More stories

  • in

    Biosynthetic gene cluster profiling predicts the positive association between antagonism and phylogeny in Bacillus

    Positive correlation between biosynthetic gene cluster (BGC) and phylogenetic distance in the genus Bacillus
    BGCs are responsible for the synthesis of secondary metabolites involved in microbial interference competition. To investigate the relationship between BGC and phylogenetic distance within the genus Bacillus, we collected 4268 available Bacillus genomes covering 139 species from the NCBI database (Supplementary Data 1). Phylogenetic analysis based on the sequences of 120 ubiquitous single-copy proteins27 showed that the 139 species could be generally clustered into four clades (Fig. 1 and Supplementary Data 2; the phylogenetic tree including all the detailed species information is shown in Supplementary Fig. 1), including a subtilis clade that includes species from diverse niches and can be further divided into the subtilis and pumilus subclades, a cereus clade that contains typical pathogenic species (B. cereus, B. anthracis, B. thuringiensis, etc.), a megaterium clade, and a circulans clade.Fig. 1: Phylogram of the tested Bacillus genomes.The maximum likelihood (ML) phylogram of 4268 Bacillus genomes was based on the sequences of 120 ubiquitous single-copy proteins27. The phylogenetic tree shows that Bacillus species can be generally clustered into the subtilis (light green circle; further includes subtilis (dark green) and pumilus (blue) subclades as shown in the branches), cereus (red), megaterium (yellow), and circulans (gray) clades. For detailed information of the species, please refer to the phylogenetic tree in Supplementary Fig. 1.Full size imagePrediction using the bioinformatic tool antiSMASH15 detected 49,671 putative BGCs in the 4268 genomes, corresponding to an average of 11.6 BGCs per genome (Supplementary Data 3). The subtilis clade had the most BGCs, 13.1 BGCs per genome (Fig. 2a); the subtilis subclade especially accommodates a high abundance of BGCs as 13.6 per genome (Supplementary Fig. 2a), which corresponds to their adaptation in diverse competitive habitats such as plant rhizosphere. The cereus and megaterium clades possessed moderate number of BGCs as 11.7 and 7.4 per genome, respectively; while the circulans clade only had 4.3 BGCs/genome (Fig. 2a and Supplementary Table 1), suggesting a distinct physiological feature and niche adaptation strategy. The two most abundant BGC classes were nonribosomal peptide-synthetase (NRPS) and RiPPs, which had an abundance of 3.7 and 3.1 per genome on average, respectively (Supplementary Fig. 2b and Supplementary Table 1). Interestingly, subtilis clade accommodated significantly higher abundance of BGCs in another polyketide synthase (PKSother; 2.0 per genome vs. 0.0–1.1 per genome) and PKS-NRPS Hybrids (0.7 vs. 0.0–0.2) classes, as compared with the three other clades (Supplementary Table 1); while cereus clade had more BGCs in RiPPs than other clades on average (Supplementary Table 1). Overall, the profile of BGC products and classification was generally consistent with the phylogenetic tree (Supplementary Fig. 3).Fig. 2: Biosynthetic gene cluster (BGC) distribution is correlated with phylogeny in the genus Bacillus.a The numbers of BGCs in the 4268 Bacillus genomes from different clades as defined by antiSMASH15. In the violin plot, the centre line represents the median, violin edges show the 25th and 75th percentiles, and whiskers extend to 1.5× the interquartile range. b Hierarchal clustering among the 545 representative Bacillus genomes based on the abundance of the different biosynthesis gene cluster families (GCFs). Each column represents a GCF, which was classified through BiG-SCAPE by calculating the Jaccard index (JI), adjacency index (AI), and domain sequence similarity (DSS) of each BGC28; the color bar on the top of the heatmap represents the BGC class of each GCF, where PKS includes classes of PKSother and PKSI, PKS-NRPS means PKS-NRPS Hybrids, Others includes classes of saccharides, terpene, and others. Each row represents a Bacillus genome, and the abundance of each GCF in different genomes is shown in the heatmap. The left tree was constructed based on the distribution pattern of GCFs, which showes a similar pattern to the phylogram in Fig. 1. c The correlation between the BGC and phylogenetic distance of the 545 representative Bacillus genomes (P  More

  • in

    Influences of summer warming and nutrient availability on Salix glauca L. growth in Greenland along an ice to sea gradient

    Meredith, M. et al. Polar regions. IPCC Intergov. Panel Clim. Chang. Geneva, Switz. 3, 203–320 (2019).Raftery, A. E., Zimmer, A., Frierson, D. M. W., Startz, R. & Liu, P. Less than 2 °C warming by 2100 unlikely. Nat. Clim. Chang. 7, 637–641 (2017).CAS 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 
    Ernakovich, J. G. et al. Predicted responses of arctic and alpine ecosystems to altered seasonality under climate change. Glob. Chang. Biol. 20, 3256–3269 (2014).PubMed 
    ADS 

    Google Scholar 
    Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003).CAS 
    PubMed 
    ADS 

    Google Scholar 
    Myers-Smith, I. H. & Hik, D. S. Climate warming as a driver of tundra shrubline advance. J. Ecol. 106, 547–560 (2018).
    Google Scholar 
    Martin, A. C., Jeffers, E. S., Petrokofsky, G., Myers-Smith, I. & Macias-Fauria, M. Shrub growth and expansion in the Arctic tundra: An assessment of controlling factors using an evidence-based approach. Environ. Res. Lett. 12, (2017).Myers-Smith, I. H. et al. Climate sensitivity of shrub growth across the tundra biome. Nat. Clim. Chang. 5, 887–891 (2015).ADS 

    Google Scholar 
    Myers-Smith, I. H. et al. Complexity revealed in the greening of the Arctic. Nat. Clim. Chang. 10, 106–117 (2020).ADS 

    Google Scholar 
    Epstein, H. E., Myers-Smith, I. & Walker, D. A. Recent dynamics of arctic and sub-arctic vegetation. Environ. Res. Lett. 8, 015040 (2013).ADS 

    Google Scholar 
    Ackerman, D., Griffin, D., Hobbie, S. E. & Finlay, J. C. Arctic shrub growth trajectories differ across soil moisture levels. Glob. Chang. Biol. 23, 4294–4302 (2017).PubMed 

    Google Scholar 
    Carrer, M., Pellizzari, E., Prendin, A. L., Pividori, M. & Brunetti, M. Winter precipitation – not summer temperature – is still the main driver for Alpine shrub growth. Sci. Total Environ. 682, 171–179 (2019).CAS 
    PubMed 
    ADS 

    Google Scholar 
    Xu, Y., Ramanathan, V. & Washington, W. M. Observed high-altitude warming and snow cover retreat over Tibet and the Himalayas enhanced by black carbon aerosols. Atmos. Chem. Phys. 16, 1303–1315 (2016).CAS 
    ADS 

    Google Scholar 
    Francon, L. et al. Assessing the effects of earlier snow melt-out on alpine shrub growth: The sooner the better? Ecol. Indic. 115, (2020).López-Blanco, E. et al. Exchange of CO2 in Arctic tundra: impacts of meteorological variations and biological disturbance. Biogeosciences 14, 4467–4483 (2017).ADS 

    Google Scholar 
    Lund, M. et al. Larval outbreaks in West Greenland: Instant and subsequent effects on tundra ecosystem productivity and CO2 exchange. Ambio 46, 26–38 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Prendin, A. L. et al. Immediate and carry-over effects of insect outbreaks on vegetation growth in West Greenland assessed from cells to satellite. J. Biogeogr. 47, 87–100 (2020).
    Google Scholar 
    Hobbie, S. E., Nadelhoffer, K. J. & Högberg, P. A synthesis: The role of nutrients as constraints on carbon balances in boreal and arctic regions. Plant Soil 242, 163–170 (2002).CAS 

    Google Scholar 
    Bret-Harte, M. S., Shaver, G. R. & Chapin, F. S. Primary and secondary stem growth in arctic shrubs: Implications for community response to environmental change. J. Ecol. 90, 251–267 (2002).
    Google Scholar 
    Sullivan, P. F., Ellison, S. B. Z., McNown, R. W., Brownlee, A. H. & Sveinbjörnsson, B. Evidence of soil nutrient availability as the proximate constraint on growth of treeline trees in northwest Alaska. Ecology 96, 716–727 (2015).PubMed 

    Google Scholar 
    Craine, J. M. et al. Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol. 183, 980–992 (2009).CAS 
    PubMed 

    Google Scholar 
    Shaver, G. R. & Chapin, F. S. Long-term responses to factorial, NPK fertilizer treatment by Alaskan wet and moist tundra sedge species. Ecography (Cop.) 18, 259–275 (1995).
    Google Scholar 
    Choudhary, S., Blaud, A., Osborn, A. M., Press, M. C. & Phoenix, G. K. Nitrogen accumulation and partitioning in a High Arctic tundra ecosystem from extreme atmospheric N deposition events. Sci. Total Environ. 554–555, 303–310 (2016).PubMed 
    ADS 

    Google Scholar 
    Bergström, A. K. & Jansson, M. Atmospheric nitrogen deposition has caused nitrogen enrichment and eutrophication of lakes in the northern hemisphere. Glob. Chang. Biol. 12, 635–643 (2006).ADS 

    Google Scholar 
    Wild, B. et al. Plant-derived compounds stimulate the decomposition of organic matter in arctic permafrost soils. Sci. Rep. 6, 25607 (2016).CAS 
    PubMed 
    PubMed Central 
    ADS 

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

    Google Scholar 
    Mack, M. C., Schuur, E. A. G. & Bret-harte, M. S. Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization. 431, 658–661 (2004).
    Google Scholar 
    Zamin, T. J. & Grogan, P. Birch shrub growth in the low Arctic: the relative importance of experimental warming, enhanced nutrient availability, snow depth and caribou exclusion. Environ. Res. Lett. 7, 034027 (2012).ADS 

    Google Scholar 
    DeMarco, J., MacK, M. C., Bret-Harte, M. S., Burton, M. & Shaver, G. R. Long-term experimental warming and nutrient additions increase productivity in tall deciduous shrub tundra. Ecosphere 5, 1–22 (2014).
    Google Scholar 
    Zamin, T. J., Bret-Harte, M. S. & Grogan, P. Evergreen shrubs dominate responses to experimental summer warming and fertilization in Canadian mesic low arctic tundra. J. Ecol. 102, 749–766 (2014).
    Google Scholar 
    Fenger-Nielsen, R. et al. Footprints from the past: The influence of past human activities on vegetation and soil across five archaeological sites in Greenland. Sci. Total Environ. 654, 895–905 (2019).CAS 
    PubMed 
    ADS 

    Google Scholar 
    Forbes, B. C., Ebersole, J. J. & Strandberg, B. Anthropogenic disturbance and patch dynamics in Circumpolar Arctic ecosystems. Conserv. Biol. 15, 954–969 (2001).
    Google Scholar 
    Andersen, E. A. S. et al. Nitrogen isotopes reveal high N retention in plants and soil of old Norse and Inuit deposits along a wet-dry arctic fjord transect in Greenland. Plant Soil 455, 241–255 (2020).CAS 

    Google Scholar 
    Normand, S. et al. Legacies of historical human activities in Arctic woody plant dynamics. Annu. Rev. Environ. Resour. 42, 541–567 (2017).
    Google Scholar 
    Walker, D. A. et al. The Circumpolar Arctic vegetation map. J. Veg. Sci. 16, 267–282 (2005).
    Google Scholar 
    Cappelen, J., Vinther, B. M., Kern-Hansen, C., Laursen, E. V. & Jørgensen, P. V. Greenland-DMI Historical Climate Data Collection 1784–2020 (Danish Meteorological Institute, 2021).
    Google Scholar 
    Hollesen, J. et al. Predicting the loss of organic archaeological deposits at a regional scale in Greenland. Sci. Rep. 9, 9097 (2019).PubMed 
    PubMed Central 
    ADS 

    Google Scholar 
    Fenger-Nielsen, R. et al. Arctic archaeological sites threatened by climate change: A regional multi-threat assessment of sites in south-west Greenland. Archaeometry 62, 1280–1297 (2020).CAS 

    Google Scholar 
    Fettweis, X. et al. Reconstructions of the 1900–2015 Greenland ice sheet surface mass balance using the regional climate MAR model. Cryosphere 11, 1015–1033 (2017).ADS 

    Google Scholar 
    Berner, L. T. et al. Summer warming explains widespread but not uniform greening in the Arctic tundra biome. Nat. Commun. 11, 1–12 (2020).ADS 

    Google Scholar 
    Assmann, J. J. et al. Local snow melt and temperature—but not regional sea ice—explain variation in spring phenology in coastal Arctic tundra. Glob. Chang. Biol. 25, 2258–2274 (2019).PubMed 
    ADS 

    Google Scholar 
    Bhatt, U. S. et al. Climate drivers of Arctic tundra variability and change using an indicators framework. Environ. Res. Lett. 16, (2021).Hollesen, J., Matthiesen, H. & Elberling, B. The impact of Climate Change on an archaeological site in the Arctic. Archaeometry 59, 1175–1189 (2017).CAS 

    Google Scholar 
    Tolvanen, A. & Henry, G. H. R. Responses of carbon and nitrogen concentrations in high arctic plants to experimental warming. Can. J. Bot. 79, 711–718 (2001).CAS 

    Google Scholar 
    Oppen, J. et al. Annual air temperature variability and biotic interactions explain tundra shrub species abundance. J. Veg. Sci. 32, (2021).Hobbie, S. E. Temperature and plant species control over litter decomposition in Alaskan tundra. Ecol. Monogr. 66, 503–522 (1996).
    Google Scholar 
    Nadelhoffer, K. J., Giblin, A. E., Shaver, G. R. & Laundre, J. A. Effects of temperature and substrate quality on element mineralization in six Arctic soils. Ecology 72, 242–253 (1991).
    Google Scholar 
    Arens, S. J. T., Sullivan, P. F. & Welker, J. M. Nonlinear responses to nitrogen and strong interactions with nitrogen and phosphorus additions drastically alter the structure and function of a high Arctic ecosystem. J. Geophys. Res. Biogeosciences 113, 1–10 (2008).
    Google Scholar 
    Baddeley, J. A., Woodin, S. J. & Alexander, I. J. Effects of increased nitrogen and phosphorus availability on the photosynthesis and nutrient relations of three Arctic dwarf shrubs from Svalbard. Funct. Ecol. 8, 676 (1994).
    Google Scholar 
    Anadon-Rosell, A. et al. Xylem anatomical and growth responses of the dwarf shrub Vaccinium myrtillus to experimental CO2 enrichment and soil warming at treeline. Sci. Total Environ. 642, 1172–1183 (2018).CAS 
    PubMed 
    ADS 

    Google Scholar 
    Dawes, M. A. et al. Soil warming and CO2 enrichment induce biomass shifts in alpine tree line vegetation. Glob. Chang. Biol. 21, 2005–2021 (2015).PubMed 
    ADS 

    Google Scholar 
    Walker, M. D. et al. Plant community responses to experimental warming across the tundra biome. Proc. Natl. Acad. Sci. 103, 1342–1346 (2006).CAS 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 
    Matthiesen, H., Fenger-Nielsen, R. F., Harmsen, H., Madsen, C. K. & Hollesen, J. The impact of vegetation on archaeological sites in the low arctic in light of climate change. Arctic 73, 141–152 (2020).
    Google Scholar 
    Dahl, M. B. et al. Warming, shading and a moth outbreak reduce tundra carbon sink strength dramatically by changing plant cover and soil microbial activity. Sci. Rep. 7, 1–13 (2017).CAS 

    Google Scholar 
    Westergaard-Nielsen, A., Karami, M., Hansen, B. U., Westermann, S. & Elberling, B. Contrasting temperature trends across the ice-free part of Greenland. Sci. Rep. 8, 1586 (2018).PubMed 
    PubMed Central 
    ADS 

    Google Scholar 
    Schweingruber, F. H., Börner, A. & Schulze, E.-D. Atlas of Stem Anatomy in Herbs, Shrubs and Trees. (Springer, Berlin, 2013). https://doi.org/10.1007/978-3-642-20435-7Pellizzari, E., Camarero, J. J., Gazol, A., Sangüesa-Barreda, G. & Carrer, M. Wood anatomy and carbon-isotope discrimination support long-term hydraulic deterioration as a major cause of drought-induced dieback. Glob. Chang. Biol. 22, 2125–2137 (2016).PubMed 
    ADS 

    Google Scholar 
    Myers-Smith, I. H. et al. Methods for measuring arctic and alpine shrub growth: A review. Earth-Science Rev. 140, 1–13 (2015).ADS 

    Google Scholar 
    Stokes, M. A. & Smiley, T. L. Introduction to Tree-Ring Dating. (University of Chicago Press, 1968).Cook, E. R., Briffa, K., Shiyatov, S. & Mazepa, V. Methods of Dendrochronology: Applications in the Environmental Sciences. (Kluwer Academic Publisher, 1990).Gärtner, H. & Schweingruber, F. H. Microscopic preparation techniques for plant stem analysis. Kessel 95, 132–150 (2013).
    Google Scholar 
    von Arx, G., Crivellaro, A., Prendin, A. L., Čufar, K. & Carrer, M. Quantitative wood anatomy—practical guidelines. Front. Plant Sci. 7, 781 (2016).
    Google Scholar 
    Holmes, R. L. Computer-assisted quality control in tree- ring dating and measurement. Tree-ring Bulletin 43, 69–78 (1983).
    Google Scholar 
    Belokopytova, L. V, Babushkina, E. A., Zhirnova, D. F., Panyushkina, I. P. & Vaganov, E. A. Pine and larch tracheids capture seasonal variations of climatic signal at moisture-limited sites. Trees 33, 227–242 (2019).Büntgen, U. et al. Temperature-induced recruitment pulses of Arctic dwarf shrub communities. J. Ecol. 103, 489–501 (2015).
    Google Scholar 
    Fritts., H. C. Dendrochronology and Dendroclimatology. in Tree Rings and Climate 1–54 (1976). https://doi.org/10.1016/B978-0-12-268450-0.50006-9Briffa, K. & Jones, P. Basic chronology statistics and assessment. in Methods of Dendrochronology: Applications in the Environmental Sciences 137–152 (Kluwer Academic Publishers, 1990).Zuur, A. F., Ieno, E. N., Walker, N., Saveliev, A. A. & Smith, G. M. Mixed effects models and extensions in ecology with R. (Springer New York, 2009). https://doi.org/10.1007/978-0-387-87458-6Gazol, A. & Camarero, J. J. Mediterranean dwarf shrubs and coexisting trees present different radial-growth synchronies and responses to climate. Plant Ecol. 213, 1687–1698 (2012).
    Google Scholar 
    Crawley, M. J. Mixed-Effects Models. in R Book Second edition 681–714 (2007).Zar, J. H. Biostatistical analysis Fifth edition. USA Prentice Hall 4165 4159–4165, (1999).Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Softw. 67, arXiv:1406.5823 (2015).Pinheiro, J. C. & Bates, D. M. Linear Mixed-Effects Models: Basic Concepts and Examples. in Mixed-Effects Models in S and S-PLUS 3–56 (Springer-Verlag, 2000). https://doi.org/10.1007/0-387-22747-4_1Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest Package: Tests in Linear Mixed Effects Models. J. Stat. Softw. 82, (2017).R Core Team (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. More

  • in

    Carex pulicaris abundance is positively associated with soil acidity, rainfall and floristic diversity in the eastern distribution range

    Lawler, J.J. Climate change adaptation strategies for resource management and conservation planning. The year in ecology and conservation biology. Ann. N.Y. Acad. Sci. 1162, 79–98. https://doi.org/10.1111/j.1749-6632.2009.04147.x (2009).Dawson, T. P., Jackson, S. T., House, J. I., Prentice, I. C. & Mace, G. M. Beyond predictions: biodiversity conservation in a changing climate. Science 332(6025), 53–58. https://doi.org/10.1126/science.1200303 (2011).CAS 
    Article 
    PubMed 
    ADS 

    Google Scholar 
    Walsworth, T. E. et al. Management for network diversity speeds evolutionary adaptation to climate change. Nat. Clim. Change 9(8), 632–636. https://doi.org/10.1038/s41558-019-0518-5 (2019).Article 

    Google Scholar 
    Morelli, T. L. et al. Climate-change refugia: Biodiversity in the slow lane. Front Ecol. Environ. 18(5), 228–234. https://doi.org/10.1002/fee.2189 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Vincent, H., Bornand, C. N., Kempel, A. & Fischer, M. Rare species perform worse than widespread species under changed climate. Biol. Conserv. 246, 108586. https://doi.org/10.1016/j.biocon.2020.108586 (2020).Article 

    Google Scholar 
    Corlett, R. T. & Westcott, D. A. Will plant movements keep up with climate change?. Trends Ecol. Evol. 28(8), 482–488. https://doi.org/10.1016/j.tree.2013.04.003 (2013).Article 
    PubMed 

    Google Scholar 
    Janssen, J. & Bijlsma, R.J. Molinia meadows on calcareous, peaty or clayey-silt-laden soils (Molinion caeruleae) (6410) in the Netherlands, in: Bijlsma, R.J. et al. Defining and applying the concept of favourable reference values for species habitats under the EU Birds and Habitats Directives: examples of setting favourable reference values. Wageningen Environmental Research, Wageningen, 2929, pp. 201–203 (2019).Arnell, M., Cousins, S. A. O. & Eriksson, O. Does historical land use affect the regional distribution of fleshy-fruited woody plants?. PLoS ONE 14(12), e0225791. https://doi.org/10.1371/journal.pone.0225791 (2019).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Welk, A., Welk, E., Baudis, M., Böckelmann, J. & Bruelheide, H. Plant species range type determines local responses to biotic interactions and land use. Ecology 100(12), e02890. https://doi.org/10.1002/ecy.2890 (2019).Article 
    PubMed 

    Google Scholar 
    Caissy, P., Klemet-N’Guessan, S., Jackiw, R., Eckert, C.G. & Hargreaves, A.L. High conservation priority of range-edge plant populations not matched by habitat protection or research effort. Biol. Conserv. 249, 108732. https://doi.org/10.1101/682823 (2020).Kreyling, J. et al. Rewetting does not return drained fen peatlands to their old selves. Nat. Commun. 12, 5693. https://doi.org/10.1038/s41467-021-25619-y (2021).CAS 
    Article 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 
    Sotek, Z. Distribution patterns, history, and dynamics of peatland vascular plants in Pomerania (NW Poland). Biodiv. Res. Conserv. 18, 1–82. https://doi.org/10.2478/v10119-010-0020-4 (2010).Article 

    Google Scholar 
    Hultén, E. & Fries, M. Atlas of north European vascular plants, North of the tropic of cancer, I, Introduction, taxonomic index to the maps (Koeltz Scientific Books, 1986).
    Google Scholar 
    Buse, J., Boch, S., Hilgers, J. & Griebeler, E. M. Conservation of threatened habitat types under future climate change—lessons from plant-distribution models and current extinction trends in southern Germany. J. Nat. Conserv. 27, 18–25. https://doi.org/10.1016/j.jnc.2015.06.001 (2015).Article 

    Google Scholar 
    Dítě, D., Melečková, Z. & Eliáš, P. jun. Flea sedge (Carex pulicaris)—a new species in the Great Fatra. Acta Carpathica Occidentalis 6, 23–27, (in Slovak) (2015).Sotek, Z. et al. Distribution and habitat properties of Carex pulicaris and Pedicularis sylvatica at their range margin in NW Poland. Acta Soc. Bot. Pol. 85(3), 3507. https://doi.org/10.5586/asbp.3507 (2016).Article 

    Google Scholar 
    Kukk, T., Kull, T., Luuk, O., Mesipuu, M. & Saar, P. Atlas of the Estonian flora 2020. Tartu, Estonia (2020).Grulich, V. Red list of vascular plants of the Czech Republic, 3rd ed. Preslia 84, 631–645 (2012).Eliáš, P. jun, Dítě, D., Kliment, J., Hrivnák, R. & Feráková, V. Red list of ferns and flowering plants of Slovakia, 5th edition (October 2014). Biologia 70(2), 218–228. https://doi.org/10.1515/biolog-2015-0018 (2015).Kaźmierczakowa, R. et al. Polish red list of pteridophytes and flowering plants. Institute of Nature Conservation of the Polish Academy of Sciences, Cracow (2016).Aronsson, M. et al. Kärlväxter—vascular plants (Tracheophyta). In The 2010 Red List of Swedish Species (ed. Gärdenfors, U.) 201–221 (ArtDatabanken, Uppsala, 2010).
    Google Scholar 
    Kalliovirta, M. et al. Vascular plants, in: Rassi, P., Hyvärinen, E., Juslén, A. & Mannerkoski, I. (Eds.), The 2010 red list of Finnish species. Ministry of the Environment and Finnish Environment Institute, Helsinki, pp. 183–203 (2010).Kull, T. et al. Kokkuvõte soontaimede ohustatuse hindamistulemustest 2017–2018. Liikide ohustatuse hindamine riigihanke 183098 osa nr 15 – Õistaimed (Anthophyta), okaspuutaimed (Coniferophyta), lehtsooneostaimed (Monilophyta) ja pärisraigastaimed (Lycopodiophyta) vastavalt lepingule nr 7–27/17/59 (16. juuni 2017.a.). Lõpparuanne Keskkonnaametile. Eesti Maaülikool. Lk 1–6 + lisa, (in Estonian). Available from https://infoleht.keskkonnainfo.ee/GetFile.aspx?id=1947479558 (2018).Bartoszek, W., Mirek, Z. & Koczur, A. Flea sedge – Carex pulicaris L., in: Kaźmierczakowa, R., Zarzycki, K. & Mirek, Z., (Eds), Polish red data book of plants. Pteridophytes and flowering plants, 3rd ed. Polish Academy of Sciences, Institute of Nature Conservation, Cracow, pp. 737–739, (in Polish) (2014).Matuszkiewicz, W. Guide to the identification of plant communities in Poland. Scientific Publisher Warsaw, Poland, (in Polish) (2006).Hájek, M., Horsák, M., Hájková, P. & Dítě, D. Habitat diversity of central European fens in relation to environmental gradients and an effort to standardise fen terminology in ecological studies. Perspect. Plant Ecol. Evol. Syst. 8, 97–114. https://doi.org/10.1016/j.ppees.2006.08.002 (2006).Article 

    Google Scholar 
    Šefferová-Stanová, V., Šeffer, J. & Janák, M. Management of Natura 2000 habitats. 7230 Alkaline fens. Technical Report 2008 20/24. European Commission. Available from http://ec.europa.eu/environment/nature/natura2000/management/habitats/pdf/7230_Alkaline_fens.pdf. Accessed 15 June 2018 (2008).O’Connell, M., Ryan, J. B. & Macgowran, B. A. Wetland communities in Ireland: a phytosociological review. In European Mires (ed. Moore, P. D.) 303–364 (Academic Press INC, LTD, 1984).Chapter 

    Google Scholar 
    Dítě, D., Kubandová, M. & Pukajová, D. Chorological, ecological and phytocenological notes on the occurrence of flea sedge (Carex pulicaris L.) in Slovakia. Bull. Slovak Bot. Soc. 27, 77–84, (in Slovak) (2005).Hällfors, M. H. et al. Assessing the need and potential of assisted migration using species distribution models. Biol. Conserv. 196(7), 60–68. https://doi.org/10.1016/j.biocon.2016.01.031 (2016).Article 

    Google Scholar 
    Emsens, W.-J., Aggenbach, C. J. S., Rydin, H., Smolders, A. J. P. & van Diggelen, R. Competition for light as a bottleneck for endangered fen species: an introduction experiment. Biol. Conserv. 220, 76–83. https://doi.org/10.1016/j.biocon.2018.02.002 (2018).Article 

    Google Scholar 
    Kącki, Z. & Śliwiński, M. The polish vegetation database: structure, resources and development. Acta Soc. Bot. Pol. 81(2), 75–79. https://doi.org/10.5586/asbp.2012.014 (2012).Article 

    Google Scholar 
    Ellenberg, H. et al. Indicator values of plants in Central Europe. 2nd ed. Scripta Geobotanica 18, 1–258 (in Germany) (1992).PN-R-04031. Chemical and agricultural analysis of soil. Sampling of soil. Polish Committee for Standardization (1997).PN-R-04024. Chemical and agricultural analysis of soil. Determination of the Content of Available P, K, Mg and Mn in organic soils. Polish Committee for Standardization (1997).PN-R-04016-21. Chemical and Agricultural Analysis of Soil. Determination of the Content of Available Zinc, Copper, Manganese, Iron. Polish Committee for Standardization. (1992).Ostrowska, A., Gawliński, S. & Szczubiałka, Z. Methods of analysis and evaluation of soil and plant properties. Institute of Environmental Protection, Warsaw, Poland, (in Polish) (1991).WRB, I.W.G. World reference base for soil resources 2014. International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Report, 106 (2014).IUNG (Institute of Soil Science and Plant Cultivation). Fertiliser Recommendations Part I. Limits for Estimating Soil Macro- and Microelement Content. Series P (44), Puławy, Poland, pp. 26–28 (1990).IUNG (Institute of Soil Science and Plant Cultivation). Evaluation of heavy metal and sulfur contamination of soils and plants. Framework guidelines for agriculture. Series P (53), Puławy, Poland, pp. 1–22 (1993).Oksanen, J. et al. Vegan: community ecology package. R package version 2.3–0. Available from https://cran.r-project.org/web/packages/vegan/vegan.pdf. Accessed date: 4 January 2021 (2019).R Core Team. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria Accessed 30 May 2020. https://www.R-project.org (2020).Hammer, Ø., Harper, D.A.T. & Ryan, P.D. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontol. Electron. 4 (1), 1–9; http://palaeo-electronica.org/2001_1/past/issue1_01.htm (2001).Zelnik, I. & Čarni, A. Wet meadows of the alliance Molinion and their environmental gradients in Slovenia. Biologia 63(2), 187–196. https://doi.org/10.2478/s11756-008-0042-y (2008).CAS 
    Article 

    Google Scholar 
    Lindén, C. Local plant species diversity in coastal grasslands in the Stockholm archipelago. The effect of isostatic land-uplift, different management and future sea level rise. Stockholm University, Master’s thesis, Physical Geography and Quaternary Geology, 45 Credits, Stockholm, pp. 1–33 (2017).Muller, S. Diversity of management practices required to ensure conservation of rare and locally threatened plant species in grasslands: A case study at a regional scale (Lorraine, France). Biodiv. Conserv. 11(7), 1173–1184. https://doi.org/10.1023/A:1016049605021 (2002).Article 

    Google Scholar 
    Rodwell, J. S. (ed.) British plant communities. Grasslands and montane communities. Vol. 3 (Cambridge University Press. 1992).Rodwell, J.S., Morgan, V., Jefferson, R.G. & Moss, D. The European context of British Lowland Grasslands. JNCC Report No. 394, JNCC, Peterborough, UK (2007).Carter, S. P., Proctor, J. & Slingsby, D. R. Soil and vegetation of the Keen of Hamar serpentine. Shetland. J. Ecol. 75(1), 21–42. https://doi.org/10.2307/2260534 (1987).CAS 
    Article 

    Google Scholar 
    de Vere, N. Biological flora of the British Isles: Cirsium dissectum (L.) Hill (Cirsium tuberosum (L.) All. subsp. anglicum (Lam.) Bonnier; Cnicus pratensis (Huds.) Willd., non Lam.; Cirsium anglicum (Lam.) DC.). J. Ecol. 95, 876–894. https://doi.org/10.1111/j.1365-2745.2007.01265.x (2007).Fernández-Pascual, E. Comparative seed germination traits in bog and fen mire wetlands. Aquat. Bot. 130, 21–26. https://doi.org/10.1016/j.aquabot.2016.01.001 (2016).Article 

    Google Scholar 
    Otsus, M., Kukk, D., Kattai, K. & Sammul, M. Clonal ability, height and growth form explain species’ response to habitat deterioration in Fennoscandian wooded meadows. Plant Ecol. 215(9), 953–962. https://doi.org/10.1007/s11258-014-0347-6 (2014).Article 

    Google Scholar 
    Meusel, H., Jäger, E. & Weinert, E. Comparative chorology of the Central European flora. VEB Gustav Fischer Verlag, Jena, Germany, (in German) (1965).Hill, M.O., Preston, C.D. & Roy, D.B. PLANTATT. Attributes of British and Irish Plants: Status, Size, Life History, Geography and Habits. Centre for Ecology and Hydrology, Huntingdon, UK (2004).Dahl, E. The phytogeography of Northern Europe (British Isles, Fennoscandia and adjacent areas). Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9780511565182 (1998).Bartoszek, W., Koczur, A., Mirek, Z. & Oklejewicz, K. Flea sedge Carex pulicaris L., in: Mirek, Z. & Piękoś-Mirkowa, H. (Eds.), Red data book of the Polish Carpathians. Vascular plants. Polish Academy of Sciences Institute of Botany W. Szafer, Cracow, pp. 523–525, (in Polish) (2008).Hereźniak, J. Carex pulicaris L. – flea sedge, in: Olaczek R. (Ed.), Red Book of Plants of the Lodzkie Voivodship. Botanical Garden in Łódź, University of Łódź, Łódź, pp. 50–51, (in Polish) (2012).Wołejko, L., Pawlaczyk, P. & Stańko, R. (Eds.). Alkaline fens in Poland—diversity, resources, conservation. Naturalists’ Club, Świebodzin, Poland (2019).Koopman, J., Timmerman, A., Hosper, U. & Więcław, H. Distribution, ecology and morphology of three Ceratocystis hybrids in the Province of Fryslân, the Netherlands (Carex, Cyperaceae). Gorteria 41(1), 14–20 (2019).
    Google Scholar 
    Laughlin, D. C. & Abella, S. R. Abiotic and biotic factors explain independent gradients of plant community composition in ponderosa pine forests. Ecol. Modell. 205(1–2), 231–240. https://doi.org/10.1016/j.ecolmodel.2007.02.018 (2007).Article 

    Google Scholar 
    Austrheim, G., Gunilla, E., Olsson, A. & Grøntvedt, E. Land-use impact on plant communities in semi-natural sub-alpine grasslands of Budalen, central Norway. Biol. Conserv. 87(3), 369–379. https://doi.org/10.1016/S0006-3207(98)00071-8 (1999).Article 

    Google Scholar 
    Gough, M. W. & Marrs, R. H. A comparison of soil fertility between semi-natural and agricultural plant communities: Implications for the creations of species-rich grassland on abandoned agricultural land. Biol. Conserv. 51(2), 83–96. https://doi.org/10.1016/0006-3207(90)90104-w (1990).Article 

    Google Scholar 
    Bobbink, R., Hornung, M. & Roelofs, J. G. M. The effects of air-borne nitrogen pollutants on species diversity in natural and semi-natural European vegetation. J. Ecol. 86(5), 717–738 (1998).CAS 
    Article 

    Google Scholar 
    McCrea, A. R., Trueman, I. C., Fullen, M. A., Atkinson, M. D. & Besenyei, L. Relationships between soil characteristics and species richness in two botanically heterogeneous created meadows in the urban English West Midlands. Biol. Conserv. 97(2), 171–180 (2001).Article 

    Google Scholar 
    Wamelink, W., van Dobben, H.F., Goedhart, P.W. & Jones-Walters, L.M. The role of abiotic soil parameters as a factor in the success of invasive plant species. Emerg. Sci. J. 2(6), 308–365. https://doi.org/10.28991/esj-2018-01155 (2018).Janssens, F. et al. Relationship between soil chemical factors and grassland diversity. Plant Soil 202(1), 69–78. https://doi.org/10.1023/A:1004389614865 (1998).CAS 
    Article 

    Google Scholar 
    Tallowin, J. R. B. & Smith, R. E. N. Restoration of a Cirsio-Molinietum fen meadow on an agriculturally improved pasture. Restor. Ecol. 9(2), 167–178. https://doi.org/10.1046/j.1526-100x.2001.009002167.x (2001).Article 

    Google Scholar 
    Venterink, H. O., van der Vliet, R. E. & Wassen, M. J. Nutrient limitation along a productivity gradient in wet meadows. Plant Soil 234(2), 171–179. https://doi.org/10.1023/A:1017922715903 (2001).Article 

    Google Scholar 
    Linderoth, E. Management of nature reserves—with Valön nature reserve in focus. Bachelor of Science with specialization in Environmental Analysis 15 hp, VT18. Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science, pp 1–26, (in Swedish) (2018).Jansen, A. M. & Roelofs, J. G. Restoration of Cirsio-Molinietum wet meadows by sod cutting. Ecol. Eng. 7(4), 279–298. https://doi.org/10.1016/S0925-8574(96)00022-5 (1996).Article 

    Google Scholar 
    Jurzyk, S. & Wrobel, M. Co-occurrence of two species Molinia caerulea L. and “red-list” species Carex pulicaris L. in western Pomerania (Poland). Pol. J. Ecol. 51 (3), 363–367 (2003).Boyer, M. L. H. & Wheeler, B. D. Vegetation patterns in spring-fed calcareous fens: Calcite precipitation and constraints on fertility. J. Ecol. 77(2), 597–609. https://doi.org/10.2307/2260772 (1989).CAS 
    Article 

    Google Scholar  More

  • in

    Host microbiome responses to the Snake Fungal Disease pathogen (Ophidiomyces ophidiicola) are driven by changes in microbial richness

    Daszak, P., Cunningham, A. A. & Hyatt, A. D. Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science 287, 443–449 (2000).CAS 
    PubMed 
    ADS 

    Google Scholar 
    Pedersen, A. B., Jones, K. E., Nunn, C. L. & Altizer, S. Infectious diseases and extinction risk in wild mammals. Conserv. Biol. 21, 1269–1279 (2007).PubMed 
    PubMed Central 

    Google Scholar 
    Smith, K. F., Sax, D. F. & Lafferty, K. D. Evidence for the role of infectious disease in species extinction and endangerment. Conserv. Biol. 20, 1349–1357 (2006).PubMed 

    Google Scholar 
    Fisher, M. C. et al. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194 (2012).CAS 
    PubMed 
    ADS 

    Google Scholar 
    Paré, J. A. & Sigler, L. An overview of reptile fungal pathogens in the genera Nannizziopsis, Paranannizziopsis, and Ophidiomyces. J. Herpetol. Med. Surg. 26, 46–53 (2016).
    Google Scholar 
    Warnecke, L. et al. Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc. Natl. Acad. Sci. 109, 6999–7003 (2012).CAS 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 
    Skerratt, L. F. et al. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4, 125 (2007).
    Google Scholar 
    Franklinos, L. H. V. et al. Emerging fungal pathogen Ophidiomyces ophiodiicola in wild European snakes. Sci. Rep. 7, 3844 (2017).PubMed 
    PubMed Central 
    ADS 

    Google Scholar 
    Lorch, J. M. et al. Snake fungal disease: an emerging threat to wild snakes. Philos. Trans. R. Soc. B Biol. Sci. 371, 20150457 (2016).
    Google Scholar 
    Bustos, M. L., Nicolás Sánchez, M., Peichoto, M. E. & Teibler, G. P. First report of fungal disease in a South American snake. Rev. Investig. Vet. Perú 29, 1036–1042 (2018).Sun, P.-L. et al. Infection with Nannizziopsis guarroi and Ophidiomyces ophiodiicola in reptiles in Taiwan. Transbound. Emerg. Dis. https://doi.org/10.1111/tbed.14049 (2021).Article 
    PubMed 

    Google Scholar 
    Haynes, E. et al. First report of ophidiomycosis in a free-ranging California kingsnake (Lampropeltis californiae) in California, USA. J. Wildl. Dis. 57, 246–249 (2021).CAS 
    PubMed 

    Google Scholar 
    Takami, Y. et al. First report of ophidiomycosis in Asia caused by Ophidiomyces ophiodiicola in captive snakes in Japan. J. Vet. Med. Sci. 83, 1234–1239 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lorch, J. M. et al. Experimental infection of snakes with Ophidiomyces ophiodiicola causes pathological changes that typify snake fungal disease. MBio 6, e01534 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Koenig, J. E. et al. Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. 108, 4578–4585 (2011).CAS 
    PubMed 
    ADS 

    Google Scholar 
    Huttenhower, C. et al. Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214 (2012).CAS 
    ADS 

    Google Scholar 
    Grice, E. A. & Segre, J. A. The skin microbiome. Nat. Rev. Microbiol. 9, 244–253 (2011).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gall, C. A. et al. The bacterial microbiome of Dermacentor andersoni ticks influences pathogen susceptibility. ISME J. 10, 1846–1855 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gould, A. L. et al. Microbiome interactions shape host fitness. Proc. Natl. Acad. Sci. 115, E11951–E11960 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hanning, I. & Diaz-Sanchez, S. The functionality of the gastrointestinal microbiome in non-human animals. Microbiome 3, 51 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Jani, A. J. & Briggs, C. J. The pathogen Batrachochytrium dendrobatidis disturbs the frog skin microbiome during a natural epidemic and experimental infection. Proc. Natl. Acad. Sci. 111, E5049–E5058 (2014).CAS 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 
    Walker, D. M. et al. Variability in snake skin microbial assemblages across spatial scales and disease states. ISME J. 13, 2209–2222 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Allender, M. C., Baker, S., Britton, M. & Kent, A. D. Snake fungal disease alters skin bacterial and fungal diversity in an endangered rattlesnake. Sci. Rep. 8, 12147 (2018).PubMed 
    PubMed Central 
    ADS 

    Google Scholar 
    Rykiel, E. J. Jr. Towards a definition of ecological disturbance. Aust. J. Ecol. 10, 361–365 (1985).
    Google Scholar 
    Kong, H. H. et al. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res. 22, 850–859 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ferrenberg, S. et al. Changes in assembly processes in soil bacterial communities following a wildfire disturbance. ISME J. 7, 1102–1111 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    Mackey, R. L. & Currie, D. J. The diversity–disturbance relationship: is it generally strong and peaked?. Ecology 82, 3479–3492 (2001).
    Google Scholar 
    Connell, J. H. Diversity in tropical rain forests and coral reefs: high diversity of trees and corals is maintained only in a nonequilibrium state. Science 199, 1302–1310 (1978).CAS 
    PubMed 
    ADS 

    Google Scholar 
    Guthrie, A. L., Knowles, S., Ballmann, A. E. & Lorch, J. M. Detection of snake fungal disease due to Ophidiomyces ophiodiicola in Virginia, USA. J. Wildl. Dis. 52, 143–149 (2016).PubMed 

    Google Scholar 
    Chandler, H. C. et al. Ophidiomycosis prevalence in Georgia’s eastern indigo snake (Drymarchon couperi) populations. PLoS ONE 14, e0218351 (2019).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Tetzlaff, S. J. et al. Snake fungal disease affects behavior of free-ranging massasauga rattlesnakes (Sistrurus catenatus). Herpetol. Conserv. Biol. 12, 624–634 (2017).
    Google Scholar 
    Lind, C. M., McCoy, C. M. & Farrell, T. M. Tracking outcomes of snake fungal disease in free-ranging pygmy rattlesnakes (Sistrurus miliarius). J. Wildl. Dis. 54, 352–356 (2018).PubMed 

    Google Scholar 
    Lind, C. M., Lorch, J. M., Moore, I. T., Vernasco, B. J. & Farrell, T. M. Seasonal sex steroids indicate reproductive costs associated with snake fungal disease. J. Zool. 307, 104–110 (2019).
    Google Scholar 
    McKenzie, J. M. et al. Field diagnostics and seasonality of Ophidiomyces ophiodiicola in wild snake populations. EcoHealth 16, 141–150 (2019).PubMed 

    Google Scholar 
    McCoy, C. M., Lind, C. M. & Farrell, T. M. Environmental and physiological correlates of the severity of clinical signs of snake fungal disease in a population of pigmy rattlesnakes, Sistrurus miliarius. Conserv. Physiol. 5, cow077 (2017).Hill, A. J. et al. Common cutaneous bacteria isolated from snakes inhibit growth of Ophidiomyces ophiodiicola. EcoHealth 15, 109–120 (2018).PubMed 

    Google Scholar 
    Baker, S. et al. Case definition and diagnostic testing for Snake Fungal Disease. Herpetol. Rev. 50, 279–285 (2019).
    Google Scholar 
    Chase, J. M., Kraft, N. J. B., Smith, K. G., Vellend, M. & Inouye, B. D. Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2, art24 (2011).Agugliaro, J., Lind, C. M., Lorch, J. M. & Farrell, T. M. An emerging fungal pathogen is associated with increased resting metabolic rate and total evaporative water loss rate in a winter-active snake. Funct. Ecol. 34, 486–496 (2020).
    Google Scholar 
    Frick, W. F. et al. Pathogen dynamics during invasion and establishment of white-nose syndrome explain mechanisms of host persistence. Ecology 98, 624–631 (2017).PubMed 

    Google Scholar 
    Gervasi, S. S., Hunt, E. G., Lowry, M. & Blaustein, A. R. Temporal patterns in immunity, infection load and disease susceptibility: understanding the drivers of host responses in the amphibian-chytrid fungus system. Funct. Ecol. 28, 569–578 (2014).
    Google Scholar 
    Allender, M. C. et al. Development of snake fungal disease after experimental challenge with Ophidiomyces ophiodiicola in cottonmouths (Agkistrodon piscivorous). PLoS ONE 10, e0140193 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Briggs, C. J., Knapp, R. A. & Vredenburg, V. T. Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proc. Natl. Acad. Sci. 107, 9695–9700 (2010).CAS 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 
    Neuman-Lee, L. A. et al. Assessing multiple endpoints of atrazine ingestion on gravid Northern Watersnakes (Nerodia sipedon) and their offspring. Environ. Toxicol. 29, 1072–1082 (2014).CAS 
    PubMed 
    ADS 

    Google Scholar 
    Turnbaugh, P. J. et al. A core gut microbiome in obese and lean twins. Nature 457, 480–484 (2009).CAS 
    PubMed 
    ADS 

    Google Scholar 
    Kueneman, J. G. et al. Community richness of amphibian skin bacteria correlates with bioclimate at the global scale. Nat. Ecol. Evol. 3, 381–389 (2019).PubMed 

    Google Scholar 
    Manichanh, C. et al. Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut 55, 205–211 (2006).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Murphy, G. E. P. & Romanuk, T. N. A meta-analysis of declines in local species richness from human disturbances. Ecol. Evol. 4, 91–103 (2014).PubMed 

    Google Scholar 
    Jani, A. J. et al. The amphibian microbiome exhibits poor resilience following pathogen-induced disturbance. ISME J. 15, 1628–1640 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Zaneveld, J. R., McMinds, R. & Vega Thurber, R. Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat. Microbiol. 2, 1–8 (2017).
    Google Scholar 
    Anderson, M. J. et al. Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecol. Lett. 14, 19–28 (2011).PubMed 
    ADS 

    Google Scholar 
    Lankau, E. W., Hong, P.-Y. & Mackie, R. I. Ecological drift and local exposures drive enteric bacterial community differences within species of Galápagos iguanas. Mol. Ecol. 21, 1779–1788 (2012).PubMed 

    Google Scholar 
    Mebert, K. Good species despite massive hybridization: genetic research on the contact zone between the watersnakes Nerodia sipedon and N. fasciata in the Carolinas, USA. Mol. Ecol. 17, 1918–1929 (2008).CAS 
    PubMed 

    Google Scholar 
    Bohuski, E., Lorch, J. M., Griffin, K. M. & Blehert, D. S. TaqMan real-time polymerase chain reaction for detection of Ophidiomyces ophiodiicola, the fungus associated with snake fungal disease. BMC Vet. Res. 11, 95 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Wiens, J. A. Spatial scaling in ecology. Funct. Ecol. 3, 385–397 (1989).
    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).CAS 
    PubMed 
    ADS 

    Google Scholar 
    Fadrosh, D. W. et al. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2, 6 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541 (2009).CAS 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 
    Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K. & Schloss, P. D. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the Miseq Illumina sequencing platform. Appl. Environ. Microbiol. 79, 5112–5120 (2013).CAS 
    PubMed 
    PubMed Central 
    ADS 

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

    Google Scholar 
    Yilmaz, P. et al. The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucl. Acids Res. 42, D643–D648 (2014).CAS 
    PubMed 

    Google Scholar 
    Weiss, S. et al. Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome 5, 27 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    R Core Team. R: A language and environment for statistical computing. (R Foundation for Statistical Computing, 2021).Bozdogan, H. Model selection and akaike’s information criterion (AIC): the general theory and its analytical extensions. Psychometrika 52, 345–370 (1987).MathSciNet 
    MATH 

    Google Scholar 
    Fox, J. & Weisberg, S. An R Companion to Applied Regression (SAGE Publications, Thousand Oaks, 2011).
    Google Scholar 
    Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R (Springer, 2009).MATH 

    Google Scholar 
    Heip, C. A new index measuring evenness. J. Mar. Biol. Assoc. UK 54, 555–557 (1974).
    Google Scholar  More

  • in

    Microbotanical residues for the study of early hominin tools

    Mercader, J., Panger, M. & Boesch, C. Excavation of a Chimpanzee stone tool site in the African rainforest. Science 296, 1452–1455 (2002).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Mercader, J. et al. 4,300-year-old chimpanzee sites and the origins of percussive stone technology. PNAS 104, 3043–3048 (2007).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Haslam, M. et al. Primate archaeology. Nature 460, 339–344 (2009).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Plummer, T. W. & Finestone, E. Rethinking Human Evolution (ed. Schwartz, J.). 267–296. (MIT Press, 2018).Toth, N. & Schick, K. An overview of the cognitive implications of the Oldowan industrial complex. Azania Archaeol. Res. Afr. 53, 3–39 (2018).Plummer, T. Flaked stones and old bones: Biological and cultural evolution at the dawn of technology. Yearb. Phys. Anthropol. 47, 118–164 (2004).
    Google Scholar 
    Ferraro, J. V. et al. Earliest archaeological evidence of persistent hominin carnivory. PLoS ONE 8, e62174 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Braun, D. R. et al. Early hominin diet included diverse terrestrial and aquatic animals 1.95 Ma in East Turkana, Kenya. Proc. Natl. Acad. Sci. 107, 10002–10007 (2010).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sahnouni, M. et al. 1.9-million- and 2.4-million-year-old artefacts and stone tool-cutmarked bones from Ain Boucherit, Algeria. Science 362, 1297–1301 (2018).Stahl, A. B. Hominid dietary selection before fire. Curr. Anthropol. 25, 151–168 (1984).
    Google Scholar 
    Laden, G. & Wrangham, R. The rise of hominids as an adaptive shift in fallback foods: Plant underground storage organs (USOs) and Australopith origins. J. Hum. Evol. 49, 482–498 (2005).PubMed 

    Google Scholar 
    Peters, C. & Vogel, J. Africa’s wild C4 plant foods and possible early hominid diets. J. Hum. Evol. 48, 219–236 (2005).PubMed 

    Google Scholar 
    Copeland, S. R. Vegetation and plant food reconstruction of lowermost bed II, Olduvai Gorge, using modern analogs. J. Hum. Evol. 53, 146–175 (2007).PubMed 

    Google Scholar 
    Domínguez Rodrigo, M. Interdisciplinary Approaches to the Oldowan (eds. Hovers, E. & Braun, D.R.). 129–147. (Springer, 2009).Hovers, E. Origins of Human Innovation and Creativity (ed Elias, S.). 51–68. (Elsevier, 2012).Domínguez Rodrigo, M. Meat eating by early hominids at the FLK 22 Zinjanthropus site, Olduvai Gorge, Tanzania: An experimental approach using cut mark data. J. Hum. Evol. 33, 669–690 (1997).PubMed 

    Google Scholar 
    Pobiner, B. L., Rogers, M. J., Monahan, C. M. & Harris, J. W. New evidence for hominin carcass processing strategies at 1.5 Ma, Koobi Fora, Kenya. J. Hum. Evolut. 55, 103–130 (2018).
    Google Scholar 
    Marreiros, J. et al. Rethinking use-wear analysis and experimentation as applied to the study of past hominin tool use. J. Paleolithic Archaeol. 3, 475–502 (2020).
    Google Scholar 
    de la Torre, I., Benito-Calvo, A., Arroyo, A., Zupancich, A. & Proffitt, T. Experimental protocols for the study of battered stone anvils from Olduvai Gorge (Tanzania). J. Archaeol. Sci. 40, 313–332. https://doi.org/10.1016/j.jas.2012.08.007 (2013).Article 

    Google Scholar 
    Caruana, M. V., Carvalho, S., Braun, D. R., Presnyakova, D. & Haslam, M. Quantifying traces of tool use: A novel morphometric analysis of damage patterns on percussive tools. PLoS ONE 9, e113856 (2014).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Benito-Calvo, A., Carvalho, S., Arroyo, A., Matsuzawa, T. & de la Torre, I. First GIS analysis of modern stone tools used by wild chimpanzees (Pan troglodytes verus) in Bossou, Guinea, West Africa (PLOS One, 2015). https://doi.org/10.1371/journal.pone.0121613.Book 

    Google Scholar 
    Sánchez-Yustos, P. et al. Production and use of percussive stone tools in the Early Stone Age: Experimental approach to the lithic record of Olduvai Gorge, Tanzania. J. Archaeol. Sci. Rep. 2, 367–383 (2015).
    Google Scholar 
    Arroyo, A., Hirata, S., Matsuzawa, T. & De La Torre, I. Nut cracking tools used by captive chimpanzees (Pan troglodytes) and their comparison with Early Stone Age percussive artefacts from Olduvai Gorge. PLoS ONE 11, e0166788 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Arroyo, A. & de la Torre, I. Assessing the function of pounding tools in the early stone age: A microscopic approach to the analysis of percussive artefacts from beds I and II, Olduvai Gorge (Tanzania). J. Archaeol. Sci. 74, 23–34 (2016).
    Google Scholar 
    Proffitt, T. et al. Analysis of wild macaque stone tools used to crack oil palm nuts 5, 1–16 (2018).
    Google Scholar 
    Titton, S. et al. Active percussion tools from the Oldowan site of Barranco León (Orce, Andalusia, Spain): The fundamental role of pounding activities in hominin lifeways. J. Archaeol. Sci. 96, 131–147 (2018).
    Google Scholar 
    Lemorini, C. et al. Old stones’ song: Use-wear experiments and analysis of the Oldowanquartz and quartzite assemblage from Kanjera South (Kenya). J. Hum. Evol. 72, 10–25 (2014).PubMed 

    Google Scholar 
    Keeley, L. H. & Toth, N. Microwear polishes on early stone tools from Koobi Fora, Kenya. Nature 293, 464–465 (1981).ADS 

    Google Scholar 
    Longo, L. et al. A multi-dimensional approach to investigate use-related biogenic residues on palaeolithic ground stone tools. Environ. Archaeol. 21, 1–29 (2021).
    Google Scholar 
    Langejans, G. H. J. Remains of the day-preservation of organic micro-residues on stone tools. J. Archaeol. Sci. 37, 971–985 (2010).
    Google Scholar 
    Langejans, G. H. J. Micro-residue analysis on early stone age tools from Sterkfontein, South Africa: A methodological enquiry. S. Afr. Archaeol. Bull. 67, 200–213 (2012).
    Google Scholar 
    Pedergnana, A. & Ollé, A. Building an experimental comparative reference collection for lithic micro-residue analysis based on a multi-analytical approach. J. Archaeol. Method Theory 25, 117–154 (2018).
    Google Scholar 
    Crowther, A., Haslam, M., Oakden, N., Walde, D. & Mercader, J. Documenting contamination in ancient starch laboratories. J. Archaeol. Sci. 49, 90–104 (2014).CAS 

    Google Scholar 
    Pedergnana, A., Asryan, L., Fernández-Marchena, J. L. & Ollé, A. Modern contaminants affecting microscopic residue analysis on stone tools: A word of caution. Micron 86, 1–21. https://doi.org/10.1016/j.micron.2016.04.003 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    Mercader, J. et al. Starch contamination landscapes in field archaeology: Olduvai Gorge, Tanzania. Boreas 46, 918–934. https://doi.org/10.1111/bor.12241.ISSN0300-9483 (2017).Article 

    Google Scholar 
    Barton, H., Torrence, R. & Fullagar, R. Clues to stone tool function re-examined: Comparing starch grain frequencies on used and unused obsidian artefacts. J. Archaeol. Sci. 25, 1231–1238 (1998).
    Google Scholar 
    Atchison, J. & Fullagar, R. A Closer Look: Recent Australian Studies of Stone Tools Sydney University Archaeological Methods Series (ed Fullagar, R.). Chap. 8. 110–125. (1998).Hardy, B. L. & Garufi, G. T. Identification of woodworking on stone tools through residue and use-wear analyses: Experimental results. J. Archaeol. Sci. 25, 177–184 (1998).
    Google Scholar 
    Kealhofer, L., Torrence, R. & Fullagar, R. Integrating phytoliths within use-wear/residue studies of stone tools. J. Archaeol. Sci. 26, 527–546 (1999).
    Google Scholar 
    Fullagar, R. et al. Evidence for Pleistocene seed grinding at Lake Mungo, south-eastern Australia. Archaeol. Ocean. 50, 3–19 (2015).
    Google Scholar 
    Ma, Z., Perry, L., Li, Q. & Yang, X. Morphological changes in starch grains after dehusking and grinding with stone tools. Sci. Rep. 9, 2355 (2019).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Briuer, F. L. New clues to stone tool function: Plant and animal residues. Am. Antiq. 41, 478–484 (1976).
    Google Scholar 
    Mora, R. & de la Torre, I. Percussion tools in Olduvai Beds I and II (Tanzania): Implication for early human activities. J. Anthropol. Archaeol. 24, 179–192 (2005).
    Google Scholar 
    Diez-Martín, F., Sánchez, P., Domínguez-Rodrigo, M., Mabulla, A. & Barba, R. Were Olduvai Hominins making butchering tools or battering tools? Analysis of a recently excavated lithic assemblage from BK (Bed II, Olduvai Gorge, Tanzania). J. Anthropol. Archaeol. 28, 274–289 (2009).
    Google Scholar 
    McHenry, L. J. & de la Torre, I. Hominin raw material procurement in the Oldowan-Acheulean transition at Olduvai Gorge. J. Hum. Evol. https://doi.org/10.1016/j.jhevol.2017.11.010 (2018).Article 
    PubMed 

    Google Scholar 
    Soto, M. et al. Systematic sampling of quartzite in sourcing analysis: intra-outcrop variability at Naibor Soit, Tanzania (part I). Archaeol. Anthropol. Sci. 12, 1–14 (2020).
    Google Scholar 
    Zupancich, A. & Cristiani, E. Functional analysis of sandstone ground stone tools: Arguments for a qualitative and quantitative synergetic approach. Sci. Rep. 10, 1–13 (2020).
    Google Scholar 
    Mercader, J. et al. Soil and plant phytoliths from the Acacia-Commiphora mosaics at Oldupai Gorge (Tanzania). PeerJ 7, e8211 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Krumbein, W. C. Measurement and geological significance of shape and roundness of sedimentary particles. Journal of Sedimentary Research 11, 64–72 (1941).CAS 

    Google Scholar 
    Favreau, J. et al. Petrographic Characterization of Raw Material Sources at Oldupai Gorge, Tanzania. Frontiers in Earth Science 8, 1–26, https://doi.org/10.31219/osf.io/s2vgr (2020).Article 

    Google Scholar 
    Soto, M. et al. Fingerprinting of quartzitic outcrops at Oldupai Gorge, Tanzania. Journal of Archaeological Science: Reports 29, 102010 (2020).
    Google Scholar 
    Anderson, G. D. & Talbot, L. M. Soil Factors Affecting the Distribution of the Grassland Types and their Utilization by Wild Animals on the Serengeti Plains, Tanganyika. Journal of Ecology 53, 33–56 (1965).
    Google Scholar 
    Leakey, M. D. Olduvai Gorge Vol. 3: Excavations in Beds I and II, 1960–1963. (Cambridge University Press, 1971).Dorn, R. I. Rock Coatings. Vol. 6 (Elsevier, 1998).Madella, M., Alexandre, A. & Ball, T. International code for phytolith nomenclature 10. Ann. Bot. 96, 253–260 (2005).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Mercader, J. et al. Morphometrics of Starch Granules From Sub-Saharan Plants and the Taxonomic Identification of Ancient Starch. Frontiers in Earth Science 6, https://doi.org/10.3389/feart.2018.00146 (2018).ADS 
    Article 

    Google Scholar 
    Rots, V., Hayes, E., Cnuts, D., Lepers, C. & Fullagar, R. Making sense of residues on flaked stone artefacts: learning from blind tests. PLOS One 11, e0150437. https://doi.org/10.1371/journal.pone.0150437 (2016).Hayes, E. & Rots, V. Documenting scarce and fragmented residues on stone tools: an experimental approach using optical microscopy and SEM-EDS. Archaeological and Anthropological Sciences 11, 3065–3099 (2019).
    Google Scholar 
    Stoodley, P., Sauer, K., Davies, D. G. & Costerton, J. W. Biofilms as Complex Differentiated Communities. Annual Review of Microbiology 56, 187–209 (2002).CAS 
    PubMed 

    Google Scholar 
    Krumbein, W. E., Paterson, D. M. & Zavarzin, G. A. Fossil and Recent Biofilms: A Natural History of Life on Earth. (Springer Science & Business Media, 2003).Wanger, G., Southam, G. & Onstott, T. C. Structural and Chemical Characterization of a Natural Fracture Surface from 2.8 Kilometers Below Land Surface: Biofilms in the Deep Subsurface. Geomicrobiology Journal 23, 443-452 (2006).CAS 

    Google Scholar 
    Anders, M. H., Laubach, S. E. & Scholz, C. H. Microfractures: A Review. Journal of Structural Geology 69, 377–394 (2014).Fletcher, M. Attachment of Pseudomonas fluorescens to glass and influence of electrolytes on bacterium substratum separation distance. Journal of Bacteriology 170, 2027–2030 (1988).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Fong, J. N. & Tildiz, F. H. Biofilm Matrix Proteins. Microbiology Spectrum 3, 1–16 (2015).CAS 

    Google Scholar 
    Cnuts, D. & Rots, V. Extracting residues from stone tools for optical analysis: towards an experiment-based protocol. Archaeological and Anthropological Sciences 10, 1717–1736 (2018).
    Google Scholar 
    Xhauflair, H. et al. Use-related or contamination? Residue and use-wear mapping on stone tools used for experimental processing of plants from Southeast Asia. Quaternary International 427, 80–93 (2017).Pedergnana, A. “All that glitters is not gold”: Evaluating the Nature of the Relationship Between Archeological Residues and Stone Tool Function. Journal of Paleolithic Archaeology 3, 225–254 (2019).
    Google Scholar  More

  • in

    Marching in the streets for climate-crisis action

    CAREER Q&A
    22 February 2022

    Marching in the streets for climate-crisis action

    Conservationist Charlie Gardner explains why he joined Scientists for Extinction Rebellion and its civil-disobedience protests.

    Christine Ro

    0

    Christine Ro

    Christine Ro is a freelance journalist based in Buenos Aires.

    View author publications

    You can also search for this author in PubMed
     Google Scholar

    Twitter

    Facebook

    Email

    Charlie Gardner speaks at an Extinction Rebellion protest.Credit: Louise Jasper Photography

    Conservationist, consultant and activist Charlie Gardner is a lecturer in conservation biology at the Durrell Institute of Conservation and Ecology at the University of Kent in Canterbury, UK. He regularly participates in protests with Scientists for Extinction Rebellion, an offshoot of a broader movement that uses nonviolent civil disobedience to push for action on the climate and biodiversity crises. He has also advised on legislation such as the UK Climate and Ecological Emergency Bill, which seeks to curb UK greenhouse-gas emissions and biodiversity loss, and is currently making its way through Parliament. What drove you to activism? Teaching. Five or six years ago, I was standing in front of a lecture theatre, full of young people who are going to suffer the consequences of climate change much more than I am. I couldn’t stand that I wasn’t doing everything I could. When Extinction Rebellion (XR) was launched in the United Kingdom in October 2018, it felt like the answer. As conservationists, we silently wish that members of the general public cared more about the destruction of nature. Now they are taking to the streets and I have this moral obligation to be there in support.How have you been working with Scientists for XR?In October 2019, a group of scientists came together to create Scientists for XR, which has carried out many actions. These include pasting scientific papers to the walls of the London headquarters of News Corp in 2021 in protest against inadequate climate-change coverage in the company’s newspapers. The group has different functions. One is to provide scientific support for the wider XR movement, so that it remains founded on solid scientific ground. And a second is to advocate. Scientists vocally supporting XR sends a powerful message. Society trusts scientists. A third function is direct action. Scientists for XR groups have been involved in a number of XR events, such as marches and roadblocks. For example, at the 2021 opening of a London Science Museum exhibition sponsored by oil and gas company Shell, some scientists locked themselves to parts of the exhibition in protest against the sponsorship, while our scientist group set up a table outside to demonstrate principles of atmospheric cooling to engage with the public. Events such as this serve to highlight the issue of science museums accepting sponsorship from fossil-fuel companies.How can scientists dip their toes into this type of work?What the public sees of these direct actions is the tip of the iceberg. For every person out on the streets, there are 20 more behind the scenes involved in other tasks: organizing, producing press releases, baking cakes for marchers. Whatever you enjoy doing and have skills in, there is a role for you. Taking part does not have to involve engaging in civil disobedience yourself, or putting yourself in a risky position. One of the most important jobs at a protest is for people to stand at the edges, engaging the public in conversations. That’s a role that scientists can perform fantastically.How have your advocacy and activism benefited you?There’s this crazy notion that scientists shouldn’t speak out because it will damage their reputations. But activism has had the opposite effect on my career. My research is based on conservation in Madagascar; it’s fairly niche. I previously had no global reputation. Since becoming a vocal scientist-activist, my reputation and my visibility as a scientist have soared. Also, activism is great for my mental health. Knowing I’m doing what I can is important to me. There are simply the best people in these movements, and there’s a sense of community. Does being a vocal activist diminish your scientific credibility?Popular perception holds that scientists must be neutral purveyors of information and not speak up about what that information means. Somehow, if we do so, it could damage our credibility.But when scientists take personal risks and make personal sacrifices, that communicates the urgency of the situation in an important way. If scientists are saying that it’s time for action, but not acting themselves, that undermines their own arguments. How do you balance your academic responsibilities with advocacy?For five years, I worked half-time at the University of Kent. I did this deliberately, to allow me the freedom to engage in other activities, including conservation consultancy, activism and writing popular non-fiction. I left that post last year, partly to focus on activism and writing, and partly out of frustration with the precarity of academic life.There are things that enable me to be less single-minded in the pursuit of my career: I come from a position of relative privilege; I’m not interested in accumulating money; and I don’t have children. So I think academia has been a good fit for me, but only because it doesn’t fill my life.

    doi: https://doi.org/10.1038/d41586-022-00518-4This interview has been edited for length and clarity.

    Related Articles

    How junior scientists can land a seat at the leadership table

    An IPCC reviewer shares his thoughts on the climate debate

    A ‘no-brainer’ decision to become a COVID-19 vaccine-centre volunteer

    Subjects

    Policy

    Ethics

    Conservation biology

    Latest on:

    Policy

    Two scientists will replace disgraced US science adviser Eric Lander
    News 17 FEB 22

    NIH issues a seismic mandate: share data publicly
    News 16 FEB 22

    China: reform research-evaluation criteria
    Correspondence 15 FEB 22

    Ethics

    Global Disability Summit demands health equity
    Correspondence 17 FEB 22

    Expand diversity definitions beyond their Western perspective
    Correspondence 08 FEB 22

    Research evaluation needs to change with the times
    Editorial 11 JAN 22

    Jobs

    Research Fellow

    Dana-Farber Cancer Institute (DFCI)
    Boston, MA, United States

    Post Doctoral Associate

    University of Massachusetts Medical School (UMass Medical School)
    Worcester, MA, United States

    Senior Research Scientist – Artificial Molecular Machinery Lab

    Francis Crick Institute
    London, United Kingdom

    Call for Applications: Clinical and Public Health Fellowships

    Wellcome Trust/DBT India Alliance
    India, India More

  • in

    The role of the endolithic alga Ostreobium spp. during coral bleaching recovery

    Moberg, F. & Folke, C. Ecological goods and services of coral reef ecosystems. Ecol. Econ. 29, 215–233 (1999).
    Google Scholar 
    Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742 (2007).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Muscatine, L., Pool, R. R. & Trench, R. K. Symbiosis of algae and invertebrates: Aspects of the symbiont surface and the host-symbiont interface. Trans. Am. Microsc. Soc. 94, 450–469 (1975).CAS 
    PubMed 

    Google Scholar 
    Muscatine, L. & Porter, J. W. Reef corals: Mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27, 454–460 (1977).
    Google Scholar 
    LaJeunesse, T. C. et al. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. https://doi.org/10.1016/j.cub.2018.07.008 (2018).Article 
    PubMed 

    Google Scholar 
    Colombo-Pallotta, M. F., Rodríguez-Román, A. & Iglesias-Prieto, R. Calcification in bleached and unbleached Montastraea faveolata: Evaluating the role of oxygen and glycerol. Coral Reefs 29, 899–907 (2010).ADS 

    Google Scholar 
    Hoegh-Guldberg, O. & Smith, G. J. The effect of sudden changes in temperature, light and salinity on the population density and export of zooxanthellae from the reef corals Stylphora pistillata Esper and Seriatopora hystrix Dana. J. Exp. Mar. Biol. Ecol. 129, 279–303 (1989).
    Google Scholar 
    Iglesias-Prieto, R., Matta, J. L., Robins, W. A. & Trench, R. K. Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc. Natl. Acad. Sci. 89, 10302–10305 (1992).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Scheufen, T., Krämer, W. E., Iglesias-Prieto, R. & Enríquez, S. Seasonal variation modulates coral sensibility to heat-stress and explains annual changes in coral productivity. Sci. Rep. 7, 1–15 (2017).CAS 

    Google Scholar 
    Enríquez, S., Méndez, E. R. & Iglesias-Prieto, R. Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol. Oceanogr. 50, 1025–1032 (2005).ADS 

    Google Scholar 
    Terán, E., Méndez, E. R., Enríquez, S. & Iglesias-Prieto, R. Multiple light scattering and absorption in reef-building corals. Appl. Opt. 49, 5032 (2010).ADS 
    PubMed 

    Google Scholar 
    Swain, T. D. et al. Skeletal light-scattering accelerates bleaching response in reef-building corals. BMC Ecol. 16, 1–18 (2016).
    Google Scholar 
    Rodríguez-Román, A., Hernández-Pech, X., E Thome, P., Enríquez, S. & Iglesias-Prieto, R. Photosynthesis and light utilization in the Caribbean coral Montastraea faveolata recovering from a bleaching event. Limnol. Oceanogr. 51, 2702–2710 (2006).ADS 

    Google Scholar 
    Kemp, D. W., Hernandez-Pech, X., Iglesias-Prieto, R., Fitt, W. K. & Schmidt, G. W. Community dynamics and physiology of Symbiodinium spp. before, during, and after a coral bleaching event. Limnol. Oceanogr. 59, 788–797 (2014).ADS 
    CAS 

    Google Scholar 
    Thornhill, D. J., LaJeunesse, T. C., Kemp, D. W., Fitt, W. K. & Schmidt, G. W. Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar. Biol. 148, 711–722 (2006).
    Google Scholar 
    Schoepf, V. et al. Annual coral bleaching and the long-term recovery capacity of coral. Proc. R. Soc. B Biol. Sci. 282, 20151887 (2015).
    Google Scholar 
    Hughes, T. P. et al. Global warming and recurrent mass bleaching of corals. Nature 543, 373–377 (2017).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Hoegh-Guldberg, O. Climate change, coral bleaching and the future of the world’s coral reefs. Mar. Freshw. Res. https://doi.org/10.1071/MF99078 (1999).Article 

    Google Scholar 
    Scheufen, T., Iglesias-Prieto, R. & Enríquez, S. Changes in the number of symbionts and Symbiodinium cell pigmentation modulate differentially coral light absorption and photosynthetic performance. Front. Mar. Sci. 4, 309 (2017).
    Google Scholar 
    Warner, M. E., Fitt, W. K. & Schmidt, G. W. Damage to photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching. Proc. Natl. Acad. Sci. U. S. A. 96, 8007–8012 (1999).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Takahashi, S., Nakamura, T., Sakamizu, M., van Woesik, R. & Yamasaki, H. Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef-building corals. Plant Cell Physiol. 45, 251–255 (2004).CAS 
    PubMed 

    Google Scholar 
    Bollati, E. et al. Optical feedback loop involving dinoflagellate symbiont and scleractinian host drives colorful coral bleaching. Curr. Biol. https://doi.org/10.1016/j.cub.2020.04.055 (2020).Article 
    PubMed 

    Google Scholar 
    Dove, S. G., Hoegh-Guldberg, O. & Ranganathan, S. Major colour patterns of reef-building corals are due to a family of GFP-like proteins. Coral Reefs 19, 197–204 (2001).
    Google Scholar 
    Salih, A., Larkum, A., Cox, G., Kühl, M. & Hoegh-Guldberg, O. Fluorescent pigments in corals are photoprotective. Nature 408, 850–853 (2000).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Fine, M. & Loya, Y. Endolithic algae: An alternative source of photoassimilates during coral bleaching. Proc. Biol. Sci. 269, 1205–1210 (2002).PubMed 
    PubMed Central 

    Google Scholar 
    Carilli, J. E., Godfrey, J., Norris, R. D., Sandin, S. A. & Smith, J. E. Periodic endolithic algal blooms in Montastraea faveolata corals may represent periods of low-level stress. Bull. Mar. Sci. 86, 10 (2010).
    Google Scholar 
    Le Campion-Alsumard, T., Golubic, S. & Hutchings, P. Microbial endoliths in skeletons of live and dead corals: Porites lobata (Moorea, French Polynesia). Mar. Ecol. Prog. Ser. 117, 149–157 (1995).ADS 

    Google Scholar 
    Schlichter, D., Kampmann, H. & Conrady, S. Trophic potential and photoecology of endolithic algae living within coral skeletons. Mar. Ecol. 18, 299–317 (1997).ADS 

    Google Scholar 
    Sangsawang, L. et al. 13C and 15N assimilation and organic matter translocation by the endolithic community in the massive coral Porites lutea. R. Soc. Open Sci. 4, 171201 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Yamazaki, S. S., Nakamura, T. & Yamasaki, H. Photoprotective role of endolithic algae colonized in coral skeleton for the host photosynthesis. In Photosynthesis. Energy from the Sun (eds. Allen, J. F., et al.) 1391–1395 (Springer Netherlands, 2008). https://doi.org/10.1007/978-1-4020-6709-9_300.Halldal, P. Photosynthetic capacities and photosynthetic action spectra of endozoic algae of the massive coral Favia. Biol. Bull. 134, 411–424 (1968).CAS 

    Google Scholar 
    Koehne, B., Elli, G., Jennings, R. C., Wilhelm, C. & Trissl, H.-W. Spectroscopic and molecular characterization of a long wavelength absorbing antenna of Ostreobium sp. Biochim. Biophys. Acta BBA Bioenerg. 1412, 94–107 (1999).CAS 

    Google Scholar 
    Wangpraseurt, D. et al. In vivo microscale measurements of light and photosynthesis during coral bleaching: Evidence for the optical feedback loop?. Front. Microbiol. 8, 59 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Lukas, K. J. Two species of the chlorophyte genus Ostreobium from skeletons of Atlantic and Caribbean reef corals. J. Phycol. 10, 331–335 (1974).
    Google Scholar 
    Fork, D. C. & Larkum, A. W. D. Light harvesting in the green alga Ostreobium sp., a coral symbiont adapted to extreme shade. Mar. Biol. 103, 381–385 (1989).
    Google Scholar 
    Massé, A., Domart-Coulon, I., Golubic, S., Duché, D. & Tribollet, A. Early skeletal colonization of the coral holobiont by the microboring Ulvophyceae Ostreobium sp. Sci. Rep. 8, 1–11 (2018).
    Google Scholar 
    Godinot, C., Tribollet, A., Grover, R. & Ferrier-Pagès, C. Bioerosion by euendoliths decreases in phosphate-enriched skeletons of living corals. Biogeosci. Discuss. 9, 2425–2444 (2012).ADS 

    Google Scholar 
    Vásquez-Elizondo, R. M. et al. Absorptance determinations on multicellular tissues. Photosynth. Res. 132, 311–324 (2017).PubMed 

    Google Scholar 
    Tribollet, A. The boring microflora in modern coral reef ecosystems: A review of its roles. In Current Developments in Bioerosion (eds. Wisshak, M. & Tapanila, L.) 67–94 (Springer Berlin Heidelberg, 2008). https://doi.org/10.1007/978-3-540-77598-0_4.Fine, M., Meroz-Fine, E. & Hoegh-Guldberg, O. Tolerance of endolithic algae to elevated temperature and light in the coral Montipora monasteriata from the southern Great Barrier Reef. J. Exp. Biol. 208, 75–81 (2005).PubMed 

    Google Scholar 
    Pernice, M. et al. Down to the bone: The role of overlooked endolithic microbiomes in reef coral health. ISME J. 14, 325–334 (2020).PubMed 

    Google Scholar 
    Schlichter, D., Zscharnack, B. & Krisch, H. Transfer of photoassimilates from endolithic algae to coral tissue. Naturwissenschaften 82, 564–567 (1995).ADS 

    Google Scholar 
    Kühl, M., Cohen, Y., Dalsgaard, T., Barker Jorgersen, B. & Revsbech, N. P. Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Mar. Ecol. Prog. Ser. 117, 159–172 (1995).ADS 

    Google Scholar 
    Marcelino, L. A. et al. Modulation of light-enhancement to symbiotic algae by light-scattering in corals and evolutionary trends in bleaching. PLoS One 8, e61492 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wangpraseurt, D. et al. Lateral light transfer ensures efficient resource distribution in symbiont-bearing corals. J. Exp. Biol. 217, 489–498 (2014).PubMed 

    Google Scholar 
    Wangpraseurt, D., Jacques, S. L., Petrie, T. & Kühl, M. Monte Carlo modeling of photon propagation reveals highly scattering coral tissue. Front. Plant Sci. 7, 1404 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Carilli, J., Donner, S. D. & Hartmann, A. C. Historical temperature variability affects coral response to heat stress. PLoS One 7, e34418 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Marcelino, V. R. & Verbruggen, H. Multi-marker metabarcoding of coral skeletons reveals a rich microbiome and diverse evolutionary origins of endolithic algae. Sci. Rep. 6, 1–9 (2016).
    Google Scholar 
    del Campo, J., Pombert, J.-F., Šlapeta, J., Larkum, A. & Keeling, P. J. The ‘other’ coral symbiont: Ostreobium diversity and distribution. ISME J. 11, 296–299 (2017).PubMed 

    Google Scholar 
    Massé, A. et al. Functional diversity of microboring Ostreobium algae isolated from corals. Environ. Microbiol. 22, 4825–4846 (2020).PubMed 

    Google Scholar 
    Iglesias-Prieto, R., Beltran, V. H., LaJeunesse, T. C., Reyes-Bonilla, H. & Thome, P. E. Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc. R. Soc. B Biol. Sci. 271, 1757–1763 (2004).CAS 

    Google Scholar 
    Fisher, P. L., Malme, M. K. & Dove, S. The effect of temperature stress on coral–Symbiodinium associations containing distinct symbiont types. Coral Reefs 31, 473–485 (2012).ADS 

    Google Scholar 
    Jeffrey, S. W. & Humphrey, G. F. New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. BPP 167, 191–194 (1975).CAS 

    Google Scholar 
    Marsh, J. A. Primary productivity of reef-building calcareous red algae. Ecology 51, 255–263 (1970).
    Google Scholar 
    Shibata, K. Pigments and a UV-absorbing substance in corals and a blue-green alga living in the Great Barrier Reef1. Plant Cell Physiol. https://doi.org/10.1093/oxfordjournals.pcp.a074411 (1969).Article 

    Google Scholar 
    López-Londoño, T. et al. Physiological and ecological consequences of the water optical properties degradation on reef corals. Coral Reefs 40, 1243–1256 (2021).
    Google Scholar  More

  • in

    Thermal imaging reveals audience-dependent effects during cooperation and competition in wild chimpanzees

    Byrne, R. W. & Bates, L. A. Sociality, evolution and cognition. Curr. Biol. 17, R714–R723 (2007).CAS 
    PubMed 

    Google Scholar 
    Wittig, R. M. & Boesch, C. Food competition and linear dominance hierarchy among female chimpanzees of the Tai National Park. Int. J. Primatol. 24, 847–867 (2003).
    Google Scholar 
    Mitani, J. C. Male chimpanzees form enduring and equitable social bonds. Anim. Behav. 77, 633–640 (2009).
    Google Scholar 
    Van Hooff, J. A. & Van Schaik, C. P. Male bonds: Afilliative relationships among nonhuman primate males. Behaviour 130, 309–337 (1994).
    Google Scholar 
    Herbinger, I., Papworth, S., Boesch, C. & Zuberbühler, K. Vocal, gestural and locomotor responses of wild chimpanzees to familiar and unfamiliar intruders: A playback study. Anim. Behav. 78, 1389–1396 (2009).
    Google Scholar 
    Watts, D. P., Muller, M., Amsler, S. J., Mbabazi, G. & Mitani, J. C. Lethal intergroup aggression by chimpanzees in Kibale National Park, Uganda. Am. J. Primatol. Off. J. Am. Soc. Primatol. 68, 161–180 (2006).
    Google Scholar 
    Watts, D. & Mitani, J. Boundary patrols and intergroup encounters in wild chimpanzees. Behaviour 138, 299–327 (2001).
    Google Scholar 
    Silk, J. B. et al. Strong and consistent social bonds enhance the longevity of female baboons. Curr. Biol. 20, 1359–1361 (2010).CAS 
    PubMed 

    Google Scholar 
    Schülke, O., Bhagavatula, J., Vigilant, L. & Ostner, J. Social bonds enhance reproductive success in male macaques. Curr. Biol. 20, 2207–2210 (2010).PubMed 

    Google Scholar 
    Surbeck, M. et al. Males with a mother living in their group have higher paternity success in bonobos but not chimpanzees. Curr. Biol. 29, R354–R355 (2019).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Aureli, F. & Schaffner, C. Relationship assessment through emotional mediation. Behaviour 139, 393–420 (2002).
    Google Scholar 
    Aureli, F. et al. Fission-fusion dynamics: New research frameworks. Curr. Anthropol. 49, 627–654 (2008).
    Google Scholar 
    Zuberbühler, K. Audience effects. Curr. Biol. 18, R189–R190 (2008).PubMed 

    Google Scholar 
    Wittig, R. M., Crockford, C., Langergraber, K. E. & Zuberbühler, K. Triadic social interactions operate across time: A field experiment with wild chimpanzees. Proc. R. Soc. B Biol. Sci. 281, 20133155 (2014).
    Google Scholar 
    Slocombe, K. E. & Zuberbühler, K. Chimpanzees modify recruitment screams as a function of audience composition. Proc. Natl. Acad. Sci. 104, 17228–17233 (2007).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Crockford, C., Wittig, R. M., Mundry, R. & Zuberbühler, K. Wild chimpanzees inform ignorant group members of danger. Curr. Biol. 22, 142–146 (2012).CAS 
    PubMed 

    Google Scholar 
    Townsend, S. W. & Zuberbuhler, K. Audience effects in chimpanzee copulation calls. Commun. Integr. Biol. 2, 282–284 (2009).PubMed 
    PubMed Central 

    Google Scholar 
    Laporte, M. N. & Zuberbühler, K. Vocal greeting behaviour in wild chimpanzee females. Anim. Behav. 80, 467–473 (2010).
    Google Scholar 
    Kreibig, S. D. Autonomic nervous system activity in emotion: A review. Biol. Psychol. 84, 394–421 (2010).PubMed 

    Google Scholar 
    Crockford, C. et al. Urinary oxytocin and social bonding in related and unrelated wild chimpanzees. Proc. R. Soc. B Biol. Sci. 280, 20122765 (2013).CAS 

    Google Scholar 
    Samuni, L. et al. Oxytocin reactivity during intergroup conflict in wild chimpanzees. Proc. Natl. Acad. Sci. 114, 268–273 (2017).CAS 
    PubMed 

    Google Scholar 
    Crockford, C., Deschner, T., Ziegler, T. E. & Wittig, R. M. Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: A review. Front. Behav. Neurosci. 8, 68 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Harrap, M. J., Hempel de Ibarra, N., Whitney, H. M. & Rands, S. A. Reporting of thermography parameters in biology: A systematic review of thermal imaging literature. R. Soc. Open Sci. 5, 181281 (2018).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ioannou, S., Gallese, V. & Merla, A. Thermal infrared imaging in psychophysiology: Potentialities and limits. Psychophysiology 51, 951–963 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Vianna, D. M. & Carrive, P. Changes in cutaneous and body temperature during and after conditioned fear to context in the rat. Eur. J. Neurosci. 21, 2505–2512 (2005).PubMed 

    Google Scholar 
    Dezecache, G., Zuberbühler, K., Davila-Ross, M. & Dahl, C. D. Skin temperature changes in wild chimpanzees upon hearing vocalizations of conspecifics. R. Soc. Open Sci. 4, 160816 (2017).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Dezecache, G., Wilke, C., Richi, N., Neumann, C. & Zuberbühler, K. Skin temperature and reproductive condition in wild female chimpanzees. PeerJ 5, e4116 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Dunbar, R. I. Functional significance of social grooming in primates. Folia Primatol. (Basel) 57, 121–131 (1991).
    Google Scholar 
    Bekoff, M. & Allen, C. The evolution of social play: Interdisciplinary analyses of cognitive processes. In The cognitive animal: empirical and theoretical perspectives on animal cognition (eds Bekoff, M. et al.) 429–435 (The MIT Press, 2002).
    Google Scholar 
    Muller, M. N. & Mitani, J. C. Conflict and cooperation in wild chimpanzees. Adv. Study Behav. 35, 275–331 (2005).
    Google Scholar 
    Slocombe, K. E. & Zuberbühler, K. Agonistic screams in wild chimpanzees (Pan troglodytes schweinfurthii) vary as a function of social role. J. Comp. Psychol. 119, 67 (2005).PubMed 

    Google Scholar 
    Hosaka, K. Intimidation display. In Mahale Chimpanzees: 50 Years of Research (eds Hosaka, K. et al.) 435–447 (Cambridge University Press, 2015).
    Google Scholar 
    Muller, M. N. & Wrangham, R. W. Dominance, aggression and testosterone in wild chimpanzees: A test of the ‘challenge hypothesis’. Anim. Behav. 67, 113–123 (2004).
    Google Scholar 
    Wrangham, R. W. The cost of sexual attraction in female Pan. In Behavioural Diversity in Chimpanzees and Bonobos (eds Boesch, C. et al.) 204-215 (Cambridge University Press, 2002).
    Google Scholar 
    Townsend, S. W., Slocombe, K. E., Thompson, M. E. & Zuberbühler, K. Female-led infanticide in wild chimpanzees. Curr. Biol. 17, R355–R356 (2007).CAS 
    PubMed 

    Google Scholar 
    Herborn, K. A. et al. Skin temperature reveals the intensity of acute stress. Physiol. Behav. 152, 225–230 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kuraoka, K. & Nakamura, K. The use of nasal skin temperature measurements in studying emotion in macaque monkeys. Physiol. Behav. 102, 347–355 (2011).CAS 
    PubMed 

    Google Scholar 
    Ermatinger, F. A., Brügger, R. K. & Burkart, J. M. The use of infrared thermography to investigate emotions in common marmosets. Physiol. Behav. 211, 112672 (2019).CAS 
    PubMed 

    Google Scholar 
    Manson, J. H. et al. Intergroup aggression in chimpanzees and humans [and comments and replies]. Curr. Anthropol. 32, 369–390 (1991).
    Google Scholar 
    Tamioso, P. R., Rucinque, D. S., Taconeli, C. A., da Silva, G. P. & Molento, C. F. M. Behavior and body surface temperature as welfare indicators in selected sheep regularly brushed by a familiar observer. J. Vet. Behav. 19, 27–34 (2017).
    Google Scholar 
    Grandi, L. C. & Heinzl, E. Data on thermal infrared imaging in laboratory non-human primates: Pleasant touch determines an increase in nasal skin temperature without affecting that of the eye lachrymal sites. Data Brief 9, 536–539 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Brügger, R. K., Willems, E. P. & Burkart, J. M. Do marmosets understand others’ conversations? A thermography approach. Sci. Adv. 7, e8790 (2021).ADS 

    Google Scholar 
    Salazar-López, E. et al. The mental and subjective skin: Emotion, empathy, feelings and thermography. Conscious. Cogn. 34, 149–162 (2015).PubMed 

    Google Scholar 
    Muller, M. N., Thompson, M. E. & Wrangham, R. W. Male chimpanzees prefer mating with old females. Curr. Biol. 16, 2234–2238 (2006).CAS 
    PubMed 

    Google Scholar 
    Watts, D. P. Coalitionary mate guarding by male chimpanzees at Ngogo, Kibale National Park, Uganda. Behav. Ecol. Sociobiol. 44, 43–55 (1998).
    Google Scholar 
    Heinrichs, M. & Domes, G. Neuropeptides and social behaviour: Effects of oxytocin and vasopressin in humans. Prog. Brain Res. 170, 337–350 (2008).CAS 
    PubMed 

    Google Scholar 
    Surbeck, M., Mundry, R. & Hohmann, G. Mothers matter! Maternal support, dominance status and mating success in male bonobos (Pan paniscus). Proc. R. Soc. B Biol. Sci. 278, 590–598 (2011).
    Google Scholar 
    Reddy, R. B. & Sandel, A. A. Social relationships between chimpanzee sons and mothers endure but change during adolescence and adulthood. Behav. Ecol. Sociobiol. 74, 1–14 (2020).
    Google Scholar 
    Kosonogov, V. et al. Facial thermal variations: A new marker of emotional arousal. PLoS One 12, e0183592 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Stanley, R. O. & Burrows, G. D. Varieties and functions of human emotion. Emot. Work Theory Res. Appl. Manag. 3–19 (2001).Fredrickson, B. L. The role of positive emotions in positive psychology: The broaden-and-build theory of positive emotions. Am. Psychol. 56, 218 (2001).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Or, C. K. & Duffy, V. G. Development of a facial skin temperature-based methodology for non-intrusive mental workload measurement. Occup. Ergon. 7, 83–94 (2007).
    Google Scholar 
    Reynolds, V. The Chimpanzees of the Budongo Forest: Ecology, Behaviour and Conservation (OUP, 2005).
    Google Scholar 
    Steketee, J. Spectral emissivity of skin and pericardium. Phys. Med. Biol. 18, 686 (1973).CAS 
    PubMed 

    Google Scholar 
    Chotard, H., Ioannou, S. & Davila-Ross, M. Infrared thermal imaging: Positive and negative emotions modify the skin temperatures of monkey and ape faces. Am. J. Primatol. 80, e22863 (2018).PubMed 

    Google Scholar 
    Newton-Fisher, N. Association by male chimpanzees: A social tactic?. Behaviour 136, 705–730 (1999).
    Google Scholar 
    Kano, F., Hirata, S., Deschner, T., Behringer, V. & Call, J. Nasal temperature drop in response to a playback of conspecific fights in chimpanzees: A thermo-imaging study. Physiol. Behav. 155, 83–94 (2016).CAS 
    PubMed 

    Google Scholar 
    Hobaiter, C. & Byrne, R. W. The gestural repertoire of the wild chimpanzee. Anim. Cogn. 14, 745–767 (2011).PubMed 

    Google Scholar 
    Nishida, T., Kano, T., Goodall, J., McGrew, W. C. & Nakamura, M. Ethogram and ethnography of Mahale chimpanzees. Anthropol. Sci. 107, 141–188 (1999).
    Google Scholar 
    Muller, M.N. Agonistic relations among Kanyawara chimpanzees. In Behavioural Diversity in Chimpanzees and Bonobos (eds Boesch, C. et al.) 212–220 (Cambridge University Press, 2002).
    Google Scholar 
    Goodall, J. The Chimpanzees of Gombe: Patterns of Behavior (Harvard University Press, 1986).
    Google Scholar 
    Wallis, J. Chimpanzee genital swelling and its role in the pattern of sociosexual behavior. Am. J. Primatol. 28, 101–113 (1992).PubMed 

    Google Scholar 
    Davila-Ross, M., Allcock, B., Thomas, C. & Bard, K. A. Aping expressions? Chimpanzees produce distinct laugh types when responding to laughter of others. Emotion 11, 1013 (2011).PubMed 

    Google Scholar 
    Schel, A. M., Townsend, S. W., Machanda, Z., Zuberbühler, K. & Slocombe, K. E. Chimpanzee alarm call production meets key criteria for intentionality. PLoS One 8, e76674 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Vardasca, R. The influence of angles and distance on assessing inner-canthi of the eye skin temperature. Thermol. Int. 27, 130–135 (2017).
    Google Scholar 
    Josse, J. & Husson, F. missMDA: A package for handling missing values in multivariate data analysis. J. Stat. Softw. 70, 1–31 (2016).
    Google Scholar 
    Neumann, C. et al. Assessing dominance hierarchies: Validation and advantages of progressive evaluation with Elo-rating. Anim. Behav. 82, 911–921 (2011).
    Google Scholar 
    Noë, R., de Waal, F. B. & van Hooff, J. A. Types of dominance in a chimpanzee colony. Folia Primatol. (Basel) 34, 90–110 (1980).
    Google Scholar 
    Maechler, M., Rousseeuw, P., Struyf, A., Hubert, M., Hornik, K. (2019). cluster: Cluster Analysis Basics and Extensions. R package version 2.1.0.Barton, K. MuMIn: Multi-model inference, R package version 0.12. 0. Httpr-Forge R-Proj. Orgprojectsmumin (2020).Zeileis, A. & Hothorn, T. Diagnostic checking in regression relationships. R News 2, 7–10 (2002).
    Google Scholar 
    Lüdecke, D., Ben-Shachar, M. S., Patil, I., Waggoner, P. & Makowski, D. Performance: An R package for assessment, comparison and testing of statistical models. J. Open Source Softw. 6, 3139 (2021).ADS 

    Google Scholar 
    Bolker, B. M. et al. Generalized linear mixed models: A practical guide for ecology and evolution. Trends Ecol. Evol. 24, 127–135 (2009).
    Google Scholar 
    Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
    Google Scholar 
    Fox, J. & Weisberg, S. An R Companion to Applied Regression (Sage, 2019).
    Google Scholar 
    Lenth, R. emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.5.4. (2021).R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/ (2017). More