Ecology

Leibniz Institute DSMZ German Collection of Microorganisms and Cell Cultures, Braunschweig, GermanyAmber Hartman Scholz, Rodrigo Sara, Scarlett Sett, Andrew Lee Hufton & Jörg OvermannLeibniz Institute of Plant Genetics and Crop Plant Research (IPK), Seeland, GermanyJens FreitagNatural History Museum, London, UKChristopher H. C. LyalOne Planet Solutions, Montpellier, FranceRodrigo SaraUniversidad de los Andes, Bogotá, ColombiaMartha Lucia CepedaPlentzia Marine Station (PiE-UPV/EHU), European Marine Biological Resource Centre – Spain (EMBRC-Spain), Plentzia, SpainIbon CancioEthiopian Biotechnology Institute, Addis Ababa, EthiopiaYemisrach Abebaw & Kassahun TesfayeNational Academy of Agricultural Science and Global Plant Council, New Delhi, IndiaKailash BansalNational Council of Scientific Research and Technologies (NCSRT), Algiers, AlgeriaHalima BenbouzaMinistry of Agriculture, Livestock, Fisheries and Cooperatives, Nairobi, KenyaHamadi Iddi BogaInstitut Pasteur, Paris, FranceSylvain Brisse, Anne-Caroline Deletoille & Raquel Hurtado-OrtizSchool of Biosciences, Cardiff University, Cardiff, UKMichael W. BrufordWellcome Sanger Institute, Hinxton, UKHayley Clissold & David NicholsonEuropean Molecular Biology Laboratory European Bioinformatics Institute (EMBL-EBI), Hinxton, UKGuy CochraneGlobal Genome Initiative, Smithsonian National Museum of Natural History, Washington, DC, USAJonathan A. CoddingtonAlexander von Humboldt Biological Resources Research Institute, Bogota, ColombiaFelipe García-CardonaSouth African National Biodiversity Institute, Cape Town, South AfricaMichelle Hamer, Jessica da Silva & Krystal A. TolleyUniversity of Nairobi, Nairobi, KenyaDouglas W. MianoInstituto Tecnologico Vale (ITV), Belem, BrazilGuilherme OliveiraMinistry of Environment and Sustainable Development, Bogota, ColombiaCarlos Ospina BravoUniversity of Lethbridge, Lethbridge, CanadaFabian RohdenNatural History Museum of Denmark, Copenhagen, DenmarkOle SebergUniversity of Freiburg, Freiburg, GermanyGernot SegelbacherNational Centre for Cell Science, Pune, IndiaYogesh ShoucheMariano Galvez University, Guatemala City, GuatemalaAlejandra Sierra National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, USAIlene Karsch-MizrachiCentre for Ecological Genomics and Wildlife Conservation, University of Johannesburg, Johannesburg, South AfricaJessica da Silva & Krystal A. TolleyUniversity of the Philippines Los Banos, Laguna, PhilippinesDesiree M. HauteaFundação Oswaldo Cruz (FIOCRUZ), Rio de Janeiro, BrazilManuela da SilvaNational Institute of Genetics, Mishima, JapanMutsuaki SuzukiInstitute of Biotechnology, Addis Ababa University, Addis Ababa, EthiopiaKassahun TesfayeCentre for Tropical Livestock Genetics and Health (CTLGH) – International Livestock Research Institute (ILRI), Nairobi, KenyaChristian Keambou TiamboMurdoch University, Murdoch, AustraliaRajeev VarshneyCorporación CorpoGen, Bogotá, ColombiaMaría Mercedes ZambranoTechnical University of Braunschweig, Braunschweig, GermanyJörg OvermannConceptualization: A.H.S., J.F., C.H.C.L., R.S., M.L.C., I.C., S.S., Y.A., K.B., H.B., H.I.B., S.Y., M.W.B., H.C., G.C., J.A.C., A.D., F.G.C., M.H., R.H.O., D.W.M., G.O., C.O.B., F.B., O.S., G.S., Y.S., A.S., J.d.S., M.d.S., M.S., K.T., K.A.T., M.M.Z., and J.O. Visualization: J.O., I.C., S.S., R.S., C.H.C.L., G.C., and A.H.S. Funding acquisition: A.H.S., J.F., and J.O. Writing—original draft: A.H.S., R.S., M.L.C., C.H.C.L., I.C., and S.S. Writing—review & editing: A.H.S., J.F., C.H.C.L., R.S., M.L.C., I.B., S.S., A.L.H., D.N., M.d.S., S.B., M.M.Z., O.S., K.T., K.A.T., R.H.O., J.d.S., C.K.T., R.V., J.O., D.H., and I.K.M. More

Rykiel EJ. Towards a definition of ecological disturbance. Austral Ecology. 1985;10:361–5.
Google Scholar 
Glasby TM, Underwood AJ. Sampling to differentiate between pulse and press perturbations. Environ Monit. Assess. 1996;42:241–52.CAS 
PubMed 

Google Scholar 
Sullivan TP, Sullivan DS. Vegetation management and ecosystem disturbance: impact of glyphosate herbicide on plant and animal diversity in terrestrial systems. Environ Rev. 2003;11:37–59.CAS 

Google Scholar 
Landers TF, Cohen B, Wittum TE, Larson EL. A review of antibiotic use in food animals: perspective, policy, and potential. Public Health Rep. 2012;127:4–22.PubMed 
PubMed Central 

Google Scholar 
Shade A, Peter H, Allison SD, Baho DL, Berga M, Bürgmann H, et al. Fundamentals of microbial community resistance and resilience. Front Microbiol. 2012;3:417.PubMed 
PubMed Central 

Google Scholar 
Hahn M. The rising threat of fungicide resistance in plant pathogenic fungi: Botrytis as a case study. J Chem Biol. 2014;7:133–41.PubMed 
PubMed Central 

Google Scholar 
Schaeffer RN, Vannette RL, Brittain C, Williams NM, Fukami T. Non-target effects of fungicides on nectar-inhabiting fungi of almond flowers. Environ. Microbiol. Rep. 2017;9:79–84.PubMed 

Google Scholar 
Zubrod JP, Bundschuh M, Arts G, Brühl CA, Imfeld G, Knäbel A, et al. Fungicides: An Overlooked Pesticide Class? Environ Sci Technol. 2019;53:3347–65.CAS 
PubMed 
PubMed Central 

Google Scholar 
Delmas CEL, Dussert Y, Delière L, Couture C, Mazet ID, Richart Cervera S, et al. Soft selective sweeps in fungicide resistance evolution: recurrent mutations without fitness costs in grapevine downy mildew. Mol. Ecol. 2017;26:1936–51.CAS 
PubMed 

Google Scholar 
McDonald MC, Renkin M, Spackman M, Orchard B, Croll D, Solomon PS, et al. Rapid parallel evolution of azole fungicide resistance in Australian populations of the wheat pathogen Zymoseptoria tritici. Appl Environ Microbiol. 2019;85:e01908–e01918.CAS 
PubMed 
PubMed Central 

Google Scholar 
Riat A, Plojoux J, Gindro K, Schrenzel J, Sanglard D. Azole Resistance of environmental and clinical Aspergillus fumigatus isolates from Switzerland. Antimicrob Agents Chemother. 2018;62:e02088–e02017.CAS 
PubMed 
PubMed Central 

Google Scholar 
Verweij PE, Snelders E, Kema GHJ, Mellado E, Melchers WJG. Azole resistance in Aspergillus fumigatus: a side-effect of environmental fungicide use? Lancet Infect Dis. 2009;9:789–95.CAS 
PubMed 

Google Scholar 
Wise K, Mueller D Are fungicides no longer just for fungi? An analysis of foliar fungicide use in corn. APSnet Features doi 2011; 10.Kandel YR, Hunt C, Ames K, Arneson N, Bradley CA, Byamukama E, et al. Meta-Analysis of Soybean Yield Response to Foliar Fungicides Evaluated from 2005 to 2018 in the United States and Canada. Plant Dis. 2021;105:1382–9.PubMed 

Google Scholar 
Imfeld G, Vuilleumier S. Measuring the effects of pesticides on bacterial communities in soil: A critical review. Eur J Soil Biol. 2012;49:22–30.CAS 

Google Scholar 
Fournier B, Dos Santos SP, Gustavsen JA, Imfeld G, Lamy F, Mitchell EAD, et al. Impact of a synthetic fungicide (fosetyl-Al and propamocarb-hydrochloride) and a biopesticide (Clonostachys rosea) on soil bacterial, fungal, and protist communities. Sci Total Environ. 2020;738:139635.CAS 
PubMed 

Google Scholar 
Morton V, Staub T A Short History of Fungicides. APSnet Feature Articles. 2008.Brent KJ, Hollomon DW Fungicide resistance in crop pathogens: how can it be managed? 2007. FRAC Monogr. No. 1, Global Prot. Fed.Perazzolli M, Antonielli L, Storari M, Puopolo G, Pancher M, Giovannini O, et al. Resilience of the natural phyllosphere microbiota of the grapevine to chemical and biological pesticides. Appl Environ Microbiol. 2014;80:3585–96.PubMed 
PubMed Central 

Google Scholar 
Knorr K, Jørgensen LN, Nicolaisen M. Fungicides have complex effects on the wheat phyllosphere mycobiome. PLoS One. 2019;14:e0213176.CAS 
PubMed 
PubMed Central 

Google Scholar 
Sapkota R, Knorr K, Jørgensen LN, O’Hanlon KA, Nicolaisen M. Host genotype is an important determinant of the cereal phyllosphere mycobiome. New Phytol. 2015;207:1134–44.CAS 
PubMed 

Google Scholar 
Southwell RJ, Brown JF, Welsby SM. Microbial interactions on the phylloplane of wheat and barley after applications of mancozeb and triadimefon. Australasian Plant Pathol. 1999;28:139.
Google Scholar 
Dickinson CH, Wallace B. Effects of late applications of foliar fungicides on activity of micro-organisms on winter wheat flag leaves. Trans Br Mycological Soc. 1976;67:103–12.
Google Scholar 
Freimoser FM, Rueda-Mejia MP, Tilocca B, Migheli Q. Biocontrol yeasts: mechanisms and applications. World J Microbiol Biotechnol. 2019;35:154.PubMed 
PubMed Central 

Google Scholar 
Fonseca Á, Inácio J Phylloplane Yeasts. In: Péter G, Rosa C (eds). Biodiversity and Ecophysiology of Yeasts. 2006. Springer Berlin Heidelberg, Berlin, Heidelberg, pp. 263–301.Cobban A, Edgcomb VP, Burgaud G, Repeta D, Leadbetter ER. Revisiting the pink-red pigmented basidiomycete mirror yeast of the phyllosphere. Microbiologyopen. 2016;5:846–55.CAS 
PubMed 
PubMed Central 

Google Scholar 
Cadez N, Zupan J, Raspor P. The effect of fungicides on yeast communities associated with grape berries. FEMS Yeast Res. 2010;10:619–30.CAS 
PubMed 

Google Scholar 
Schaeffer RN, Mei YZ, Andicoechea J, Manson JS, Irwin RE. Consequences of a nectar yeast for pollinator preference and performance. Funct Ecol. 2017;31:613–21.
Google Scholar 
Agler MT, Ruhe J, Kroll S, Morhenn C, Kim S-T, Weigel D, et al. Microbial Hub Taxa Link Host and Abiotic Factors to Plant Microbiome Variation. PLoS Biol. 2016;14:e1002352.PubMed 
PubMed Central 

Google Scholar 
Tilman D. The ecological consequences of changes in biodiversity: a search for general principles. Ecology. 1999;80:1455.
Google Scholar 
Ripple WJ, Beschta RL. Linking wolves and plants: aldo leopold on trophic cascades. BioScience. 2005;55:613.
Google Scholar 
Sahasrabudhe S, Motter AE. Rescuing ecosystems from extinction cascades through compensatory perturbations. Nat Commun. 2011;2:170.PubMed 

Google Scholar 
Zhou J, Deng Y, Luo F, He Z, Tu Q, Zhi X. Functional molecular ecological networks. mBio. 2010;1:e00169–e00210.PubMed 
PubMed Central 

Google Scholar 
Wagg C, Schlaeppi K, Banerjee S, Kuramae EE, van der Heijden MGA. Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning. Nat Commun. 2019;10:4841.PubMed 
PubMed Central 

Google Scholar 
Claassen R, Bowman M, McFadden J, Smith D, Wallander S. Tillage intensity and conservation cropping in the United States. US Dep Agric Bull Econ Rese Ser. 2018;197:1–21.
Google Scholar 
Gdanetz K, Trail F. The wheat microbiome under four management strategies, and potential for endophytes in disease protection. Phytobiomes J. 2017;1:158–68.
Google Scholar 
Longley R, Noel ZA, Benucci GMN, Chilvers MI, Trail F, Bonito G. Crop management impacts the soybean microbiome. Front Microbiol. 2020;11:1116.PubMed 
PubMed Central 

Google Scholar 
Sułowicz S, Cycoń M, Piotrowska-Seget Z. Non-target impact of fungicide tetraconazole on microbial communities in soils with different agricultural management. Ecotoxicology. 2016;25:1047–60.PubMed 
PubMed Central 

Google Scholar 
Karlsson I, Friberg H, Steinberg C, Persson P. Fungicide effects on fungal community composition in the wheat phyllosphere. PLoS One. 2014;9:e111786.PubMed 
PubMed Central 

Google Scholar 
Robertson GP, Hamilton SK Long-term ecological research at the Kellogg Biological Station LTER site. The ecology of agricultural landscapes: Long-term research on the path to sustainability 2015; 1–32.Fehr WR, Caviness CE, Burmood DT, Pennington JS. Stage of development descriptions for soybeans, Glycine max (L.) Merrill 1. Crop Sci. 1971;11:929–31.
Google Scholar 
Gdanetz K, Noel Z, Trail F. Influence of plant host and organ, management strategy, and spore traits on microbiome composition. Phytobiomes J. 2021;5:202–19.
Google Scholar 
Lundberg DS, Yourstone S, Mieczkowski P, Jones CD, Dangl JL. Practical innovations for high-throughput amplicon sequencing. Nat Methods. 2013;10:999–1002.CAS 
PubMed 

Google Scholar 
Bowsher AW, Benucci GMN, Bonito G, Shade A. Seasonal Dynamics of Core Fungi in the Switchgrass Phyllosphere, and Co-Occurrence with Leaf Bacteria. Phytobiomes J. 2021;5:60–68.
Google Scholar 
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: Community Ecology Package v. 2.5-7. 2020Anderson MJ, Willis TJ. Canonical analysis of principle coordinates: a useful method of constrained ordination for ecology. Ecology. 2003;84:511–25.
Google Scholar 
Mandal S, Van Treuren W, White RA, Eggesbø M, Knight R, Peddada SD. Analysis of composition of microbiomes: a novel method for studying microbial composition. Microb Ecol Health Dis. 2015;26:27663.PubMed 

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

Google Scholar 
Liaw A, Wiener M. Classification and regression by randomForest. R News. 2002;2:18–22.
Google Scholar 
Kursa MB, Rudnicki WR. Feature selection with the Boruta package. J Stat Softw. 2010;36:1–13.
Google Scholar 
Kurtz ZD, Müller CL, Miraldi ER, Littman DR, Blaser MJ, Bonneau RA. Sparse and compositionally robust inference of microbial ecological networks. PLoS Comput Biol. 2015;11:e1004226.PubMed 
PubMed Central 

Google Scholar 
Lindow SE, Brandl MT. Microbiology of the phyllosphere. Appl Environ Microbiol. 2003;69:1875–83.CAS 
PubMed 
PubMed Central 

Google Scholar 
Wang K, Sipilä TP, Overmyer K. The isolation and characterization of resident yeasts from the phylloplane of Arabidopsis thaliana. Sci Rep. 2016;6:39403.CAS 
PubMed 
PubMed Central 

Google Scholar 
Sun PF, Fang WT, Shin LY, Wei JY, Fu SF, Chou JY. Indole-3-acetic acid-producing yeasts in the phyllosphere of the carnivorous plant Drosera indica L. PLoS One. 2014;9:e114196.PubMed 
PubMed Central 

Google Scholar 
Yurkov AM, Kurtzman CP. Three new species of Tremellomycetes isolated from maize and northern wild rice. FEMS Yeast Res. 2019;19:foz004.CAS 
PubMed 

Google Scholar 
Sommermann L, Geistlinger J, Wibberg D, Deubel A, Zwanzig J, Babin D, et al. Fungal community profiles in agricultural soils of a long-term field trial under different tillage, fertilization and crop rotation conditions analyzed by high-throughput ITS-amplicon sequencing. PLOS ONE. 2018;13:e0195345.PubMed 
PubMed Central 

Google Scholar 
Li A-H, Yuan F-X, Groenewald M, Bensch K, Yurkov AM, Li K, et al. Diversity and phylogeny of basidiomycetous yeasts from plant leaves and soil: proposal of two new orders, three new families, eight new genera and one hundred and seven new species. Stud Mycol. 2020;96:17–140.PubMed 
PubMed Central 

Google Scholar 
Gilbert DG. Dispersal of yeasts and bacteria by Drosophila in a temperate forest. Oecologia. 1980;46:135–7.PubMed 

Google Scholar 
Starmer WT, Peris F, Fontdevila A. The transmission of yeasts by Drosophila buzzatii during courtship and mating. Animal Behaviour. 1988;36:1691–5.
Google Scholar 
Murrell EG. Can agricultural practices that mitigate or improve crop resilience to climate change also manage crop pests? Curr Opin Insect Sci. 2017;23:81–88.PubMed 

Google Scholar 
Latin R A Practical Guide to Turfgrass Fungicides. 2017.Banerjee S, Walder F, Büchi L, Meyer M, Held AY, Gattinger A, et al. Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots. ISME J. 2019;13:1722–36.PubMed 
PubMed Central 

Google Scholar 
Schmidt JE, Kent AD, Brisson VL, Gaudin ACM. Agricultural management and plant selection interactively affect rhizosphere microbial community structure and nitrogen cycling. Microbiome. 2019;7:146.PubMed 
PubMed Central 

Google Scholar 
Brockhurst MA, Buckling A, Gardner A. Cooperation peaks at intermediate disturbance. Curr Biol. 2007;17:761–5.CAS 
PubMed 

Google Scholar 
Brockhurst MA, Habets MGJL, Libberton B, Buckling A, Gardner A. Ecological drivers of the evolution of public-goods cooperation in bacteria. Ecology. 2010;91:334–40.PubMed 

Google Scholar 
Kwak M-J, Jeong H, Madhaiyan M, Lee Y, Sa T-M, Oh TK, et al. Genome information of Methylobacterium oryzae, a plant-probiotic methylotroph in the phyllosphere. PLoS One. 2014;9:e106704.PubMed 
PubMed Central 

Google Scholar 
Yoshida S, Hiradate S, Koitabashi M, Kamo T, Tsushima S. Phyllosphere Methylobacterium bacteria contain UVA-absorbing compounds. J Photochem Photobiol B. 2017;167:168–75.CAS 
PubMed 

Google Scholar 
Grady KL, Sorensen JW, Stopnisek N, Guittar J, Shade A. Assembly and seasonality of core phyllosphere microbiota on perennial biofuel crops. Nat Commun. 2019;10:4135.PubMed 
PubMed Central 

Google Scholar 
Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R, et al. Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci USA. 2009;106:16428–33.CAS 
PubMed 
PubMed Central 

Google Scholar  More

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

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

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Christine Ro

Christine Ro is a freelance journalist based in Buenos Aires.

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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.

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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

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

CORRESPONDENCE
22 February 2022

Apply Singapore Index on Cities’ Biodiversity at scale

Lena Chan

 ORCID: http://orcid.org/0000-0001-7930-7678

0
,

Kenneth Er

 ORCID: http://orcid.org/0000-0003-4485-7260

1
&

Elizabeth Maruma Mrema

2

Lena Chan

National Parks Board, Singapore Botanic Gardens, Singapore.

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Kenneth Er

National Parks Board, Singapore Botanic Gardens, Singapore.

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Elizabeth Maruma Mrema

Secretariat of the Convention on Biological Diversity, Montreal, Canada.

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In the run-up to the 15th meeting of the Conference of the Parties to the Convention on Biological Diversity, the Singapore Index on Cities’ Biodiversity has been updated to align with the post-2020 global biodiversity framework to halt biodiversity loss (see Nature 601, 298; 2022) and for application at scale (see go.nature.com/3cqrknw).

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Nature 602, 578 (2022)
doi: https://doi.org/10.1038/d41586-022-00476-x

Competing Interests
The authors declare no competing interests.

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Cranial myologyThe muscular origin and insertion sites interpreted in the cranium and mandible of each species are identified in Fig. 1; the 3D reconstructed cranial adductor muscles are shown in Fig. 2 (Incisivosaurus and Citipati) and Fig. 3 (Khaan and Conchoraptor).Figure 1Locations of reconstructed jaw adductor muscle origin and insertion sites for Incisivosaurus gauthieri (a-c), Citipati osmolskae (d-f), Khaan mckennai (g-i), and Conchoraptor gracilis (j-l). Crania are shown in dorsolateral view (a,d,g,j) with temporal and postorbital bars removed to better show medial regions within supratemporal fenestra. The left sides of the crania are shown in anteroventral view (b,e,h,k) with lower temporal and postorbital bars removed to better show posterior and lateral regions within supratemporal fenestra. Mandibles shown in dorsolateral view (c,f,i,l), lateral muscle insertions sites are shown on the left rami, medial insertion sites on the right rami. Scale bars 50 mm. Muscle abbreviations given in results section.Full size imageFigure 2Reconstructed jaw adductor musculature of Incisivosaurus gauthieri (a-d) and Citipati osmolskae (e–h) shown complete in lateral view (a,e), anterolateral view with mAMES removed (b,f), posterolateral view with mAME complex removed (c,g), and ventral view with only the mPT muscles (mPTv removed on left). Scale bars 50 mm, legend colour coded to identify individual muscles. Muscle abbreviations given in results section.Full size imageFigure 3Reconstructed jaw adductor musculature of Khaan mckennai (a-d) and Conchoraptor gracilis (e–h) shown complete in lateral view (a,e), anterolateral view with mAMES removed (b,f), posterolateral view with mAME complex removed (c,g), and ventral view with only the mPT muscles (mPTv removed on left). Scale bars 50 mm, legend colour coded to identify individual muscles. Muscle abbreviations given in results section.Full size imagem. adductor mandibulae externus medialis (mAMEM)The origin site of the mAMEM is less clear than others of the mAME group31 and we reconstruct it, as others have done, in the posterior portion of the supratemporal fossa12,13,16 where it is constrained anterolaterally and anteromedially by the positions of mAMES and mAMEP (Fig. 1). This region comprises parts of the squamosal and parietal in all four taxa and is generally vertical, concave, and featureless in all apart from Citipati. In this taxon, within the supratemporal fossa, the squamosals and parietals are flattened and orientated to form a deep and concave platform directly perpendicular to the line of action of this muscle (Fig. 1e).
The extent and direction of the mAMEM body are somewhat constrained in all taxa by the anterior, dorsal, and posterior edges of the squamosal, quadrate flange, and epipterygoid respectively.The insertion sites are typically unclear12,31. The surangular dorsomedially forms a shelf that overhangs the adductor fossa in Citipati, Khaan, and Conchoraptor (potentially taphonomically exaggerated in the latter two). Insertion onto the dorsomedial and posterior margin of the coronoid eminence (along with insertion of the mAMEP onto the eminence) has been suggested for the mAMEM12,13,31,38, but the palatal morphology (especially in the oviraptorids) restricts space around the coronoid eminence so that we do not reconstruct both the mAMEM and mAMEP as inserting in this area. Instead, we reconstruct the mAMEM as inserting on the shelf-like upper part of the surangular’s dorsomedial surface, posterior to the more anterior insertion of the mAMEP, allocating roughly half of the available surface to each (Fig. 1c,f,i,l). This insertion surface is unclear and largely reconstructed in Incisivosaurus where there is less well-defined slight convexity on the upper part of the medial surangular surface (Fig. 1c). This area of the retrodeformed mandible model for Conchoraptor uses material from Khaan and the two are thus similar (Fig. 1i,l).It is possible the mAMEM and mAMEP merged along their path or did indeed both insert in relation to the coronoid eminence39 but ultimately this would not change reconstructed bite force results significantly.m. adductor mandibulae externus profundus (mAMEP)The mAMEP generally has a medial and/or anteromedial origin within the supratemporal fenestra. A vertical crest, similar to that interpreted as the anterior border of the origination site in Carcharodontosaurus and Daspletosaurus31, Allosaurus40, Corythosaurus41, and Erlikosaurus12, is also identified in Citipati19 (Fig. 1d). We interpret it as the boundary between the mAMEP and mPSTs origins. A small sharp prominence, perhaps similar, is present on the lateral surface of the braincase in Incisivosaurus (Fig. 1a). The surface is more featureless in Khaan and Conchoraptor (Fig. 1g,j), so the anterior limit of the mAMEP origin is constrained by the origin area of the mPSTs (in turn based on the extent and position of the laterosphenoid).In Citipati, a pneumatic opening in the posterolateral wall of the parietal (visible at the posterior of the mAMEP origin in Fig. 1d), underneath where the squamosal contacts the parietal to form the posteromedial margins of the supratemporal fenestra, seems to limit the mAMEP origin posteriorly, dividing it from the mAMEM. A similar opening is not as large or obvious in the other taxa, but similar limits to the origination sites are constrained by the geometry of the supratemporal fenestra. The dorsal extent of the origin is also clear in Citipati where a sharp lateral edge, running from the frontal-parietal contact posterolaterally to form the posterior boundary of the supratemporal fossa, separates the dorsal surface of the parietals from their lateral surfaces that contribute to the supratemporal fossa (Fig. 1d). This edge may function for muscle attachment similarly as suggested for a parietal ridge in the oviraptorid Osoko2.We reconstruct the mAMEP inserting more anteriorly than mAMEM on the mandible (Fig. 1c,f,i,l), including around the apex of the coronoid elevation itself, along with the mAMES, specifically on the dorsomedial surface of coronoid prominence31,39.m. adductor mandibulae externus superficialis (mAMES)In all taxa, the mAMES can be reliably hypothesised to originate on the supratemporal bar31 (Fig. 1b,e,h,k). In oviraptorosaurs, this is formed by the postorbital and squamosal. The supratemporal bars in all taxa are mediolaterally flattened, with the medial surface directed slightly ventromedially, more so in Citipati than the others (Fig. 1e). The postorbital bars are concave along almost the entire medial surface in Citipati. In the other taxa, only the squamosal contribution is concave, with the postorbital ramus being flat or perhaps weakly convex in Khaan (Fig. 1h). There are no clear osteological signs of the extent of the mAMES origin site so we restrict it to the medial surfaces of the supratemporal bar as the ventral surface is narrow (as the bars are mediolaterally thin) and the medial surface is slightly orientated in the correct muscle direction in all taxa. The mAMES is reconstructed as originating along the full extent of this medial surface with its anterior and posterior limits constrained by the origins of the mPSTs and mAMEM respectively.The main body of the jugal has a trough-like gently concave medial surface in all taxa (especially so in Conchoraptor where the postorbital process of the jugal also has confluent concavity on its posteromedial surface) that appears like its form would neatly wrap over the exterior of the mAMES as it bulged outwards laterally and followed it anteroventrally on its origin-insertion path.The mAMES likely inserts onto the dorsolateral edge and lateral surface of the surangular31,39, on a shelf running from the coronoid process to the articular (Fig. 1c,f,i,l). This shelf is more strongly defined in the later diverging taxa, especially Citipati (Fig. 1f) and Khaan (Fig. 1i). The mandibles of the oviraptorids bear apically triangular coronoid eminences, which are anteriorly displaced compared to those of other herbivorous dinosaurs. This has been hypothesized to increase mechanical advantage and attachment area for the temporal musculature as an adaptation for a stronger crushing bite3,8,38. The anteriorly displaced coronoid eminence in oviraptorids has been hypothesized to indicate a more anteriorly extending mAMES (as suggested for some ornithischians39,42). The mAMES is reconstructed thus here. The insertion site is constrained ventrally by the reconstructed extent of the mPTv insertion site, and dorsomedially by the insertions of the mAMEM and mAMEP, which insert onto the dorsomedial surface of the surangular.m. adductor mandibulae posterior (mAMP)The mAMP is a well-constrained muscle of the adductor chamber, consistently attaching to the lateral surface of the quadrate in an extant phylogenetic bracket31. We reconstruct the origin site as the lateral surface of the pterygoid flange of the quadrate (Fig. 1), covering most of this broad flat wing but not encroaching on the epipterygoid (where the mPSTp is present) and pterygoids (where the mPTd originates). No clear muscle scar is apparent in any of the studied taxa. The mAMP origin may also have extended posterodorsally onto the confluent lateral surface of the squamosal, where a curved ridge may demark an expanded origin site for the mAMP in Conchoraptor (Fig. 1j)5; Khaan has a similar morphology (Fig. 1g). This expansion is not reconstructed in earnest—the organization of the other muscle volumes, particularly the passage of the mAMEM, would only permit a thin sliver of extra volume to be created on the expanded origin site, not significantly increasing overall volume, direction, or morphology of the mAMP.The mAMP inserts in the adductor fossa on the medial mandibular surface (Fig. 1c,f,i,l), occupying most of its main extent and posterior and ventral margins31. The adductor fossa in the oviraptorids is large and anteriorly displaced19,38,39 and much more significant than that of Incisivosaurus (Fig. 1c).m. pseudotemporalis superficialis (mPSTs)In all four taxa, the mPSTs originates on the anterior and/or anteromedial wall of the supratemporal fenestra. In Citipati, the area is formed predominantly by the capitate process of the laterosphenoid and the posterior portions of the frontal (Fig. 1d). This surface is concave and rugose. The lateral surface of the laterosphenoid is also rugose, indicating a muscle attachment19. The site is bounded laterally by the postorbital, and two ridges may constrain the origin site of the mPSTs 19: a sharp ridge runs posteromedially from the capitate process of the laterosphenoid to the epipterygoid contact, forming the ventral boundary, and a vertical ridge on the medial wall of the supratemporal fossa constrains the origin posteromedially, demarking it from the mAMEM. A triangular anterodorsal-posteroventral sloping surface (where a clear frontoparietal fossa has been lost in derived oviraptorids) extends to the dorsotemporal fossa. The anterodorsal extent of the mPSTs origin site on this surface is unclear. The frontoparietal fossa has been argued as a vascular space in dinosaurs rather than a site of muscle attachment43, and we place the mPSTs similarly (43; Fig. 7 therein), extending into this sloping triangular space but not wholly filling it. We do not reconstruct any attachment of the mPSTs extending onto the frontal processes of the postorbitals.In Khaan, the origin site is less well preserved (Fig. 1g). The mPSTs origin is placed in a similar position to Citipati and may extend slightly onto the lateral surface of parietals which contribute to the area. Similarly, in Conchoraptor (Fig. 1j), there is more of a contribution of the parietal to the anterior wall of supratemporal fenestra, but very little or no contribution of the frontal. In Conchoraptor, the whole origin site is more anteromedially positioned, and exhibits a large smooth exposure of the laterosphenoid. There are no obvious scars or ridges in the above-mentioned area of Khaan and Conchoraptor. In Incisivosaurus, the anterior corner of the supratemporal fossa is narrow and the mPSTs is more anteromedially positioned (Fig. 1a). The origin site likely comprises the laterosphenoid and small parts of the frontal and parietal.The insertion of the mPSTs is likely related to the medial aspect of the coronoid elevation and parts of the medial adductor chamber39. As the medial regions of the coronoid elevation are occupied by the mAMEP in our reconstruction we position the mPSTs, as the deepest temporal muscle, inserting into the anterior portion of the medial mandibular fossa31 and its anterodorsal rim (Fig. 1c,f,i,l).m. pseudotemporalis profundus (mPSTp)The mPSTp likely attached to the epipterygoid when present in dinosaurs31. When first described in detail, the epipterygoid of C. osmolskae (Fig. 1d) was noted as the largest of any known theropod, with a unique strongly twisted body and dorsal tip hosting robust muscle scars19. We therefore locate the mPSTp origin site on the epipterygoid of each taxon with confidence and reconstruct its origin along the length of the epipterygoid, which is present in all four taxa (though partially reconstructed in Khaan and Conchoraptor) (Fig. 1g,j).The insertion site is problematic but based on extant taxa the muscle likely inserted along the medial surface of the coronoid process or surangular 31. As the coronoid process is occupied by the insertions of the mAMES and mAMEP, we position the insertion of the mPSTp dorsomedially on the surangular, occupying the dorsal rim of the mandibular adductor fossa, the position being largely constrained dorsally by the insertions of the mAMEM and mAMEP (Fig. 1c,f,i,l).m. pterygoideus dorsalis (mPTd)The origin site of the mPTd is reconstructed as the linear dorsal surface of the pterygoid in all oviraptorids where a longitudinal concavity runs anteriorly along their length anterior of the pterygoid flange (Khaan has a convex dorsal surface but the origin site is modelled similarly (Fig. 1h), and possibly the anteriormost dorsolateral surface of the pterygoid flange. The site is limited anteriorly and anterolaterally by the palatines and ectopterygoids, onto which no attachment was modelled as they are relatively small and delicate. In Incisivosaurus, the anterior extent of the origin site is constrained by the level of the jugal ramus of the ectopterygoid anterolaterally and the main body of the ectopterygoid laterally to around a longitudinal concavity on the dorsal surface of the pterygoid (Fig. 1a)—there seems very little/no origination on the palatine.The mandibular insertion of the mPTd is commonly regarded to be onto the medial surface of the articular and retroarticular process31. We reconstruct the mPTd in this position (Fig. 1c,f,i,l), inserting in the narrow medial surface of the posterior aspect of the mandibular ramus, under the medial facet of the articular glenoid and posteriorly onto the medial surface of the retroarticular process.m. pterygoideus ventralis (mPTv)The mPTv is well constrained through phylogenetic bracketing and we reconstruct it in the oviraptorids as originating along the ventral surface of the pterygoid, probably also extending onto the ventral aspect of the pterygoid flange31 and posteriorly terminating before the contact with the quadrate. The anterior of the origin is reconstructed as the level of the ectopterygoid contact, with the site entering the longitudinal ventral concavity that is anteriorly confluent with the choanae. In Citipati, the pterygoid flange is noted as reduced compared to typically carnivorous theropods, maintaining a roughly consistent width throughout its length (Fig. 1e), as suggested by19 to indicate a relatively small m. pterygoideus. However, the main pterygoid body of oviraptorids is relatively elongate. This may be an adaptation to open space for an expanded mAME group to insert onto the mandible, whilst maintaining volume of the mPT. The pterygoids of Incisivosaurus are also elongate and reduced in width (Fig. 1b), though not as extreme as in the derived oviraptorids 24. The origin of the mPTv on the pterygoid ventral surface is interpreted as running from the posteroventral margin anteriorly into a trough medial to the ectopterygoid, and lateral of a ventral flange termed the accessory ventral flange by Xu et al.22, terminating anteriorly before the palatine contact.In all taxa, the mPTv wraps around the ventral surface of the mandibular rami and inserts on the broad section of the lateral surface of the mandible (Fig. 1c,f,i,l), predominantly comprising the angular.Bite force estimatesMeasurements of the final volumetric muscle reconstructions are given in Table 1 along with the calculated muscle contraction force, resultant force acting on the mandible, and relative contribution of each muscle. The oviraptorid oviraptorosaurians show greater muscle volumes compared to the earlier diverging Incisivosaurus. This is confirmed by greater muscle CSA values relative to cranial surface area in Citipati (1.80 × 10–2), Khaan (1.77 × 10–2), and Conchoraptor (1.37 × 10–2), compared to Incisivosaurus (1.21 × 10–2). Table 2 shows the inlever and outlever measurements used to calculate bite force resulting from each cranial muscle (and their relative contribution) and the total estimated bite force in each species, for three different bite positions. These range from 349–499 N in Citipati down in order of cranial size to 53–83 N in Incisivosaurus. Complete calculations and values for Tables 1 and 2 along with measurements for the cranial models are documented in SI 2.Table 1 Geometric measurements of reconstructed muscles and estimated contraction force (Fmus = (volume / length) × 0.3 N/mm2 × 1.532,34). Insertion angles of muscles measured in the sagittal ((alpha)) and coronal ((beta)) planes used to calculate resultant vertical force acting on mandible ((Fres = Fmus times cosalpha times cosbeta)).Full size tableTable 2 Bite force estimates (newtons) for each species, calculated (Fbite = (Fres × Linlever) ÷ Loutlever) for three points on their primary palate: the anterior tip of the beak/teeth; the middle level of the palate/toothrow; the tooth-like projection in the posterior of the oviraptorid palate/the posteriormost teeth. Percentages in brackets reported next to the bite force estimates for the oviraptorid taxa show how much greater these estimates are compared to values that would be predicted by scaling up the bite force estimates of Incisivosaurus by cranial surface area.Full size tableThe condition of the oviraptorid oviraptorosaurian skull is characterised by an increased volume for adductor musculature and increased mechanical advantage resulting from anteroposterior shortening, compared with the more conventional theropod skull geometry of the earlier diverging Incisivosaurus. Estimated bite forces conserve a greater proportion of the resultant force applied to the mandible (Fbite/Fres) in the oviraptorids compared with Incisivosaurus. This results from greater mechanical advantage in the oviraptorids’ jaw for all bite positions, though the difference relative to Incisivosaurus is greatest anteriorly (see Table 3.) These two factors result in their comparatively stronger estimated bite forces, an increase of 17–84% greater (depending on species and bite position; see Table 2) than would be predicted by scaling by cranial surface area. The increased relative bite force of the oviraptorids is not a result of more beneficial muscle insertion angles; there is no clear difference in the ratio of resultant muscle force acting on the mandible to the actual muscle force produced (Fres/Fmus) between Incisivosaurus (0.894) and the three later diverging taxa (Citipati, 0.856; Khaan, 0.851; Conchoraptor, 0.899).Table 3 Mechanical advantage values for the three different positions of the bite force estimates.Full size tableThe relative contribution of the different cranial muscles to bite force is broadly similar in each species (Fig. 4). The mPTv is typically the largest component, followed closely by the mAMES, then the rest of the mAME complex. Citipati differs from the others with a relatively stronger mAMES and mAMEM, and a relatively low value for the mPTv. The width of the Citipati cranium and mandible make the mPTv less vertically orientated and the reconstruction of the mPTv (in all taxa) is less well constrained by bone and other muscle volumes—its volume could be underestimated in all models. No clear difference emerges between Incisivosaurus and the later diverging oviraptorids in the relative contributions of cranial muscles to bite, apart from a slightly relatively weaker mPSTp and mPSTs—reconstructed muscles are proportionally similar but relatively larger in the oviraptorids. The bite force estimates of the four oviraptorosaurians (including Incisivosaurus) are significantly greater than estimates (from similar digital methods) made for other putatively herbivorous theropods of much larger body mass (Fig. 5) both relatively and absolutely.Figure 4The relative contribution of each cranial muscle to total estimated bite force by species. Note that the condition of Citipati appears the most dissimilar to all others in its comparatively stronger mAMEM, mAMES and weaker mPTv.Full size imageFigure 5Comparison of the estimated bite forces in multiple positions of Incisivosaurus and three oviraptorid oviraptorosaurians with other likely herbivorous theropod taxa that have had estimates made using similar digital volumetric methods12,13 show the oviraptorosaurians (oviraptorids especially) are capable of much stronger bite forces both relative to body mass and absolutely. Body mass values from Zanno and Makovicky11.Full size imageGape analysisThe early diverging oviraptorosaurian Incisivosaurus showed the highest estimates of optimal (25.0°) and maximum gape limit (49.5°) compared with the oviraptorid oviraptorosaurians, though not by much; estimates for gape limit in Khaan were lowest (20.5° and 40.0°), marginally less than Citipati (21.0° and 41.0°). Values for Conchoraptor (23.0° and 46.0°) lie between Incisivosaurus and the others. Figure 6 shows these estimates along with charts of the muscle cylinder strains that they are derived from. The anteriormost cylinder representing the mPTv constrains optimal and maximum gape in all but Citipati, in which it is constrained by the anteriormost regions of the mAMES. In this taxon the postorbital half of the skull is particularly low, sloping posteriorly, and the relatively low upper temporal bar directs the strong mAMES ventromedially to a prominent coronoid process of the surangular of the mandible. This leads to a shorter resting length for this muscle, causing its extension during jaw opening to exceed our tension limits just before the mPTv (which is the next most extended). The mAMEM is also relatively more extended in Citipati. The other three species are more similar in relative muscular strain, reinforcing the finding that relative muscle strength and arrangement in Citipati has more differences compared with other oviraptorids, than between some oviraptorids (Khaan and Conchoraptor) and earlier diverging oviraptorosaurians (Incisivosaurus).Figure 6Estimates of the gape angle limit of optimal tension and the maximum limit of gape for muscle tension in Incisivosaurus gauthieri (a), Citipati osmolskae (b), Khaan mckennai (c), and Conchoraptor gracilis (d) from a muscle resting length at a gape angle of 5°. Bar charts show the strain factors of individual modelled muscle cylinders at optimal and maximum tension limit; anteriormost muscle cylinders suffixed ‘1’, posteriormost suffixed ‘2’. Muscle cylinders (and corresponding bars) are colour coded yellow and red when exceeding 130% and 170% of resting length respectively, otherwise green. Note that the anterior mPTv constrains gape in all species apart from Citipati which is constrained by the anterior mAMES. Scale bars 50 mm. Muscle abbreviations given in results section.Full size imageActing antagonistically to the jaw closing muscles is the m. depressor mandibulae (mDM), primarily responsible for jaw depression (opening). It originates from around the paroccipital processes of the cranium, inserting onto the dorsal aspect of the retroarticular process of the mandible31,39. During the gape analysis, we checked mDM length change (from a shorter state at the maximum and optimal estimated gape angles to an elongated state at the 5° resting jaw angle) was not unrealistic. Strain values of the mDM were all calculated to be below the maximum strain limit (1.7) we modelled for the jaw adductors. From its shortest (maximum gape limit) the mDM in Incisivosaurus was extended by a factor of 1.08 at the estimated optimal gape limit and 1.20 the 5° resting jaw angle, Citipati reached 1.11 and 1.33 respectively, Khaan reached 1.16 and 1.48, and Conchoraptor reached 1.19 and 1.67.The oviraptorosaurians show estimated gape limits much lower than those of carnivorous theropods tested by Lautenschlager12, more like herbivorous theropod Erlikosaurus (optimal tension limit 24.0°; maximum tension limit 49.0°; resting gape of 6°). It is noted that herbivorous species exhibit lower gape angles than carnivorous species23,44, and thus our estimates of gape angle may be further support for a herbivorous diet among oviraptorosaurians (when considered against other theropods). Lautenschlager 12 notes that experimental results document gape angle in modern birds can reach angles up to around 40°. The maximum gape angles estimated for these oviraptorosaurians are similar to experimental results of gape angle in birds among passerines and Galliformes, which can reach around 40°45,46,47,48 (though this can be greater in parrots49)—a functional similarity between the crania of birds and oviraptorids which, beyond superficial beaked appearance, are quite dissimilar. More