers. In The Global Assessment Report on Biodiversity and Ecosystem Services (eds Díaz, S. et al.) 1–56 (IPBES, 2019).Heath, J. P. Quantifying temporal variability in population abundances. Oikos 115, 573–581 (2006).Article 

    Google Scholar 
    Fernández-Martínez, M., Vicca, S., Janssens, I. A., Martín-Vide, J. & Peñuelas, J. The consecutive disparity index, D, as measure of temporal variability in ecological studies. Ecosphere 9, e02527 (2018).Article 

    Google Scholar 
    Kreft, H. & Jetz, W. Global patterns and determinants of vascular plant diversity. Proc Natl Acad Sci USA 104, 5925–5930 (2007).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ackerman, D. E., Chen, X. & Millet, D. B. Global nitrogen deposition (2° × 2.5° grid resolution) simulated with GEOS-Chem for 1984–1986, 1994–1996, 2004–2006, and 2014–2016 (University of Minnesota, 2018); https://conservancy.umn.edu/handle/11299/197613.Harris, I., Jones, P. D. D., Osborn, T. J. J. & Lister, D. H. H. Updated high-resolution grids of monthly climatic observations—the CRU TS3.10 Dataset. Int. J. Climatol. 34, 623–642 (2013).Article 

    Google Scholar 
    Graven, H. D. et al. Enhanced seasonal exchange of CO2 by northern ecosystems since 1960. Science 341, 1085–1089 (2013).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Wang, K. et al. Causes of slowing-down seasonal CO2 amplitude at Mauna Loa. Glob. Change Biol. 26, 4462–4477 (2020).Article 
    ADS 

    Google Scholar 
    Tilman, D., Reich, P. B. & Knops, J. M. H. Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441, 629–632 (2006).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Liang, J. et al. Positive biodiversity–productivity relationship predominant in global forests. Science 354, aaf8957–aaf8957 (2016).Article 
    PubMed 

    Google Scholar 
    Gessner, M. O. et al. Diversity meets decomposition. Trends Ecol. Evol. 25, 372–380 (2010).Article 
    PubMed 

    Google Scholar 
    Peguero, G. et al. Fast attrition of springtail communities by experimental drought and richness–decomposition relationships across Europe. Glob. Change Biol. 25, 2727–2738 (2019).Article 
    ADS 

    Google Scholar 
    Díaz, S. & Cabido, M. Vive la différence: plant functional diversity matters to ecosystem processes. Trends Ecol. Evol. 16, 646–655 (2001).Article 

    Google Scholar 
    Cardinale, B. J. Biodiversity improves water quality through niche partitioning. Nature 472, 86–91 (2011).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Ciais, P. et al. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437, 529–533 (2005).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Scheffer, M. Critical Transitions in Nature and Society (Princeton University Press, 2009).Ostfeld, R. & Keesing, F. Pulsed resources and community dynamics of consumers in terrestrial ecosystems. Trends Ecol. Evol. 15, 232–237 (2000).Article 
    CAS 
    PubMed 

    Google Scholar 
    Chevallier, F. et al. CO2 surface fluxes at grid point scale estimated from a global 21 year reanalysis of atmospheric measurements. J. Geophys. Res. 115, D21307 (2010).Article 
    ADS 

    Google Scholar 
    Chevallier, F. et al. Toward robust and consistent regional CO2 flux estimates from in situ and spaceborne measurements of atmospheric CO2. Geophys. Res. Lett. 41, 1065–1070 (2014).Article 
    ADS 
    CAS 

    Google Scholar 
    Rödenbeck, C., Houweling, S., Gloor, M. & Heimann, M. CO2 flux history 1982–2001 inferred from atmospheric data using a global inversion of atmospheric transport. Atmos. Chem. Phys. 3, 1919–1964 (2003).Article 
    ADS 

    Google Scholar 
    Rödenbeck, C., Zaehle, S., Keeling, R. & Heimann, M. How does the terrestrial carbon exchange respond to interannual climatic variations? A quantification based on atmospheric CO2 data. Biogeosciences 15, 2481–2498 (2018).Sitch, S. et al. Recent trends and drivers of regional sources and sinks of carbon dioxide. Biogeosciences 12, 653–679 (2015).Article 
    ADS 

    Google Scholar 
    Fernández‐Martínez, M. & Peñuelas, J. Measuring temporal patterns in ecology: the case of mast seeding. Ecol. Evol. 11, 2990–2996 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wood, S. N. Generalized Additive Models: An introduction with R 2nd edn (Chapman and Hall/CRC, 2017).Ohlson, J. A. & Kim, S. Linear Valuation Without OLS: The Theil–Sen Estimation Approach (SSRN, 2015); https://ssrn.com/abstract=2276927.Komsta, L. Package mblm, 0.12.1: Median-based linear models (2013).Keeling, C. D. et al. in A History of Atmospheric CO2 and its effects on Plants, Animals, and Ecosystems (eds Ehleringer, J. R. et al.) 83–113 (Springer Verlag, 2005).Leroux, B. G., Lei, X. & Breslow, N. in Statistical Models in Epidemiology, the Environment and Clinical Trials (eds Halloran, M. & Berry, D.) 179–191 (Springer-Verlag, 2000).Lee, D. CARBayes: an R package for Bayesian spatial modeling with conditional autoregressive priors. J. Stat. Softw. 55, 1–24 (2013).Article 

    Google Scholar 
    Gonzalez, A. et al. Scaling‐up biodiversity–ecosystem functioning research. Ecol. Lett. 15, ele.13456 (2020).
    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020). More

  • in

    Rethinking river water temperature in a changing, human-dominated world

    Ouellet, V. et al. Sci. Total Environ. 736, 139679 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Sutadian, A. D., Muttil, N., Yilmaz, A. G. & Perera, B. J. C. Environ. Monit. Assess. 188, 58 (2016).Article 
    PubMed 

    Google Scholar 
    Murdoch, P. S., Baron, J. S. & Miller, T. L. J. Am. Water Resour. Assoc. 36, 347–366 (2000).Article 
    CAS 

    Google Scholar 
    Hannah, D. M. & Garner, G. Prog Phys Geogr. 39, 68–92 (2015).Article 

    Google Scholar 
    Abbott, B. W. et al. Nat. Geosci. 12, 533–540 (2019).Article 
    CAS 

    Google Scholar 
    Grill, G. et al. Nature 569, 215–221 (2019).Article 
    CAS 
    PubMed 

    Google Scholar 
    Hermanson, L. et al. Bull. Am. Meteorol. Soc. 103, E1117–E1129 (2022).Article 

    Google Scholar 
    Webb, B. W., Hannah, D. M., Moore, R. D., Brown, L. E. & Nobilis, F. Hydrol. Process. 22, 902–918 (2008).Article 

    Google Scholar 
    Hester, E. T. & Doyle, M. W. J. Am. Water Resour. Assoc. 47, 571–587 (2011).Article 

    Google Scholar 
    Schliemann, S. A., Grevstad, N. & Brazeau, R. H. Hydrol. Process 35, e14001 (2021).Article 

    Google Scholar 
    Jackson, F. L., Fryer, R. J., Hannah, D. M., Millar, C. P. & Malcolm, I. A. Sci. Total Environ. 612, 1543–1558 (2018).Article 
    CAS 
    PubMed 

    Google Scholar 
    O’Sullivan, A. M., Devito, K. J. & Curry, R. A. Catena 177, 70–83 (2019).Article 

    Google Scholar 
    Chang, H. & Psaris, M. Sci. Total Environ. 461, 587–600 (2013).Article 
    PubMed 

    Google Scholar 
    Hester, E. T. & Bauman, K. S. J. Am. Water Resour. Assoc. 49, 328–342 (2013).Article 

    Google Scholar 
    Croghan, D., Van Loon, A. F., Sadler, J. P., Bradley, C. & Hannah, D. M. Hydrol. Process. 33, 144–159 (2018).Article 

    Google Scholar 
    Levia, D. F. et al. Nat. Geosci. 13, 656–658 (2020).Article 
    CAS 

    Google Scholar 
    Nelson, K. C. & Palmer, M. A. J. Am. Water Resour. Assoc 43, 440–452 (2007).Article 

    Google Scholar 
    Heggenes, J. et al. River Res. Appl. 37, 743–765 (2021).Article 

    Google Scholar 
    Menberg, K., Blum, P., Kurylyk, B. L. & Bayer, P. Hydrol. Earth Syst. Sci. 18, 4453–4466 (2014).Article 

    Google Scholar 
    Tissen, C., Benz, S. A., Menberg, K., Bayer, P. & Blum, P. Environ. Res. Lett. 14, 104012 (2019).Article 
    CAS 

    Google Scholar 
    Hannah, D. M. et al. Hydrol. Process. 36, e14525 (2022).Article 

    Google Scholar 
    Carothers, C. et al. Ecol. Soc. https://doi.org/10.5751/ES-11972-260116 (2021).Dugdale, S. J., Hannah, D. M. & Malcolm, I. A. Earth Sci. Rev. 175, 97–113 (2017).Article 

    Google Scholar 
    Wanders, N., van Vliet, M. T. H., Wada, Y., Bierkens, M. F. P. & van Beek, L. P. H. Water Resour. Res. 55, 2760–2778 (2019).Article 

    Google Scholar 
    Tavares, M. H. et al. Remote Sens. Environ. 241, 11172 (2020).Article 

    Google Scholar 
    Dugdale, S. J., Klaus, J. & Hannah, D. M. Water Resour. Res. 58, e2021WR031168 (2022).Article 

    Google Scholar 
    Mao, F. et al. Environ. Sci. Technol. 54, 9145–9158 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Hannah, D. M. et al. Hydrol. Process. 25, 1191–1200 (2011).Article 

    Google Scholar 
    Do, H. X., Gudmundsson, L., Leonard, M. & Westra, S. Earth Syst. Sci. Data 10, 765–785 (2018).Article 

    Google Scholar  More

  • in

    Ostreopsis Schmidt and Coolia Meunier (Dinophyceae, Gonyaulacales) from Cook Islands and Niue (South Pacific Ocean), including description of Ostreopsis tairoto sp. nov.

    Verma, A. et al. The genetic basis of toxin biosynthesis in dinofagellates. Microorganisms 7, 222 (2019).Article 
    CAS 

    Google Scholar 
    Hallegraeff, G. M. Ocean climate change, phytoplankton community responses, and harmful algal blooms: A formidable predictive challenge1. J. Phycol. 46, 220–235 (2010).Article 
    CAS 

    Google Scholar 
    Hoppenrath, M., Murray, S., Chomérat, N., Horiguchi, T. Marine Benthic Dinoflagellates – Unveiling Their Worldwide Biodiversity (Kleine Senckenberg-reihe 54). E. Schweizerbart’sche Verlagbuchhandlung (2014).Luo, Z. et al. Cryptic diversity within the harmful dinoflagellate Akashiwo sanguinea in coastal Chinese waters is related to differentiated ecological niches. Harmful Algae 66, 88–96 (2017).Article 

    Google Scholar 
    Litaker, R. W. et al. Taxonomy of Gambierdiscus including four new species, Gambierdiscus caribaeus, Gambierdiscus carolinianus, Gambierdiscus carpenteri and Gambierdiscus ruetzleri (Gonyaulacales, Dinophyceae). Phycologia 48, 344–390 (2009).Article 

    Google Scholar 
    Hoppenrath, M. et al. Taxonomy and phylogeny of the benthic Prorocentrum species (Dinophyceae)—A proposal and review. Harmful Algae 27, 1–28 (2013).Article 

    Google Scholar 
    Wells, M. L. et al. Future HAB science: Directions and challenges in a changing climate. Harmful Algae 91, 101632 (2020).Article 

    Google Scholar 
    Rhodes, L. World-wide occurrence of the toxic dinoflagellate genus Ostreopsis Schmidt. Toxicon 57, 400–407 (2011).Article 
    CAS 

    Google Scholar 
    Parsons, M. L. et al. Gambierdiscus and Ostreopsis: Reassessment of the state of knowledge of their taxonomy, geography, ecophysiology, and toxicology. Harmful Algae 14, 107–129 (2012).Article 
    CAS 

    Google Scholar 
    Schmidt, J. Preliminary report of the botanical results of the Danish expedition to Siam (1899–1900). Part IV Peridiniales. Bot. Tidsskr. 24, 212–221 (1901).
    Google Scholar 
    Accoroni, S. et al. Ostreopsis fattorussoi sp. nov. (Dinophyceae), a new benthic toxic Ostreopsis species from the eastern Mediterranean Sea. J. Phycol. 52, 1064–1084 (2016).Article 
    CAS 

    Google Scholar 
    Verma, A., Hoppenrath, M., Dorantes-Aranda, J. J., Harwood, D. T. & Murray, S. A. Molecular and phylogenetic characterization of Ostreopsis (Dinophyceae) and the description of a new species, Ostreopsis rhodesae sp. nov., from a subtropical Australian lagoon. Harmful Algae 60, 116–130 (2016).Article 
    CAS 

    Google Scholar 
    Fukuyo, Y. Taxonomical study on benthic dinoflagellates collected in coral reefs. Nippon Suisan Gakk. 47, 967–978 (1981).Article 

    Google Scholar 
    Faust, M. A. Three new Ostreopsis species (Dinophyceae): O. marinus sp. nov., O. belizeanus sp. nov., and O. caribbeanus sp. nov.. Phycologia 38, 92–99 (1999).Article 

    Google Scholar 
    Faust, M. A. & Morton, S. L. Morphology and ecology of the marine dinoflagellate Ostreopsis labens sp. nov. (Dinophyceae). J. Phycol. 31, 456–463 (1995).Article 

    Google Scholar 
    Chomérat, N., Bilien, G., Couté, A. & Quod, J.-P. Reinvestigation of Ostreopsis mascarenensis Quod (Dinophyceae, Gonyaulacales) from Reunion Island (SW Indian Ocean): Molecular phylogeny and emended description. Phycologia 59, 140–153 (2020).Article 

    Google Scholar 
    Boisnoir, A., Bilien, G., Lemée, R. & Chomérat, N. First insights on the diversity of the genus Ostreopsis (Dinophyceae, Gonyaulacales) in Guadeloupe Island, with emphasis on the phylogenetic position of O. heptagona. Eur. J. Protistol. 83, 125875 (2022).Article 

    Google Scholar 
    Chomérat, N. et al. Ostreopsis lenticularis Y. Fukuyo (Dinophyceae, Gonyaulacales) from French Polynesia (South Pacific Ocean): A revisit of its morphology, molecular phylogeny and toxicity. Harmful Algae 84, 95–111 (2019).Article 

    Google Scholar 
    Nguyen-Ngoc, L. et al. Morphological and genetic analyses of Ostreopsis (Dinophyceae, Gonyaulacales, Ostreopsidaceae) species from Vietnamese waters with a re-description of the type species, O. siamensis 1. J. Phycol. 57, 1059–1083 (2021).Article 

    Google Scholar 
    Faust, M. A. Observation of sand-dwelling toxic dinoflagellates (Dinophyceae) from widely differing sites, including two new species. J. Phycol. 31, 996–1003 (1995).Article 

    Google Scholar 
    David, H., Laza-Martínez, A., Miguel, I. & Orive, E. Broad distribution of Coolia monotis and restricted distribution of Coolia cf. canariensis (Dinophyceae) on the Atlantic coast of the Iberian Peninsula. Phycologia 53, 342–352 (2014).Article 

    Google Scholar 
    Rhodes, L. L. et al. Toxic dinoflagellates (Dinophyceae) from Rarotonga Cook Islands. Toxicon 56, 751–758 (2010).Article 
    CAS 

    Google Scholar 
    Meunier, A. Coolia monotis sp. nov. in Mémoires du Musée Royal d’Histoire Naturelle de Belgique. Microplankton Mer Flamande, Méme partie—Les Péridiniens 8, 68–69 (1919).
    Google Scholar 
    Rhodes, L. et al. Epiphytic dinoflagellates in sub-tropical New Zealand, in particular the genus Coolia Meunier. Harmful Algae 34, 36–41 (2014).Article 

    Google Scholar 
    Rhodes, L., Adamson, J., Suzuki, T., Briggs, L. & Garthwaite, I. Toxic marine epiphytic dinoflagellates, Ostreopsis siamensis and Coolia monotis (Dinophyceae), in New Zealand. N. Z. J. Mar. Freshw. Res. 34, 371–383 (2000).Article 

    Google Scholar 
    Fraga, S., Penna, A., Bianconi, I., Paz, B. & Zapata, M. Coolia canariensis sp. nov. (Dinophyceae), a new nontoxic epiuphytic benthic dinoflagellate from the Canary Islands 1. J. Phycol. 44, 1060–1070 (2008).Article 
    CAS 

    Google Scholar 
    Lindemann, E. Abteilung Peridineae (Dinoflagellate). In Die Natürlichen Pflanzenfamilien nebst ihren Gattungen und wichtigeren Arten insbesondere den Nutzpflanzen, 3–104 (1928).Biecheler, B. Recherches sur les Péridiniens. Bulletin biologique de France et de Belgique Supplement 36, 1–149 (1952).
    Google Scholar 
    Balech, E. Étude des dinoflagellés du sable de Roscoff. Revue Algologique, Nouvelle Serie 2, 29–52 (1956).

    Google Scholar 
    Mohammad-Noor, N. et al. Autecology and phylogeny of Coolia tropicalis and Coolia malayensis (Dinophyceae), with emphasis on taxonomy of C. tropicalis based on light microscopy, scanning electron microscopy and LSU r DNA 1. J. Phycol. 49, 536–545 (2013).Article 

    Google Scholar 
    Leaw, C. P., Lim, P. T., Cheng, K. W., Ng, B. K. & Usup, G. Morphology and molecular characterization of a new species of thecate benthic dinoflagellate, Coolia malayensis sp. nov. (Dinophyceae) 1. J. Phycol. 46, 162–171 (2010).Article 
    CAS 

    Google Scholar 
    Ten-Hage, L., Turquet, J., Quod, J. & Couté, A. Coolia areolata sp. nov. (Dinophyceae), a new sand-dwelling dinoflagellate from the southwestern Indian Ocean. Phycologia 39, 377–383 (2000).Article 

    Google Scholar 
    Karafas, S., York, R. & Tomas, C. Morphological and genetic analysis of the Coolia monotis species complex with the introduction of two new species, Coolia santacroce sp. nov. and Coolia palmyrensis sp. nov. (Dinophyceae). Harmful Algae 46, 18–33 (2015).Article 
    CAS 

    Google Scholar 
    David, H., Laza-Martínez, A., Rodríguez, F., Fraga, S. & Orive, E. Coolia guanchica sp. nov.(Dinophyceae) a new epibenthic dinoflagellate from the Canary Islands (NE Atlantic Ocean). Eur. J. Phycol. 55, 76–88 (2020).Article 
    CAS 

    Google Scholar 
    Sato, S. et al. Phylogeography of Ostreopsis along west Pacific coast, with special reference to a novel clade from Japan. PLoS One 6, e27983 (2011).Article 
    ADS 
    CAS 

    Google Scholar 
    Penna, A. et al. Characterization of Ostreopsis and Coolia (Dinophyceae) isolates in the western Mediterranean Sea based on morphology, toxicity and internal transcribed spacer 5.8 S rDNA sequences. J. Phycol. 41, 212–225 (2005).Article 
    CAS 

    Google Scholar 
    Tawong, W. et al. Distribution and molecular phylogeny of the dinoflagellate genus Ostreopsis in Thailand. Harmful Algae 37, 160–171 (2014).Article 

    Google Scholar 
    Faimali, M. et al. Toxic effects of harmful benthic dinoflagellate Ostreopsis ovata on invertebrate and vertebrate marine organisms. Mar. Environ. Res. 76, 97–107 (2012).Article 
    CAS 

    Google Scholar 
    Tubaro, A. et al. Case definitions for human poisonings postulated to palytoxins exposure. Toxicon 57, 478–495 (2011).Article 
    CAS 

    Google Scholar 
    Ciminiello, P. et al. Investigation of the toxin profile of Greek mussels Mytilus galloprovincialis by liquid chromatography mass spectrometry. Toxicon 47, 174–181 (2006).Article 
    CAS 

    Google Scholar 
    Giussani, V. et al. Active role of the mucilage in the toxicity mechanism of the harmful benthic dinoflagellate Ostreopsis cf. ovata. Harmful Algae 44, 46–53 (2015).Article 
    CAS 

    Google Scholar 
    Usami, M. et al. Palytoxin analogs from the dinoflagellate Ostreopsis siamensis. J. Am. Chem. Soc. 117, 5389–5390 (1995).Article 
    CAS 

    Google Scholar 
    Ukena, T. et al. Structure elucidation of ostreocin D, a palytoxin analog isolated from the dinoflagellate Ostreopsis siamensis. Biosci. Biotechnol. Biochem. 65, 2585–2588 (2001).Article 
    CAS 

    Google Scholar 
    Amzil, Z. et al. Ovatoxin-a and palytoxin accumulation in seafood in relation to Ostreopsis cf. ovata blooms on the French Mediterranean coast. Mar. Drugs 10, 477–496 (2012).Article 
    CAS 

    Google Scholar 
    Ciminiello, P. et al. Unique toxin profile of a Mediterranean Ostreopsis cf. ovata strain: HR LC-MS n characterization of ovatoxin-f, a new palytoxin congener. Chem. Res. Toxicol. 25, 1243–1252 (2012).Article 
    CAS 

    Google Scholar 
    Laza-Martinez, A., Orive, E. & Miguel, I. Morphological and genetic characterization of benthic dinoflagellates of the genera Coolia, Ostreopsis and Prorocentrum from the south-eastern Bay of Biscay. Eur. J. Phycol. 46, 45–65 (2011).Article 

    Google Scholar 
    Holmes, M. J., Lewis, R. J., Jones, A. & Hoy, A. W. W. Cooliatoxin, the first toxin from Coolia monotis (Dinophyceae). Nat. Toxins 3, 355–362 (1995).Article 
    CAS 

    Google Scholar 
    Rhodes, L. L. & Thomas, A. E. Coolia monotis (Dinophyceae): A toxic epiphytic microalgal species found in New Zealand (Note). N. Z. J. Mar. Freshw. Res. 31, 139–141 (1997).Article 
    CAS 

    Google Scholar 
    Tibiriçá, C. EJd. A. et al. Diversity and toxicity of the genus Coolia Meunier in Brazil, and detection of 44-methyl Gambierone in Coolia tropicalis. Toxins 12, 327 (2020).Article 

    Google Scholar 
    Tillmann, U., Hoppenrath, M. & Gottschling, M. Reliable determination of Prorocentrum micans Ehrenb. (Prorocentrales, Dinophyceae) based on newly collected material from the type locality. Eur. J. Phycol 54, 417–431 (2019).Article 
    CAS 

    Google Scholar 
    Chomérat, N. et al. Taxonomy and toxicity of a bloom-forming Ostreopsis species (Dinophyceae, Gonyaulacales) in Tahiti island (South Pacific Ocean): One step further towards resolving the identity of O. siamensis. Harmful Algae 98, 101888 (2020).Article 

    Google Scholar 
    Rhodes, L. L. et al. The dinoflagellate genera Gambierdiscus and Ostreopsis from subtropical Raoul Island and North Meyer Island, Kermadec Islands. N. Z. J. Mar. Freshw. Res. 51, 490–504 (2017).Article 
    CAS 

    Google Scholar 
    Penna, A. et al. A phylogeographical study of the toxic benthic dinoflagellate genus Ostreopsis Schmidt. J. Biogeogr. 37, 830–841 (2010).Article 

    Google Scholar 
    Zhang, H. et al. Morphology and molecular phylogeny of Ostreopsis cf. ovata and O. lenticularis (Dinophyceae) from Hainan Island South China Sea. Phycol. Res. 66, 3–14 (2018).Article 
    ADS 
    CAS 

    Google Scholar 
    Carnicer, O., García-Altares, M., Andree, K. B., Diogène, J. & Fernández-Tejedor, M. First evidence of Ostreopsis cf. ovata in the eastern tropical Pacific Ocean Ecuadorian coast. Bot. Mar. 59, 267–274 (2016).
    Google Scholar 
    Nascimento, S. M. et al. Ostreopsis cf. ovata (Dinophyceae) molecular phylogeny, morphology, and detection of ovatoxins in strains and field samples from Brazil. Toxins 12, 70 (2020).Article 
    CAS 

    Google Scholar 
    Caron, D. A. et al. Defining DNA-based operational taxonomic units for microbial-eukaryote ecology. Appl. Environ. Microbiol. 75, 5797–5808 (2009).Article 
    ADS 
    CAS 

    Google Scholar 
    McManus, G. B. & Katz, L. A. Molecular and morphological methods for identifying plankton: What makes a successful marriage?. J. Plankton Res. 31, 1119–1129 (2009).Article 
    CAS 

    Google Scholar 
    De Vargas, C. et al. Eukaryotic plankton diversity in the sunlit ocean. Science 348, 1261605 (2015).Article 

    Google Scholar 
    del Campo, J. et al. Ecological and evolutionary significance of novel protist lineages. Eur. J. Protistol. 55, 4–11 (2016).Article 

    Google Scholar 
    Hallegraeff, G. Harmful algal blooms: A global overview. Man. Harmful Mar. Microalgae 33, 1–22 (2003).
    Google Scholar 
    Penna, A., Casabianca, S., Guerra, A. F., Vernesi, C. & Scardi, M. Analysis of phytoplankton assemblage structure in the Mediterranean Sea based on high-throughput sequencing of partial 18S rRNA sequences. Mar. Genom. 36, 49–55 (2017).Article 

    Google Scholar 
    Zarauz, L. & Irigoien, X. Effects of Lugol’s fixation on the size structure of natural nano–microplankton samples, analyzed by means of an automatic counting method. J. Plankton Res. 30, 1297–1303 (2008).Article 

    Google Scholar 
    De Luca, D., Piredda, R., Sarno, D. & Kooistra, W. H. Resolving cryptic species complexes in marine protists: phylogenetic haplotype networks meet global DNA metabarcoding datasets. ISME J. 15, 1931–1942 (2021).Article 

    Google Scholar 
    Wang, Z. et al. Phytoplankton community and HAB species in the South China Sea detected by morphological and metabarcoding approaches. Harmful Algae 118, 102297 (2022).Article 
    CAS 

    Google Scholar 
    Le Bescot, N. et al. Global patterns of pelagic dinoflagellate diversity across protist size classes unveiled by metabarcoding. Environ. Microbiol. 18, 609–626 (2016).Article 

    Google Scholar 
    Hoppenrath, M. Dinoflagellate taxonomy—A review and proposal of a revised classification. Mar. Biodivers. 47, 381–403 (2017).Article 

    Google Scholar 
    Boenigk, J., Ereshefsky, M., Hoef-Emden, K., Mallet, J. & Bass, D. Concepts in protistology: Species definitions and boundaries. Eur. J. Protistol. 48, 96–102 (2012).Article 

    Google Scholar 
    David, H., Laza-Martínez, A., Miguel, I. & Orive, E. Ostreopsis cf. siamensis and Ostreopsis cf. ovata from the Atlantic Iberian Peninsula: Morphological and phylogenetic characterization. Harmful Algae 30, 44–55 (2013).Article 
    CAS 

    Google Scholar 
    Aligizaki, K. & Nikolaidis, G. The presence of the potentially toxic genera Ostreopsis and Coolia (Dinophyceae) in the North Aegean Sea Greece. Harmful Algae 5, 717–730 (2006).Article 

    Google Scholar 
    Selina, M. S. & Orlova, T. Y. First occurrence of the genus Ostreopsis (Dinophyceae) in the Sea of Japan. Bot. Mar. 53, 243–249 (2010).Article 

    Google Scholar 
    Kang, N. S. et al. Morphology and molecular characterization of the epiphytic benthic dinoflagellate Ostreopsis cf. ovata in the temperate waters off Jeju Island Korea. Harmful Algae 27, 98–112 (2013).Article 
    CAS 

    Google Scholar 
    Momigliano, P., Sparrow, L., Blair, D. & Heimann, K. The diversity of Coolia spp. (Dinophyceae Ostreopsidaceae) in the central Great Barrier Reef region. PloS One 8, e79278 (2013).Article 
    ADS 
    CAS 

    Google Scholar 
    Nguyen, L. N. Morphology and distribution of the three epiphytic dinoflagellate species Coolia monotis, C. tropicalis, and C. canariensis (Ostreopsidaceae, Gonyaulacales, Dinophyceae) from Vietnamese coastal waters. Ocean Sci. 49, 211–221 (2014).Article 

    Google Scholar 
    Verma, A. et al. Functional significance of phylogeographic structure in a toxic benthic marine microbial eukaryote over a latitudinal gradient along the East Australian Current. Ecol. Evol. 10, 6257–6273 (2020).Article 

    Google Scholar 
    Wayne Litaker, R. et al. Recognizing dinoflagellate species using ITS rDNA sequences 1. J. Phycol. 43, 344–355 (2007).Article 

    Google Scholar 
    Kremp, A. et al. Phylogenetic relationships, morphological variation, and toxin patterns in the Alexandrium ostenfeldii (D inophyceae) complex: Implications for species boundaries and identities. J. Phycol. 50, 81–100 (2014).Article 
    CAS 

    Google Scholar 
    Nascimento, S. M., da Silva, R. A., Oliveira, F., Fraga, S. & Salgueiro, F. Morphology and molecular phylogeny of Coolia tropicalis, Coolia malayensis and a new lineage of the Coolia canariensis species complex (Dinophyceae) isolated from Brazil. Eur. J. Phycol. 54, 484–496 (2019).Article 
    CAS 

    Google Scholar 
    Phua, Y. H., Roy, M. C., Lemer, S., Husnik, F. & Wakeman, K. C. Diversity and toxicity of Pacific strains of the benthic dinoflagellate Coolia (Dinophyceae), with a look at the Coolia canariensis species complex. Harmful Algae 109, 102120 (2021).Article 

    Google Scholar 
    Selwood, A. I. et al. A sensitive assay for palytoxins, ovatoxins and ostreocins using LC-MS/MS analysis of cleavage fragments from micro-scale oxidation. Toxicon 60, 810–820 (2012).Article 
    CAS 

    Google Scholar 
    Ciminiello, P. et al. Isolation and structure elucidation of ovatoxin-a, the major toxin produced by Ostreopsis ovata. J. Am. Chem. Soc. 134, 1869–1875 (2012).Article 
    CAS 

    Google Scholar 
    Dell’Aversano, C. et al. Ostreopsis cf. ovata from the Mediterranean area. Variability in toxinprofiles and structural elucidation of unknowns through LC-HRMSn. In Proc. of the 16th International Conference on Harmful Algae, 70–73 (2014).Terajima, T., Uchida, H., Abe, N. & Yasumoto, T. Structure elucidation of ostreocin-A and ostreocin-E1, novel palytoxin analogs produced by the dinoflagellate Ostreopsis siamensis, using LC/Q-TOF MS. Biosci. Biotechnol. Biochem. 83, 381–390 (2019).Article 
    CAS 

    Google Scholar 
    Tartaglione, L. et al. Chemical, molecular, and eco-toxicological investigation of Ostreopsis sp. from Cyprus Island: Structural insights into four new ovatoxins by LC-HRMS/MS. Anal. Bioanal. Chem. 408, 915–932 (2016).Article 
    CAS 

    Google Scholar 
    Murray, J. S. et al. The role of 44-methylgambierone in ciguatera fish poisoning: Acute toxicity, production by marine microalgae and its potential as a biomarker for Gambierdiscus spp. Harmful Algae 97, 101853 (2020).Article 
    CAS 

    Google Scholar 
    Nakajima, I., Oshima, Y. & Yasumoto, T. Toxicity of benthic dinoflagellates found in coral reef. Toxicity of benthic dinoflagellates in Okinawa. Nippon Suisan Gakk. 47, 1029–1033 (1981).Article 

    Google Scholar 
    Boente-Juncal, A. et al. Structure elucidation and biological evaluation of maitotoxin-3, a homologue of gambierone, from Gambierdiscus belizeanus. Toxins 11, 79 (2019).Article 
    CAS 

    Google Scholar 
    Stuart, J. et al. Geographical distribution, molecular and toxin diversity of the dinoflagellate species Gambierdiscus honu in the Pacific region. Harmful Algae 118, 102308 (2022).Article 
    CAS 

    Google Scholar 
    Smith, K. F. et al. A new Gambierdiscus species (Dinophyceae) from Rarotonga, Cook Islands: Gambierdiscus cheloniae sp. nov. Harmful Algae 60, 45–56 (2016).Article 
    CAS 

    Google Scholar 
    Guillard, R. R. L. Culture of Marine Invertebrates Animals 29–60 (Plenum Press, 1975).Book 

    Google Scholar 
    Chomérat, N., iti Gatti, C. M., Nézan, É. & Chinain, M. Studies on the benthic genus Sinophysis (Dinophysales, Dinophyceae) II. S. canaliculata from Rapa Island (French Polynesia). Phycologia 56, 193–203 (2017).Article 

    Google Scholar 
    Abràmoff, M. D., Magalhães, P. J. & Ram, S. J. Image processing with ImageJ. Biophotonics Int. 11, 36–42 (2004).
    Google Scholar 
    Verma, A. et al. Molecular phylogeny, morphology and toxigenicity of Ostreopsis cf. siamensis (Dinophyceae) from temperate south-east Australia. Phycol. Res. 64, 146–159 (2016).Article 
    CAS 

    Google Scholar 
    Kearse, M. et al. Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649 (2012).Article 

    Google Scholar 
    Kumar, S., Stecher, G. & Tamura, K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).Article 
    CAS 

    Google Scholar 
    Posada, D. & Crandall, K. A. MODELTEST: Testing the model of DNA substitution. Bioinformatics 14, 817–818 (1998).Article 
    CAS 

    Google Scholar 
    Ronquist, F. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574 (2003).Article 
    CAS 

    Google Scholar 
    Murray, J. S. et al. Acute toxicity of gambierone and quantitative analysis of gambierones produced by cohabitating benthic dinoflagellates. Toxins 13, 333 (2021).Article 
    CAS 

    Google Scholar 
    Murray, J. S., Boundy, M. J., Selwood, A. I. & Harwood, D. T. Development of an LC-MS/MS method to simultaneously monitor maitotoxins and selected ciguatoxins in algal cultures and P-CTX-1B in fish. Harmful Algae 80, 80–87 (2018).Article 
    CAS 

    Google Scholar  More

  • in

    Diverse flower-visiting responses among pollinators to multiple weather variables in buckwheat pollination

    Mooney, H. et al. Biodiversity, climate change, and ecosystem services. Curr. Opin. Environ. Sustain. 1, 46–54 (2009).Article 

    Google Scholar 
    Perrings, C., Duraiappah, A., Larigauderie, A. & Mooney, H. The biodiversity and ecosystem services science-policy interface. Science 331, 1139–1140 (2011).Article 
    ADS 
    CAS 

    Google Scholar 
    Yachi, S. & Loreau, M. Biodiversity and ecosystem productivity in a fluctuating environment: The insurance hypothesis. Proc. Natl. Acad. Sci. USA 96, 1463–1468 (1999).Article 
    ADS 
    CAS 

    Google Scholar 
    Elmqvist, T. et al. Response diversity, ecosystem change, and resilience. Front. Ecol. Environ. 1, 488–494 (2003).Article 

    Google Scholar 
    Gonzalez, A. & Loreau, M. The causes and consequences of compensatory dynamics in ecological communities. Annu. Rev. Ecol. Evol. Syst. 40, 393–414 (2009).Article 

    Google Scholar 
    Blüthgen, N. & Klein, A.-M. Functional complementarity and specialisation: The role of biodiversity in plant–pollinator interactions. Basic Appl. Ecol. 12, 282–291 (2011).Article 

    Google Scholar 
    Brittain, C., Kremen, C. & Klein, A. M. Biodiversity buffers pollination from changes in environmental conditions. Glob. Change Biol. 19, 540–547 (2013).Article 
    ADS 

    Google Scholar 
    Rader, R., Reilly, J., Bartomeus, I. & Winfree, R. Native bees buffer the negative impact of climate warming on honey bee pollination of watermelon crops. Glob. Chang. Biol. 19, 3103–3110 (2013).Article 
    ADS 

    Google Scholar 
    Rogers, S. R., Tarpy, D. R. & Burrack, H. J. Bee species diversity enhances productivity and stability in a perennial crop. PLoS ONE 9, e97307 (2014).Article 
    ADS 

    Google Scholar 
    Kühsel, S. & Blüthgen, N. High diversity stabilizes the thermal resilience of pollinator communities in intensively managed grasslands. Nat. Commun. 6, 1–10 (2015).Article 

    Google Scholar 
    Knop, E. et al. Rush hours in flower visitors over a day-night cycle. Insect Conserv. Divers. 11, 267–275 (2018).Article 

    Google Scholar 
    Goodwin, E. K., Rader, R., Encinas-Viso, F. & Saunders, M. E. Weather conditions affect the visitation frequency, richness and detectability of insect flower visitors in the Australian Alpine zone. Environ. Entomol. 50, 348–358 (2021).Article 

    Google Scholar 
    Feit, B. et al. Landscape complexity promotes resilience of biological pest control to climate change. Proc. Biol. Sci. 288, 20210547 (2021).
    Google Scholar 
    Tomas, F., Martínez-Crego, B., Hernán, G. & Santos, R. Responses of seagrass to anthropogenic and natural disturbances do not equally translate to its consumers. Glob. Chang. Biol. 21, 4021–4030 (2015).Article 
    ADS 

    Google Scholar 
    Mori, A. S., Furukawa, T. & Sasaki, T. Response diversity determines the resilience of ecosystems to environmental change. Biol. Rev. 88, 349–364 (2013).Article 

    Google Scholar 
    Cariveau, D. P., Williams, N. M., Benjamin, F. E. & Winfree, R. Response diversity to land use occurs but does not consistently stabilise ecosystem services provided by native pollinators. Ecol. Lett. 16, 903–911 (2013).Article 

    Google Scholar 
    Garibaldi, L. A. et al. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339, 1608. https://doi.org/10.1126/science.1230200 (2013).Article 
    ADS 
    CAS 

    Google Scholar 
    Kennedy, C. M. et al. A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol. Lett. 16, 584–599 (2013).Article 

    Google Scholar 
    Rader, R. et al. Non-bee insects are important contributors to global crop pollination. Proc. Natl. Acad. Sci. 113, 146–151 (2016).Article 
    ADS 
    CAS 

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

    Google Scholar 
    Smith, M. R., Singh, G. M., Mozaffarian, D. & Myers, S. S. Effects of decreases of animal pollinators on human nutrition and global health: A modelling analysis. Lancet 386, 1964–1972 (2015).Article 

    Google Scholar 
    González-Varo, J. P. et al. Combined effects of global change pressures on animal-mediated pollination. Trends Ecol. Evol. 28, 524–530 (2013).Article 

    Google Scholar 
    Marshall, L. et al. The interplay of climate and land use change affects the distribution of EU bumblebees. Glob. Change Biol. 24, 101–116 (2018).Article 
    ADS 

    Google Scholar 
    Millard, J. et al. Global effects of land-use intensity on local pollinator biodiversity. Nat. Commun. 12, 1–11 (2021).Article 
    ADS 

    Google Scholar 
    Vasiliev, D. & Greenwood, S. The role of climate change in pollinator decline across the Northern Hemisphere is underestimated. Sci. Total Environ. 775, 145788 (2021).Article 
    ADS 
    CAS 

    Google Scholar 
    Steffan-Dewenter, I., Münzenberg, U., Bürger, C., Thies, C. & Tscharntke, T. Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83, 1421–1432 (2002).Article 

    Google Scholar 
    Hass, A. L. et al. Landscape configurational heterogeneity by small-scale agriculture, not crop diversity, maintains pollinators and plant reproduction in western Europe. Proc. R. Soc. B Biol. Sci. https://doi.org/10.1098/rspb.2017.2242 (2018).Article 

    Google Scholar 
    Winfree, R. & Kremen, C. Are ecosystem services stabilized by differences among species? A test using crop pollination. Proc. R. Soc. B Biol. Sci. 276, 229–237 (2009).Article 

    Google Scholar 
    Jauker, F., Diekoetter, T., Schwarzbach, F. & Wolters, V. Pollinator dispersal in an agricultural matrix: Opposing responses of wild bees and hoverflies to landscape structure and distance from main habitat. Landsc. Ecol. 24, 547–555 (2009).Article 

    Google Scholar 
    Weiner, C. N., Werner, M., Linsenmair, K. E. & Blüthgen, N. Land-use impacts on plant–pollinator networks: Interaction strength and specialization predict pollinator declines. Ecology 95, 466–474 (2014).Article 

    Google Scholar 
    Chain-Guadarrama, A., Martínez-Salinas, A., Aristizábal, N. & Ricketts, T. H. Ecosystem services by birds and bees to coffee in a changing climate: A review of coffee berry borer control and pollination. Agric. Ecosyst. Environ. 280, 53–67 (2019).Article 

    Google Scholar 
    Hegland, S. J., Nielsen, A., Lázaro, A., Bjerknes, A. L. & Totland, Ø. How does climate warming affect plant–pollinator interactions?. Ecol. Lett. 12, 184–195 (2009).Article 

    Google Scholar 
    Bartomeus, I. et al. Contribution of insect pollinators to crop yield and quality varies with agricultural intensification. PeerJ 2, e328 (2014).Article 

    Google Scholar 
    Albrecht, M., Schmid, B., Hautier, Y. & Müller, C. B. Diverse pollinator communities enhance plant reproductive success. Proc. R. Soc. B Biol. Sci. 279, 4845–4852 (2012).Article 

    Google Scholar 
    Ellis, C. R., Feltham, H., Park, K., Hanley, N. & Goulson, D. Seasonal complementary in pollinators of soft-fruit crops. Basic Appl. Ecol. 19, 45–55 (2017).Article 

    Google Scholar 
    Brittain, C., Williams, N., Kremen, C. & Klein, A.-M. Synergistic effects of non-Apis bees and honey bees for pollination services. Proc. R. Soc. B Biol. Sci. 280, 20122767 (2013).Article 

    Google Scholar 
    Miñarro, M. & Twizell, K. W. Pollination services provided by wild insects to kiwifruit (Actinidia deliciosa). Apidologie 46, 276–285 (2015).Article 

    Google Scholar 
    Senapathi, D., Goddard, M. A., Kunin, W. E. & Baldock, K. C. Landscape impacts on pollinator communities in temperate systems: Evidence and knowledge gaps. Funct. Ecol. 31, 26–37 (2017).Article 

    Google Scholar 
    Papanikolaou, A. D., Kuehn, I., Frenzel, M. & Schweiger, O. Landscape heterogeneity enhances stability of wild bee abundance under highly varying temperature, but not under highly varying precipitation. Landsc. Ecol. 32, 581–593 (2017).Article 

    Google Scholar 
    Papanikolaou, A. D., Kühn, I., Frenzel, M. & Schweiger, O. Semi-natural habitats mitigate the effects of temperature rise on wild bees. J. Appl. Ecol. 54, 527–536 (2017).Article 

    Google Scholar 
    Orford, K. A., Vaughan, I. P. & Memmott, J. The forgotten flies: The importance of non-syrphid Diptera as pollinators. Proc. R. Soc. B Biol. Sci. 282, 20142934 (2015).Article 

    Google Scholar 
    Settele, J., Bishop, J. & Potts, S. G. Climate change impacts on pollination. Nat. Plants 2, 1–3 (2016).Article 

    Google Scholar 
    Taki, H., Okabe, K., Makino, S. I., Yamaura, Y. & Sueyoshi, M. Contribution of small insects to pollination of common buckwheat, a distylous crop. Ann. Appl. Biol. 155, 121–129 (2009).Article 

    Google Scholar 
    Krkošková, B. & Mrazova, Z. Prophylactic components of buckwheat. Food Res. Int. 38, 561–568 (2005).Article 

    Google Scholar 
    Campbell, J. W., Irvin, A., Irvin, H., Stanley-Stahr, C. & Ellis, J. D. Insect visitors to flowering buckwheat, Fagopyrum esculentum (Polygonales: Polygonaceae), in north-central Florida. Fla. Entomol. 99, 264–268 (2016).Article 

    Google Scholar 
    Hadley, N. F. Water Relations of Terrestrial Arthropods (CUP Archive, 1994).
    Google Scholar 
    Sgolastra, F. et al. Temporal activity patterns in a flower visitor community of Dictamnus albus in relation to some biotic and abiotic factors. Bull. Insectol. 69, 291–300 (2016).
    Google Scholar 
    Vicens, N. & Bosch, J. Weather-dependent pollinator activity in an apple orchard, with special reference to Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae and Apidae). Environ. Entomol. 29, 413–420 (2000).Article 

    Google Scholar 
    Carlucci, M. B., Brancalion, P. H., Rodrigues, R. R., Loyola, R. & Cianciaruso, M. V. Functional traits and ecosystem services in ecological restoration. Restor. Ecol. 28, 1372–1383 (2020).Article 

    Google Scholar 
    Lavorel, S. Plant functional effects on ecosystem services. (2013).Defra. (ed Food and Rural Affairs Department for Environment) (2019).Agency, J. M. Amedas, https://tenki.jp/past/2019/09/amedas/ (2019).Jacquemart, A.-L., Gillet, C. & Cawoy, V. Floral visitors and the importance of honey bee on buckwheat (Fagopyrum esculentum Moench) in central Belgium. J. Hortic. Sci. Biotechnol. 82, 104–108 (2007).Article 

    Google Scholar 
    Taki, H. et al. Effects of landscape metrics on Apis and non-Apis pollinators and seed set in common buckwheat. Basic Appl. Ecol. 11, 594–602 (2010).Article 

    Google Scholar 
    Dray, S., Legendre, P. & Peres-Neto, P. R. Spatial modelling: A comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecol. Model. 196, 483–493 (2006).Article 

    Google Scholar 
    Legendre, P. & Legendre, L. Numerical Ecology (Elsevier, 2012).MATH 

    Google Scholar 
    Dray S, et al. adespatial: Multivariate Multiscale Spatial Analysis. R package version 0.3-20, https://CRAN.R-project.org/package=adespatial. (2022).Benjamin, F. E., Reilly, J. R. & Winfree, R. Pollinator body size mediates the scale at which land use drives crop pollination services. J. Appl. Ecol. 51, 440–449 (2014).Article 

    Google Scholar 
    Földesi, R. et al. Relationships between wild bees, hoverflies and pollination success in apple orchards with different landscape contexts. Agric. For. Entomol. 18, 68–75 (2016).Article 

    Google Scholar 
    Oksanen J, et al. vegan: Community Ecology Package. R package version 2.6-4. https://CRAN.R-project.org/package=vegan. (2022)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., Carlin, J. B., Stern, H. S. & Rubin, D. B. Bayesian Data Analysis (Chapman and Hall/CRC, 1995).Book 
    MATH 

    Google Scholar 
    Team, R. C. R: A Language and Environment for Statistical Computing (2019).Sasaki, H. & Wagatsuma, T. Bumblebees (Apidae: Hymenoptera) are the main pollinators of common buckwheat, Fogopyrum esculentum, in Hokkaido, Japan. Appl. Entomol. Zool. 42, 659–661 (2007).Article 

    Google Scholar 
    Nagano, Y., Miyashita, T., Taki, H. & Yokoi, T. Diversity of co-flowering plants at field margins potentially sustains an abundance of insects visiting buckwheat, Fagopyrum esculentum, in an agricultural landscape. Ecol. Res. 36, 882–891 (2021).Article 

    Google Scholar 
    Samra, S., Samocha, Y., Eisikowitch, D. & Vaknin, Y. Can ants equal honeybees as effective pollinators of the energy crop Jatropha curcas L. under Mediterranean conditions?. Gcb Bioenergy 6, 756–767 (2014).Article 

    Google Scholar 
    Sugiura, N., Miyazaki, S. & Nagaishi, S. A supplementary contribution of ants in the pollination of an orchid, Epipactis thunbergii, usually pollinated by hover flies. Plant Syst. Evol. 258, 17–26 (2006).Article 

    Google Scholar 
    Natsume, K., Hayashi, S. & Miyashita, T. Ants are effective pollinators of common buckwheat Fagopyrum esculentum. Agric. For. Entomol. 24, 446–452 (2022).Article 

    Google Scholar 
    Carvalheiro, L. G., Seymour, C. L., Nicolson, S. W. & Veldtman, R. Creating patches of native flowers facilitates crop pollination in large agricultural fields: Mango as a case study. J. Appl. Ecol. 49, 1373–1383 (2012).Article 

    Google Scholar 
    Michiyama, H., Arikuni, M. & Hirano, T. Effect of air temperature on the growth, flowering and ripening in common buckwheat. In The Procceeding of the 8th ISB (2001)Isbell, F. et al. High plant diversity is needed to maintain ecosystem services. Nature 477, 199-U196. https://doi.org/10.1038/nature10282 (2011).Article 
    ADS 
    CAS 

    Google Scholar 
    McCain, C. M. & Colwell, R. K. Assessing the threat to montane biodiversity from discordant shifts in temperature and precipitation in a changing climate. Ecol. Lett. 14, 1236–1245 (2011).Article 

    Google Scholar 
    Choi, S.-W. Effects of weather factors on the abundance and diversity of moths in a temperate deciduous mixed forest of Korea. Zool. Sci. 25, 53–58 (2008).Article 

    Google Scholar 
    Feldmeier, S. et al. Climate versus weather extremes: Temporal predictor resolution matters for future rather than current regional species distribution models. Divers. Distrib. 24, 1047–1060 (2018).Article 

    Google Scholar  More